Abstract
Actinomycetota in the phylum of bacteria has been explored extensively as a source of antibiotics and secondary metabolites. In addition to acting as plant growth-promoting agents, they also possess the potential to control various plant pathogens; however, there are limited studies that report the facultative predatory ability of Actinomycetota spp. Furthermore, the mechanisms that underline predation are poorly understood. We assessed the diversity of strategies employed by predatory bacteria to attack and subsequently induce the cell lysing of their prey. We revisited the diversity and abundance of secondary metabolite molecules linked to the different predation strategies by bacteria species. We analyzed the pros and cons of the distinctive predation mechanisms and explored their potential for the development of new biocontrol agents. The facultative predatory behaviors diverge from group attack “wolfpack,” cell-to-cell proximity “epibiotic,” periplasmic penetration, and endobiotic invasion to degrade host-cellular content. The epibiotic represents the dominant facultative mode of predation, irrespective of the habitat origins. The wolfpack is the second-used approach among the Actinomycetota harboring predatory traits. The secondary molecules as chemical weapons engaged in the respective attacks were reviewed. We finally explored the use of predatory Actinomycetota as a new cost-effective and sustainable biocontrol agent against plant pathogens.
1. Introduction
Cellular tropism also referred to as “cellular predation,” is a regular interspecific antagonistic that occurs in diverse living habitats. It also defines an act of a predatory organism to kill and devour a prey organism for its nutritional requirements (Pérez et al., 2016). Predation behavior expands from primitive prokaryotic microbes to highly evolved mammals in the animal kingdom (Sinclair et al., 2003; Ripple and Beschta, 2004). Among the microorganisms, a family member of the virus, bacteria have developed predatory behaviors that are well investigated under in vivo and ex vivo conditions (Curds, 1982; Gonzalez et al., 1990; Parry, 2004). Myxobacteria and Bdellovibrio are δ-Proteobacteria in the bacteria phyla with well-known bacteriophagic nature (Stolp and Starr, 1963; Casida, 1982; Berleman et al., 2006; Martins et al., 2022). Through predation attitude, Myxobacteria, and Bdellovibrio contribute to community structuring and carbon recycling in the soil food web systems and play an important ecosystem function are well-known keystone taxa (Bratanis et al., 2020; Cavallo et al., 2021; Mookherjee and Jurkevitch, 2022; Ogundero et al., 2022; Whitworth, 2022; Wu et al., 2022). Thus, bacteria species in the actinomycetes species are gram-positive and mostly studied for secondary metabolites production and were recently discovered to exert a facultative predatory role (Zeph and Casida, 1986; Hoshino et al., 2015; Ait Barka et al., 2016; Katz and Baltz, 2016; Baltz, 2019; Ouchari et al., 2019; Ibrahimi et al., 2020; Korichi et al., 2021). Studies deciphering or investigating the facultative predation role of Actinomycetota are gaining growing research attention (Kumbhar et al., 2014; Ibrahimi et al., 2019, 2020; Baig et al., 2021) owing to their lifestyles adjustment to adapt to complex limited resources (Ibrahimi et al., 2019, 2020) and importantly potential application to design bio-pesticides molecules/products alternatives to heavy toxic pesticides inorganic molecules (Palaniyandi et al., 2013). The approach is driven by increasing consumer demands for safe, healthy, and organically produced foods globally (Alvarez et al., 2017, Sathya et al., 2017; AbdElgawad et al., 2020). However, in the context of Actinomycetota species, the mechanisms that underline opportunistic predation behaviors are under-investigated (Ibrahimi et al., 2019, 2020).
Predation is a bacteria co-evolutional trait in the Actinomycetota, owing to adjustments in lifestyles among the species, possible geographical local adaptations, and habitat change (Jousset, 2012; Ibrahimi et al., 2020). For a long time, Actinomycetota were only viewed as competitive, rather than predatory organisms (Kumbhar and Watve, 2013; Kumbhar et al., 2014; Ibrahimi et al., 2020; Pérez et al., 2020). As a consequence, despite their widespread ecological importance in the environment, there are very few investigations on Actinomycetota predation (Bentley et al., 2002; Mawang et al., 2021; Boubekri et al., 2022; Santos-Aberturas and Vior, 2022). The first evidence of the Actinomycetota opportunistic predation behaviors is described in the Streptomyces and Agromyces genera (Waksman and Woodruff, 1941; Casida, 1980). The author examined the utilization of Micrococcus luteus as prey by Streptomyces species. As versatile-opportunistic Actinomycetota, Streptomyces is also a non-obligate epibiotic predator of various microorganisms, specifically, Staphylococcus aureus, Escherichia coli, Bacillus sp., Pseudomonas aeruginosa, and Klebsiella sp. (Kumbhar et al., 2014). In addition, It was reported in the literature that under in vivo conditions, Streptomyces isolates exhibited the predatory ability on various prey bacteria cells (Gram+, Gram−) and multidrug-resistant strains (Ibrahimi et al., 2020). The latest supportive evidence of good predatory behavior by Streptomyces against various types of prey is reported by Baig et al. (2021). However, studies examining the mechanisms that underline predator–prey relationships and the diversity or identity of small signal molecules are lacking (Ibrahimi et al., 2020).
Increasing plant diseases due to pathogenic microbes represent an important global constraint for agricultural production and economic losses (Collinge and Sarrocco, 2022). Current interventions are toward the use of synthetic heavy toxic molecules pesticides for crop protection that negatively poses acute risks to human health and the environment (Rani et al., 2021). It is imperative to find alternative solutions for a sustainable crop yield (Collinge and Sarrocco, 2022). The increasing knowledge and understanding of plant–microbe interactions, in particular the predatory capability of Actinomycetota to design as a biopesticide product to combat plant-associated pathogenic microbes (Shivlata and Satyanarayana, 2017). The objective of the present study was to:
- a)
critically review the facultative predatory mechanisms of bacteria and Actinomycetota;
- b)
discuss the various small molecules synthesized from bacteria and Actinomycetota species during their opportunistic predatory lifestyle stage; and
- c)
explore the potential beneficial use of Actinomycetota synthesized small molecules during the predation stages in the development of biocontrol agents for plant disease suppression and protection.
2. Mechanisms of predation by bacteria and Actinomycetota species
Predation by bacteria has traditionally attracted lower attention than their multicellular development or their production of bioactive compounds (Furness et al., 2020). In recent years, many aspects of bacterial predation are starting to be explored through research (Table 1). Since the purpose of a predatory bacteria is to kill and digest its prey, it remains necessary to understand the hunting and killing behavior of the predator. Most authors propose to classify bacterial hunting strategies into four general categories: epibiotic, group attack, or wolfpack, periplasmic penetration, and endobiotic predation or direct invasion (Martin, 2002; Jurkevitch, 2007; Berleman and Kirby, 2009; Pasternak et al., 2014; Pérez et al., 2016). Epibiotic is a tactic that requires close cell-to-cell proximity (Shi et al., 1993). When the predation is extracellular, the predator attached to the prey from outside does not invade either the periplasm or the cytoplasm of the prey, degrades and assimilates host molecules through specialized structures, but without penetrating the prey (Martin, 2002; Pérez et al., 2016), consuming it from the exterior before dividing into the daughter cells via binary division (Koval et al., 2013; Figure 1). Ensifer adhaerens (Druga et al., 2011), Myxococcus xanthus (Nair, 2016; Thiery and Kaimer, 2020), and Streptomyces (Casida, 1988; Ibrahimi et al., 2020) are some examples of epibiotic strategy. The cell-to-cell contact between the epibiotic predator and its prey is crucial for the transfer of compounds between their cells (Castelle and Banfield, 2018; Yakimov et al., 2022). As a consequence of the limited literature on culture-based investigations, our current state of understanding of the behavior of epibiotic lifestyles is relatively poor (Bor et al., 2020; Batinovic et al., 2021; Yakimov et al., 2022). However, Cross et al. (2019) suggested that to clearly demonstrate cell-to-cell contact, conditions that could enhance predator abundance to the degree that allows detailed microscopic characterization must be evaluated.
TABLE 1
| Group | Known habitat | Prey Gram+ Gram− | Predatory strategy | Antibiotic production | Predation type | References | |
| α-Proteobacteria | |||||||
| Ensifer adhaerens | Soil | + | Epibiotic | Yes | Facultative | Casida, 1982; Germida and Casida, 1983; Druga et al., 2011 | |
| Micavibrio sp. | Soil | + | Epibiotic | No | Obligate | Davidov et al., 2006; Kadouri et al., 2007 | |
| β-Proteobacteria | |||||||
| Cupriavidus necator | Soil | + | + | Epibiotic | Yes | Facultative | Makkar and Casida, 1987; Kreutzer et al., 2012 |
| Aristabacter necator | Soil | + | + | Epibiotic | Yes | Facultative | Casida, 1992; Cain et al., 2003 |
| γ-Proteobacteria | |||||||
| Lysobacter sp. | Soil | + | + | Wolfpack | Yes | Facultative | Li et al., 2008; Seccareccia et al., 2015 |
| Stenotrophomonas maltophilia | Soil | + | + | Epibiotic | Yes | Facultative | Ryan et al., 2009; Kumbhar and Watve, 2013 |
| Pseudomonas | Soil | + | + | Epibiotic | Yes | Facultative | Casida, 1992 |
| δ-Proteobacteria | |||||||
| Bdellovibrionales (d-BALOs) Bdellovibrionaceae Bdellovibrio spp. | Soil, freshwater, sewage, marine sediments perialpine lakes, marine waters, river, estuaries, terrestrial plants, gut of animals and humans | + | Periplasmic Epibiotic | Not characterized | Obligate | Cotter and Thomashow, 1992; Fratamico and Cooke, 1996; Jurkevitch and Ramati, 2000; Jurkevitch et al., 2000; Schwudke et al., 2001; Davidov et al., 2006; Jurkevitch, 2007; Sockett, 2009; Hobley et al., 2012; Ezzedine et al., 2020 | |
| Bacteriovoracaceae Bacteriovorax sp. Peredibacter sp. | Periplasmic | No | |||||
| Myxobacteria | Cell contact, Soil, dung, bark, Sediments | + | + | Wolfpack | Yes | Facultative | Reichenbach and Höfle, 1993; McBride and Zusman, 1996 |
| Chloroflexi | |||||||
| Herpetosiphon sp. | Cell contact freshwater | + | + | Wolfpack | Yes | Facultative | Quinn and Skerman, 1980; Trick and Lingens, 1984; Nett et al., 2006; Kiss et al., 2011 |
| Bacteroidetes | |||||||
| Saprospira sp. | Coastal sediment Sea water | + | + | Wolfpack Epibiotic | Yes | Facultative | Furusawa et al., 2003; Saw et al., 2012 |
| Flavobacterium | Marine Fresh Water | + | + | Yes | Facultative | McBride et al., 2009; Banning, 2010 | |
| Actinomycetota | |||||||
| Streptomyces | Soil, marine water, marine sponge Marine water | + | + | Epibiotic Wolfpack Epibiotic | Yes | Facultative | Waksman and Woodruff, 1941; Casida, 1988; Kumbhar et al., 2014; Ibrahimi et al., 2020; Baig et al., 2021 |
| Agromyces ramosus | Soil | + | Yes | Facultative | Casida, 1983; Arcamone et al., 2000; Chernyakovskaya et al., 2004 | ||
| Brevibacterium, Glutamicibacter, Micromonospora, Nocardiopsis, Rhodococcus Rothia | Marine sponge | + | Epibiotic | Yes | Facultative | Baig et al., 2021 | |
| Bacillales | |||||||
| Bacillus | Soil | + | Epibiotic | Yes | Facultative | Gumbo et al., 2010 | |
| Paenibacillus | Soil Water Rhizosphere Veg. matter | + | Epibiotic | Yes | Facultative | Raza et al., 2008; Be’Er et al., 2009 | |
Predatory bacteria and their biological activity.
FIGURE 1
The second strategy is wolfpack or group attack or group predation, predatory bacteria in this kind of predation work as a group (Marshall and Whitworth, 2019), they are assumed to hunt collectively to attack prey (Figure 1). They assemble and collectively secrete a diversity of diffusible compounds like hydrolytic enzymes and extracellular antibiotics that degrade and kill nearby bacteria. Wolfpack strategy lyse prey cells from the exterior through concerted action (Martin, 2002). Furthermore, the aim of the process of lysis is to produce small molecules that are easily assimilated by the predator (Xiao et al., 2011). Moreover, higher predatory cell densities suggest higher diffusible compounds (Keane and Berleman, 2016). The most important property of wolfpack is the lysed prey will be consumed by the predatory bacteria secreting and non-secreting (Mendes-Soares and Velicer, 2013). Lysobacter sp. (Hashizume et al., 2004; Li et al., 2008), Myxobacteria (McBride and Zusman, 1996; Thiery and Kaimer, 2020), and Herpetosiphon sp. (Nett et al., 2006) are examples of predatory bacteria using this strategy.
The third approach is when cells enter the prey periplasm (Figure 1). The predator invades and develops in the periplasm of gram-negative bacteria (Hobot et al., 1984; Ferguson, 1990; Ferguson et al., 1992). Predator produces hydrolytic enzymes that promote penetration and damage the prey cell wall (Lerner et al., 2012). In parallel, the infected prey is destroyed once respiration comes to a halt and the outer membrane is damaged (Thomashow and Rittenberg, 1978). The invading predator attaches to the prey’s cytoplasmic membrane and initiates growth using the cytoplasm of the prey as a nutrient supply. The predator grows like a polynucleotide filament, the length of which is dependent on the prey size (Kessel and Shilo, 1976). In the end, filaments septate into individual attack-phase cells that grow a flagellum, induce the formation of pores in the cell wall and burst into the external medium to engage in another cycle (Fenton et al., 2010). Therefore, the predator kills the prey by ingesting its cytoplasm. Bdellovibrionales (Jurkevitch and Davidov, 2006), Bdellovibrio bacteriovorus, Bacteriovorax marinus, Bacteriolyticum stolpii, and Peredibacter starrii, use periplasmic predation (Sockett and Lambert, 2004; Pasternak et al., 2014). However, the mechanism used by predators to release their intracellular contents to achieve their original cell cycle is poorly described (Laloux, 2020).
Moreover, some predatory bacteria can utilize more than one hunting strategy, like Bdellovibrio, which employs the periplasmic and epibiotic strategy; also, Myxobacteria can use both epibiotic and wolfpack strategies.
The last category of predation includes all predators that penetrate the host cytoplasm (Figure 1). This approach is also known as the invasion of cytoplasm or diacytotic strategy (Moulder, 1985). After the penetration, the predator grows and divides inside the cytoplasm. Daptobacter is the only bacteria that employ this strategy (Guerrero et al., 1986), but no other study has been reported about this group. Among predatory Actinomycetota, a few investigations have highlighted strategies used in predation because they have not received the level of attention of competitors (Ibrahimi, 2020). Pérez et al. (2016) suggest that bacteria secreting secondary metabolites, including Actinomycetota, can attack their prey in groups, which is supported by the fact that they are social prokaryotes that form and develop in multicellular structures. Correspondingly, Kumbhar and Watve (2013) reported that antibiotic producers such as Actinomycetota are unable to use an endobiotic strategy and direct contact with the prey is not required. Kumbhar et al. (2014) showed that Actinomycetota are non-obligate epibiotic predators of diverse prey such as S. aureus, E. coli, Bacillus spp., Pseudomonas aeruginosa, and Klebsiella spp. Recently, a study by Zeng et al. (2021) demonstrated that Streptomyces globisporus, a predatory Actinomycetota, preyed on Microcystis through an epibiotic mode of predation. Overall, among the phylum Actinomycetota, only two genera, Agromyces and Streptomyces, are known to have an epibiotic predatory behavior against other bacterial species (Casida, 1983; Arcamone et al., 2000; Ibrahimi et al., 2020). All this information allows us to believe that the predatory Actinomycetota can hunt their prey through wolfpack and epibiotic strategies. Therefore, our understanding of Actinomycetota predation is still very fragmentary, including gaps in their mechanisms of predation. Understanding these mechanisms by Actinomycetota species is required for better knowledge and understanding of their effect on prey structure to develop a new strategy to control plant disease and multidrug-resistant pathogens.
3. Identity and diversity of small molecules produced from bacteria and Actinomycetota during predation lifestyles
Predatory bacteria represent a diversified collection of prokaryotic organisms that have the ability to consume other bacteria (Jurkevitch, 2007). While some of these bacteria act as solitary hunters, others are known to hunt in groups in a wide mixture before they attack their prey (Martin, 2002). This predatory strategy generally implicates the production of lytic enzymes and small bioactive compounds as predatory weapons (Rosenberg and Varon, 1984; Reichenbach and Höfle, 1993; Berleman and Kirby, 2009), while genome sequencing programs of these microorganisms have revealed the presence of very broad and varied secondary metabolites (Kiss et al., 2011). Therefore, extraction and purification of antimicrobial molecules from predatory bacteria have yielded the discovery of numerous novel molecules, as illustrated by jahnellamides (Plaza et al., 2013), salimyxins (Felder et al., 2013), cystomanamides (Etzbach et al., 2014), and precorallopyronin (Schäberle et al., 2015). It is confirmed by Xiao et al. (2011) that this variety of secondary metabolites is supposed to be involved in the death of the prey. It has been found that a defect in the production of these substances significantly affects predatory activity. In this section, all research relative to the results of chemical studies of compounds produced by predatory bacteria will be reviewed and critically analyzed in Table 2.
TABLE 2
| Predatory Bacteria | Product | Chemical Formula | Biological activity | References |
| Aristabacter necator | Banegasine | C11H12N2O2 | Potentiate the antimicrobial activity of pyrrolnitrin | Cain et al., 2003 |
| Pyrrolnitrin | C10H6Cl2N2O2 | Anti-fungal, anti-bacterial | ||
| Maculosin | C14H16N2O3 | Potentiate the antimicrobial activity of pyrrolnitrin | ||
| Herpetosiphon sp. | (+)-O-methylkolavelool | C20H34O | Anti-bacterial | Nakano et al., 2015 |
| Auriculamide | C17H24ClNO4 | Antibiotic properties are still open | Schieferdecker et al., 2015 | |
| Siphonazole | C25H25N3O6 | Not reported | Nett et al., 2006 | |
| M. xanthus DK1622 | Myxalamid B | C25H40NO3 | Yeasts and Gram-positive bacteria | Gerth et al., 1983 |
| Myxochelin A | C20H25N2O7 | Anti-bacterial and antitumoral activity | Kunze et al., 1989; Miyanaga et al., 2006; Krug et al., 2008 | |
| Myxovirescin A1 | C34H60NO8 | Bactericidal | Gerth et al., 1982; Xiao et al., 2012 | |
| Myxochromide A3 | C45H64N7O9 | Not reported | Korp et al., 2016 | |
| DKxanthene-534 | C29H34N4O6 | Antioxidative activity | Meiser et al., 2006; Wenzel and Müller, 2009 | |
| Myxoprincomide | C45H76N10O16 | Not reported | Cortina et al., 2012 | |
| Myxococcus fulvus Mxf50 | Myxopyronins A | C23H31NO6 | Anti-bacterial activity | Kohl et al., 1983 |
| Myxopyronins B | C24H33NO6 | |||
| Streptomyces althioticus Myxococcus Virescens M. xanthus Cystobacter fuscus | Althiomycin | C16H17N5O6S2 | Anti-bacterial activity | Fujimoto et al., 1970; Kunze et al., 1982 |
| Myxobacterium | Gulmirecin B | C22H34O9 | Anti-bacterial activity | Schieferdecker et al., 2014 |
| Myxobacterium Pyxidicoccus fallax HKI 727 | Gulmirecin A | C27H42O1 | Anti-bacterial activity | Schieferdecker et al., 2014 |
| Cystobacter sp. | Cystobactamids 919-2 | C25H29N3O7 | Anti-bacterial activity | Baumann et al., 2014 |
| Cystobactamids 919-1 | C46H45N7O14 | Anti-bacterial activity | Baumann et al., 2014 | |
| Corallococcus coralloides | Precorallopyronin A | C29H39NO7 | Not reported | Korp et al., 2016 |
| Corallopyronins A | C30H41NO7 | Block specifically eubacterial RNA polymerase | Irschik et al., 1985 | |
| Corallopyronins C | C30H41NO7 | |||
| Corallopyronins B | C31H43NO7 | |||
| Lysobacter spp. | Lysobactin | C58H97N15O17 | Anti-bacterial activity | O’Sullivan et al., 1988 |
| Myxobacterium Enhygromyxa salina | Salimyxin A | C21H30O | Anti-bacterial activity | Felder et al., 2013 |
| Salimyxin B | C21H32O |
Secondary metabolites from different predatory bacteria and their biological activity.
Traditionally, Actinomycetota species are renowned for their excellent potential to produce secondary metabolites and antibiotics compounds (Hoshino et al., 2015; Ait Barka et al., 2016; Ouchari et al., 2019; Ibrahimi et al., 2020; Korichi et al., 2021). These molecules are produced to antagonize the growth of surrounding microbes (Ortiz-Ortiz et al., 2013). To date, up to 33 new secondary metabolites have been successfully isolated from 12 Actinomycetota through the co-culture (Hoshino et al., 2019). With their novel roles as predatory microbes, the diversity and identity of molecules produced during predation strategies should be considered an untapped source of biomolecules. A further co-culturing of predator and prey monitored for 15 days induced an increase in the total amount of methylated fatty acids biomarker of the predatory Actinomycetota responsible for the predation process (Ibrahimi et al., 2019). Therefore, secondary metabolites engaged in the facultative predation and antagonistic mechanism are likely to differ, from the Actinomycetota strain, the origin of habitat, or the ecology of isolated strains (McBride and Zusman, 1996; Jurkevitch, 2007; Octaviana, 2021).
Predatory Actinomycetota are mostly isolated from marine and soil environments (Kumbhar et al., 2014; Ibrahimi et al., 2020; Baig et al., 2021). They exhibit a wide range of predatory activities against diverse bacteria (Kumbhar et al., 2014; Ibrahimi et al., 2020; Baig et al., 2021). This is explained by the bioactive compound that they produce, which possess a range of antimicrobial activities. These molecules are used as a weapon by predatory Actinomycetota to kill their prey (Kumbhar and Watve, 2013). Recently, Baig et al. (2021) demonstrated a strong correlation between predation and enzyme inhibition, particularly trypsin and chymotrypsin inhibition, in which predatory Actinomycetota were found to release more enzymes in the presence of prey. On this basis, it has become apparent that Actinomycetota can exhibit the great potential to produce antibiotics and enzymes during predation. Also, it should be noted that, to date, no compounds produced by predatory Actinomycetota during predation behavior have been elucidated. Therefore, it will be interesting to conduct further studies to isolate new predatory Actinomycetota as well as the extraction and identification of their molecules involved in predation lifestyle.
4. Predatory Actinomycetota as an eco-friendly and promising tool in agricultural and environmental sustainability
4.1. Plant pathogens
Recent years have been marked by an expanding array of virulent infectious diseases caused by pests which are increasingly recognized as presenting a worldwide threat to food security (Olsen et al., 2011; Bosso et al., 2015; Hartmann, 2022). In addition, the extensive use of agrochemicals molecules has led to the development of bacterial resistance, causing significant risks to the environment and human health (Ebele Mbachu et al., 2022). Consequently, providing food for the world’s population without disrupting the environmental balance is becoming eminent (Pandit et al., 2022). It is highly recommended to provide sustainable solutions for agriculture (Jamiołkowska, 2020). Microbes are an alternative to agrochemical molecules like synthetic pesticides for controlling plant pathogens (Elnahal et al., 2022). Different microorganisms are used as biocontrol agents, such as bacteria, fungi, and Actinomycetota (Table 3). Direct antagonism and predation are the possible modes of action of biocontrol agents to eliminate plant parasites (Ebele Mbachu et al., 2022).
TABLE 3
| Predatory bacteria | Pathogen | Application | References |
| Bacillus | Bacteria, fungi and oomycetes | Biocontrol against phytopathogens, including bacteria, fungi and oomycetes | Ongena and Jacques, 2008 |
| Fusarium fungi | Biocontrol agent of Fusarium head blight of wheat | Schisler et al., 2002 | |
| Phytophthora species such as P. capsica | Biocontrol agent for P. capsici pathogenic fungi | Douillet, 2003 | |
| Bacteriovorax spp. | Vibrio vulnificus and Vibrio parahaemolyticus | Reduced Vibrio sp. populations | Richards et al., 2012, 2013 |
| Bdellovibrio bacteriovorus | Pseudomonas aeruginosa and Staphylococcus aureus | Reduced S. aureus (periplasmic on Gram-negative and epibiotic on Gram-positive). | Iebba et al., 2014 |
| Staphylococcus aureus | Reduced biofilm formation | Monnappa et al., 2014 | |
| Multidrug resistant Gram-negative bacteria | Reduced biofilm formation | Kadouri et al., 2013 | |
| Gram-negative foodborne pathogens and spoilage bacteria | Lysed foodborne and spoilage bacteria | Fratamico and Whiting, 1995 | |
| Salmonella enterica Klebsiella pneumoniae Escherichia coli Enterobacter | Biocontrol agent to treat urban wastewater treatment | Jafarian et al., 2020 | |
| Microbial biomass in sludge | Alteration of the microbial community composition of activated sludge flocs and granules | Feng et al., 2017 | |
| Bdellovibrio bacteriovorus Lysobacter enzymogenes | Pseudomonas tolaasii | Reduced bacterial cells in vitro and blotch severity on pilei of mushroom at post-harvest | Saxon et al., 2014 |
| Shrimp pathogens V. cholerae | Biocontrol agent in freshwater farming industry as a biological control | Cao et al., 2015, 2019 | |
| Alcaligenes, campylobacter, Erwinia, Escherichia, Helicobacter, Pseudomonas, Legionella, and Shigella | Biocontrol agent | Markelova, 2010 | |
| Escherichia coli | Lyse gram-negative foodborne pathogenic and spoilage bacteria Novel antibody-modulating tools | Fratamico and Whiting, 1995; Bratanis et al., 2017; Bratanis and Lood, 2019 | |
| Bipolaris sorokiniana | Role in fungal plant disease control | Li et al., 2008 | |
| Myxobacteria | Cylindrocarpon spp., Fusarium oxysporum. sp. apii, Phytophthora capsici, Pythium ultimum, Rhizoctonia spp., Sclerotinia minor… | Plant pathogenic fungi | Bull et al., 2002 |
| Pseudomonas fluorescens | Tobacco necrosis virus | Biocontrol agent against phytopathogens | Maurhofer et al., 1998 |
| Micavibrio aeruginosavorus and B. bacteriovorus | Gram-negative bacteria: Pseudomonas aeruginosa and Escherichia coli | Biocontrol agent against phytogenic bacteria | Dashiff et al., 2011 |
| Streptomyces griseoflavus EMM111 Streptomyces coelicoflavus EMM112 Streptomyces mutabilis EMM183 Streptomyces champavatii EMM184 | Micrococcus luteus, Staphylococcus aureus (native and methicillin-resistant) Escherichia coli (native and ampicillin-resistant) | Biocontrol agent against multidrug-resistant bacteria | Ibrahimi et al., 2019, 2020 |
| Brevibacterium, Glutamicibacter, Micromonospora, Nocardiopsis, Rhodococcus and Rothia | Acetobacter pasteurianus Alcaligenes fecalis Bacillus subtilis Enterobacter fecalis, Escherichia coli Klebsiella pneumoniae Micrococcus luteus Mycobacterium smegmatis Proteus vulgaris Pseudomonas aeruginosa Salinicoccus roseus Salmonella enterica Serratia marcescens Staphylococcus aureus | Biocontrol agent against pathogenic bacteria | Baig et al., 2021 |
Predatory bacteria application.
Predatory bacteria can be used as alternative applications in biological control (Olanya and Lakshman, 2015; Swain et al., 2017). Most of the Bacillus strains can control the plant pathogen as Fusarium fungi (Ongena and Jacques, 2008). Bdellovibrio also attacks a large variety of different plant pathogens (Baer et al., 2000; Jurkevitch et al., 2000; Dwidar et al., 2012). In addition, a very promising result in the control by Bdellovibrio of Pseudomonas glycinea blight of soybean was demonstrated by Scherff (1973). Recently, Ye et al. (2020) demonstrated the use of the Myxobacterium Corallococcus coralloides to control cucumber Fusarium wilt by migrating to the plant root and regulating the soil microbial community.
In the case of Actinomycetota, several investigations showed their successful ability to function as biocontrol agents against plant pathogens (Goudjal et al., 2014; Braga et al., 2016; Ebrahimi-Zarandi et al., 2022). The co-cultivation of Actinomycetota with other microorganisms generates several new secondary metabolites, which are not present during pure culture conditions (Scherlach and Hertweck, 2009; Sung et al., 2017; Wakefield et al., 2017; Shin et al., 2018; Vikeli et al., 2019; Yu M. et al., 2019). Indeed, the production of secondary metabolites in co-culture is enhanced by competitive or antagonistic interactions (Ibrahimi et al., 2020). For example, the co-cultivation of the Streptomyces coelicolor with the agricultural pathogen Aspergillus niger has activated the actinorhodin silent pathway in Actinomycetota (Wu et al., 2015).
Prior research suggests that Actinomycetota in co-culture can inhibit pathogens’ growth, decrease, and degrade toxins. For example, a recent investigation demonstrated that coculturing Streptomyces roseolus with the phytopathogen Aspergillus flavus could reduce the contamination generated by the mycotoxin aflatoxin B1, which is produced by A. flavus (Caceres et al., 2018). In addition, several Streptomyces strains showed the ability to inhibit Aspergillus flavus growth and decrease and degrade mycotoxin (Verheecke et al., 2015; Campos-Avelar et al., 2021). Another field that seems promising for the use of Actinomycetota in agriculture is their function as eco-friendly biofertilizers since they are involved in nutrient management, soil quality, decomposing of organic matter, enhancing plant growth promoting, recycling organic residues, and activating plant immune responses (Shivlata and Satyanarayana, 2017; Boubekri et al., 2022; Ebrahimi-Zarandi et al., 2022).
Using predatory Actinomycetota in co-culture may be a potential biocontrol agent and biofertilizer used in agriculture. Indeed, the plant can benefit on several different levels. It was reported in the literature that the co-cultivation of Streptomyces with the phytopathogenic fungus Sclerotinia sclerotiorum induces the deformation and fragmentation of the fungal mycelium through the production of hydrolytic enzymes and secondary metabolites (Liu et al., 2019). In parallel, the same study linked the promotion of plant growth through the solubilization of inorganic phosphate and the production of 1-aminocyclopropane-1-carboxylate deaminase and indole acetic acid by the Actinomycetota (Liu et al., 2019).
The predation of gram-negative and gram-positive bacteria by Actinomycetota may enhance their potential application for the biocontrol of foodborne and plant pathogens (Ibrahimi et al., 2019, 2020). Thus, predatory Actinomycetota can provide an ecologically sustainable solution for agricultural farming. This is explained by the fact that they will not increase the accumulation of antibiotics in the environment, which may generate antibiotic resistance (Pérez et al., 2020).
4.2. Cyanobacterial bloom
Cyanobacterial bloom can produce toxic molecules called cyanotoxins in freshwater (Saraf et al., 2018). The presence of such molecules can affect the functionality of ecosystems and water quality for recreation, drinking water, fisheries, and agriculture (O’Neil et al., 2012; Corbel et al., 2014). In the agriculture field, several publications have appeared in recent years documenting the bioaccumulation of cyanotoxins in plants used for human and animal food (Corbel et al., 2014; Machado et al., 2017; Ai et al., 2020; Melaram et al., 2022). Consequently, several physical, chemical, and biological strategies were deployed to control cyanobacterial bloom (Jia et al., 2018; Sun et al., 2018; Yu Y. et al., 2019; El Amrani Zerrifi et al., 2020). Although the physic-chemical techniques represent a high cost, the risk of contamination and toxicity to humans has limited their general use (Moreira et al., 2014). Whereas biological techniques involving microorganisms have attracted researchers for their promising eco-friendly tools and high potential (Yu Y. et al., 2019).
One of the most promising aspects is the use of microbes of predatory bacteria as a control agent of cyanobacterial blooms. However, despite some initial promising discoveries, this field has been almost completely ignored. The first predatory bacteria able to lyse various species of cyanobacteria was first reported in 1967 (Shilo, 1967). Since then, numerous strains of lytic gliding bacteria, mainly members of the Myxobacteria and Cytophaga groups, have been isolated (Daft and Stewart, 1971; Granhall and Berg, 1972; Gumbo et al., 2008) and lysed cyanobacteria cells by attachment and secretion of diffusible lytic substances. These bacteria produce a variety of different exoenzymes capable of hydrolyzing the cyanobacterial cell wall (Sudo and Dworkin, 1972; Gnosspelius, 1978). Subsequently, Rashidan and Bird (2001) isolated two strains of Cytophaga sp., with lytic activity on different cyanobacteria with a restricted host range. The same study showed that the lysis of cyanobacteria by predatory bacteria may be an important factor in their population dynamics in lakes and may contribute to the prevention or the sudden disappearance of cyanobacteria blooms and draw attention to the possibilities of using host-specific lytic bacteria in biological control of harmful cyanobacterial blooms (Rashidan and Bird, 2001).
Furthermore, Bdellovibrio and Myxococcus have received a lot of investigation as predators of cyanobacterial bloom (Bauer and Forchhammer, 2021). In contrast, the use of Actinomycetota as a predator is still broadly uncharacterized. However, recently Zeng et al. (2021) demonstrated the use of a predatory Actinomycetota to face harmful cyanobacterial algal blooms. The research demonstrated that Streptomyces globisporus could predate Microcystis aeruginosa via cell-to-cell contact with high algicidal activity (Zeng et al., 2021). The present findings confirm the use of predatory Actinomycetota as promising eco-friendly tools to combat harmful cyanobacteria blooms. Also, further investigations are highly recommended to assess the predation toward cyanobacteria. In addition, it is necessary to recognize the predatory Actinomycetota-cyanobacteria ratio due to their important role as a key to achieving effective lysis of cyanobacteria.
5. Future perspectives and conclusion
Nowadays, one of the most alarming world wild problems is the increase of plant diseases caused by pathogenic bacteria, which causes great economic, environmental, and human health damage. Therefore, finding alternative and sustainable solutions to confront these pathogens represent one of the biggest challenges. In this review, we suggest the use of predatory Actinomycetota as an effective biocontrol agent. Predation is an important cause of mortality and determines the structure and activity of microbial communities in both terrestrial and aquatic ecosystems, with a complex process involving several components such as prey finding, recognition, consumption, and digestion. The literature has concentrated largely on the presence of predatory Actinomycetota and their effective activity against a panel of pathogenic microorganisms but has not examined the mechanisms of the prey lysis. Indeed, a good knowledge of the predation mechanism used by predatory Actinomycetota is essential to improve the efficiency of the lysis of the prey cells and predation performance. The application of predatory Actinomycetota in large-scale systems and field experiments must be examined to determine if there will be ecological consequences. Furthermore, it is suggested that research evaluating predators’ efficiency should include molecular viability assays, such as EMAqPCR and EMA-Illumina, to determine the efficacy of treatment. Finally, during this review, we noticed that antibiotics produced during the process of predation by predatory Actinomycetota are demonstrated but have not yet been identified. Consequently, it seems advisable to discover such compounds. In the future, actinobacterial predation could be a new approach to control plant pathogen, cyanobacterial blooms; however, intensive research efforts are required to pursue this aim.
Statements
Author contributions
MI wrote the manuscript. YO and MJ refining and critical reading of the manuscript. LL, SL, and MH revised the manuscript. All authors contributed to the manuscript and approved the submitted version.
Funding
This study was financially supported by the French Ministries of Europe and Foreign Affairs (MEAE), French Ministries of Higher Education, Research and Innovation (MESRI), the Moroccan Ministry of Higher Education, Research and Managerial Training via the Partnership Hubert Curien (PHC) Toubkal n° 17/48–Campus France n° 36856WA, and the OCP Africa to Mohamed VI Polytechnic University to develop sustainable production in Africa (no. 01/OCP AFRICA/UM6P).
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
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Summary
Keywords
bacteria, interactions, diversity, ecology, survival mechanism, prokaryotic predation
Citation
Ibrahimi M, Loqman S, Jemo M, Hafidi M, Lemee L and Ouhdouch Y (2023) The potential of facultative predatory Actinomycetota spp. and prospects in agricultural sustainability. Front. Microbiol. 13:1081815. doi: 10.3389/fmicb.2022.1081815
Received
27 October 2022
Accepted
28 December 2022
Published
25 January 2023
Volume
13 - 2022
Edited by
Akram Sadeghi, Agricultural Biotechnology Research Institute of Iran, Iran
Reviewed by
Saira Ali, SGS (Canada), Canada; Malek Marian, Agriculture, University of Trento, Italy
Updates
Copyright
© 2023 Ibrahimi, Loqman, Jemo, Hafidi, Lemee and Ouhdouch.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Yedir Ouhdouch, youhdouch@gmail.com
This article was submitted to Microbiotechnology, a section of the journal Frontiers in Microbiology
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