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MINI REVIEW article

Front. Microbiol., 13 April 2018
Sec. Fungi and Their Interactions
This article is part of the Research Topic Soil Fungal Biodiversity for Plant and Soil Health View all 12 articles

Fungal Biodiversity and Their Role in Soil Health

  • 1Institute of Agrophysics, Polish Academy of Sciences, Lublin, Poland
  • 2Netherlands Institute of Ecology, Wageningen, Netherlands
  • 3Department of Forest Pathology, Poznań University of Life Sciences, Poznań, Poland
  • 4Institute of Plant Genetics, Polish Academy of Sciences, Poznań, Poland

Soil health, and the closely related terms of soil quality and fertility, is considered as one of the most important characteristics of soil ecosystems. The integrated approach to soil health assumes that soil is a living system and soil health results from the interaction between different processes and properties, with a strong effect on the activity of soil microbiota. All soils can be described using physical, chemical, and biological properties, but adaptation to environmental changes, driven by the processes of natural selection, are unique to the latter one. This mini review focuses on fungal biodiversity and its role in the health of managed soils as well as on the current methods used in soil mycobiome identification and utilization next generation sequencing (NGS) approaches. The authors separately focus on agriculture and horticulture as well as grassland and forest ecosystems. Moreover, this mini review describes the effect of land-use on the biodiversity and succession of fungi. In conclusion, the authors recommend a shift from cataloging fungal species in different soil ecosystems toward a more global analysis based on functions and interactions between organisms.

Fungi in Soils

Fungi are very successful inhabitants of soil, due to their high plasticity and their capacity to adopt various forms in response to adverse or unfavorable conditions (Sun et al., 2005). Due to their ability to produce a wide variety of extracellular enzymes, they are able to break down all kinds of organic matter, decomposing soil components and thereby regulating the balance of carbon and nutrients (Žifčáková et al., 2016). Fungi convert dead organic matter into biomass, carbon dioxide, and organic acids (Figure 1). Many species of fungi possess the ability to act as an effective biosorbent of toxic metals such as cadmium, copper, mercury, lead, and zinc, by accumulating them in their fruiting bodies. Though these elements may inhibit their growth and affect their reproduction (Baldrian, 2003). The diversity and activity of fungi is regulated by various biotic (plants and other organisms) and abiotic (soil pH, moisture, salinity, structure, and temperature) factors (López-Bucio et al., 2015; Rouphael et al., 2015). Fungi can be found in almost every environment and can live in wide range of pH and temperature (Frąc et al., 2015).

FIGURE 1
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FIGURE 1. Aspects of soil fungal biodiversity.

Soil fungi can be classified into three functional groups including: (1) biological controllers, (2) ecosystem regulators, and (3) species participating in organic matter decomposition and compound transformations (Swift, 2005; Gardi and Jeffery, 2009). Ecosystem regulators are responsible for soil structure formation and modification of habitats for other organisms by regulating the dynamics of physiological processes in the soil environment. Biological controllers can regulate diseases, pests, and the growth of other organisms (Bagyaraj and Ashwin, 2017). For example, the mycorrhizal fungi improve plant growth by increasing the uptake of nutrients and protect them against pathogens (Bagyaraj and Ashwin, 2017).

Fungal populations are strongly influenced by the diversity and composition of the plant community and in return affect plant growth through mutualism, pathogenicity and their effect on nutrient availability and cycling (Wardle, 2002; Wagg et al., 2014; Hannula et al., 2017). Moreover, fungi participate in nitrogen fixation, hormone production, biological control against root pathogens and protection against drought (Jayne and Quigley, 2014; Baum et al., 2015; El-Komy et al., 2015). They also play an important role in stabilization of soil organic matter and decomposition of residues (Treseder and Lennon, 2015).

Methods and Recent Achievements in Studies of Soil-Borne Fungi

The advent of next generation sequencing (NGS) has facilitated a sea-change in the analysis of soil and plant-associated fungal communities. Standardized pipelines for preparing rhizosphere soil samples for Illumina sequencing are widely available (Lindahl et al., 2013; Schöler et al., 2017) and in a relatively short time following sampling, files with millions of sequences can be generated. Important points to consider when preparing samples for NGS are: sufficient biological replication (Prosser, 2010), sufficient sequencing depth (Smith and Peay, 2014; Weiss et al., 2015), adequate coverage of target organisms (i.e., primer selection and DNA extraction), and the avoidance of contamination and bias (Salter et al., 2014; Schöler et al., 2017). There are multiple pipelines for the analysis of fungal NGS data available (Bálint et al., 2014; Gweon et al., 2015), so it is not data-analysis that is problematic, but the interpretation of results.

Alpha-diversity, representing either the number of species or diversity indices that account for evenness, was proposed as an indicator for robust, healthy soil (Ferris and Tuomisto, 2015). However, it is open to question whether absolute diversity or functional diversity should be emphasized (Wagg et al., 2014; Ferris and Tuomisto, 2015). Usually the second step in analysis is to look at beta-diversity to see the effects of treatment/manipulation on the fungal community. Recently, it has been shown that fungal biodiversity in soils is strongly affected by plant community (Yang et al., 2017), soil moisture (Bagyaraj and Ashwin, 2017), and the intensity of agricultural practices (Thomson et al., 2015). Studies identified key fungal species affected by soil treatments, but it is unknown if results obtained from studies conducted on one particular soil and ecosystem can be used to infer trends and identify key fungal groups at a global or continental scale (Tedersoo et al., 2014; Delgado-Baquerizo et al., 2017).

Unlike the analysis of bacteria and archaea, where 16S rRNA is used as a barcode, fungi are usually identified based on the sequence of the Internal Transcribed Spacer (ITS) region allowing identification up to species level (Schoch et al., 2012; Porras-Alfaro et al., 2014). Although in some cases, such as for soil-dwelling Fusaria, sequencing of additional genes, such as β-tubulin gene (β-Tub), and aminoadipate reductase gene (LYS2) was proposed to obtain the correct taxonomic identification at the species level (Watanabe et al., 2011), whereas others have suggested the use of Translation Elongation Factor (Geiser et al., 2004). Many researchers have in-house databases for functional classification of fungi but recently online resources for functional annotation of fungi have been made publicly available (Nguyen et al., 2016).

Species level identification is, however only the first step from ‘What is there?’ toward the question ‘What role does it play?’ (Figure 2). Identification neither implies the microorganisms are alive and active (Blagodatskaya and Kuzyakov, 2013) nor does it describe their function (Prosser, 2015). To unravel the function of the community, either (shotgun) metagenomics (Uroz et al., 2013; Hannula and van Veen, 2016; Castañeda and Barbosa, 2017), metatranscriptomics (Damon et al., 2012; Turner et al., 2013; Hesse et al., 2015) or time-intensive culture based methods combined with functional tests must be used (Behnke-Borowczyk et al., 2012; Gałązka et al., 2017; Wolińska et al., 2017). A fast, but coarse alternative to molecular methods is MicroResp (Creamer et al., 2016) or community level physiological profiles (CLPP) approach (Frąc et al., 2017), which gives an indication on substrate use of the total microbial community. This method, however, does not identify the species responsible for the process. Increasingly, especially in studies where plant community is included alongside NGS approaches, microorganisms are isolated from the soils and plant roots for further functional testing.

FIGURE 2
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FIGURE 2. Soil fungal biodiversity as an interdisciplinary research.

To construct a more complete picture of a soil fungi community their interactions with other organisms must be taken into consideration. Strong linkage was proved between functional soil biodiversity and the function of the soil ecosystem (Wagg et al., 2014; Delgado-Baquerizo et al., 2017; Morrien et al., 2017). Fungi interact with other soil organisms and thus changes in the fungal community have the potential to affect the function of the whole soil ecosystem (Yang et al., 2017). Analysis of the interactions in the soil can be achieved through indirect estimation of species interactions using co-occurrence networks (Creamer et al., 2016; Morrien et al., 2017) or directly by using isotope tracers (Hannula et al., 2017) and/or gut content analysis (Kurakov et al., 2016).

Fungal Biodiversity and Their Functions in Soil Health of Agricultural and Horticultural Ecosystems

The term ‘soil health’ is widely used in reference to sustainable agriculture (Kibblewhite et al., 2008; Cardoso et al., 2013), especially in the context of soil as a dynamic, living organism functioning holistically rather than as an inert substrate (Doran and Jones, 1996). Therefore, in this article we prefer to use the terminology of soil health, rather than soil quality, which is defined as the capacity of the soil to maintain environmental quality, sustain biological productivity, and promote animal, human, and plant health (Doran and Parkin, 1994). In recent years the potential application of cultivating soil fungal biodiversity to improve soil quality and increase productivity of agricultural ecosystems has been highlighted as a new and very promising development in plant productivity (Bagyaraj and Ashwin, 2017), which may come be called ‘the 2nd Green Revolution.’ The implementation of such solutions may offer an alternative to the current overuse of fertilizers toward more sophisticated manipulations of plant productivity. Fungi participate in decomposition of organic matter and deliver nutrients for plant growth. Their role is very important in plant protection against pathogenic microorganisms as biological agents, which influences soil health (Frąc et al., 2015). The assessment of fungal biodiversity as quality indicators cannot be limited only to the determination of biodiversity indexes, but also should include a structure analysis of fungal population in order to determine the functions they play in affecting soil quality and plant health. The use of different kinds of organic manure has a strong influence on soil health, through indirect effects (i.e., via changes in physicochemical characteristics) and a direct effect on soil fungal communities. Soil management is fundamental to all agricultural systems, and the reduction of soil degradation is a priority to sustain future production. This effect can be only achieved by taking soil fungal biodiversity into account. All cultural practices, such as the use of cover and rotational crops, composts and tillage systems, besides their known effects on soil-borne pathogens (Abawi and Widmer, 2000), are likely to affect also the other groups of soil fungi, especially beneficial fungal populations. It has long been known that the suppressiveness of soils can be enhanced by adding biopolymers such as chitin and its derivatives (i.e., chitosan). This suppressiveness is related to a change in the activity and structure of soil microorganisms (Cretoiu et al., 2013). Therefore, we should utilize our knowledge on the interactions between different fungal groups and their ecology in the management of agricultural systems. It is worth mentioning that chitin addition to the soil increases bacteria and fungi that can degrade pathogenic fungal cell walls and can thus, increase the soil suppressiveness against plant pathogens. This might be a good alternative to fungicides that kill all fungi, including beneficial ones. Different tillage treatments can also impact soil fungi by soil disturbances that affect the functioning of fungal communities. Reduced tillage decreases the breakdown of hyphae causing fungal populations to remain more stable, retaining more nutrients and providing more suppressive effects against pathogenic microorganisms (Goss and deVarennes, 2002). Understanding and selecting the appropriate cultural practices, increasing fungal biodiversity, can prevent or decrease damage of root diseases and play a crucial role in the maintenance of soil quality and health. It should be taken into account that fungal diversity determines plant biodiversity, ecosystem variability, and productivity (van der Heijden et al., 1998; Wagg et al., 2014).

Arbuscular mycorrhizal fungi (AMF) are the most important class of beneficial microorganisms in agri- and horticultural soils (Smith and Read, 2008, Table 1). Significant increases in the yield of crop plants following inoculation with AMF have been observed in numerous experiments (Thilagar and Bagyaraj, 2015; Bagyaraj and Ashwin, 2017). The key effects of AMF symbiosis include: improvement of rooting and plant establishment, stimulation of nutrient cycling, improvement of soil structure, enhancement of plant tolerance to stresses, increased uptake of low mobility ions, and enhancement of plant community diversity (Azcón-Aguilar and Barea, 1997). The diseases of crop plants can be controlled by some antagonistic fungi such as Glomus sp. or Trichoderma sp. suppressing fungal pathogens (Dawidziuk et al., 2016). Species of Trichoderma (T. asperellum, T. atroviride, T. harzianum, T. virens, and T. viride) are frequently used in biocontrol and are known as biostimulants for horticultural crops (López-Bucio et al., 2015). Other positive effects of fungi on soil quality and plant health include inoculation by microbial consortia of AMF together with plant growth promoting rhizobacteria (PGPR) and others such as N-fixing and P-solubilizing microorganisms (Bagyaraj and Ashwin, 2017). A synergistic, favorable impact of AMFs and PGPRs on horticultural plant growth and soil microbial diversity and activity has been reported (Azcón-Aguilar and Barea, 1997; De Coninck et al., 2015).

TABLE 1
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TABLE 1. Fungal community composition in different soil ecosystems and their function.

Besides beneficial fungi, agri- and horticultural ecosystems contain also plant pathogens. The major groups of soil-borne root pathogenic fungi and oomycetes constitute of genera Fusarium (Michielse and Rep, 2009), Verticillium (Klosterman et al., 2009), Rhizoctonia (Gonzalez et al., 2011), Pythium, Phytophthora (van West et al., 2003) and many others, of global and local importance. The soil fungal diversity and methods of increasing it, particularly the populations of beneficial fungi within ecosystems should be used in practice for more sustainable plant production, decrease of chemical applications and protection of the soil environment.

Fungal Biodiversity and Their Functions in Soil Health of Grassland Ecosystems

Soil microorganisms, including fungi are an important component of grassland ecosystems due to their biochemical activity and engagement in nutrient cycling (Dengler et al., 2014). Grasslands provide many forms of ecosystem services including: supporting, provisioning, regulatory, and cultural services. Importantly, the role of biodiversity has been established as fundamental in ensuring the performance of ecosystem functioning. Grazing activities influence soil fungal community structure by changing edaphic conditions and the vegetation biodiversity in plant communities (Yang et al., 2017). It has been proven that moderate grazing sustains plants diversity while heavy grazing results in species loss (Joubert et al., 2017). Furthermore, plant-fungal interactions can inhibit biodiversity in grasslands due to the production of different root exudates such as enzymes, organic compounds, and polysaccharides (Huhe et al., 2017).

Plant pathogenic fungi also have a large impact on plant diversity in grasslands by limiting the abundance of their hosts, affecting biomass production. The study by Allan et al. (2010) suggests that fungal pathogens could affect nutrient cycling in grasslands reducing the abundance of dominant grasses and enhancing the growth of legumes. Soil fungal communities in grasslands can also be influenced by human activities and the components of long-term fertilization and other treatments (Cassman et al., 2016). Unlike in agricultural soils, where ascomycetes dominate, in grasslands, basidiomycetes are major decomposers of dead organic matter (Deacon et al., 2006).

Fungal Biodiversity and Their Functions in Soil Health of Forest Ecosystems

Knowledge of the soil chemical and physical properties has always been of interest to foresters to evaluate the capacity of sites and to increase forest productivity (Schoenholtz et al., 2000). Forest soils (including humus, litter, and coarse woody debris) are an important reservoir of microorganisms and soil biota that in turn influence carbon storage, soil structure, fertility, productivity, and plant/tree growth.

Ectomycorrhizal associations are created by a specific group of plant families that includes the Pinaceae, Fabaceae, Betulaceae, and Fagaceae (Phosri et al., 2012). The results of research obtained by Högberg and Högberg (2002), indicate a significant contribution by ectomycorrhizal mycelium to forest soil microbial biomass and by ectomycorrhizal roots to the production of extractable dissolved organic carbon, which is a carbon source for other microbes.

During the processes of thinning, the transfer of nutrients from aboveground biomass to forest soil takes place (Tian et al., 2010). A higher concentration of nutrients comes from the green litter of thinned trees than litter returned to the forest floor after senescence (Girisha et al., 2003) or from the woody residue left on the ground after harvesting (Cookson et al., 2008). Consequently, the quality and quantity of organic substrates presented to the soil fungal community by thinned and non-thinned forests may vary to a great extent. The community of soil microorganisms depends highly on organic matter as it provides a suitable environment and energy sources for them that are critical to maintain the nutritional quality and water-retaining capacity of forest soils (Jiménez-Morillo et al., 2016). Soil organic matter is of key relevance in maintaining soil resistance and stability, although it is uncertain how deterioration of soil properties and changes in fungal communities affect the functional stability of soils. Degradation of soil properties followed by deforestation may lead to decreases in soil fungal diversity and functional stability (Chaer et al., 2009).

Concluding Remarks

Soil health conditions have a tremendous impact on environmental sustainability including sustainability in agriculture, horticulture, and forestry. Moreover, soil health is directly connected with the production of healthy food which impacts public and animal health. More research is required to find the best way to maintain fungal biodiversity in soil, taking into consideration fungal functions and ecosystem services, including disease control, contamination detection, and bioremediation. Having the right tools, and being able to both identify species and characterize their role in the environment is important. The ability to compare functional structures between ecosystems and predict responses to environmental changes and interventions would be a useful advance.

Author Contributions

MF, SH, MB, and MJ: wrote, drafted, read, corrected, improved, revised, and accepted the last version of manuscript.

Funding

This paper was co-financed by The National Centre for Research and Development in frame of the project BIOSTRATEG, contract number BIOSTRATEG3/347464/5/NCBR/2017.

Conflict of Interest Statement

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.

Acknowledgments

The authors greatly thank Dr. William Truman, Institute of Plant Genetics, Polish Academy of Sciences for the critical correction of the manuscript.

References

Abawi, G. S., and Widmer, T. L. (2000). Impact of soil health management practices on soilborne pathogens, nematodes and root diseases of vegetable crops. Appl. Soil Ecol. 15, 37–47. doi: 10.1016/S0929-1393(00)00070-6

CrossRef Full Text | Google Scholar

Allan, E., Van Ruijven, J., and Crawley, M. J. (2010). Foliar fungal pathogens and grassland biodiversity. Ecology 91, 2572–2582. doi: 10.1890/09-0859.1

CrossRef Full Text | Google Scholar

Arnolds, E. (2001). “The future of fungi in Europe: threats, conservation and management,” in Fungal Conservation - Issues and Solutions, eds D. Moore, M. M. Nauta, S. E. Evans, and M. Rotheroe (Cambridge: Cambridge University Press), 64–80. doi: 10.1017/CBO9780511565168.005

CrossRef Full Text | Google Scholar

Azcón-Aguilar, C., and Barea, J. M. (1997). Applying mycorrhiza biotechnology to horticulture: significance and potentials. Sci. Hortic. 68, 1–24. doi: 10.1016/S0304-4238(96)00954-5

CrossRef Full Text | Google Scholar

Bagyaraj, D. J., and Ashwin, R. (2017). Soil biodiversity: role in sustainable horticulture. Biodivers. Hortic. Crops 5, 1–18. doi: 10.1016/j.jenvman.2017.08.001

PubMed Abstract | CrossRef Full Text

Baldrian, P. (2003). Interactions of heavy metals with white-rot fungi. Enzyme Microb. Technol. 32, 78–91. doi: 10.1016/S0141-0229(02)00245-4

CrossRef Full Text | Google Scholar

Bálint, M., Schmidt, P. A., Sharma, R., Thines, M., and Schmitt, I. (2014). An Illumina metabarcoding pipeline for fungi. Ecol. Evol. 4, 2642–2653. doi: 10.1002/ece3.1107

PubMed Abstract | CrossRef Full Text | Google Scholar

Bastida, F., Torres, I. F., Hernandez, T., and García, C. (2017). The impacts of organic amendments: do they confer stability against drought on the soil microbial community? Soil Biol. Biochem. 113, 173–183. doi: 10.1016/j.soilbio.2017.06.012

CrossRef Full Text | Google Scholar

Baum, C., El-Tohamy, W., and Gruda, N. (2015). Increasing the productivity and product quality of vegetable crops using arbuscular mycorrhizal fungi: a review. Sci. Hortic. 187, 131–141. doi: 10.1016/j.scienta.2015.03.002

CrossRef Full Text | Google Scholar

Behnke-Borowczyk, J., Kwaśna, H., and Bełka, M. (2012). Molecular methods used in studies of diversity of the soil microorganisms. Sylwan 156, 294–304.

Google Scholar

Blagodatskaya, E., and Kuzyakov, Y. (2013). Active microorganisms in soil: critical review of estimation criteria and approaches. Soil Biol. Biochem. 67, 192–211. doi: 10.1016/j.soilbio.2013.08.024

CrossRef Full Text | Google Scholar

Cai, X. B., Peng, Y. L., Yang, M. N., Zhang, T., and Zhang, Q. (2014). Grassland degradation decrease the diversity of arbuscular mycorrhizal fungi species in Tibet Plateau. Not. Bot. Horti Agrobot. 42, 333–339. doi: 10.15835/nbha4229458

CrossRef Full Text | Google Scholar

Cardoso, E. J. B. N., Vasconcellos, R. L. F., Bini, D., Miyauchi, M. Y. H., dos Santos, C. A., Alves, P. R. L., et al. (2013). Soil health: looking for suitable indicators. What should be considered to assess the effects of use and management on soil health? Sci. Agric. 70, 274–289. doi: 10.1590/S0103-90162013000400009

CrossRef Full Text | Google Scholar

Cassman, N. A., Leite, M. F. A., Pan, Y., de Hollander, M., van Veen, J. A., and Kuramae, E. E. (2016). Plant and soil fungal but not soil bacterial communities are linked in long-term fertilized grassland. Sci. Rep. 6:23680. doi: 10.1038/srep23680

PubMed Abstract | CrossRef Full Text | Google Scholar

Castañeda, L. E., and Barbosa, O. (2017). Metagenomic analysis exploring taxonomic and functional diversity of soil microbial communities in Chilean vineyards and surrounding native forests. PeerJ 5:e3098. doi: 10.7717/peerj.3098

PubMed Abstract | CrossRef Full Text | Google Scholar

Chaer, G., Fernandes, M., Myrold, D., and Bottomley, P. (2009). Comparative resistance and resilience of soil microbial communities and enzyme activities in adjacent native forest and agricultural soils. Microb. Ecol. 58, 414–424. doi: 10.1007/s00248-009-9508-x

PubMed Abstract | CrossRef Full Text | Google Scholar

Cookson, W. R., O’Donnell, A. J., Grant, C. D., Grierson, P. F., and Murphy, D. V. (2008). Impact of ecosystem management on microbial community level physiological profiles of postmining forest rehabilitation. Microb. Ecol. 55, 321–332. doi: 10.1007/s00248-007-9278-2

PubMed Abstract | CrossRef Full Text | Google Scholar

Creamer, R. E., Hannula, S. E., and van Leeuwen, J. P. (2016). Ecological network analysis reveals the inter-connection between soil biodiversity and ecosystem function as affected by land use across Europe. Appl. Soil Ecol. 97, 112–124. doi: 10.1016/j.apsoil.2015.08.006

CrossRef Full Text | Google Scholar

Cretoiu, M. S., Korthals, G. W., Visser, J. H. M., and van Elsas, J. D. (2013). Chitin amendment increases soil suppressiveness toward plant pathogens and modulates the actinobacterial and oxalobacteraceal communities in an experimental agricultural field. Appl. Environ. Microbiol. 79, 5291–5301. doi: 10.1128/AEM.01361-13

PubMed Abstract | CrossRef Full Text | Google Scholar

Damon, C., Lehembre, F., Oger-Desfeux, C., Luis, P., Ranger, J., Fraissinet-Tachet, L., et al. (2012). Metatranscriptomics reveals the diversity of genes expressed by eukaryotes in forest soils. PLoS One 7:e28967. doi: 10.1371/journal.pone.0028967

PubMed Abstract | CrossRef Full Text | Google Scholar

Dawidziuk, A., Popiel, D., Kaczmarek, J., Strakowska, J., and Jedryczka, M. (2016). Morphological and molecular properties of Trichoderma species help to control stem canker of oilseed rape. BioControl 61, 755–768.

De Coninck, B., Timmermans, P., Vos, C., Cammue, B. P. A., and Kazan, K. (2015). What lies beneath: belowground defense strategies in plants. Trends Plant Sci. 20, 91–101. doi: 10.1016/j.tplants.2014.09.007

PubMed Abstract | CrossRef Full Text | Google Scholar

Deacon, L. J., Pryce-Miller, E. J., Frankland, J. C., Bainbridge, B. W., Moore, P. D., and Robinson, C. H. (2006). Diversity and function of decomposer fungi from a grassland soil. Soil Biol. Biochem. 38, 7–20. doi: 10.1016/j.soilbio.2005.04.013

CrossRef Full Text | Google Scholar

Delgado-Baquerizo, M., Powell, J. R., Hamonts, K., Reith, F., Mele, P., Brown, M. V., et al. (2017). Circular linkages between soil biodiversity, fertility and plant productivity are limited to topsoil at the continental scale. New Phytol. 215, 1186–1196. doi: 10.1111/nph.14634

PubMed Abstract | CrossRef Full Text | Google Scholar

Dengler, J., Janisová, M., Török, P., and Wellstein, C. (2014). Biodiversity of Palaearctic grasslands: a synthesis. Agric. Ecosyst. Environ. 182, 1–14. doi: 10.1016/j.agee.2013.12.015

CrossRef Full Text | Google Scholar

Ding, J., Jiang, X., Guan, D., Zhao, B., Ma, M., Zhou, B., et al. (2017). Influence of inorganic fertilizer and organic manure application on fungal communities in a long-term field experiment of Chinese Mollisols. Appl. Soil Ecol. 111, 114–122. doi: 10.1016/j.apsoil.2016.12.003

CrossRef Full Text | Google Scholar

Doran, J. W., and Jones, A. J. (1996). “Soil quality and health: indicators of sustainability,” in Methods for Assessing Soil Quality. SSSA Special Publication Number 49, eds J. W. Doran and A. J. Jones (Madison, WI: Soil Science Society of America), XI–XIV.

Google Scholar

Doran, J. W., and Parkin, T. B. (1994). “Defining and assessing soil quality,” in Defining Soil Quality for a Sustainable Environment. SSSA Special Publication Number 35, eds J. W. Doran, D. C. Coleman, D. F. Bezdicek, and B. A. Stewart (Madison, WI: Soil Science Society of America), 3–21. doi: 10.2136/sssaspecpub35.c1

CrossRef Full Text | Google Scholar

El-Komy, M. H., Saleh, A. A., Eranthodi, A., and Molan, Y. Y. (2015). Characterization of novel Trichoderma asperellum isolates to select effective biocontrol agents against tomato Fusarium wilt. Plant Pathol. J. 31, 50–60. doi: 10.5423/PPJ.OA.09.2014.0087

PubMed Abstract | CrossRef Full Text | Google Scholar

Ferris, H., and Tuomisto, H. (2015). Unearthing the role of biological diversity in soil health. Soil Biol. Biochem. 85, 101–109. doi: 10.1016/j.soilbio.2015.02.037

PubMed Abstract | CrossRef Full Text | Google Scholar

Frąc, M., Jezierska-Tys, S., and Takashi, Y. (2015). Occurrence, detection, and molecular and metabolic characterization of heat-resistant fungi in soils and plants and their risk to human health. Adv. Agron. 132, 161–204.

Google Scholar

Frąc, M., Weber, J., Gryta, A., Dêbicka, M., Kocowicz, A., Jamroz, E., et al. (2017). Microbial functional diversity in podzol ectohumus horizons affected by alkaline fly ash in the vicinity of electric power plant. Geomicrobiol. J. 34, 579–586.

Google Scholar

Gałązka, A., Gawryjołek, K., Grządziel, J., Frąc, M., and Księżak, J. (2017). Microbial community diversity and the interaction of soil under maize growth in different cultivation techniques. Plant Soil Environ. 63, 264–270. doi: 10.17221/171/2017-PSE

CrossRef Full Text | Google Scholar

Gardi, C., and Jeffery, S. (2009). Soil Biodiversity. Brussels: European Commission, 27.

Google Scholar

Geiser, D. M., del Mar Jiménez-Gasco, M., Kang, S., Makalowska, I., Veeraraghavan, N., Ward, T. J., et al. (2004). FUSARIUM-ID v. 1.0: a DNA sequence database for identifying Fusarium. Eur. J. Plant Pathol. 110, 473–479.

Google Scholar

Girisha, G. K., Condron, L. M., Clinton, P. W., and Davis, M. R. (2003). Decomposition and nutrient dynamics of green and freshly fallen radiata pine (Pinus radiata) needles. For. Ecol. Manag. 179, 169–181. doi: 10.1016/S0378-1127(02)00518-2

CrossRef Full Text | Google Scholar

Gonzalez, M., Pujol, M., Metraux, J. P., Gonzalez-Garcia, V., Bolton, M. D., and Borrás-Hidalgo, O. (2011). Tobacco leaf spot and root rot caused by Rhizoctonia solani Kuhn. Mol. Plant Pathol. 12, 209–216. doi: 10.1111/j.1364-3703.2010.00664.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Goss, M. J., and deVarennes, A. (2002). Soil disturbance reduces the efficacy of mycorrhizal associations for early soybean growth and N2 fixation. Soil Biol. Biochem. 34, 1167–1173. doi: 10.1016/S0038-0717(02)00053-6

CrossRef Full Text | Google Scholar

Gweon, H. S., Oliver, A., Taylor, J., Booth, T., Gibbs, M., Read, D. S., et al. (2015). PIPITS: an automated pipeline for analyses of fungal internal transcribed spacer sequences from the Illumina sequencing platform. Methods Ecol. Evol. 6, 973–980. doi: 10.1111/2041-210X.12399

PubMed Abstract | CrossRef Full Text | Google Scholar

Hannula, S. E., Morrien, E., and de Hollander, M. (2017). Shifts in rhizosphere fungal community during secondary succession following abandonment from agriculture. ISME J. 11, 2294–2304. doi: 10.1038/ismej.2017.90

PubMed Abstract | CrossRef Full Text | Google Scholar

Hannula, S. E., and van Veen, J. A. (2016). Primer sets developed for functional genes reveal shifts in functionality of fungal community in soils. Front. Microbiol. 7:1897. doi: 10.3389/fmicb.2016.01897

PubMed Abstract | CrossRef Full Text | Google Scholar

Hesse, C. N., Mueller, R. C., Vuyisich, M., Gallegos-Graves, L. V., Gleasner, C. D., Zak, D. R., et al. (2015). Forest floor community metatranscriptomes identify fungal and bacterial responses to N deposition in two maple forests. Front. Microbiol. 6:337. doi: 10.3389/fmicb.2015.00337

PubMed Abstract | CrossRef Full Text | Google Scholar

Högberg, M. N., and Högberg, P. (2002). Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phytol. 154, 791–795. doi: 10.1046/j.1469-8137.2002.00417.x

CrossRef Full Text | Google Scholar

Huhe, Y. C., Chen, X., Hou, F., Wu, Y., and Cheng, Y. (2017). Bacterial and fungal community structures in loess plateau grasslands with different grazing intensities. Front. Microbiol. 8:606. doi: 10.3389/fmicb.2017.00606

PubMed Abstract | CrossRef Full Text | Google Scholar

Jayne, B., and Quigley, M. (2014). Influence of arbuscular mycorrhiza on growth and reproductive response of plants under water deficit: a meta-analysis. Mycorrhiza 24, 109–119. doi: 10.1007/s00572-013-0515-x

PubMed Abstract | CrossRef Full Text | Google Scholar

Jiménez-Morillo, N. T., González-Pérez, J. A., Jordán, A., Zavala, L. M., de la Rosa, J. M., Jiménez-González, M. A., et al. (2016). Organic matter fractions controlling soil water repellency in sandy soils from the Doñana National Park (Southwestern Spain). Land Degrad. Dev. 27, 1413–1423. doi: 10.1002/ldr.2314

CrossRef Full Text | Google Scholar

Johnson, D., Vandenkoornhuyse, P. J., Leake, J. R., Gilbert, L., Booth, R. E., Grime, J. P., et al. (2003). Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytol. 161, 503–515. doi: 10.1046/j.1469-8137.2003.00938.x

CrossRef Full Text | Google Scholar

Joubert, L., Pryke, J. S., and Samways, M. J. (2017). Applied vegetation science 20 (2017) 340–351 moderate grazing sustains plant diversity in Afromontane grassland. Appl. Veg. Sci. 20, 340–351. doi: 10.1111/avsc.12310

CrossRef Full Text | Google Scholar

Kibblewhite, M. G., Ritz, K., and Swift, M. J. (2008). Soil health in agricultural systems. Philos. Trans. R. Soc. B Biol. Sci. 363, 685–701. doi: 10.1098/rstb.2007.2178

PubMed Abstract | CrossRef Full Text | Google Scholar

Klosterman, S. J., Atallah, Z. K., Vallad, G. E., and Subbarao, K. V. (2009). Diversity, pathogenicity, and management of Verticillium species. Annu. Rev. Phytopathol. 47, 39–62. doi: 10.1146/annurev-phyto-080508-081748

PubMed Abstract | CrossRef Full Text | Google Scholar

Kurakov, A. V., Kharin, S. A., and Byzov, B. A. (2016). Changes in the composition and physiological and biochemical properties of fungi during passage through the digestive tract of earthworms. Biol. Bull. 43, 290–299.

Google Scholar

Leff, J. W., Jones, S. E., Prober, S. M., Barberán, A., Borer, E. T., Firn, J. L., et al. (2015). Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc. Natl. Acad. Sci. U.S.A. 112, 10967–10972. doi: 10.1073/pnas.1508382112

PubMed Abstract | CrossRef Full Text | Google Scholar

Lindahl, B. D., Nilsson, R. H., Tedersoo, L., Abarenkov, K., Carlsen, T., Kjøller, R., et al. (2013). Fungal community analysis by high-throughput sequencing of amplified markers – a user’s guide. New Phytol. 199, 288–299. doi: 10.1111/nph.12243

PubMed Abstract | CrossRef Full Text | Google Scholar

Liu, J., Sui, Y., Yu, Z., Shi, Y., Chu, H., Jin, J., et al. (2015). Soil carbon content drives the biogeographical distribution of fungal communities in the black soil zone of northeast China. Soil Biol. Biochem. 83, 29–39. doi: 10.1016/j.soilbio.2015.01.009

CrossRef Full Text | Google Scholar

López-Bucio, J., Pelagio-Flores, R., and Herrera-Estrell, A. (2015). Trichoderma as biostimulant: exploiting the multilevel properties of a plant beneficial fungus. Sci. Hortic. 196, 109–123. doi: 10.1016/j.scienta.2015.08.043

CrossRef Full Text | Google Scholar

Lucas, R. W., Casper, B. B., Jackson, J. K., and Balser, T. C. (2007). Soil microbial communities and extracellular enzyme activity in the New Jersey Pinelands. Soil Biol. Biochem. 39, 2508–2519. doi: 10.1016/j.soilbio.2007.05.008

CrossRef Full Text | Google Scholar

Małecka, I., Blecharczyk, A., Sawińska, Z., Swêdrzyńska, D., and Piechota, T. (2015). Winter wheat yield and soil properties response to long-term non-inversion tillage. J. Agric. Sci. Technol. 17, 1571–1584.

Google Scholar

Michielse, C. B., and Rep, M. (2009). Pathogen profile update: Fusarium oxysporum. Mol. Plant Pathol. 10, 311–324. doi: 10.1111/j.1364-3703.2009.00538.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Morrien, E., Hannula, S. E., Snoek, L. B., Helmsing, N. R., Zweers, H., de Hollander, M., et al. (2017). Soil networks become more connected and take up more carbon as nature restoration progresses. Nat. Commun. 8:14349. doi: 10.1038/ncomms14349

PubMed Abstract | CrossRef Full Text | Google Scholar

Nguyen, N. H., Song, Z., Bates, S. T., Branco, S., Tedersoo, L., Menke, J., et al. (2016). FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol. 20, 241–248. doi: 10.1016/j.funeco.2015.06.006

CrossRef Full Text | Google Scholar

Öster, M. (2006). Biological Diversity Values in Semi-natural Grasslands - Indicators, Landscape Context and Restoration. Doctoral dissertation, Stockholm University, Stockholm.

Google Scholar

Pal, A., Ghosh, S., and Paul, A. K. (2006). Biosorption of cobalt by fungi from serpentine soil of Andaman. Bioresour. Technol. 97, 1253–1258.

PubMed Abstract | Google Scholar

Phosri, C., Polme, S., Taylor, A. F. S., Koljalg, U., Suwannasai, N., and Tedersoo, L. (2012). Diversity and community composition of ectomycorrhizal fungi in a dry deciduous dipterocarp forest in Thailand. Biodivers. Conserv. 21, 2287–2298. doi: 10.1007/s10531-012-0250-1

CrossRef Full Text | Google Scholar

Porras-Alfaro, A., Herrera, J., Natvig, D. O., Lipinski, K., and Sinsabaugh, R. L. (2011). Diversity and distribution of soil fungal communities in a semiarid grassland. Mycologia 103, 10–21. doi: 10.3852/09-297

PubMed Abstract | CrossRef Full Text | Google Scholar

Porras-Alfaro, A., Liu, K. L., Kuske, C. R., and Xie, G. (2014). From genus to phylum: large-subunit and internal transcribed spacer rRNA operon regions show similar classification accuracies influenced by database composition. Appl. Environ. Microbiol. 80, 829–840. doi: 10.1128/AEM.02894-13

PubMed Abstract | CrossRef Full Text | Google Scholar

Prosser, J. I. (2010). Replicate or lie. Environ. Microbiol. 12, 1806–1810. doi: 10.1111/j.1462-2920.2010.02201.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Prosser, J. I. (2015). Dispersing misconceptions and identifying opportunities for the use of ‘omics’ in soil microbial ecology. Nat. Rev. Microbiol. 13, 439–446. doi: 10.1038/nrmicro3468

PubMed Abstract | CrossRef Full Text | Google Scholar

Rillig, M. C., and Mummey, D. L. (2006). Mycorrhizas and soil structure. New Phytol. 171, 41–53. doi: 10.1111/j.1469-8137.2006.01750.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Rouphael, Y., Franken, P., Schneider, C., Schwarz, D., Giovannetti, M., Agnolucci, M., et al. (2015). Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Sci. Hortic. 196, 91–108. doi: 10.1016/j.scienta.2015.09.002

CrossRef Full Text | Google Scholar

Salter, S. J., Cox, M. J., Turek, E. M., Calus, S. T., Cookson, W. O., Moffatt, M. F., et al. (2014). Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol. 12:87. doi: 10.1186/s12915-014-0087-z

PubMed Abstract | CrossRef Full Text | Google Scholar

Santos-González, J. C. (2007). Diversity of Arbuscular Mycorrhizal Fungi in Grasslands and Arable Fields. Doctor’s dissertation, Swedish University of Agricultural Sciences, Uppsala.

Google Scholar

Schoch, C. L., Seifert, K. A., Huhndorf, S., Robert, V., Spouge, J. L., Levesque, C. A., et al. (2012). Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc. Natl. Acad. Sci. U.S.A. 109, 6241–6246. doi: 10.1073/pnas.1117018109

PubMed Abstract | CrossRef Full Text | Google Scholar

Schoenholtz, S. H., Van Miegroet, H., and Burger, J. A. (2000). A review of chemical and physical properties as indicators of forest soil quality: challenges and opportunities. For. Ecol. Manag. 138, 335–356. doi: 10.1016/S0378-1127(00)00423-0

CrossRef Full Text | Google Scholar

Schöler, A., Jacquiod, S., Vestergaard, G., Schulz, S., and Schloter, M. (2017). Analysis of soil microbial communities based on amplicon sequencing of marker genes. Biol. Fertil. Soil 53, 485–489. doi: 10.1007/s00374-017-1205-1

CrossRef Full Text | Google Scholar

Smith, D. P., and Peay, K. G. (2014). Sequence depth, not PCR replication, improves ecological inference from next generation DNA sequencing. PLoS One 9:e90234. doi: 10.1371/journal.pone.0090234

PubMed Abstract | CrossRef Full Text | Google Scholar

Smith, S. E., and Read, D. J. (2008). Mycorrhizal Symbiosis, 3rd Edn. London: Academic Press.

Google Scholar

Sun, J. M., Irzykowski, W., Jędryczka, M., and Han, F. X. (2005). Analysis of the genetic structure of Sclerotinia sclerotiorum (Lib.) de Bary populations from different regions and host plants by Random Amplified Polymorphic DNA markers. J. Integr. Plant Biol. 47, 385–395. doi: 10.1111/j.1744-7909.2005.00077.x

CrossRef Full Text | Google Scholar

Swift, M. J. (2005). “Human impacts on biodiversity and ecosystem services: an overview,” in The Fungal Community its Organization and Role in Ecosystems, eds J. Dighton, J. F. White, and P. Oudemans (Boca Raton, FL: CRC Press), 627–641.

Google Scholar

Tedersoo, L., Bahram, M., Põlme, S., Kõljalg, U., Yorou, N. S., Wijesundera, R., et al. (2014). Global diversity and geography of soil fungi. Science 346:1256688. doi: 10.1126/science.1256688

PubMed Abstract | CrossRef Full Text | Google Scholar

Thilagar, G., and Bagyaraj, D. J. (2015). Influence of different arbuscular mycorrhizal fungi on growth and yield of chilly. Proc. Natl. Acad. Sci. India B Biol. Sci. 85, 71–75. doi: 10.1007/s40011-013-0262-y

CrossRef Full Text | Google Scholar

Thomson, B. C., Tisserant, E., Plassart, P., Uroz, S., Griffiths, R. I., Hannula, E. S., et al. (2015). Soil conditions and land use intensification effects on soil microbial communities across a range of European field sites. Soil Biol. Biochem. 88, 403–413. doi: 10.1016/j.soilbio.2015.06.012

CrossRef Full Text | Google Scholar

Tian, D. L., Peng, Y. Y., Yan, W. D., Fang, X., Kang, W. X., Wang, G. J., et al. (2010). Effects of thinning and litter fall removal on fine root production and soil organic carbon content in Masson pine plantations. Pedosphere 20, 486–493. doi: 10.1016/S1002-0160(10)60038-0

CrossRef Full Text | Google Scholar

Treseder, K. K., and Lennon, J. T. (2015). Fungal traits that drive ecosystem dynamics on land. Microbiol. Mol. Biol. Rev. 79, 243–262. doi: 10.1128/MMBR.00001-15

PubMed Abstract | CrossRef Full Text | Google Scholar

Turner, T. R., Ramakrishna, K., Walshaw, J., Heavens, D., Alston, M., Swarbreck, D., et al. (2013). Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME J. 7, 2248–2258. doi: 10.1038/ismej.2013.119

PubMed Abstract | CrossRef Full Text | Google Scholar

Uroz, S., Ioannidis, P., Lengelle, J., Cébron, A., Morin, E., Buée, M., et al. (2013). Functional assays and metagenomic analyses reveals differences between the microbial communities inhabiting the soil horizons of a Norway spruce plantation. PLoS One 8:e55929. doi: 10.1371/journal.pone.0055929

PubMed Abstract | CrossRef Full Text | Google Scholar

van der Heijden, M. G. A., Klironomos, J. N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boller, T., et al. (1998). Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 69–72. doi: 10.1038/23932

CrossRef Full Text | Google Scholar

van West, P., Appiah, A. A., and Gow, N. A. R. (2003). Advances in research on oomycete root pathogens. Physiol. Mol. Plant Pathol. 62, 99–113. doi: 10.1016/S0885-5765(03)00044-4

CrossRef Full Text | Google Scholar

Wagg, C., Bender, S. F., Widmer, F., and Van der Heijden, M. G. A. (2014). Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc. Natl. Acad. Sci. U.S.A. 111, 5266–5270. doi: 10.1073/pnas.1320054111

PubMed Abstract | CrossRef Full Text | Google Scholar

Wakelin, S. A., Macdonald, L. M., O’Callaghan, M., Forrester, S. T., and Condron, L. M. (2014). Soil functional resistance and stability are linked to different ecosystem properties. Austral. Ecol. 39, 522–531. doi: 10.1111/aec.12112

CrossRef Full Text | Google Scholar

Wardle, D. A. (2002). Communities and Ecosystems: Linking Aboveground and Belowground Components. Princeton, NJ: Princeton University Press.

Google Scholar

Watanabe, M., Yonezawa, T., Lee, K., Kumagai, S., Sugita-Konishi, Y., Goto, K., et al. (2011). Evaluation of genetic markers for identifying isolates of the species of the genus Fusarium. J. Sci. Food Agric. 91, 2500–2504. doi: 10.1002/jsfa.4507

PubMed Abstract | CrossRef Full Text | Google Scholar

Weiss, S. J., Xu, Z., Amir, A., Peddada, S., Bittinger, K., Gonzalez, A., et al. (2015). Effects of library size variance, sparsity, and compositionality on the analysis of microbiome data. PeerJ 3:e1157v1. doi: 10.7287/peerj.preprints.1157v1

CrossRef Full Text | Google Scholar

Winder, R. S., and Shamoun, S. F. (2006). Forest pathogens: friends or foe to biodiversity? Can. J. Plant Pathol. 28, 221–227. doi: 10.1080/07060660609507378

CrossRef Full Text | Google Scholar

Wolińska, A., Frąc, M., Oszust, K., Szafranek-Nakonieczna, A., Zielenkiewicz, U., and Stêpniewska, Z. (2017). Microbial biodiversity of meadows under different modes of land use: catabolic and genetic fingerprinting. World J. Microbiol. Biotechnol. 33:154. doi: 10.1007/s11274-017-2318-2

PubMed Abstract | CrossRef Full Text | Google Scholar

Yang, T., Adams, J. M., Shi, Y., He, J., Jing, X., Chen, L., et al. (2017). Soil fungal diversity in natural grasslands of the Tibetan Plateau: associations with plant diversity and productivity. New Phytol. 215, 756–765. doi: 10.1111/nph.14606

PubMed Abstract | CrossRef Full Text | Google Scholar

Zhou, J., Jiang, X., Zhou, B., Zhao, B., Ma, M., Guan, D., et al. (2016). Thirty four years of nitrogen fertilization decreases fungal diversity and alters fungal community composition in black soil in northeast China. Soil Biol. Biochem. 95, 135–143. doi: 10.1016/j.soilbio.2015.12.012

CrossRef Full Text | Google Scholar

Žifčáková, L., Vetrovský, T., Howe, A., and Baldrian, P. (2016). Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter. Environ. Microbiol. 18, 288–301. doi: 10.1111/1462-2920.13026

PubMed Abstract | CrossRef Full Text | Google Scholar

Keywords: soil health, soil ecosystem, microbial communities, fungal diversity, fungal functions, fungal plant pathogens, soil biology, soil mycobiome

Citation: Frąc M, Hannula SE, Bełka M and Jędryczka M (2018) Fungal Biodiversity and Their Role in Soil Health. Front. Microbiol. 9:707. doi: 10.3389/fmicb.2018.00707

Received: 30 September 2017; Accepted: 27 March 2018;
Published: 13 April 2018.

Edited by:

Mohamed Hijri, Université de Montréal, Canada

Reviewed by:

Mariusz Cycoń, Medical University of Silesia, Poland
Bořivoj Šarapatka, Palacký University, Czechia

Copyright © 2018 Frąc, Hannula, Bełka and Jędryczka. 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 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: Małgorzata Jędryczka, mjed@igr.poznan.pl

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