Laccases: Production, Expression Regulation, and Applications in Pharmaceutical Biodegradation

Abstract

Laccases are a family of copper-containing oxidases with important applications in bioremediation and other various industrial and biotechnological areas. There have been over two dozen reviews on laccases since 2010 covering various aspects of this group of versatile enzymes, from their occurrence, biochemical properties, and expression to immobilization and applications. This review is not intended to be all-encompassing; instead, we highlighted some of the latest developments in basic and applied laccase research with an emphasis on laccase-mediated bioremediation of pharmaceuticals, especially antibiotics. Pharmaceuticals are a broad class of emerging organic contaminants that are recalcitrant and prevalent. The recent surge in the relevant literature justifies a short review on the topic. Since low laccase yields in natural and genetically modified hosts constitute a bottleneck to industrial-scale applications, we also accentuated a genus of laccase-producing white-rot fungi, Cerrena, and included a discussion with regards to regulation of laccase expression.

Introduction

Laccases (EC 1.10.3.2) are a family of copper-containing oxidases found in a variety of bacteria, fungi, insects, and plants (Forootanfar and Faramarzi, 2015). The four copper atoms of a typical laccase molecule are divided into Type 1 (T1), Type 2 (T2), and binuclear Type 3 (T3) Cu sites based on unique spectroscopic features. In the resting enzyme, the four copper ions are in the +2 oxidation state. The T1 and T3 coppers are characterized by absorption at ~600 and 330 nm, respectively, whereas the T2 site lacks strong absorption features. Substrate oxidation occurs at the T1, and electrons are transferred to the T2/T3 trinuclear copper cluster (TNC), where molecular oxygen is reduced to water (Wong, 2009; Jones and Solomon, 2015). Redox potentials of the T1 sites in laccases range from 0.4 to 0.8 V; plant and bacterial laccases (e.g., 0.43 and 0.46 V for Rhus vernicifera and wild-type Bacillus subtilis CotA laccases, respectively) typically have potentials on the low end of this range, whereas fungal laccases have higher redox potentials (0.47–0.79 V) (Forootanfar and Faramarzi, 2015; Jones and Solomon, 2015; Mate and Alcalde, 2015; Pogni et al., 2015). With one-electron oxidation and radical formation, laccases catalyze oxidative coupling or bond cleavage of target compounds (Jeon and Chang, 2013).

Laccases have diverse substrate spectra, which overlap with those of tyrosinase and bilirubin oxidase (Baldrian, 2006; Reiss et al., 2013). They can oxidize a wide range of compounds, such as mono-, di-, poly-, and methoxy-phenols, aromatic and aliphatic amines, hydroxyindoles, benzenethiols, carbohydrates, and inorganic/organic metal compounds (Giardina et al., 2010; Jeon et al., 2012; Karaki et al., 2016). ABTS is the most popular substrate in laccase activity assays, and 2,6-dimethoxyphenol (2,6-DMP), catechol, guaiacol, and syringaldazine are also commonly used. The scope of laccase substrates can be further broadened with the help of redox mediators from natural and synthetic sources, i.e., suitable laccase substrates that can serve as diffusible electron shuttles between enzymes and other compounds (Morozova et al., 2007; Cañas and Camarero, 2010).

Since laccases have wide substrate ranges and use only oxygen as the final electron receptor, they have widespread applications in various industries, such as textile, food, biofuel, organic synthesis, bioremediation, paper and pulp, pharmaceutical, and cosmetic industries (Arora and Sharma, 2010; Majeau et al., 2010; Osma et al., 2010; Kudanga et al., 2011; Jeon et al., 2012; Betancor et al., 2013; Kudanga and Roes-Hill, 2014; Mogharabi and Faramarzi, 2014; Viswanath et al., 2014; Pezzella et al., 2015; Mate and Alcalde, 2016; Senthivelan et al., 2016; Sitarz et al., 2016; Upadhyay et al., 2016). In fact, a few laccase products are already commercially available for food, paper, textile, and other industries (Osma et al., 2010; Rodríguez-Couto, 2012). Laccase-based biocatalysts fit well with the development of industries that are efficient, sustainable, and environment-friendly.

Nonetheless, large-scale applications of laccases are limited by the economy and efficiency of the enzymes (Osma et al., 2010; Strong and Claus, 2011; Singh G. et al., 2015). Efforts have been made to produce large amounts of laccases at lower costs with the use of recombinant organisms or screening for natural hypersecretory strains. Enzyme activity and stability can be improved through immobilization and protein engineering (Pezzella et al., 2015; Upadhyay et al., 2016). The present article is not intended to be a comprehensive review on laccases, instead, it highlights the latest developments in laccase production and applications in bioremediation, especially degradation of emerging micropollutants including antibiotics.

Natural laccase producers

Laccase-producing fungi

Although, the first discovered laccase came from the exudates of the plant R. vernicifera, laccases of fungal origins have been the most intensively studied. Fungal laccases are implicated in both intra- and extra-cellular physiological processes including delignification, morphogenesis, pigmentation, and pathogenesis (Arora and Sharma, 2010; Kües and Rühl, 2011; Forootanfar and Faramarzi, 2015).

Among fungi, ascomycetes, basidiomycetes, and deuteromycetes can produce laccases, and white-rot basidiomycetes are the most efficient lignin degraders and laccase producers (Rodríguez-Couto and Toca-Herrera, 2007; Arora and Sharma, 2010). Laccases are secreted by white-rot fungi along with other ligninolytic enzymes including manganese peroxidase, lignin peroxidase, and versatile peroxidase, although the specific types of enzymes secreted may differ with the fungus (Wong, 2009; Arora and Sharma, 2010).

Pleurotus ostreatus and Trametes versicolor can be regarded as the model organisms in basic and applied laccase research. Other well-known laccase-producing basidiomycetes include Agaricus bisporus, Cerrena unicolor, Coprinopsis cinerea, Coriolopsis gallica, Cryptococcus neoformans, Cyathus bulleri, Fomes fomentarius, Ganoderma lucidum, Panus rudis, Phlebia radiata, Polyporus brumalis, Pycnoporus cinnabarinus, Pycnoporus sanguineus, Rigidoporus microporus, Schizophyllum commune, as well as various Pleurotus (e.g., P. eryngii, P. florida, P. pulmonarius, and P. sajor-caju) and Trametes (e.g., T. hirsuta, T. pubescens, T. trogii, and T. villosa) species (Baldrian, 2006; Arora and Sharma, 2010; Forootanfar and Faramarzi, 2015).

Efforts are still being made to screen naturally-occurring laccase producers with desired laccase yields and properties (Chen et al., 2012; Si et al., 2013; Fang Z. et al., 2015; Iracheta-Cárdenas et al., 2016; Kandasamy et al., 2016; Olajuyigbe and Fatokun, 2017). Laccase yields are variable depending on the species and strain, but most naturally-occurring species appear to be poor laccase producers. However, screening and selection of promising laccase producers from nature, followed by optimization of culture conditions, still constitute a viable and effective approach to obtain organisms with tremendous laccase synthesis ability (Elisashvili and Kachlishvili, 2009). The genus Cerrena with high laccase yields and application potentials deserves attention, and the properties of its laccase can be even more desirable compared to the commercial ones (Chen et al., 2012). However, Cerrena species are relatively less studied, especially compared with Trametes species. C. unicolor, a medicinal mushroom with antitumor and other activities (Mizerska-Dudka et al., 2015; Matuszewska et al., 2016), has been reported as a constitutive laccase producer (Al-Adhami et al., 2002); indeed, for many reported Cerrena strains, an organic inducer is not necessary, but copper ions are beneficial for laccase production. On the contrary, there are also some Cerrena strains that respond to lignocellulosic substrates or aromatic compounds, corroborating that enzyme production varies with the strain and should be characterized for each potentially valuable strain. Laccase production by reported Cerrena species is summarized in Table 1, which is comparable to that by Trametes species (Majeau et al., 2010) or G. lucidum (Postemsky et al., 2017).

Fungal laccases exist in gene families, and reported basidiomycete laccase gene families contain 5–17 members (Table 2). Laccase isozymes are compared with respect to sequences, phylogenetic relationship, catalytic properties, and expression regulation. Sequence and evolutionary relationship examinations indicate that modern laccase gene families are derived from duplication-divergence events of a small set of ancestral enzymes (Valderrama et al., 2003; Kilaru et al., 2006a; Courty et al., 2009; Kües and Rühl, 2011; Bao et al., 2013; Wang W. et al., 2015). During natural evolution, the laccase paralogs may diversify in their functions, which is supported by numerous biochemical and expression characterization data (Hoegger et al., 2004, 2006; Pezzella et al., 2013; Fan et al., 2014; Yang et al., 2016b). Expression patterns provide valuable information for deducing the physiological roles played by the laccase isoforms. For example, Lcc5 in Auricularia auricula-judae is implicated in the sexual reproduction stage (Fan et al., 2014), LACC10 of P. ostreatus seems to function during vegetative growth (Pezzella et al., 2013), and Lcc3 is possibly involved in stipe elongation of Volvariella volvacea (Lu et al., 2015). Transcriptomic analysis of Flammulina velutipes implies that laccase isozymes are involved in growth and development, such as lignin bioconversion, stipe elongation and pileus formation (Wang W. et al., 2015). Sometimes, functional redundancy among laccase isozymes is suggested (Sakamoto et al., 2015; Wang W. et al., 2015). Furthermore, evidence for in vivo laccase function has been provided by genetic experiments. A siRNA knockdown study demonstrates that Lcc2 in A. bisporus contributes to toxin metabolism and defense against green mold disease (Sjaarda et al., 2015). On the other hand, overexpression of Hypsizygus marmoreus Lcc1 facilitates mycelial growth and fruiting body initiation (Zhang et al., 2015). Indeed, laccase has been developed as a novel screening marker in mushroom breeding (Sun et al., 2014). The levels of secreted laccase activity in edible mushrooms and their growing cycles are closely related, and short growing cycles are accompanied by high laccase activity (Sun et al., 2011).

Other laccase producers

Laccases also play diverse physiological roles in plants and bacteria, aside from metabolism of xenobiotics (Dwivedi et al., 2011; Singh et al., 2011; Chandra and Chowdhary, 2015; Forootanfar and Faramarzi, 2015; Wang J. et al., 2015). Plant laccase families are even larger than fungal laccase families. For example, there are at least 22 laccase genes in rice (Oryza sativa) (Huang et al., 2016). The model plant, Arabidopsis thaliana, has 17 members in its laccase gene family, which play several roles in plant growth and development, based on mutant characterization and expression profiling (Cai et al., 2006; Turlapati et al., 2011). Cotton contains 84, 44, and 46 laccase genes in cultivated allotetraploid Gossypium hirsutum and its two progenitor diploids G. arboreum and G. raimondii (Balasubramanian et al., 2016). In opposite to fungal laccases, plant laccases participate in lignin synthesis and therefore can be engineered for energy plant improvement (Wang J. et al., 2015). Plant laccases are also involved in pigmentation (Liang et al., 2006) or pigment breakdown (Fang F. et al., 2015), root elongation (Liang et al., 2006), and responses to external stresses (Cho et al., 2014; Kim et al., 2014).

Bacterial laccases were discovered relatively late compared to plant and fungal laccases (Ausec et al., 2011), but research on bacterial laccases have gained momentum over the past two decades. Bacterial laccases are implicated in various processes ranging from UV protection, pigmentation, metal oxidation, sporulation to xenobiotic degradation (Singh et al., 2011; Chandra and Chowdhary, 2015; Forootanfar and Faramarzi, 2015). Due to the widespread existence and versatility of bacteria, bacterial laccases have higher thermostability, alkaline pH optimum and halotolerance despite their low redox potentials and are valuable functional complements to fungal laccases in dye decolorization, pulp biobleaching, biofuel production as well as various other industrial and biotechnological fields (Santhanam et al., 2011; Singh et al., 2011; Chandra and Chowdhary, 2015; Martins et al., 2015).

Insect laccases are the least characterized of all known laccases. Insect laccases also play important roles in insect physiology such as cuticle sclerotization and melanization (Dittmer and Kanost, 2010; Jeon et al., 2012; Ni and Tokuda, 2013).

Classical and molecular breeding for enhancing laccase production

Classical breeding approaches

In addition to isolating natural, efficient laccase producers, classical and molecular breeding approaches are also used to increase laccase production. A successful example was provided by N-methyl-N-nitro-N-nitrosoguanidine and ultraviolet light treatments of C. gallica TCK. A mutated strain T906 was obtained, which showed three-fold higher laccase activity than the starting strain and a maximum laccase activity of 303 U/mL after 13 days (Xu et al., 2016). Mating of monokaryotic compatible P. ostreatus strains led to dikaryotic strains with higher laccase activity, and the best one produced 110 U/mL after induction for 8 days (Lettera et al., 2011; del Vecchio et al., 2012). The dikaryotic superiority in laccase activity is derived from non-additive increases in laccase transcription (Castanera et al., 2013). Furthermore, N⁺ ion implantation has recently been successfully applied to improve laccase production in Paecilomyces sp. WSH-L07 (Liu et al., 2010) and Ceriporiopsis subvermispora (Wang C. et al., 2012).

Heterologous expression

Heterologous expression is invaluable in obtaining laccase proteins based only on metagenomic sequences (Beloqui et al., 2006; Fang et al., 2011, 2012). Heterologous expression is also important for isolating a laccase from other isozymes, especially when the enzyme is not abundantly expressed or silent. In addition to structural and biochemical characterization, heterologously expressed laccases can be engineered by rational design or directed evolution for enhanced expression, catalytic activity, stability, etc. The readers are referred to the recent reviews on laccase engineering (Rodgers et al., 2010; Alcalde, 2015; Mate and Alcalde, 2015; Pardo and Camarero, 2015). Enzyme resurrection, which is heterologous expression of ancestral enzymes reconstructed based on phylogenetic analysis and inference, is of particular interest (Alcalde, 2015). Ancestral enzymes are likely to have unique and extreme properties, such as greater stability and substrate promiscuity than extant ones, considering characteristics of ancient life (e.g., thermophilic) and generalist-specialist conversion of enzymes during the course of evolution (Risso et al., 2014). White-rot fungi and lignin degradation are dated back to the Permo-Carboniferous period (Floudas et al., 2012), therefore laccase resurrection brings an intriguing and promising toolset to laccase engineering and deserves more research efforts. The resurrected enzymes can then be subjected to further engineering by directed evolution (Alcalde, 2015).

The most common heterologous host is the methylotrophic yeast Pichia pastoris with its inducible alcohol oxidase (AOX1) promoter (Antošovǎ and Sychrová, 2016; Ergün and Çalık, 2016). Other hosts, such as prokaryotes (e.g., E. coli and B. subtilis), yeasts (e.g., Saccharomyces cerevisiae and Yarrowia lipolytica), filamentous fungi (e.g., Trichoderma reesei and Aspergillus niger), and plants (e.g., Nicotiana tabacum and O. sativa), are also used (Piscitelli et al., 2010; Kittl et al., 2012; Liebeton et al., 2014; Mate and Alcalde, 2015; Antošovǎ and Sychrová, 2016). In particular, heterologous laccases were constitutively expressed in basidiomycetes Phanerochaete chrysosporium (Coconi-Linares et al., 2015) and C. cinerea (Muraguchi et al., 2011). Although, filamentous fungi are efficient in protein secretion and have actually given rise to some of the highest recombinant laccase yields reported, genetic techniques are more readily available for yeasts (Piscitelli et al., 2010; Mate and Alcalde, 2015; Antošovǎ and Sychrová, 2016).

Expression systems like P. pastoris are used to produce enzymes at the industrial scale, but ligninolytic enzymes like laccases are notoriously difficult to express heterologously (Gu et al., 2014; Ergün and Çalık, 2016). Summaries of heterologously expressed laccases can be found in recent publications (Kittl et al., 2012; Mate and Alcalde, 2015; Antošovǎ and Sychrová, 2016; Ergün and Çalık, 2016). Occasionally, high recombinant laccase activity is obtained (Hong et al., 2002, 2007; Nishibori et al., 2013), but many recombinant laccases are expressed at levels below 10 U/mL, which can be even lower than that in the native strain (Yang et al., 2016b). An appropriate host is needed for heterologous expression of laccases, but “the best host” remains elusive (Piscitelli et al., 2010; Rivera-Hoyos et al., 2013). Cryptococcus sp. S-2 is a better yeast host than P. pastoris for expression of T. versicolor and Gaeumannomyces graminis laccase genes. The expression advantage is likely due to similar codon usage and GC content of Cryptococcus sp. S-2 with those of T. versicolor and G. graminis (Nishibori et al., 2013). Nonetheless, different codon preferences of the expression host and the gene source fails to explain the variability in production yields between laccase genes derived from the same organism (Piscitelli et al., 2010). Strategies employed to increase laccase production in heterologous systems include promoter and signal peptide selection, protein engineering, codon optimization, and optimization of cultivation medium composition and process. Since different and sometimes controversial results have been recorded, it is still difficult to predict the most promising combination of parameters to maximize heterologous laccase production (Piscitelli et al., 2010; Antošovǎ and Sychrová, 2016).

Homologous expression

Due to low laccase yields in heterologous hosts, homologous expression in laccase-producing hosts might be of value for promoting laccase production. Homologous laccase expression has been attempted in A. niger (Ramos et al., 2011), C. cinerea (Kilaru et al., 2006b), Gloeophyllum trabeum (Arimoto et al., 2015), P. cinnabarinus (Alves et al., 2004), and T. versicolor (Kajita et al., 2004). For overexpression, the laccase gene is often driven by a strong promoter such as the constitutive glyceraldehyde-3-phosphate dehydrogenase gene (gpd) promoter (Alves et al., 2004; Kajita et al., 2004; Kilaru et al., 2006b; Arimoto et al., 2015) and maltose-induced glucoamylase gene (glaA) promoter (Ramos et al., 2011). In particular, when various basidiomycete promoters were compared, the A. bisporus gpdII promoter is more efficient in driving expression of the homolgous Lcc1 gene in C. cinerea than the C. cinerea tub1 (β-tubulin gene) promoter, Lentinus edodes priA (fruiting body gene) promoter or S. commune Sc3 (hydrophobin gene) promoter (Kilaru et al., 2006b). The native laccase promoter was also used, and a high laccase production level of 1 g/L was achieved in the presence of 40 g/L ethanol after fermentation of transgenic P. cinnabarinus for 24 days (Alves et al., 2004).

Regulation of laccase expression

Following successful screening of laccase-producing native hosts, laccase production is improved by fermentation technology development with respect to fermentation type, medium composition, and cultivation parameters (Elisashvili and Kachlishvili, 2009; Forootanfar and Faramarzi, 2015). Enhancing laccase yields is essential to lower production costs and promote industrial applications of the enzyme, which relies on understanding of laccase expression regulation. Numerous publications and reviews have been devoted to expression regulation of laccases (Piscitelli et al., 2011; Janusz et al., 2013).

Expression of laccase isozyme genes is differentially regulated throughout fermentation and in response to medium composition, such as metal ions, xenobiotics as well as nutrient types and levels. Laccase expression analysis has been performed on mRNA and protein levels, and the distinct responses of species, strains as well as genes no doubt paint a complex picture of laccase expression regulation. In accordance, various cis-acting responsive elements have been identified in laccase promoter regions, such as metal response element (MREs), ACE1 copper-responsive transcription factor binding sites (ACE1), xenobiotic response elements (XREs), antioxidant response elements (AREs), heat shock response elements (HSEs), CreA binding sites (CreA), and NIT2 binding sites (NIT2) (Piscitelli et al., 2011; Janusz et al., 2013). Nonetheless, function of most of the putative responsive elements is not experimentally validated, and how they interact with transcription factors remains elusive.

Copper ions are probably the most used inducer in laccase production, and the ACE1 binding site represents the most well-understood regulatory element in the laccase promoter region. Copper ions interact with the transcription factor ACE1 in P. brumalis (Nakade et al., 2013) or CUF1 in C. neoformans (Jiang et al., 2009) to increase laccase expression. In yeast, ACE1 and CUF1 have interchangeable N-terminal copper-fist DNA binding motifs despite opposite roles in maintaining copper homeostasis (Beaudoin et al., 2003). On the other hand, a copper-responsive laccase gene without an orthodox ACE1 binding site within its promoter might be regulated through a nonconventional copper-responsive element or a different mechanism (Yang et al., 2016a). Even when copper ions are not able to induce laccase production, they stabilize the copper-containing catalytic center of the enzyme (Solé et al., 2012), thus contributing to laccase activity. Besides copper, manganese and zinc are also commonly found to stimulate laccase synthesis (Lu and Ding, 2010; Solé et al., 2012; Yang et al., 2016a).

Literature describing laccase induction by xenobiotics, e.g., lignin breakdown products, dyestuffs and organic pollutants, has been accumulating. The effects of organic compounds on laccase production depend on the compound structure, fungal strain, and growth stage, laccase isozyme as well as the culture medium (Elisashvili et al., 2010; Giardina et al., 2010; Lu and Ding, 2010; Piscitelli et al., 2011; Solé et al., 2012; Janusz et al., 2013; Yang Y. et al., 2013). Combinational induction of laccase production by metal ions and organic compounds can be either synergistic (Yang Y. et al., 2013) or antagonistic (Lu and Ding, 2010).

Coculture of laccase-producing strains with other microbes is a natural way to induce laccase production, in the form of either yield increase or induction of new isozymes, and can be more effective than chemical induction. Microbial interactions with laccase inducing effects vary with the strain, but the structure of inducing metabolites and the inducing mechanism remain largely unknown (Zhang et al., 2006; Elisashvili and Kachlishvili, 2009; Flores et al., 2009; Wei et al., 2010; Pan et al., 2014; Li et al., 2016). One proposed mechanism for laccase overproduction in the coculture process is carbon source succession. Li et al. found that glycerol produced from glucose by the yeast Candida sp. is an efficient carbon source for G. lucidum upon glucose deprivation and crucial for laccase overproduction by prolonging laccase secretion time (Li et al., 2011). Phenolics and lysing enzymes produced by opposing microbes have also been suggested to have laccase-inducing ability (Zhang et al., 2006; Wei et al., 2010).

Nutrient types and concentrations have been extensively studied in the context of fungal growth and enzyme secretion. Since basidiomycetes display a wide diversity in their responses, no generalization can be made on the best carbon and nitrogen sources or their optimal concentrations (Elisashvili and Kachlishvili, 2009; Piscitelli et al., 2011; Janusz et al., 2013). Lignocellulosic wastes containing carbohydrates and inducers are often added resulting in benefits such as lower production costs, waste reuse, and laccase production enhancement (Elisashvili and Kachlishvili, 2009; Postemsky et al., 2017).

In many fungi, laccase is produced by secondary metabolism, that is, laccase synthesis is activated by carbon or nitrogen depletion. This no doubt necessitates a long production cycle and encumbers industrial production of laccase. Therefore, a promising commercial laccase producer should produce laccase with high yields and a short fermentation cycle. A recently reported Cerrena sp. HYB07 is an example of such laccase producers (Yang et al., 2016a). Its laccase production is not inhibited by high nutrient levels, which allows biomass accumulation and a quick peak of laccase activity (Table 1). Furthermore, the laccase yield of HYB07 is mostly attributed to the predominantly expressed Lac7. The strength of the Lac7 promoter requires only copper ions and high nutrient concentrations, but not aromatic inducers, making it interesting for recombinant expression of other laccase genes.

Other factors on laccase expression are studied to a lesser extent. Laccase expression could also be regulated by oxidative stress (Yang et al., 2012; Si and Cui, 2013; Fernandez-Alejandre et al., 2016), heat shock (Wang F. et al., 2012), cAMP (Crowe and Olsson, 2001), and calmodulin (Suetomi et al., 2015).

Apparently, crosstalk exists between the internal factors (e.g., fungal strain, growth stage, laccase promoter, etc.) and external factors (metal ions, organic compounds, nutrient sources, and ratios, etc.) influencing laccase synthesis. However, until now, the bulk of the work has only attempted to decipher regulation of laccase expression by an isolated single factor or a few factors, which is undoubtedly a simplification of the complex network controlling laccase expression. The mechanism underlying the regulatory network of laccase expression awaits elucidation.

Laccase mediators

The efficiency of substrate oxidation by a laccase depends on the difference between the redox potentials of the substrate and the T1 Cu. Due to the lower redox potentials of laccases (≤0.8 V) compared to ligninolytic peroxidases (>1 V) (Wong, 2009; Rivera-Hoyos et al., 2013; Pollegioni et al., 2015; Sitarz et al., 2016), laccases are originally thought to be able to oxidize only the phenolic lignin moiety, with the majority of lignin being non-phenolic and with higher redox potentials. Low-molecular-weight redox mediators are used to expand the laccase substrate range or increase the reaction rate, especially for substrates with higher redox potentials or too large to fit in the enzyme's active site. Commonly used laccase mediators include synthetic mediators such as 2,2′-azino-bis (3-ethylbenzothiazoline-6-sulfonate) (ABTS) and 1-hydroxybenzotriazole (HBT) as well as natural phenolic mediators such as syringaldehyde (SA) and acetosyringone (AS). Despite the proven efficiency of artificial mediators, natural mediators (believed to be true mediators of fungal laccases in nature) are considered to be alternatives to the artificial ones because they are more economically feasible and environmentally friendly (Cañas and Camarero, 2010). Laccase oxidation of the substrate may proceed differently with a mediator. However, it is not always the case. Malachite green degradation products in the presence and absence of ABTS have been shown to be identical or different, depending on the enzyme (Chhabra et al., 2009; Yang et al., 2015).

Different types of mediators have different catalytic mechanisms. ABTS-mediated substrate oxidation proceeds via an electron transfer route. ABTS is first oxidized to its radical cation (ABTS^·+) and then to the di-cation (ABTS²⁺) with redox potentials of 472 and 885 mV, respectively. Unlike ABTS, an N-OH type mediator (such as HBT and violuric acid) forms the N-oxy radical upon laccase oxidation and subsequent deprotonation; the radical in turn abstracts the benzylic hydrogen atom from the substrate. Similarly, phenolic mediators also follow a radical hydrogen abstraction mechanism, but with the intermediate being a phenoxy radical (Hu et al., 2009; Wong, 2009). The effect of a mediator on laccase oxidation varies with the laccase and substrate and depends on the radicals formed, recyclability of the mediator and stability of the laccase in the presence of the mediator (Morozova et al., 2007; Wong, 2009; Cañas and Camarero, 2010; Pogni et al., 2015). Regardless of the reaction mechanism, mediators incur additional costs, and can cause toxicity (Weng et al., 2013; Becker et al., 2016) and laccase inactivation (Kurniawati and Nicell, 2007; Fillat et al., 2012; Ashe et al., 2016). Although, laccases without the requirement for facilitating mediators, the laccase/mediator system is regarded as a feasible industrial solution, ideal mediators that are cheap, green, effective, stable, recyclable, not toxic, or enzyme-inactivating should be ascertained (Morozova et al., 2007; Kües, 2015).

Laccase immobilization

Laccases are immobilized for recycling, operational stability, and resistance to application conditions. Immobilization techniques include entrapment, adsorption, covalent binding, self-immobilization as well as combinations of the aforementioned techniques. Activity recovery varies based on the enzyme, the immobilization method of choice, and preparation parameters. Compared with their free counterparts, immobilized laccases are more tolerant to high temperatures and storage and can be reused multiple times (Fernández-Fernández et al., 2013; Asgher et al., 2014), they are also more resistant to inhibitors such as NaCl (Yang et al., 2016c). Immobilization sometimes improves the catalytic activity of laccases (Arsenault et al., 2011; Sinirlioglu et al., 2013; Kumar et al., 2014) despite the common concern of reduced enzyme flexibility, steric hindrance and diffusion limitations (Sheldon, 2011; Talekar et al., 2013). Readers can refer to reviews on preparation and applications of immobilized laccases (Ba et al., 2013; Fernández-Fernández et al., 2013; Asgher et al., 2014).

Laccase applications in biodegradation of PPCPs

The value of fungi as well as fungal enzymes in pollution control and environment management has been recognized. Examples of environmentally important enzymes comprise hydrolases, laccases, lyases, peroxidases, tyrosinases, and P450 cytochrome monooxidases (Demarche et al., 2012; Yang et al., 2013a; Rao et al., 2014; Kües, 2015; Yadav and Yadav, 2015; Martinkova et al., 2016). The ability of laccases to effectively degrade and detoxify a variety of persistent organic pollutants (POPs) has received considerable attention in the field of bioremediation (Majeau et al., 2010; Strong and Claus, 2011; Gasser et al., 2014; Viswanath et al., 2014; Catherine et al., 2016), and laccases can also be used in enzymatic biosensors for environmental pollution monitoring (Rao et al., 2014). A summary of environmental contaminants as laccase substrates from published research in the year 2016 is provided in Table 3. The contaminants investigated include dyestuffs (Singh R. L. et al., 2015; Sen et al., 2016), polycyclic aromatic hydrocarbons (PAHs) (Librando and Pappalardo, 2013), endocrine disrupters (Cabana et al., 2007; Husain and Qayyum, 2012; Gasser et al., 2014), and pesticides (Maqbool et al., 2016).

Pharmaceuticals and personal care products (PPCPs) are becoming ubiquitous in the environment and are recognized as emerging trace organic contaminants (Onesios et al., 2009; Oulton et al., 2010; Wang and Wang, 2016). Laccases can be employed for their removal (Gasser et al., 2014). Laccases have been used in PPCPs as an ingredient; many products generated by laccases have antimicrobial, anticancer, antioxidant, detoxifying, or other activities (Senthivelan et al., 2016; Upadhyay et al., 2016). Specifically, laccases can be used to synthesize novel antibiotics (Mikolasch et al., 2012, 2016; Pezzella et al., 2015), and laccase-based antimicrobial formulations are considered a safe and green alternative to chemical decontamination (Grover et al., 2013). Nonetheless, the focus of this review lies in the degradation and detoxification of PPCP contaminants with laccases.

Degradation of antibiotics

Antibiotics constitute one of the most used classes of drugs in the world; they are used in human and veterinary medicine as well as livestock farming. Antibiotics that are not metabolized enter the environment (Larsson, 2014). Conventional water treatment processes cannot effectively remove antibiotics (Oulton et al., 2010), while more efficient advanced treatment methods have disadvantages such as high costs and secondary pollution (Chen et al., 2016). Antibiotics pose health risks by selecting for antibiotic-resistance bacteria (ARB). Antibiotics, ARB, and antibiotic-resistant genes have been detected in soil, sediments, and water bodies including wastewater drinking water and marine water (Thiele-Bruhn, 2003; Kümmerer, 2009; Guo et al., 2014; Larsson, 2014). There has been a fast growth in the literature describing laccase utilization in antibiotic removal, especially within the past 2 years, but this topic has not been properly reviewed.

Target antibiotics under investigation include penicillins, tetracyclines, sulfonamides, quinolones and trimethoprim, and sulfamethoxazole and tetracycline are two most studied (Table 4). The removal time ranges from minutes to hours, depending on the laccase, antibiotic and treatment parameters. Mediators such as HBT, ABTS, and SA are often used to enable or accelerate antibiotic conversion by laccases. In fact, significant antibiotic removal within 1 h usually requires involvement of an appropriate mediator (Suda et al., 2012; Weng et al., 2012, 2013; Shi et al., 2014; Ding et al., 2016). Manganese peroxidase was more efficient in tetracycline conversion than laccase, but the addition of HBT can promote laccase catalysis to a rate higher than that of manganese peroxidase (Wen et al., 2010; Suda et al., 2012) although still slower than that of lignin peroxidase (95% degradation efficiency in 5 min; Wen et al., 2009). Interestingly, mediators, i.e., ABTS, SA, and AS, are consumed without observed catalytic activity during degradation of sulfamethoxazole (Margot et al., 2015).

Sulfonamides and tetracyclines are more easily attacked by laccase compared with quinolones (Becker et al., 2016; Ding et al., 2016). This is presumably due to the strong electron donating aromatic amine group in sulfonamides and the phenol group in tetracyclines, which are not found in quinolones (Ding et al., 2016). However, identified tetracycline transformation intermediates suggest that the phenol group is not the primary target for laccase oxidation, and that oxygen addition, demethylation, water elimination reactions occur during laccase treatment (Llorca et al., 2015; Yang et al., 2017). For sulfonamides, increasing electronegativity of the substituents is accompanied by decreased degradation (Yang C. W. et al., 2016). Two sulfonamides, namely sulfapyridine and sulfathiazole, are desulfonated by laccase (Rodriguez-Rodriguez et al., 2012). Covalent cross-coupling of sulfonamides is observed with laccase and mediator SA or AS (Shi et al., 2014; Margot et al., 2015), but not ABTS (Margot et al., 2015). Trimethoprim has 2 amine groups and 3 methoxy groups and is usually administered in combination with sulfamethoxazole. Little (Touahar et al., 2014; Arca-Ramos et al., 2016) to over 60% (Kumar and Cabana, 2016) degradation of this antibiotic without a mediator have been reported. Furthermore, SA at 1,000 μM, but not 10 μM, increases trimethoprim removal from 27 to 67%; nearly complete elimination of sulfamethoxazole is achieved under the same conditions (Becker et al., 2016). Some antibiotics (e.g., penicillins) are unstable in aqueous solutions, and attention should be paid to sample preservation and quantification (Llorca et al., 2014; Becker et al., 2016).

Laccase from T. versicolor, especially the product sold by Sigma-Aldrich, is most frequently used in biodegradation studies of antibiotics as well as other trace organic contaminants. Other laccases include laccases from basidiomycetes Cerrena sp. HYB07, Echinodontium taxodii, Perenniporia strain TFRI 707, and P. sanguineus, from ascomycetes Phoma sp. and Myceliophthora thermophila (recombinantly expressed in Aspergillus oryzae) and from actinobacteria Streptomyces ipomoeae (expressed in E. coli; Table 4). Laccases immobilized by different methods have been used for antibiotic degradation, including enzymatic membrane reactors (Nguyen et al., 2014b; Becker et al., 2016), granular activated carbon (Nguyen et al., 2016a), silica beads (Rahmani et al., 2015), oriented immobilization (Shi et al., 2014), magnetic cross-linked enzyme aggregates (Kumar and Cabana, 2016; Yang et al., 2017), and cell surface display (Chen et al., 2016). In particular, enzymatic membrane reactors (gelatin-ceramic membranes grafted with commercial T. versicolor laccase) in tetracycline degradation have been evaluated in depth with respect to membrane preparation, efficiency, kinetics, and economics (de Cazes et al., 2014, 2015; Abejón et al., 2015a,b). Mathematical cost estimation indicates that the enzymatic process is still economically uncompetitive. Improvements should be made in terms of enzyme kinetics, reactor effective lifetime and regeneration costs (Abejón et al., 2015a). For example, a pore diameter of 1.4 μm, in contrast to 0.2 μm, increases enzyme loading of the membrane reactor, avoids extensive membrane area, and facilitates tetracycline degradation (de Cazes et al., 2015).

Occasionally, laccases do not participate in antibiotic removal by white-rot fungi; for instance, laccase was not responsible for oxytetracycline degradation by P. ostreatus or T. versicolor (Migliore et al., 2012; Mir-Tutusaus et al., 2014) or sulfamethoxazole degradation by aquatic ascomycete Phoma sp. UHH 5-1-03 (Hofmann and Schlosser, 2016). In these cases, other enzymes, such as cytochrome P450, may be resorted to for biodegradation. It should still be pointed out that even when extracellular laccase is not able to directly oxidize sulfamethoxazole, when a mediator is added, significant removal is achieved (Yang et al., 2013b; Hofmann and Schlosser, 2016).

Laccases are also applied in combination with other processes in antibiotic treatment, such as ultrasound (Sutar and Rathod, 2015) and soil adsorption (Ding et al., 2016). The involvement of other processes facilitates degradation of antibiotics, e.g., quinolone antibiotics, which are recalcitrant to laccase oxidation. Laccase can also improve efficiency and stability of antibiotic removal by other organisms. When sulfamethoxazole is the transformed by non-laccase-producing bacteria Alcaligenes faecalis, the efficiency drops when some metabolites such as N4-acetyl-sulfamethoxazole are transformed back to the parent compound. The removal efficiency does not decrease when the coculture of A. faecalis with laccase-producing P. sanguineus is used or when cell-free laccase was added to A. faecalis culture (Li et al., 2016).

Toxicity of antibiotics after laccase treatment is commonly assessed via growth inhibition assay or bioluminescence inhibition test (Table 4). Antibiotic degradation by laccase mostly leads to reduced toxicity. A good example comes from the comparison of the sulfamethoxazole transformation products and their toxicity by A. faecalis with or without exogenous laccase. N-hydroxy sulfamethoxazole (HO-SMX), a toxic and recalcitrant intermediate of sulfamethoxazole, is formed upon A. faecalis treatment. Additional laccase, on the other hand, eliminates HO-SMX along with the toxicity (Li et al., 2016). However, sometimes laccase/mediator-catalyzed antibiotic transformation results in even higher toxicity, and this seems to frequently associate with the mediator SA (Weng et al., 2013; Nguyen et al., 2014b; Becker et al., 2016). It is postulated that the enhanced toxicity can be derived from oxidation of aromatic structures, especially phenols, to quinonoids (Becker et al., 2016).

The majority of studies on antibiotic degradation were carried out in aqueous environments, but there have been a few studies on remediation of soil (Singh R. et al., 2015), river sediment (Chang and Ren, 2015), and sludge (Yang C. W. et al., 2016). Laccase-containing extract from spent mushroom compost of Pleurotus eryngii and extract-containing microcapsules enhanced degradation of three tetracyclines in river sediment (Chang and Ren, 2015) as well as degradation of three sulfonamides in sewage sludge (Yang C. W. et al., 2016). Sulfonamide antibiotics can form stable covalent bonds with humic constituents, and laccase can catalyze unreactive hydroquinone moieties in humic acid to reactive, electrophilic quionone moieties which in turn react with the antibiotic. This will affect the fate, bioactivity, and extractability of sulfonamides in soils (Gulkowska et al., 2012, 2013; Schwarz et al., 2015).

Degradation of other PPCPs

Besides antibiotics, many other PPCPs are actively evaluated as laccase substrates, including anticonvulsants (e.g., carbamazepine and benzodiazepines) (Ostadhadi-Dehkordi et al., 2012), fungicides (e.g., ketoconazole) (Yousefi-Ahmadipour et al., 2016), anti-inflammatory drugs (e.g., acetaminophen, aspirin, diclofenac, and ketoprofen) (Marco-Urrea et al., 2010a; Ba et al., 2014a; Domaradzka et al., 2015; Singh et al., 2016), antidepressants (e.g., imipramine) (Tahmasbi et al., 2016), lipid regulators (e.g., clofibric acid) (Ji et al., 2016a), biocides (triclosan and chlorophene) (Shi et al., 2016), insect repellents (e.g., N,N-diethyl-m-toluamide) (Tran et al., 2013), and sunscreen agents (e.g., oxybenzone) (Garcia et al., 2011).

Among these PPCPs, diclofenac, carbamazepine, and triclosan are the most investigated (Table 5); triclosan is phenolic and the other two are non-phenolic. Carbamazepine is the most recalcitrant to oxidation by laccase (Yang et al., 2013b; Nguyen et al., 2014a,b; Touahar et al., 2014; Hofmann and Schlosser, 2016; Kumar and Cabana, 2016) or peroxidases (Zhang and Geißen, 2010; Eibes et al., 2011). Carbamazepine contains a strong electron-attracting amide group, which may account for its recalcitrance (Yang et al., 2013b). In contrast, triclosan has a strong electron donating hydroxyl group despite simultaneous presence of electron withdrawing chlorinated groups, which makes it susceptible to laccase oxidation (Garcia-Morales et al., 2015). Chlorine atoms are also found in diclofenac along with aromatic amine (Nguyen et al., 2014c, 2015), but it is more prone to laccase oxidation than carbamazepine.

In addition to removal of pharmaceutical compounds with laccases, laccase-producing fungi, bacteria and actinomycetes are also evaluated. Laccase is at least partially responsible for pollutant degradation (Marco-Urrea et al., 2010b; Tran et al., 2010; Nguyen et al., 2014d; Popa et al., 2014; Boonnorat et al., 2016; Hofmann and Schlosser, 2016; Vasiliadou et al., 2016). On the contrary, other studies failed to established dependence of pharmaceutical removal on extracellular laccase (Marco-Urrea et al., 2009; Jelic et al., 2012; Yang et al., 2013b). Laccase is also used in combination with other enzymes, such as versatile peroxidase and glucose oxidase (Touahar et al., 2014) or tyrosinase (Ba et al., 2014a) in pharmaceutical removal. Other processes, such as adsorption, are also found to improve compound removal when used in combination with laccase biodegradation (Ba et al., 2014b; Nguyen et al., 2014b,d; Xu et al., 2014; Ji et al., 2016a). Horseradish peroxidase is more efficient than laccase in triclosan removal (Melo et al., 2016), and versatile peroxidase has a wider removal spectrum than laccase (Touahar et al., 2014).

Simultaneous laccase degradation of multiple trace organic contaminants demonstrates that phenolic compounds are generally more easily degraded than non-phenolic compounds (Nguyen et al., 2014a,d), which is expected since phenolic compounds are considered natural laccase substrates. Transformation rates may be different if the compounds are present in solutions of single compounds or in mixtures. For example, Margot et al. found that diclofenac removal is enhanced whereas bisphenol A (BPA) and mefenamic acid elimination is decreased in mixtures (Margot et al., 2013b). Nair et al. also found improved degradation of diclofenac in the presence of BPA and 17-α-ethinylestradiol, whereas degradation of the latter two compounds is not affected in the mixture (Nair et al., 2013). Phenolic compounds such as BPA can serve as a mediator for non-phenolic compounds or may facilitate polymerization (Margot et al., 2013b; Nair et al., 2013; Touahar et al., 2014; Ji et al., 2016a). The majority of work on contaminant removal was carried out in buffers; biodegradation efficiency decreases in real wastewaters (Nair et al., 2013; Touahar et al., 2014; Garcia-Morales et al., 2015; Le et al., 2016), which presents a challenge for laccase applications. Real wastewater has elevated pH compared with the optimized buffer system and potential laccase inhibitors (e.g., organic matter, heavy metals, and ions). However, a few studies still achieved efficient pharmaceutical degradation in real wastewaters (Garcia et al., 2011; Ba et al., 2014a,b; Rodríguez-Delgado et al., 2016).

Laccase mediators HBT and SA are most often used in degradation of PPCPs. Degradation improvement upon mediator addition is significant in the enzymatic membrane reactor and limited in batch incubation (Nguyen et al., 2015). Different conversion mechanisms of triclosan, namely oligomerization in the presence of a laccase mediator and bond cleavage followed by dechlorination in the absence of a laccase mediator have been demonstrated (Murugesan et al., 2010). Laccase-mediated triclosan oligomerization has been confirmed, but dechlorination with only laccase has also been reported (Cabana et al., 2011). More studies comparing transformation pathways with or without a mediator should be carried out. Although, laccase most often has detoxifying effects, laccase and mediator pure preparations and mixture are toxic to bioluminescent bacteria (Nguyen et al., 2016b). Furthermore, inclusion of the natural mediator SA, but not synthetic mediator HBT, in laccase treatment of trace organic contaminants elevates effluent toxicity even though the target contaminants showed negligible toxicity at the low concentration (Nguyen et al., 2014a,c, 2016b).

Conclusions

Since the first discovery of laccase over 100 years ago, much has been elucidated about the occurrence, biochemistry, sequences, production, and application potentials of this diverse class of enzymes. We have briefly reviewed some recent developments in laccase research with a focus on production and applications in pharmaceutical degradation. Despite the exciting promise laccases bring, applied research is still mostly performed on the laboratory scale. Emphasis should be placed on augmenting the yields and efficiency and lowering application costs, which constitute bottlenecks in scalable and sustainable applications of laccases. While laccase mediators are widely used to aid laccase-catalyzed oxidation, the transformation metabolites as well as their toxicity should always be analyzed. It is clear that more work needs to be done to realize the full potential of these versatile enzymes.

References

• 1

  AbejónR.BellevilleM. P.Sanchez-MarcanoJ. (2015a). Design, economic evaluation and optimization of enzymatic membrane reactors for antibiotics degradation in wastewaters. Sep. Purif. Technol.156, 183–199. 10.1016/j.seppur.2015.09.072

  • CrossRef
  • Google Scholar

• 2

  AbejónR.De CazesM.BellevilleM. P.Sanchez-MarcanoJ. (2015b). Large-scale enzymatic membrane reactors for tetracycline degradation in WWTP effluents. Water Res.73, 118–131. 10.1016/j.watres.2015.01.012

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 3

  Al-AdhamiA. J. H.BryjakJ.Greb-MarkiewiczB.Peczyńska-CzochW. (2002). Immobilization of wood-rotting fungi laccases on modified cellulose and acrylic carriers. Process Biochem.37, 1387–1394. 10.1016/S0032-9592(02)00023-7

  • CrossRef
  • Google Scholar

• 4

  AlcaldeM. (2015). Engineering the ligninolytic enzyme consortium. Trends Biotechnol.33, 155–162. 10.1016/j.tibtech.2014.12.007

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 5

  AlvesA. M.RecordE.LomascoloA.ScholtmeijerK.AstherM.WesselsJ. G.et al. (2004). Highly efficient production of laccase by the basidiomycete Pycnoporus cinnabarinus. Appl. Environ. Microbiol.70, 6379–6384. 10.1128/AEM.70.11.6379-6384.2004

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 6

  AntošovǎZ.SychrováH. (2016). Yeast hosts for the production of recombinant laccases: a review. Mol. Biotechnol.58, 93–116. 10.1007/s12033-015-9910-1

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 7

  Arca-RamosA.KumarV. V.EibesG.MoreiraM. T.CabanaH. (2016). Recyclable cross-linked laccase aggregates coupled to magnetic silica microbeads for elimination of pharmaceuticals from municipal wastewater. Environ. Sci. Pollut. Res.23, 8929–8939. 10.1007/s11356-016-6139-x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 8

  ArimotoM.YamagishiK.WangJ.TanakaK.MiyoshiT.KameiI.et al. (2015). Molecular breeding of lignin-degrading brown-rot fungus Gloeophyllum trabeum by homologous expression of laccase gene. AMB Express5, 81. 10.1186/s13568-015-0173-9

  • CrossRef
  • Google Scholar

• 9

  AroraD. S.SharmaR. K. (2010). Ligninolytic fungal laccases and their biotechnological applications. Appl. Biochem. Biotechnol.160, 1760–1788. 10.1007/s12010-009-8676-y

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 10

  ArsenaultA.CabanaH.JonesJ. P. (2011). Laccase-based CLEAs: chitosan as a novel cross-linking agent. Enzyme Res.2011:376015. 10.4061/2011/376015

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 11

  AsgherM.ShahidM.KamalS.IqbalH. M. N. (2014). Recent trends and valorization of immobilization strategies and ligninolytic enzymes by industrial biotechnology. J. Mol. Catal. B Enzym.101, 56–66. 10.1016/j.molcatb.2013.12.016

  • CrossRef
  • Google Scholar

• 12

  AsheB.NguyenL. N.HaiF. I.LeeD.-J.van de MerweJ. P.LeuschF. D. L.et al. (2016). Impacts of redox-mediator type on trace organic contaminants degradation by laccase: degradation efficiency, laccase stability and effluent toxicity. Int. Biodeterior. Biodegradation113, 169–176. 10.1016/j.ibiod.2016.04.027

  • CrossRef
  • Google Scholar

• 13

  AshrafiS. D.NasseriS.AlimohammadiM.MahviA. H.FaramarziM. A. (2015). Optimization of the enzymatic elimination of flumequine by laccase-mediated system using response surface methodology. Desalin. Water Treat.57, 14478–14487. 10.1080/19443994.2015.1063462

  • CrossRef
  • Google Scholar

• 14

  AusecL.ZakrzewskiM.GoesmannA.SchlüterA.Mandic-MulecI. (2011). Bioinformatic analysis reveals high diversity of bacterial genes for laccase-like enzymes. PLoS ONE6:e25724. 10.1371/journal.pone.0025724

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 15

  BaS.ArsenaultA.HassaniT.JonesJ. P.CabanaH. (2013). Laccase immobilization and insolubilization: from fundamentals to applications for the elimination of emerging contaminants in wastewater treatment. Crit. Rev. Biotechnol.33, 404–418. 10.3109/07388551.2012.725390

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 16

  BaS.HarouneL.Cruz-MoratoC.JacquetC.TouaharI. E.BellengerJ. P.et al. (2014a). Synthesis and characterization of combined cross-linked laccase and tyrosinase aggregates transforming acetaminophen as a model phenolic compound in wastewaters. Sci. Total Environ.487, 748–755. 10.1016/j.scitotenv.2013.10.004

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 17

  BaS.JonesJ. P.CabanaH. (2014b). Hybrid bioreactor (HBR) of hollow fiber microfilter membrane and cross-linked laccase aggregates eliminate aromatic pharmaceuticals in wastewaters. J. Hazard. Mater.280, 662–670. 10.1016/j.jhazmat.2014.08.062

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 18

  BalasubramanianV. K.RaiK. M.ThuS. W.HiiM. M.MenduV. (2016). Genome-wide identification of multifunctional laccase gene family in cotton (Gossypium spp.); expression and biochemical analysis during fiber development. Sci. Rep.6:34309. 10.1038/srep34309

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 19

  Balcazar-LopezE.Mendez-LorenzoL. H.Batista-GarciaR. A.Esquivel-NaranjoU.AyalaM.KumarV. V.et al. (2016). Xenobiotic compounds degradation by heterologous expression of a Trametes sanguineus laccase in Trichoderma atroviride. PLoS ONE11:e0147997. 10.1371/journal.pone.0147997

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 20

  BaldrianP. (2006). Laccases-occurrence and properties. FEMS Microbiol. Rev.30, 215–242. 10.1111/j.1574-4976.2005.00010.x

  • CrossRef
  • Google Scholar

• 21

  BaoD.GongM.ZhengH.ChenM.ZhangL.WangH.et al. (2013). Sequencing and comparative analysis of the straw mushroom (Volvariella volvacea) genome. PLoS ONE8:e58294. 10.1371/journal.pone.0058294

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 22

  BeaudoinJ.MercierA.LangloisR.LabbéS. (2003). The Schizosaccharomyces pombe Cuf1 is composed of functional modules from two distinct classes of copper metalloregulatory transcription factors. J. Biol. Chem.278, 14565–14577. 10.1074/jbc.M300861200

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 23

  BeckerD.Varela Della GiustinaS.Rodriguez-MozazS.SchoevaartR.BarceloD.de CazesM.et al. (2016). Removal of antibiotics in wastewater by enzymatic treatment with fungal laccase - Degradation of compounds does not always eliminate toxicity. Bioresour. Technol.219, 500–509. 10.1016/j.biortech.2016.08.004

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 24

  BeloquiA.PitaM.PolainaJ.Martínez-AriasA.GolyshinaO. V.ZumárragaM.et al. (2006). Novel polyphenol oxidase mined from a metagenome expression library of bovine rumen: biochemical properties, structural analysis, and phylogenetic relationships. J. Biol. Chem.281, 22933–22942. 10.1074/jbc.M600577200

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 25

  BetancorL.JohnsonG. R.LuckariftH. R. (2013). Stabilized laccases as heterogeneous bioelectrocatalysts. ChemCatChem5, 46–60. 10.1002/cctc.201200611

  • CrossRef
  • Google Scholar

• 26

  BlánquezA.GuillénF.RodríguezJ.AriasM. E.HernándezM. (2016). The degradation of two fluoroquinolone based antimicrobials by SilA, an alkaline laccase from Streptomyces ipomoeae. World J. Microbiol. Biotechnol.32, 52. 10.1007/s11274-016-2032-5

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 27

  BoonnoratJ.TechkarnjanarukS.HondaR.PrachanurakP. (2016). Effects of hydraulic retention time and carbon to nitrogen ratio on micro-pollutant biodegradation in membrane bioreactor for leachate treatment. Bioresour. Technol.219, 53–63. 10.1016/j.biortech.2016.07.094

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 28

  CabanaH.AhamedA.LeducR. (2011). Conjugation of laccase from the white rot fungus Trametes versicolor to chitosan and its utilization for the elimination of triclosan. Bioresour. Technol.102, 1656–1662. 10.1016/j.biortech.2010.09.080

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 29

  CabanaH.JonesJ. P.AgathosS. N. (2007). Elimination of endocrine disrupting chemicals using white rot fungi and their lignin modifying enzymes: a review. Eng. Life Sci.7, 429–456. 10.1002/elsc.200700017

  • CrossRef
  • Google Scholar

• 30

  CaiX.DavisE. J.BallifJ.LiangM.BushmanE.HaroldsenV.et al. (2006). Mutant identification and characterization of the laccase gene family in Arabidopsis. J. Exp. Bot.57, 2563–2569. 10.1093/jxb/erl022

  • CrossRef
  • Google Scholar

• 31

  CañasA. I.CamareroS. (2010). Laccases and their natural mediators: biotechnological tools for sustainable eco-friendly processes. Biotechnol. Adv.28, 694–705. 10.1016/j.biotechadv.2010.05.002

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 32

  CastaneraR.OmariniA.SantoyoF.PérezG.PisabarroA. G.RamírezL. (2013). Non-additive transcriptional profiles underlie dikaryotic superiority in Pleurotus ostreatus laccase activity. PLoS ONE8:e73282. 10.1371/journal.pone.0073282

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 33

  CastaneraR.PérezaG.OmariniA.AlfaroM.PisabarroA. G.FaracoV.et al. (2012). Transcriptional and enzymatic profiling of Pleurotus ostreatus laccase genes in submerged and solid-state fermentation cultures. Appl. Environ. Microbiol.78, 4037–4045. 10.1128/AEM.07880-11

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 34

  CatherineH.PenninckxM.FrédéricD. (2016). Product formation from phenolic compounds removal by laccases: a review. Environ. Technol. Innov.5, 250–266. 10.1016/j.eti.2016.04.001

  • CrossRef
  • Google Scholar

• 35

  ChandraR.ChowdharyP. (2015). Properties of bacterial laccases and their application in bioremediation of industrial wastes. Environ. Sci. Process. Impacts17, 326–342. 10.1039/C4EM00627E

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 36

  ChangB.-V.RenY.-L. (2015). Biodegradation of three tetracyclines in river sediment. Ecol. Eng.75, 272–277. 10.1016/j.ecoleng.2014.11.039

  • CrossRef
  • Google Scholar

• 37

  ChangY. T.LeeJ. F.LiuK. H.LiaoY. F.YangV. (2016). Immobilization of fungal laccase onto a nonionic surfactant-modified clay material: application to PAH degradation. Environ. Sci. Pollut. Res.23, 4024–4035. 10.1007/s11356-015-4248-6

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 38

  ChenS.-C.WuP.-H.SuY.-C.WenT.-N.WeiY.-S.WangN.-C.et al. (2012). Biochemical characterization of a novel laccase from the basidiomycete fungus Cerrena sp. WR1. Protein Eng. Des. Sel.25, 761–769. 10.1093/protein/gzs082

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 39

  ChenY.StempleB.KumarM.WeiN. (2016). Cell surface display fungal laccase as a renewable biocatalyst for degradation of persistent micropollutants bisphenol A and sulfamethoxazole. Environ. Sci. Technol.50, 8799–8808. 10.1021/acs.est.6b01641

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 40

  ChhabraM.MishraS.SreekrishnanT. R. (2009). Laccase/mediator assisted degradation of triarylmethane dyes in a continuous membrane reactor. J. Biotechnol.143, 69–78. 10.1016/j.jbiotec.2009.06.011

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 41

  ChoH. Y.LeeC.HwangS.-G.ParkY. C.LimH. L.JangC. S. (2014). Overexpression of the OsChI1 gene, encoding a putative laccase precursor, increases tolerance to drought and salinity stress in transgenic Arabidopsis. Gene552, 98–105. 10.1016/j.gene.2014.09.018

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 42

  Coconi-LinaresN.Ortiz-VazquezE.FernandezF.LoskeA. M.Gomez-LimM. A. (2015). Recombinant expression of four oxidoreductases in Phanerochaete chrysosporium improves degradation of phenolic and non-phenolic substrates. J. Biotechnol.209, 76–84. 10.1016/j.jbiotec.2015.06.401

  • CrossRef
  • Google Scholar

• 43

  CourtyP. E.HoeggerP. J.KilaruS.KohlerA.BuéeM.GarbayeJ.et al. (2009). Phylogenetic analysis, genomic organization, and expression analysis of multi-copper oxidases in the ectomycorrhizal basidiomycete Laccaria bicolor. New Phytol.182, 736–750. 10.1111/j.1469-8137.2009.02774.x

  • CrossRef
  • Google Scholar

• 44

  CroweJ. D.OlssonS. (2001). Induction of laccase activity in Rhizoctonia solani by antagonistic Pseudomonas fluorescens strains and a range of chemical treatments. Appl. Environ. Microbiol.67, 2088–2094. 10.1128/AEM.67.5.2088-2094.2001

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 45

  DaâssiD.PrietoA.Zouari-MechichiH.MartínezM. J.NasriM.MechichiT. (2016). Degradation of bisphenol A by different fungal laccases and identification of its degradation products. Int. Biodeterior. Biodegradation110, 181–188. 10.1016/j.ibiod.2016.03.017

  • CrossRef
  • Google Scholar

• 46

  de CazesM.BellevilleM. P.MougelM.KellnerH.Sanchez-MarcanoJ. (2015). Characterization of laccase-grafted ceramic membranes for pharmaceuticals degradation. J. Membr. Sci.476, 384–393. 10.1016/j.memsci.2014.11.044

  • CrossRef
  • Google Scholar

• 47

  de CazesM.BellevilleM. P.PetitE.LlorcaM.Rodríguez-MozazS.de GunzburgJ.et al. (2014). Design and optimization of an enzymatic membrane reactor for tetracycline degradation. Catal. Today236, 146–152. 10.1016/j.cattod.2014.02.051

  • CrossRef
  • Google Scholar

• 48

  DebasteF.SongulashviliG.PenninckxM. J. (2014). The potential of Cerrena unicolor laccase immobilized on mesoporous silica beads for removal of organic micropollutants in wastewaters. Desalin. Water Treat.52, 2344–2347. 10.1080/19443994.2013.877851

  • CrossRef
  • Google Scholar

• 49

  del VecchioC.LetteraV.PezzellaC.PiscitelliA.LeoG.BiroloL.et al. (2012). Classical breeding in Pleurotus ostreatus: a natural approach for laccase production improvement. Biocatal. Biotransformation30, 78–85. 10.3109/10242422.2012.646032

  • CrossRef
  • Google Scholar

• 50

  DemarcheP.JunghannsC.NairR. R.AgathosS. N. (2012). Harnessing the power of enzymes for environmental stewardship. Biotechnol. Adv.30, 933–953. 10.1016/j.biotechadv.2011.05.013

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 51

  DingH.WuY.ZouB.LouQ.ZhangW.ZhongJ.et al. (2016). Simultaneous removal and degradation characteristics of sulfonamide, tetracycline, and quinolone antibiotics by laccase-mediated oxidation coupled with soil adsorption. J. Hazard. Mater.307, 350–358. 10.1016/j.jhazmat.2015.12.062

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 52

  DittmerN. T.KanostM. R. (2010). Insect multicopper oxidases: diversity, properties, and physiological roles. Insect Biochem. Mol. Biol.40, 179–188. 10.1016/j.ibmb.2010.02.006

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 53

  DomaradzkaD.GuzikU.WojcieszyńskaD. (2015). Biodegradation and biotransformation of polycyclic non-steroidal anti-inflammatory drugs. Rev. Environ. Sci. Biotechnol.14, 229–239. 10.1007/s11157-015-9364-8

  • CrossRef
  • Google Scholar

• 54

  D'SouzaD. T.TiwariR.SahA. K.RaghukumarC. (2006). Enhanced production of laccase by a marine fungus during treatment of colored effluents and synthetic dyes. Enzyme Microb. Technol.38, 504–511. 10.1016/j.enzmictec.2005.07.005

  • CrossRef
  • Google Scholar

• 55

  DwivediU. N.SinghP.PandeyV. P.KumarA. (2011). Structure–function relationship among bacterial, fungal and plant laccases. J. Mol. Catal. B Enzym.68, 117–128. 10.1016/j.molcatb.2010.11.002

  • CrossRef
  • Google Scholar

• 56

  EibesG.DebernardiG.FeijooG.MoreiraM. T.LemaJ. M. (2011). Oxidation of pharmaceutically active compounds by a ligninolytic fungal peroxidase. Biodegradation22, 539–550. 10.1007/s10532-010-9426-0

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 57

  ElisashviliV.KachlishviliE. (2009). Physiological regulation of laccase and manganese peroxidase production by white-rot Basidiomycetes. J. Biotechnol.144, 37–42. 10.1016/j.jbiotec.2009.06.020

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 58

  ElisashviliV.KachlishviliE.KhardzianiT.AgathosS. N. (2010). Effect of aromatic compounds on the production of laccase and manganese peroxidase by white-rot basidiomycetes. J. Ind. Microbiol. Biotechnol.37, 1091–1096. 10.1007/s10295-010-0757-y

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 59

  ErgünB. G.ÇalıkP. (2016). Lignocellulose degrading extremozymes produced by Pichia pastoris: current status and future prospects. Bioprocess Biosyst. Eng.39, 1–36. 10.1007/s00449-015-1476-6

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 60

  FanX.ZhouY.XiaoY.XuZ.BianY. (2014). Cloning, expression and phylogenetic analysis of a divergent laccase multigene family in Auricularia auricula-judae. Microbiol. Res.169, 453–462. 10.1016/j.micres.2013.08.004

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 61

  FangF.ZhangX. L.LuoH. H.ZhouJ. J.GongY. H.LiW. J.et al. (2015). An intracellular laccase is responsible for epicatechin-mediated anthocyanin degradation in litchi fruit pericarp. Plant Physiol.169, 2391–2408. 10.1104/pp.15.00359

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 62

  FangZ.LiT.WangQ.ZhangX.PengH.FangW.et al. (2011). A bacterial laccase from marine microbial metagenome exhibiting chloride tolerance and dye decolorization ability. Appl. Microbiol. Biotechnol.89, 1103–1110. 10.1007/s00253-010-2934-3

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 63

  FangZ.LiuX.ChenL.ShenY.ZhangX.FangW.et al. (2015). Identification of a laccase Glac15 from Ganoderma lucidum 77002 and its application in bioethanol production. Biotechnol. Biofuels8, 54. 10.1186/s13068-015-0235-x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 64

  FangZ. M.LiT. L.ChangF.ZhouP.FangW.HongY. Z.et al. (2012). A new marine bacterial laccase with chloride-enhancing, alkaline-dependent activity and dye decolorization ability. Bioresour. Technol.111, 36–41. 10.1016/j.biortech.2012.01.172

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 65

  Fernandez-AlejandreK. I.FloresN.Tinoco-ValenciaR.CaroM.FloresC.GalindoE.et al. (2016). Diffusional and transcriptional mechanisms involved in laccases production by Pleurotus ostreatus CP50. J. Biotechnol.223, 42–49. 10.1016/j.jbiotec.2016.02.029

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 66

  Fernández-FernándezM.SanrománM. Á.MoldesD. (2013). Recent developments and applications of immobilized laccase. Biotechnol. Adv.31, 1808–1825. 10.1016/j.biotechadv.2012.02.013

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 67

  FillatU.PrietoA.CamareroS.MartínezÁ. T.MartínezM. J. (2012). Biodeinking of flexographic inks by fungal laccases using synthetic and natural mediators. Biochem. Eng. J.67, 97–103. 10.1016/j.bej.2012.05.010

  • CrossRef
  • Google Scholar

• 68

  FloresC.VidalC.Trejo-HernandezM. R.GalindoE.Serrano-CarreonL. (2009). Selection of Trichoderma strains capable of increasing laccase production by Pleurotus ostreatus and Agaricus bisporus in dual cultures. J. Appl. Microbiol.106, 249–257. 10.1111/j.1365-2672.2008.03998.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 69

  FloudasD.BinderM.RileyR.BarryK.BlanchetteR. A.HenrissatB.et al. (2012). The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science336, 1715–1719. 10.1126/science.1221748

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 70

  ForootanfarH.FaramarziM. A. (2015). Insights into laccase producing organisms, fermentation states, purification strategies, and biotechnological applications. Biotechnol. Prog.31, 1443–1463. 10.1002/btpr.2173

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 71

  ForootanfarH.RezaeiS.Zeinvand-LorestaniH.TahmasbiH.MogharabiM.AmeriA.et al. (2016). Studies on the laccase-mediated decolorization, kinetic, and microtoxicity of some synthetic azo dyes. J. Environ. Health Sci. Eng.14, 7. 10.1186/s40201-016-0248-9

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 72

  GarciaH. A.HoffmanC. M.KinneyK. A.LawlerD. F. (2011). Laccase-catalyzed oxidation of oxybenzone in municipal wastewater primary effluent. Water Res.45, 1921–1932. 10.1016/j.watres.2010.12.027

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 73

  Garcia-MoralesR.Rodriguez-DelgadoM.Gomez-MariscalK.Orona-NavarC.Hernandez-LunaC.TorresE.et al. (2015). Biotransformation of endocrine-disrupting compounds in groundwater: bisphenol A, nonylphenol, ethynylestradiol and triclosan by a laccase cocktail from Pycnoporus sanguineus CS43. Water Air Soil Pollut.226, 251. 10.1007/s11270-015-2514-3

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 74

  GasserC. A.AmmannE. M.ShahgaldianP.CorviniP. F. (2014). Laccases to take on the challenge of emerging organic contaminants in wastewater. Appl. Microbiol. Biotechnol.98, 9931–9952. 10.1007/s00253-014-6177-6

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 75

  GiardinaP.FaracoV.PezzellaC.PiscitelliA.VanhulleS.SanniaG. (2010). Laccases: a never-ending story. Cell. Mol. Life Sci.67, 369–385. 10.1007/s00018-009-0169-1

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 76

  GroverN.DinuC. Z.KaneR. S.DordickJ. S. (2013). Enzyme-based formulations for decontamination: current state and perspectives. Appl. Microbiol. Biotechnol.97, 3293–3300. 10.1007/s00253-013-4797-x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 77

  GuC.ZhengF.LongL.WangJ.DingS. (2014). Engineering the expression and characterization of two novel laccase isoenzymes from Coprinus comatus in Pichia pastoris by fusing an additional ten amino acids tag at N-terminus. PLoS ONE9:e93912. 10.1371/journal.pone.0093912

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 78

  GulkowskaA.KraussM.RentschD.HollenderJ. (2012). Reactions of a sulfonamide antimicrobial with model humic constituents: assessing pathways and stability of covalent bonding. Environ. Sci. Technol.46, 2102–2111. 10.1021/es202272w

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 79

  GulkowskaA.SanderM.HollenderJ.KraussM. (2013). Covalent binding of sulfamethazine to natural and synthetic humic acids: assessing laccase catalysis and covalent bond stability. Environ. Sci. Technol.47, 6916–6924. 10.1021/es3044592

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 80

  GuoX.LiJ.YangF.YangJ.YinD. (2014). Prevalence of sulfonamide and tetracycline resistance genes in drinking water treatment plants in the Yangtze River Delta, China. Sci. Total Environ.493, 626–631. 10.1016/j.scitotenv.2014.06.035

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 81

  HataT.ShintateH.KawaiS.OkamuraH.NishidaT. (2010). Elimination of carbamazepine by repeated treatment with laccase in the presence of 1-hydroxybenzotriazole. J. Hazard. Mater.181, 1175–1178. 10.1016/j.jhazmat.2010.05.103

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 82

  HibiM.HatahiraS.NakataniM.YokozekiK.ShimizuS.OgawaJ. (2012). Extracellular oxidases of Cerrena sp. complementarily functioning in artificial dye decolorization including laccase, manganese peroxidase, and novel versatile peroxidases. Biocatal. Agric. Biotechnol.1, 220–225. 10.1016/j.bcab.2012.03.003

  • CrossRef
  • Google Scholar

• 83

  HoeggerP. J.KilaruS.JamesT. Y.ThackerJ. R.KüesU. (2006). Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS J.273, 2308–2326. 10.1111/j.1742-4658.2006.05247.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 84

  HoeggerP. J.Navarro-GonzalezM.KilaruS.HoffmannM.WestbrookE. D.KuesU. (2004). The laccase gene family in Coprinopsis cinerea (Coprinus cinereus). Curr. Genet.45, 9–18. 10.1007/s00294-003-0452-x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 85

  HofmannU.SchlosserD. (2016). Biochemical and physicochemical processes contributing to the removal of endocrine-disrupting chemicals and pharmaceuticals by the aquatic ascomycete Phoma sp. UHH 5-1-03. Appl. Microbiol. Biotechnol.100, 2381–2399. 10.1007/s00253-015-7113-0

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 86

  HongF.MeinanderN. Q.JönssonL. J. (2002). Fermentation strategies for improved heterologous expression of laccase in Pichia pastoris. Biotechnol. Bioeng.79, 438–449. 10.1002/bit.10297

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 87

  HongY. Z.ZhouH. M.TuX. M.LiJ. F.XiaoY. Z. (2007). Cloning of a laccase gene from a novel basidiomycete Trametes sp. 420 and its heterologous expression in Pichia pastoris. Curr. Microbiol.54, 260–265. 10.1007/s00284-006-0068-8

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 88

  HuM. R.ChaoY. P.ZhangG. Q.XueZ. Q.QianS. (2009). Laccase-mediator system in the decolorization of different types of recalcitrant dyes. J. Ind. Microbiol. Biotechnol.36, 45–51. 10.1007/s10295-008-0471-1

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 89

  HuangM. T.LuY. C.ZhangS.LuoF.YangH. (2016). Rice (Oryza sativa) laccases involved in modification and detoxification of herbicides atrazine and isoproturon residues in plants. J. Agric. Food. Chem.64, 6397–6406. 10.1021/acs.jafc.6b02187

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 90

  HusainQ.QayyumS. (2012). Biological and enzymatic treatment of bisphenol A and other endocrine disrupting compounds: a review. Crit. Rev. Biotechnol.33, 260–292. 10.3109/07388551.2012.694409

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 91

  Iracheta-CárdenasM. M.Rocha-PeñaM. A.Galán-WongL. J.Arévalo-NiñoK.Tovar-HerreraO. E. (2016). A Pycnoporus sanguineus laccase for denim bleaching and its comparison with an enzymatic commercial formulation. J. Environ. Manage.177, 93–100. 10.1016/j.jenvman.2016.04.008

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 92

  JanuszG.KucharzykK. H.PawlikA.StaszczakM.PaszczynskiA. J. (2013). Fungal laccase, manganese peroxidase and lignin peroxidase: gene expression and regulation. Enzyme Microb. Technol.52, 1–12. 10.1016/j.enzmictec.2012.10.003

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 93

  JanuszG.RogalskiJ.SzczodrakJ. (2007). Increased production of laccase by Cerrena unicolor in submerged liquid cultures. World J. Microbiol. Biotechnol.23, 1459–1464. 10.1007/s11274-007-9390-y

  • CrossRef
  • Google Scholar

• 94

  JelicA.Cruz-MoratoC.Marco-UrreaE.SarraM.PerezS.VicentT.et al. (2012). Degradation of carbamazepine by Trametes versicolor in an air pulsed fluidized bed bioreactor and identification of intermediates. Water Res.46, 955–964. 10.1016/j.watres.2011.11.063

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 95

  JeonJ. R.ChangY. S. (2013). Laccase-mediated oxidation of small organics: bifunctional roles for versatile applications. Trends Biotechnol.31, 335–341. 10.1016/j.tibtech.2013.04.002

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 96

  JeonJ. R.BaldrianP.MurugesanK.ChangY. S. (2012). Laccase-catalysed oxidations of naturally occurring phenols: from in vivo biosynthetic pathways to green synthetic applications. Microb. Biotechnol.5, 318–332. 10.1111/j.1751-7915.2011.00273.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 97

  JiC.HouJ.ChenV. (2016a). Cross-linked carbon nanotubes-based biocatalytic membranes for micro-pollutants degradation: performance, stability, and regeneration. J. Membr. Sci.520, 869–880. 10.1016/j.memsci.2016.08.056

  • CrossRef
  • Google Scholar

• 98

  JiC.HouJ.WangK.ZhangY.ChenV. (2016b). Biocatalytic degradation of carbamazepine with immobilized laccase-mediator membrane hybrid reactor. J. Membr. Sci.502, 11–20. 10.1016/j.memsci.2015.12.043

  • CrossRef
  • Google Scholar

• 99

  JiangN.SunN.XiaoD.PanJ.WangY.ZhuX. (2009). A copper-responsive factor gene CUF1 is required for copper induction of laccase in Cryptococcus neoformans. FEMS Microbiol. Lett.296, 84–90. 10.1111/j.1574-6968.2009.01619.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 100

  JinX.YuX.ZhuG.ZhengZ.FengF.ZhangZ. (2016). Conditions optimizing and application of laccase-mediator system (LMS) for the Laccase-catalyzed pesticide degradation. Sci. Rep.6:35787. 10.1038/srep35787

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 101

  JonesS. M.SolomonE. I. (2015). Electron transfer and reaction mechanism of laccases. Cell. Mol. Life Sci.72, 869–883. 10.1007/s00018-014-1826-6

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 102

  KajitaS.SugawaraS.MiyazakiY.NakamuraM.KatayamaY.ShishidoK.et al. (2004). Overproduction of recombinant laccase using a homologous expression system in Coriolus versicolor. Appl. Microbiol. Biotechnol.66, 194–199. 10.1007/s00253-004-1663-x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 103

  KandasamyS.MunirajI. K.PurushothamanN.SekarA.SharmilaD. J.KumarasamyR.et al. (2016). High level secretion of laccase (LccH) from a newly isolated white-rot basidiomycete, Hexagonia hirta MSF2. Front. Microbiol.7:707. 10.3389/fmicb.2016.00707

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 104

  KarakiN.AljawishA.HumeauC.MunigliaL.JasniewskiJ. (2016). Enzymatic modification of polysaccharides: mechanisms, properties, and potential applications: a review. Enzyme Microb. Technol.90, 1–18. 10.1016/j.enzmictec.2016.04.004

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 105

  KilaruS.HoeggerP.KüesU. (2006a). The laccase multi-gene family in Coprinopsis cinerea has seventeen different members that divide into two distinct subfamilies. Curr. Genet.50, 45–60. 10.1007/s00294-006-0074-1

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 106

  KilaruS.HoeggerP. J.MajcherczykA.BurnsC.ShishidoK.BaileyA.et al. (2006b). Expression of laccase gene lcc1 in Coprinopsis cinerea under control of various basidiomycetous promoters. Appl. Microbiol. Biotechnol.71, 200–210. 10.1007/s00253-005-0128-1

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 107

  KimE. Y.SeoY. S.ParkK. Y.KimS. J.KimW. T. (2014). Overexpression of CaDSR6 increases tolerance to drought and salt stresses in transgenic Arabidopsis plants. Gene552, 146–154. 10.1016/j.gene.2014.09.028

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 108

  KittlR.MueangtoomK.GonausC.KhazanehS. T.SygmundC.HaltrichD.et al. (2012). A chloride tolerant laccase from the plant pathogen ascomycete Botrytis aclada expressed at high levels in Pichia pastoris. J. Biotechnol.157, 304–314. 10.1016/j.jbiotec.2011.11.021

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 109

  KudangaT.Roes-HillM. L. (2014). Laccase applications in biofuels production: current status and future prospects. Appl. Microbiol. Biotechnol.98, 6525–6542. 10.1007/s00253-014-5810-8

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 110

  KudangaT.NyanhongoG. S.GuebitzG. M.BurtonaS. (2011). Potential applications of laccase-mediated coupling and grafting reactions: a review. Enzyme Microb. Technol.48, 195–208. 10.1016/j.enzmictec.2010.11.007

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 111

  KüesU. (2015). Fungal enzymes for environmental management. Curr. Opin. Biotechnol.33, 268–278. 10.1016/j.copbio.2015.03.006

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 112

  KüesU.RühlM. (2011). Multiple multi-copper oxidase gene families in basidiomycetes – what for?Curr. Genomics12, 72–94. 10.2174/138920211795564377

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 113

  KumarV. V.CabanaH. (2016). Towards high potential magnetic biocatalysts for on-demand elimination of pharmaceuticals. Bioresour. Technol.200, 81–89. 10.1016/j.biortech.2015.09.100

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 114

  KumarV. V.SivanesanS.CabanaH. (2014). Magnetic cross-linked laccase aggregates — bioremediation tool for decolorization of distinct classes of recalcitrant dyes. Sci. Total Environ.487, 830–839. 10.1016/j.scitotenv.2014.04.009

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 115

  KümmererK. (2009). Antibiotics in the aquatic environment – a review – Part II. Chemosphere75, 417–434. 10.1016/j.chemosphere.2008.11.086

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 116

  KurniawatiS.NicellJ. A. (2007). Efficacy of mediators for enhancing the laccase-catalyzed oxidation of aqueous phenol. Enzyme Microb. Technol.41, 353–361. 10.1016/j.enzmictec.2007.03.003

  • CrossRef
  • Google Scholar

• 117

  LarssonD. G. (2014). Antibiotics in the environment. Ups. J. Med. Sci.119, 108–112. 10.3109/03009734.2014.896438

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 118

  LeT. T.MurugesanK.LeeC. S.VuC. H.ChangY. S.JeonJ. R. (2016). Degradation of synthetic pollutants in real wastewater using laccase encapsulated in core-shell magnetic copper alginate beads. Bioresour. Technol.216, 203–210. 10.1016/j.biortech.2016.05.077

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 119

  LetteraV.Del VecchioC.PiscitelliA.SanniaG. (2011). Low impact strategies to improve ligninolytic enzyme production in filamentous fungi: the case of laccase in Pleurotus ostreatus. C. R. Biol.334, 781–788. 10.1016/j.crvi.2011.06.001

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 120

  LiP.WangH.LiuG.LiX.YaoJ. (2011). The effect of carbon source succession on laccase activity in the co-culture process of Ganoderma lucidum and a yeast. Enzyme Microb. Technol.48, 1–6. 10.1016/j.enzmictec.2010.07.005

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 121

  LiX.XuQ.-M.ChengJ.-S.YuanY.-J. (2016). Improving the bioremoval of sulfamethoxazole and alleviating cytotoxicity of its biotransformation by laccase producing system under coculture of Pycnoporus sanguineus and Alcaligenes faecalis. Bioresour. Technol.220, 333–340. 10.1016/j.biortech.2016.08.088

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 122

  LiangM.DavisE.GardnerD.CaiX.WuY. (2006). Involvement of AtLAC15 in lignin synthesis in seeds and in root elongation of Arabidopsis. Planta224, 1185–1196. 10.1007/s00425-006-0300-6

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 123

  LibrandoV.PappalardoM. (2013). In silico bioremediation of polycyclic aromatic hydrocarbon: a frontier in environmental chemistry. J. Mol. Graph. Model.44, 1–8. 10.1016/j.jmgm.2013.04.011

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 124

  LiebetonK.LengefeldJ.EckJ. (2014). The nucleotide composition of the spacer sequence influences the expression yield of heterologously expressed genes in Bacillus subtilis. J. Biotechnol.191, 214–220. 10.1016/j.jbiotec.2014.06.027

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 125

  LisovaZ. A.LisovA. V.LeontievskyA. A. (2010). Two laccase isoforms of the basidiomycete Cerrena unicolor VKMF-3196. Induction, isolation and properties. J. Basic Microbiol.50, 72–82. 10.1002/jobm.200900382

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 126

  LiuJ.TanL.WangJ.WangZ.NiH.LiL. (2016). Complete biodegradation of chlorpyrifos by engineered Pseudomonas putida cells expressing surface-immobilized laccases. Chemosphere157, 200–207. 10.1016/j.chemosphere.2016.05.031

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 127

  LiuZ.ZhangD.HuaZ.LiJ.DuG.ChenJ. (2010). Improvement of laccase production and its properties by low-energy ion implantation. Bioprocess Biosyst. Eng.33, 639–646. 10.1007/s00449-009-0389-7

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 128

  LlorcaM.GrosM.Rodriguez-MozazS.BarceloD. (2014). Sample preservation for the analysis of antibiotics in water. J. Chromatogr. A1369, 43–51. 10.1016/j.chroma.2014.09.089

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 129

  LlorcaM.Rodríguez-MozazS.CouillerotO.PanigoniK.de GunzburgJ.BayerS.et al. (2015). Identification of new transformation products during enzymatic treatment of tetracycline and erythromycin antibiotics at laboratory scale by an on-line turbulent flow liquid-chromatography coupled to a high resolution mass spectrometer LTQ-Orbitrap. Chemosphere119, 90–98. 10.1016/j.chemosphere.2014.05.072

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 130

  LloretL.EibesG.Lú-ChauT. A.MoreiraM. T.FeijooG.LemaJ. M. (2010). Laccase-catalyzed degradation of anti-inflammatories and estrogens. Biochem. Eng. J.51, 124–131. 10.1016/j.bej.2010.06.005

  • CrossRef
  • Google Scholar

• 131

  LoiM.FanelliF.ZuccaP.LiuzziV. C.QuintieriL.CimmarustiM. T.et al. (2016). Aflatoxin B₁ and M₁ degradation by Lac2 from Pleurotus pulmonarius and redox mediators. Toxins8:E245. 10.3390/toxins8090245

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 132

  LuX.DingS. (2010). Effect of Cu²⁺, Mn²⁺ and aromatic compounds on the production of laccase isoforms by Coprinus comatus. Mycoscience51, 68–74. 10.1007/S10267-009-0002-6

  • CrossRef
  • Google Scholar

• 133

  LuY.WuG.LianL.GuoL.WangW.YangZ.et al. (2015). Cloning and expression analysis of Vvlcc3, a novel and functional laccase gene possibly involved in stipe elongation. Int. J. Mol. Sci.16, 28498–28509. 10.3390/ijms161226111

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 134

  MajeauJ. A.BrarS. K.TyagiR. D. (2010). Laccases for removal of recalcitrant and emerging pollutants. Bioresour. Technol.101, 2331–2350. 10.1016/j.biortech.2009.10.087

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 135

  MaqboolZ.HussainS.ImranM.MahmoodF.ShahzadT.AhmedZ.et al. (2016). Perspectives of using fungi as bioresource for bioremediation of pesticides in the environment: a critical review. Environ. Sci. Pollut. Res.23, 16904–16925. 10.1007/s11356-016-7003-8

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 136

  Marco-UrreaE.Pérez-TrujilloM.Cruz-MoratóC.CaminalG.VicentT. (2010a). White-rot fungus-mediated degradation of the analgesic ketoprofen and identification of intermediates by HPLC–DAD–MS and NMR. Chemosphere78, 474–481. 10.1016/j.chemosphere.2009.10.009

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 137

  Marco-UrreaE.Perez-TrujilloM.Cruz-MoratoC.CaminalG.VicentT. (2010b). Degradation of the drug sodium diclofenac by Trametes versicolor pellets and identification of some intermediates by NMR. J. Hazard. Mater.176, 836–842. 10.1016/j.jhazmat.2009.11.112

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 138

  Marco-UrreaE.Perez-TrujilloM.VicentT.CaminalG. (2009). Ability of white-rot fungi to remove selected pharmaceuticals and identification of degradation products of ibuprofen by Trametes versicolor. Chemosphere74, 765–772. 10.1016/j.chemosphere.2008.10.040

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 139

  MargotJ.Bennati-GranierC.MaillardJ.BlánquezP.BarryD. A.HolligerC. (2013a). Bacterial versus fungal laccase: potential for micropollutant degradation. AMB Express3:63. 10.1186/2191-0855-3-63

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 140

  MargotJ.CopinP.-J.von GuntenU.BarryD. A.HolligerC. (2015). Sulfamethoxazole and isoproturon degradation and detoxification by a laccase-mediator system: influence of treatment conditions and mechanistic aspects. Biochem. Eng. J.103, 47–59. 10.1016/j.bej.2015.06.008

  • CrossRef
  • Google Scholar

• 141

  MargotJ.MaillardJ.RossiL.BarryD. A.HolligerC. (2013b). Influence of treatment conditions on the oxidation of micropollutants by Trametes versicolor laccase. N. Biotechnol.30, 803–813. 10.1016/j.nbt.2013.06.004

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 142

  MartinkovaL.KotikM.MarkovaE.HomolkaL. (2016). Biodegradation of phenolic compounds by Basidiomycota and its phenol oxidases: a review. Chemosphere149, 373–382. 10.1016/j.chemosphere.2016.01.022

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 143

  MartinsL. O.DuraoP.BrissosV.LindleyP. F. (2015). Laccases of prokaryotic origin: enzymes at the interface of protein science and protein technology. Cell. Mol. Life Sci.72, 911–922. 10.1007/s00018-014-1822-x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 144

  MaryskovaM.ArdaoI.Garcia-GonzalezC. A.MartinovaL.RotkovaJ.SevcuA. (2016). Polyamide 6/chitosan nanofibers as support for the immobilization of Trametes versicolor laccase for the elimination of endocrine disrupting chemicals. Enzyme Microb. Technol.89, 31–38. 10.1016/j.enzmictec.2016.03.001

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 145

  MateD. M.AlcaldeM. (2015). Laccase engineering: from rational design to directed evolution. Biotechnol. Adv.33, 25–40. 10.1016/j.biotechadv.2014.12.007

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 146

  MateD. M.AlcaldeM. (2016). Laccase: a multi-purpose biocatalyst at the forefront of biotechnology. Microb. Biotechnol. [Epub ahead print]. 10.1111/1751-7915.12422

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 147

  MatuszewskaA.KarpM.JaszekM.JanuszG.Osinska-JaroszukM.SulejJ.et al. (2016). Laccase purified from Cerrena unicolor exerts antitumor activity against leukemic cells. Oncol. Lett.11, 2009–2018. 10.3892/ol.2016.4220

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 148

  MeloC. F.DezottiM.MarquesM. R. (2016). A comparison between the oxidation with laccase and horseradish peroxidase for triclosan conversion. Environ. Technol.37, 335–343. 10.1080/09593330.2015.1069897

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 149

  MichniewiczA.UllrichR.LedakowiczS.HofrichterM. (2006). The white-rot fungus Cerrena unicolor strain 137 produces two laccase isoforms with different physico-chemical and catalytic properties. Appl. Microbiol. Biotechnol.69, 682–688. 10.1007/s00253-005-0015-9

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 150

  MiglioreL.FioriM.SpadoniA.GalliE. (2012). Biodegradation of oxytetracycline by Pleurotus ostreatus mycelium: a mycoremediation technique. J. Hazard. Mater. 215–216, 227–232. 10.1016/j.jhazmat.2012.02.056

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 151

  MikolaschA.HildebrandtO.SchluterR.HammerE.WittS.LindequistU. (2016). Targeted synthesis of novel α-lactam antibiotics by laccase-catalyzed reaction of aromatic substrates selected by pre-testing for their antimicrobial and cytotoxic activity. Appl. Microbiol. Biotechnol.100, 4885–4899. 10.1007/s00253-016-7288-z

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 152

  MikolaschA.MandaK.SchluterR.LalkM.WittS.SeefeldtS.et al. (2012). Comparative analyses of laccase-catalyzed amination reactions for production of novel α-lactam antibiotics. Biotechnol. Appl. Biochem.59, 295–306. 10.1002/bab.1026

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 153

  Mir-TutusausJ. A.Masis-MoraM.CorcellasC.EljarratE.BarceloD.SarraM.et al. (2014). Degradation of selected agrochemicals by the white rot fungus Trametes versicolor. Sci. Total Environ. 500–501, 235–242. 10.1016/j.scitotenv.2014.08.116

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 154

  Mizerska-DudkaM.JaszekM.BlachowiczA.RejczakT. P.MatuszewskaA.Osinska-JaroszukM.et al. (2015). Fungus Cerrena unicolor as an effective source of new antiviral, immunomodulatory, and anticancer compounds. Int. J. Biol. Macromol.79, 459–468. 10.1016/j.ijbiomac.2015.05.015

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 155

  MogharabiM.FaramarziM. A. (2014). Laccase and laccase-mediated systems in the synthesis of organic compounds. Adv. Synth. Catal.356, 897–927. 10.1002/adsc.201300960

  • CrossRef
  • Google Scholar

• 156

  MorozovaO. V.ShumakovichG. P.ShleevS. V.YaropolovY. I. (2007). Laccase-mediator systems and their applications: a review. Appl. Biochem. Microbiol.43, 523–535. 10.1134/S0003683807050055

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 157

  MuraguchiH.KondohM.ItoY.YanagiS. O. (2011). Molecular breeding of a novel Coprinopsis cinerea strain possessing a heterologous laccase gene, lccK, driven by a constitutive promoter. Mycoscience52, 431–435. 10.1007/S10267-011-0122-7

  • CrossRef
  • Google Scholar

• 158

  MurugesanK.ChangY. Y.KimY. M.JeonJ. R.KimE. J.ChangY. S. (2010). Enhanced transformation of triclosan by laccase in the presence of redox mediators. Water Res.44, 298–308. 10.1016/j.watres.2009.09.058

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 159

  NairR. R.DemarcheP.AgathosS. N. (2013). Formulation and characterization of an immobilized laccase biocatalyst and its application to eliminate organic micropollutants in wastewater. N. Biotechnol.30, 814–823. 10.1016/j.nbt.2012.12.004

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 160

  NakadeK.NakagawaY.YanoA.KonnoN.SatoT.SakamotoY. (2013). Effective induction of pblac1 laccase by copper ion in Polyporus brumalis ibrc05015. Fungal Biol.117, 52–61. 10.1016/j.funbio.2012.11.005

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 161

  NguyenL. N.HaiF. I.DossetoA.RichardsonC.PriceW. E.NghiemL. D. (2016a). Continuous adsorption and biotransformation of micropollutants by granular activated carbon-bound laccase in a packed-bed enzyme reactor. Bioresour. Technol.210, 108–116. 10.1016/j.biortech.2016.01.014

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 162

  NguyenL. N.HaiF. I.KangJ.LeuschF. D. L.RoddickF.MagramS. F.et al. (2014a). Enhancement of trace organic contaminant degradation by crude enzyme extract from Trametes versicolor culture: effect of mediator type and concentration. J. Taiwan Inst. Chem. Eng.45, 1855–1862. 10.1016/j.jtice.2014.03.021

  • CrossRef
  • Google Scholar

• 163

  NguyenL. N.HaiF. I.PriceW. E.KangJ.LeuschF. D. L.RoddickF.et al. (2015). Degradation of a broad spectrum of trace organic contaminants by an enzymatic membrane reactor: complementary role of membrane retention and enzymatic degradation. Int. Biodeterior. Biodegradation99, 115–122. 10.1016/j.ibiod.2014.12.004

  • CrossRef
  • Google Scholar

• 164

  NguyenL. N.HaiF. I.PriceW. E.LeuschF. D.RoddickF.NgoH. H.et al. (2014b). The effects of mediator and granular activated carbon addition on degradation of trace organic contaminants by an enzymatic membrane reactor. Bioresour. Technol.167, 169–177. 10.1016/j.biortech.2014.05.125

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 165

  NguyenL. N.HaiF. I.PriceW. E.LeuschF. D. L.RoddickF.McAdamE. J.et al. (2014c). Continuous biotransformation of bisphenol A and diclofenac by laccase in an enzymatic membrane reactor. Int. Biodeterior. Biodegradation95, 25–32. 10.1016/j.ibiod.2014.05.017

  • CrossRef
  • Google Scholar

• 166

  NguyenL. N.HaiF. I.YangS.KangJ.LeuschF. D. L.RoddickF.et al. (2014d). Removal of pharmaceuticals, steroid hormones, phytoestrogens, UV-filters, industrial chemicals and pesticides by Trametes versicolor: role of biosorption and biodegradation. Int. Biodeterior. Biodegradation88, 169–175. 10.1016/j.ibiod.2013.12.017

  • CrossRef
  • Google Scholar

• 167

  NguyenL. N.van de MerweJ. P.HaiF. I.LeuschF. D.KangJ.PriceW. E.et al. (2016b). Laccase-syringaldehyde-mediated degradation of trace organic contaminants in an enzymatic membrane reactor: removal efficiency and effluent toxicity. Bioresour. Technol.200, 477–484. 10.1016/j.biortech.2015.10.054

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 168

  NiJ.TokudaG. (2013). Lignocellulose-degrading enzymes from termites and their symbiotic microbiota. Biotechnol. Adv.31, 838–850. 10.1016/j.biotechadv.2013.04.005

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 169

  NishiboriN.MasakiK.TsuchiokaH.FujiiT.IefujiH. (2013). Comparison of laccase production levels in Pichia pastoris and Cryptococcus sp. S-2. J. Biosci. Bioeng.115, 394–399. 10.1016/j.jbiosc.2012.10.025

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 170

  OlajuyigbeF. M.FatokunC. O. (2017). Biochemical characterization of an extremely stable pH-versatile laccase from Sporothrix carnis CPF-05. Int. J. Biol. Macromol.94, 535–543. 10.1016/j.ijbiomac.2016.10.037

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 171

  OnesiosK. M.YuJ. T.BouwerE. J. (2009). Biodegradation and removal of pharmaceuticals and personal care products in treatment systems: a review. Biodegradation20, 441–466. 10.1007/s10532-008-9237-8

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 172

  OsmaJ. F.Toca-HerreraJ. L.Rodríguez-CoutoS. (2010). Uses of laccases in the food industry. Enzyme Res.2010, 1–8. 10.4061/2010/918761

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 173

  Ostadhadi-DehkordiS.Tabatabaei-SameniM.ForootanfarH.KolahdouzS.Ghazi-KhansariM.FaramarziM. A. (2012). Degradation of some benzodiazepines by a laccase-mediated system in aqueous solution. Bioresour. Technol.125, 344–347. 10.1016/j.biortech.2012.09.039

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 174

  OttoB.BeuchelC.LiersC.ReisserW.HarmsH.SchlosserD. (2015). Laccase-like enzyme activities from chlorophycean green algae with potential for bioconversion of phenolic pollutants. FEMS Microbiol. Lett.362:fnv072. 10.1093/femsle/fnv072

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 175

  OultonR. L.KohnT.CwiertnyD. M. (2010). Pharmaceuticals and personal care products in effluent matrices: a survey of transformation and removal during wastewater treatment and implications for wastewater management. J. Environ. Monit.12, 1956–1978. 10.1039/c0em00068j

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 176

  PanK.ZhaoN.YinQ.ZhangT.XuX.FangW.et al. (2014). Induction of a laccase Lcc9 from Coprinopsis cinerea by fungal coculture and its application on indigo dye decolorization. Bioresour. Technol.162, 45–52. 10.1016/j.biortech.2014.03.116

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 177

  PardoI.CamareroS. (2015). Laccase engineering by rational and evolutionary design. Cell. Mol. Life Sci.72, 897–910. 10.1007/s00018-014-1824-8

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 178

  PezzellaC.GuarinoL.PiscitelliA. (2015). How to enjoy laccases. Cell. Mol. Life Sci.72, 923–940. 10.1007/s00018-014-1823-9

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 179

  PezzellaC.LetteraV.PiscitelliA.GiardinaP.SanniaG. (2013). Transcriptional analysis of Pleurotus ostreatus laccase genes. Appl. Microbiol. Biotechnol.97, 705–717. 10.1007/s00253-012-3980-9

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 180

  PiscitelliA.GiardinaP.LetteraV.PezzellaC.SanniaG.FaracoV. (2011). Induction and transcriptional regulation of laccases in fungi. Curr. Genomics12, 104–112. 10.2174/138920211795564331

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 181

  PiscitelliA.PezzellaC.GiardinaP.FaracoV.SanniaG. (2010). Heterologous laccase production and its role in industrial applications. Bioeng. Bugs1, 252. 10.4161/bbug.1.4.11438

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 182

  PogniR.BarattoM. C.SinicropiA.BasosiR. (2015). Spectroscopic and computational characterization of laccases and their substrate radical intermediates. Cell. Mol. Life Sci.72, 885–896. 10.1007/s00018-014-1825-7

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 183

  PollegioniL.ToninF.RosiniE. (2015). Lignin-degrading enzymes. FEBS J.282, 1190–1213. 10.1111/febs.13224

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 184

  PopaC.FavierL.DinicaR.SemranyS.DjelalH.AmraneA.et al. (2014). Potential of newly isolated wild Streptomyces strains as agents for the biodegradation of a recalcitrant pharmaceutical, carbamazepine. Environ. Technol.35, 3082–3091. 10.1080/09593330.2014.931468

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 185

  PostemskyP. D.BidegainM. A.Gonzalez-MatuteR.FiglasN. D.CubittoM. A. (2017). Pilot-scale bioconversion of rice and sunflower agro-residues into medicinal mushrooms and laccase enzymes through solid-state fermentation with Ganoderma lucidum. Bioresour. Technol.231, 85–93. 10.1016/j.biortech.2017.01.064

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 186

  RahmaniK.FaramarziM. A.MahviA. H.GholamiM.EsrafiliA.ForootanfarH.et al. (2015). Elimination and detoxification of sulfathiazole and sulfamethoxazole assisted by laccase immobilized on porous silica beads. Int. Biodeterior. Biodegradation97, 107–114. 10.1016/j.ibiod.2014.10.018

  • CrossRef
  • Google Scholar

• 187

  Ramírez-CavazosL. I.JunghannsC.Ornelas-SotoN.Cárdenas-ChávezD. L.Hernández-LunaC.DemarcheP.et al. (2014). Purification and characterization of two thermostable laccases from Pycnoporus sanguineus and potential role in degradation of endocrine disrupting chemicals. J. Mol. Catal. B Enzym.108, 32–42. 10.1016/j.molcatb.2014.06.006

  • CrossRef
  • Google Scholar

• 188

  RamosJ. A. T.BarendsS.VerhaertR. M.GraaffL. H. D. (2011). The Aspergillus niger multicopper oxidase family: analysis and overexpression of laccase-like encoding genes. Microb. Cell Fact.10:78. 10.1186/1475-2859-10-78

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 189

  RaoM. A.ScelzaR.AcevedoF.DiezM. C.GianfredaL. (2014). Enzymes as useful tools for environmental purposes. Chemosphere107, 145–162. 10.1016/j.chemosphere.2013.12.059

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 190

  ReissR.IhssenJ.RichterM.EichhornE.SchillingB.Thony-MeyerL. (2013). Laccase versus laccase-like multi-copper oxidase: a comparative study of similar enzymes with diverse substrate spectra. PLoS ONE8:e65633. 10.1371/journal.pone.0065633

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 191

  RissoV. A.GaviraJ. A.GaucherE. A.Sanchez-RuizJ. M. (2014). Phenotypic comparisons of consensus variants versus laboratory resurrections of Precambrian proteins. Proteins82, 887–896. 10.1002/prot.24575

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 192

  Rivera-HoyosC. M.Morales-ÁlvarezE. D.Poutou-PiñalesR. A.Pedroza-RodríguezA. M.RodrÍguez-VázquezR.Delgado-BoadaJ. M. (2013). Fungal laccases. Fungal Biol. Rev.27, 67–82. 10.1016/j.fbr.2013.07.001

  • CrossRef
  • Google Scholar

• 193

  RodgersC. J.BlanfordC. F.GiddensS. R.SkamniotiP.ArmstrongF. A.GurrS. J. (2010). Designer laccases: a vogue for high-potential fungal enzymes?Trends Biotechnol.28, 63–72. 10.1016/j.tibtech.2009.11.001

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 194

  Rodríguez-CoutoS. (2012). Laccases for denim bleaching: an eco-friendly alternative. Open Text. J.5, 1–7. 10.2174/1876520301205010001

  • CrossRef
  • Google Scholar

• 195

  Rodríguez-CoutoS.Toca-HerreraJ. L. (2007). Laccase production at reactor scale by filamentous fungi. Biotechnol. Adv.25, 558–569. 10.1016/j.biotechadv.2007.07.002

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 196

  Rodríguez-DelgadoM.Orona-NavarC.García-MoralesR.Hernandez-LunaC.ParraR.MahlknechtJ.et al. (2016). Biotransformation kinetics of pharmaceutical and industrial micropollutants in groundwaters by a laccase cocktail from Pycnoporus sanguineus CS43 fungi. Int. Biodeterior. Biodegradation108, 34–41. 10.1016/j.ibiod.2015.12.003

  • CrossRef
  • Google Scholar

• 197

  Rodriguez-RodriguezC. E.Garcia-GalanM. A.BlanquezP.Diaz-CruzM. S.BarceloD.CaminalG.et al. (2012). Continuous degradation of a mixture of sulfonamides by Trametes versicolor and identification of metabolites from sulfapyridine and sulfathiazole. J. Hazard. Mater. 213–214, 347–354. 10.1016/j.jhazmat.2012.02.008

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 198

  RogalskiJ.JanuszG. (2010). Purification of extracellular laccase from Cerrena unicolor. Prep. Biochem. Biotechnol.40, 242–255. 10.1080/10826068.2010.488967

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 199

  RühlM.MajcherczykA.KüesU. (2013). Lcc1 and Lcc5 are the main laccases secreted in liquid cultures of Coprinopsis cinerea strains. Antonie van Leeuwenhoek103, 1029–1039. 10.1007/s10482-013-9883-7

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 200

  SakamotoY.NakadeK.YoshidaK.NatsumeS.MiyazakiK.SatoS.et al. (2015). Grouping of multicopper oxidases in Lentinula edodes by sequence similarities and expression patterns. AMB Express5, 63. 10.1186/s13568-015-0151-2

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 201

  SanthanamN.VivancoJ. M.DeckerS. R.ReardonK. F. (2011). Expression of industrially relevant laccases: prokaryotic style. Trends Biotechnol.29, 480–489. 10.1016/j.tibtech.2011.04.005

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 202

  SathishkumarP.MythiliA.HadibarataT.JayakumarR.KanthimathiM. S.PalvannanT.et al. (2014). Laccase mediated diclofenac transformation and cytotoxicity assessment on mouse fibroblast 3T3-L1 preadipocytes. RSC Adv.4, 11689–11697. 10.1039/c3ra46014b

  • CrossRef
  • Google Scholar

• 203

  SchwarzJ.KnickerH.SchaumannG. E.Thiele-BruhnS. (2015). Enzymatic transformation and bonding of sulfonamide antibiotics to model humic substances. J. Chem.2015, 1–11. 10.1155/2015/829708

  • CrossRef
  • Google Scholar

• 204

  SenS. K.RautS.BandyopadhyayP.RautS. (2016). Fungal decolouration and degradation of azo dyes: a review. Fungal Biol. Rev.30, 112–133. 10.1016/j.fbr.2016.06.003

  • CrossRef
  • Google Scholar

• 205

  SenthivelanT.KanagarajJ.PandaR. C. (2016). Recent trends in fungal laccase for various industrial applications: an eco-friendly approach - a review. Biotechnol. Bioprocess Eng.21, 19–38. 10.1007/s12257-015-0278-7

  • CrossRef
  • Google Scholar

• 206

  SheldonR. A. (2011). Characteristic features and biotechnological applications of cross-linked enzyme aggregates (CLEAs). Appl. Microbiol. Biotechnol.92, 467–477. 10.1007/s00253-011-3554-2

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 207

  ShiH.PengJ.LiJ.MaoL.WangZ.GaoS. (2016). Laccase-catalyzed removal of the antimicrobials chlorophene and dichlorophen from water: reaction kinetics, pathway and toxicity evaluation. J. Hazard. Mater.317, 81–89. 10.1016/j.jhazmat.2016.05.064

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 208

  ShiL.MaF.HanY.ZhangX.YuH. (2014). Removal of sulfonamide antibiotics by oriented immobilized laccase on Fe₃O₄ nanoparticles with natural mediators. J. Hazard. Mater.279, 203–211. 10.1016/j.jhazmat.2014.06.070

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 209

  SiJ.CuiB.-K. (2013). Study of the physiological characteristics of the medicinal mushroom Trametes pubescens (higher basidiomycetes) during the laccase-producing process. Int. J. Med. Mushrooms15, 199–210. 10.1615/IntJMedMushr.v15.i2.90

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 210

  SiJ.PengF.CuiB. (2013). Purification, biochemical characterization and dye decolorization capacity of an alkali-resistant and metal-tolerant laccase from Trametes pubescens. Bioresour. Technol.128, 49–57. 10.1016/j.biortech.2012.10.085

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 211

  SinghD.RawatS.WaseemM.GuptaS.LynnA.NitinM.et al. (2016). Molecular modeling and simulation studies of recombinant laccase from Yersinia enterocolitica suggests significant role in the biotransformation of non-steroidal anti-inflammatory drugs. Biochem. Biophys. Res. Commun.469, 306–312. 10.1016/j.bbrc.2015.11.096

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 212

  SinghG.BhallaA.KaurP.CapalashN.SharmaP. (2011). Laccase from prokaryotes: a new source for an old enzyme. Rev. Environ. Sci. Biotechnol.10, 309–326. 10.1007/s11157-011-9257-4

  • CrossRef
  • Google Scholar

• 213

  SinghG.KaurK.PuriS.SharmaP. (2015). Critical factors affecting laccase-mediated biobleaching of pulp in paper industry. Appl. Microbiol. Biotechnol.99, 155–164. 10.1007/s00253-014-6219-0

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 214

  SinghR.SidhuS. S.ZhangH.HuangQ. (2015). Removal of sulfadimethoxine in soil mediated by extracellular oxidoreductases. Environ. Sci. Pollut. Res.22, 16868–16874. 10.1007/s11356-015-4893-9

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 215

  SinghR. L.SinghP. K.SinghR. P. (2015). Enzymatic decolorization and degradation of azo dyes – a review. Int. Biodeterior. Biodegradation104, 21–31. 10.1016/j.ibiod.2015.04.027

  • CrossRef
  • Google Scholar

• 216

  SinirliogluZ. A.SinirliogluD.AkbasF. (2013). Preparation and characterization of stable cross-linked enzyme aggregates of novel laccase enzyme from Shewanella putrefaciens and using malachite green decolorization. Bioresour. Technol.146, 807–811. 10.1016/j.biortech.2013.08.032

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 217

  SitarzA. K.MikkelsenJ. D.MeyerA. S. (2016). Structure, functionality and tuning up of laccases for lignocellulose and other industrial applications. Crit. Rev. Biotechnol.36, 70–86. 10.3109/07388551.2014.949617

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 218

  SjaardaC. P.AbubakerK. S.CastleA. J. (2015). Induction of lcc2 expression and activity by Agaricus bisporus provides defence against Trichoderma aggressivum toxic extracts. Microb. Biotechnol.8, 918–929. 10.1111/1751-7915.12277

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 219

  SoléM.MüllerI.PecynaM. J.FetzerI.HarmsH.SchlosserD. (2012). Differential regulation by organic compounds and heavy metals of multiple laccase genes in the aquatic hyphomycete Clavariopsis aquatica. Appl. Environ. Microbiol.78, 4732–4739. 10.1128/AEM.00635-12

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 220

  SongulashviliG.Jimenéz-TobónG. A.JaspersC.PenninckxM. J. (2012). Immobilized laccase of Cerrena unicolor for elimination of endocrine disruptor micropollutants. Fungal Biol.116, 883–889. 10.1016/j.funbio.2012.05.005

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 221

  SongulashviliG.SpindlerD.Jimenez-TobonG. A.JaspersC.KernsG.PenninckxM. J. (2015). Production of a high level of laccase by submerged fermentation at 120-L scale of Cerrena unicolor C-139 grown on wheat bran. C. R. Biol.338, 121–125. 10.1016/j.crvi.2014.12.001

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 222

  StrongP. J.ClausH. (2011). Laccase: a review of its past and its future in bioremediation. Crit. Rev. Environ. Sci. Technol.41, 373–434. 10.1080/10643380902945706

  • CrossRef
  • Google Scholar

• 223

  SudaT.HataT.KawaiS.OkamuraH.NishidaT. (2012). Treatment of tetracycline antibiotics by laccase in the presence of 1-hydroxybenzotriazole. Bioresour. Technol.103, 498–501. 10.1016/j.biortech.2011.10.041

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 224

  SuetomiT.SakamotoT.TokunagaY.KameyamaT.HondaY.KamitsujiH.et al. (2015). Effects of calmodulin on expression of lignin-modifying enzymes in Pleurotus ostreatus. Curr. Genet.61, 127–140. 10.1007/s00294-014-0460-z

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 225

  SunK.HuangQ.GaoY. (2016). Laccase-catalyzed oxidative coupling reaction of triclosan in aqueous solution. Water Air Soil Pollut.227, 358. 10.1007/s11270-016-3064-z

  • CrossRef
  • Google Scholar

• 226

  SunS. J.LiuJ. Z.HuK. H.ZhuH. X. (2011). The level of secreted laccase activity in the edible fungi and their growing cycles are closely related. Curr. Microbiol.62, 871–875. 10.1007/s00284-010-9794-z

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 227

  SunS.LiX.RuanL.ZhangL.HuK. (2014). A novel breeding strategy for new strains of Hypsizygus marmoreus and Grifola frondosa based on ligninolytic enzymes. World J. Microbiol. Biotechnol.30, 2005–2013. 10.1007/s11274-014-1624-1

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 228

  SutarR. S.RathodV. K. (2015). Ultrasound assisted Laccase catalyzed degradation of Ciprofloxacin hydrochloride. J. Ind. Eng. Chem.31, 276–282. 10.1016/j.jiec.2015.06.037

  • CrossRef
  • Google Scholar

• 229

  TahmasbiH.KhoshayandM. R.Bozorgi-KoushalshahiM.HeidaryM.Ghazi-KhansariM.FaramarziM. A. (2016). Biocatalytic conversion and detoxification of imipramine by the laccase-mediated system. Int. Biodeterior. Biodegradation108, 1–8. 10.1016/j.ibiod.2015.11.029

  • CrossRef
  • Google Scholar

• 230

  TalekarS.JoshiA.JoshiG.KamatP.HaripurkarR.KambaleS. (2013). Parameters in preparation and characterization of cross linked enzyme aggregates (CLEAs). RSC Adv.3, 12485–12511. 10.1039/c3ra40818c

  • CrossRef
  • Google Scholar

• 231

  Thiele-BruhnS. (2003). Pharmaceutical antibiotic compounds in soils – a review. J. Plant Nutr. Soil Sci.166, 145–167. 10.1002/jpln.200390023

  • CrossRef
  • Google Scholar

• 232

  TouaharI. E.HarouneL.BaS.BellengerJ.-P.CabanaH. (2014). Characterization of combined cross-linked enzyme aggregates from laccase, versatile peroxidase and glucose oxidase, and their utilization for the elimination of pharmaceuticals. Sci. Total Environ.481, 90–99. 10.1016/j.scitotenv.2014.01.132

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 233

  TranN. H.HuJ.UraseT. (2013). Removal of the insect repellent N,N-diethyl-m-toluamide (DEET) by laccase-mediated systems. Bioresour. Technol.147, 667–671. 10.1016/j.biortech.2013.08.113

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 234

  TranN. H.UraseT.KusakabeO. (2010). Biodegradation characteristics of pharmaceutical substances by whole fungal culture Trametes versicolor and its laccase. J. Water Environ. Technol.8, 125–140. 10.2965/jwet.2010.125

  • CrossRef
  • Google Scholar

• 235

  TurlapatiP. V.KimK. W.DavinL. B.LewisN. G. (2011). The laccase multigene family in Arabidopsis thaliana: towards addressing the mystery of their gene function(s). Planta233, 439–470. 10.1007/s00425-010-1298-3

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 236

  UpadhyayP.ShrivastavaR.AgrawalP. K. (2016). Bioprospecting and biotechnological applications of fungal laccase. 3 Biotech6, 15. 10.1007/s13205-015-0316-3

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 237

  ValderramaB.OliverP.Medrano-SotoA.Vazquez-DuhaltR. (2003). Evolutionary and structural diversity of fungal laccases. Antonie van Leeuwenhoek84, 289–299. 10.1023/A:1026070122451

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 238

  VasiliadouI. A.Sanchez-VazquezR.MolinaR.MartinezF.MeleroJ. A.BautistaL. F.et al. (2016). Biological removal of pharmaceutical compounds using white-rot fungi with concomitant FAME production of the residual biomass. J. Environ. Manage.180, 228–237. 10.1016/j.jenvman.2016.05.035

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 239

  VasinaD. V.MustafaevO. N.MoiseenkoK. V.SadovskayaN. S.GlazunovaO. A.TyurinA. A.et al. (2015). The Trametes hirsuta 072 laccase multigene family: genes identification and transcriptional analysis under copper ions induction. Biochimie116, 154–164. 10.1016/j.biochi.2015.07.015

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 240

  ViswanathB.RajeshB.JanardhanA.KumarA. P.NarasimhaG. (2014). Fungal laccases and their applications in bioremediation. Enzyme Res.2014, 1–21. 10.1155/2014/163242

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 241

  WangC.ZhangL.XuH. (2012). The effects of N⁺ ion implantation mutagenesis on the laccase production of Ceriporiopsis subvermispora. Biotechnol. Bioprocess Eng.17, 946–951. 10.1007/s12257-012-0125-z

  • CrossRef
  • Google Scholar

• 242

  WangF.GuoC.WeiT.ZhangT.LiuC.-Z. (2012). Heat shock treatment improves Trametes versicolor laccase production. Appl. Biochem. Biotechnol.168, 256–265. 10.1007/s12010-012-9769-6

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 243

  WangJ.WangS. (2016). Removal of pharmaceuticals and personal care products (PPCPs) from wastewater: a review. J. Environ. Manage.182, 620–640. 10.1016/j.jenvman.2016.07.049

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 244

  WangJ.FengJ.JiaW.ChangS.LiS.LiY. (2015). Lignin engineering through laccase modification: a promising field for energy plant improvement. Biotechnol. Biofuels8, 145. 10.1186/s13068-015-0331-y

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 245

  WangS. S.NingY. J.WangS. N.ZhangJ.ZhangG. Q.ChenQ. J. (2017). Purification, characterization, and cloning of an extracellular laccase with potent dye decolorizing ability from white rot fungus Cerrena unicolor GSM-01. Int. J. Biol. Macromol.95, 920–927. 10.1016/j.ijbiomac.2016.10.079

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 246

  WangW.LiuF.JiangY.WuG.GuoL.ChenR.et al. (2015). The multigene family of fungal laccases and their expression in the white rot basidiomycete Flammulina velutipes. Gene563, 142–149. 10.1016/j.gene.2015.03.020

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 247

  WeiF.HongY.LiuJ.YuanJ.FangW.PengH.et al. (2010). Gongronella sp. induces overproduction of laccase in Panus rudis. J. Basic Microbiol.50, 98–103. 10.1002/jobm.200900155

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 248

  WenX.JiaY.LiJ. (2009). Degradation of tetracycline and oxytetracycline by crude lignin peroxidase prepared from Phanerochaete chrysosporium – A white rot fungus. Chemosphere75, 1003–1007. 10.1016/j.chemosphere.2009.01.052

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 249

  WenX.JiaY.LiJ. (2010). Enzymatic degradation of tetracycline and oxytetracycline by crude manganese peroxidase prepared from Phanerochaete chrysosporium. J. Hazard. Mater.177, 924–928. 10.1016/j.jhazmat.2010.01.005

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 250

  WengS. S.KuK. L.LaiH. T. (2012). The implication of mediators for enhancement of laccase oxidation of sulfonamide antibiotics. Bioresour. Technol.113, 259–264. 10.1016/j.biortech.2011.12.111

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 251

  WengS. S.LiuS. M.LaiH. T. (2013). Application parameters of laccase-mediator systems for treatment of sulfonamide antibiotics. Bioresour. Technol.141, 152–159. 10.1016/j.biortech.2013.02.093

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 252

  WongD. W. (2009). Structure and action mechanism of ligninolytic enzymes. Appl. Biochem. Biotechnol.157, 174–209. 10.1007/s12010-008-8279-z

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 253

  WuL.ZhuG.ChenM.WangH.BaoD. (2013). The bioinformatic analyses and the gene expression induced by Cu²⁺ of 11 laccase homologous genes from Volvariella volvacea. Mycosystema33, 323–333. 10.13346/j.mycosystema.130231

  • CrossRef
  • Google Scholar

• 254

  XiaoY. Z.HongY. Z.LiJ. F.HangJ.TongP. G.FangW.et al. (2006). Cloning of novel laccase isozyme genes from Trametes sp. AH28-2 and analyses of their differential expression. Appl. Microbiol. Biotechnol.71, 493–501. 10.1007/s00253-005-0188-2

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 255

  XiaoY. Z.TuX. M.WangJ.ZhangM.ChengQ.ZengW. Y.et al. (2003). Purification, molecular characterization and reactivity with aromatic compounds of a laccase from basidiomycete Trametes sp. strain AH28-2. Appl. Microbiol. Biotechnol.60, 700–707. 10.1007/s00253-002-1169-3

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 256

  XuR.SiY.WuX.LiF.ZhangB. (2014). Triclosan removal by laccase immobilized on mesoporous nanofibers: strong adsorption and efficient degradation. Chem. Eng. J.255, 63–70. 10.1016/j.cej.2014.06.060

  • CrossRef
  • Google Scholar

• 257

  XuR.TangR.ZhouQ.LiF.ZhangB. (2015). Enhancement of catalytic activity of immobilized laccase for diclofenac biodegradation by carbon nanotubes. Chem. Eng. J.262, 88–95. 10.1016/j.cej.2014.09.072

  • CrossRef
  • Google Scholar

• 258

  XuX.FengL.HanZ.LuoS.WuA.XieJ. (2016). Selection of high laccase-producing Coriolopsis gallica strain T906: mutation breeding, strain characterization, and features of the extracellular laccases. J. Microbiol. Biotechnol.26, 1570–1578. 10.4014/jmb.1604.04011

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 259

  YadavM.YadavH. S. (2015). Applications of ligninolytic enzymes to pollutants, wastewater, dyes, soil, coal, paper and polymers. Environ. Chem. Lett.13, 309–318. 10.1007/s10311-015-0516-4

  • CrossRef
  • Google Scholar

• 260

  YangC. W.HsiaoW. C.ChangB. V. (2016). Biodegradation of sulfonamide antibiotics in sludge. Chemosphere150, 559–565. 10.1016/j.chemosphere.2016.02.064

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 261

  YangJ.LinY.YangX.NgT. B.YeX.LinJ. (2017). Degradation of tetracycline by immobilized laccase and the proposed transformation pathway. J. Hazard. Mater.322, 525–531. 10.1016/j.jhazmat.2016.10.019

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 262

  YangJ.WangG.NgT. B.LinJ.YeX. (2016a). Laccase production and differential transcription of laccase genes in Cerrena sp. in response to metal ions, aromatic compounds, and nutrients. Front. Microbiol.6:1558. 10.3389/fmicb.2015.01558

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 263

  YangJ.XuX.NgT. B.LinJ.YeX. (2016b). Laccase gene family in Cerrena sp. HYB07: sequences, heterologous expression and transcriptional analysis. Molecules21:1017. 10.3390/molecules21081017

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 264

  YangJ.XuX.YangX.YeX.LinJ. (2016c). Cross-linked enzyme aggregates of Cerrena laccase: preparation, enhanced NaCl tolerance and decolorization of Remazol Brilliant Blue Reactive. J. Taiwan Inst. Chem. Eng.65, 1–7. 10.1016/j.jtice.2016.04.025

  • CrossRef
  • Google Scholar

• 265

  YangJ.YangX.LinY.NgT. B.LinJ.YeX. (2015). Laccase-catalyzed decolorization of malachite green: performance optimization and degradation mechanism. PLoS ONE10:e0127714. 10.1371/journal.pone.0127714

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 266

  YangJ.YangX.YeX.LinJ. (2016d). Destaining of Coomassie Brilliant Blue R-250-stained polyacrylamide gels with fungal laccase. Anal. Biochem.493, 27–29. 10.1016/j.ab.2015.10.004

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 267

  YangJ.YangX.YeX.LinJ. (2016e). Optimal parameters for laccase-mediated destaining of Coomassie Brilliant Blue R-250-stained polyacrylamide gels. Data Brief7, 1–7. 10.1016/j.dib.2016.01.029

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 268

  YangS.HaiF. I.NghiemL. D.PriceW. E.RoddickF.MoreiraM. T.et al. (2013a). Understanding the factors controlling the removal of trace organic contaminants by white-rot fungi and their lignin modifying enzymes: a critical review. Bioresour. Technol.141, 97–108. 10.1016/j.biortech.2013.01.173

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 269

  YangS.HaiF. I.NghiemL. D.RoddickF.PriceW. E. (2013b). Removal of trace organic contaminants by nitrifying activated sludge and wholecell and crude enzyme extract of Trametes versicolor. Water Sci. Technol.67, 1216–1223. 10.2166/wst.2013.684

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 270

  YangY.FanF.ZhuoR.MaF.GongY.WanX.et al. (2012). Expression of the laccase gene from a white rot fungus in Pichia pastoris can enhance the resistance of this yeast to H₂O₂-mediated oxidative stress by stimulating the glutathione-based antioxidative system. Appl. Environ. Microbiol.78, 5845–5854. 10.1128/AEM.00218-12

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 271

  YangY.WeiF.ZhuoR.FanF.LiuH.ZhangC.et al. (2013). Enhancing the laccase production and laccase gene expression in the white-rot fungus Trametes velutina 5930 with great potential for biotechnological applications by different metal Ions and aromatic compounds. PLoS ONE8:e79307. 10.1371/journal.pone.0079307

  • CrossRef
  • Google Scholar

• 272

  Yousefi-AhmadipourA.Bozorgi-KoshalshahiM.MogharabiM.AminiM.Ghazi-KhansariM.FaramarziM. A. (2016). Laccase-catalyzed treatment of ketoconazole, identification of biotransformed metabolites, determination of kinetic parameters, and evaluation of micro-toxicity. J. Mol. Catal. B Enzym.133, 77–84. 10.1016/j.molcatb.2016.07.015

  • CrossRef
  • Google Scholar

• 273

  ZengJ.ZhuQ.WuY.LinX. (2016). Oxidation of polycyclic aromatic hydrocarbons using Bacillus subtilis CotA with high laccase activity and copper independence. Chemosphere148, 1–7. 10.1016/j.chemosphere.2016.01.019

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 274

  ZhangH.HongY. Z.XiaoY. Z.YuanJ.TuX. M.ZhangX. Q. (2006). Efficient production of laccases by Trametes sp. AH28-2 in cocultivation with a Trichoderma strain. Appl. Microbiol. Biotechnol.73, 89–94. 10.1007/s00253-006-0430-6

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 275

  ZhangJ.ChenH.ChenM.RenA.HuangJ.WangH.et al. (2015). Cloning and functional analysis of a laccase gene during fruiting body formation in Hypsizygus marmoreus. Microbiol. Res.179, 54–63. 10.1016/j.micres.2015.06.005

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 276

  ZhangY.GeißenS.-U. (2010). In vitro degradation of carbamazepine and diclofenac by crude lignin peroxidase. J. Hazard. Mater.176, 1089–1092. 10.1016/j.jhazmat.2009.10.133

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 277

  ZhengF.CuiB.-K.WuX.-J.MengG.LiuH.-X.SiJ. (2016). Immobilization of laccase onto chitosan beads to enhance its capability to degrade synthetic dyes. Int. Biodeterior. Biodegradation110, 69–78. 10.1016/j.ibiod.2016.03.004

  • CrossRef
  • Google Scholar