Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Dimensions of biodiversity in the Earth mycobiome

Nature Reviews Microbiology volume 14, pages 434–447 (2016)Cite this article

Subjects

Key Points

  • Fungi have crucial ecological roles — as microbial saprotrophs, pathogens and mutualists — in both terrestrial and aquatic ecosystems.

  • Advances in DNA sequencing have facilitated the ecological exploration of the 'mycobiome' and begun to change our view of fungal taxonomic and functional diversity.

  • Molecular-based work has shown that fungal communities are more diverse than previously known across a range of spatial scales, from the diversity of local communities to biogeographical differences across continents.

  • In contrast with earlier ideas, mycobiome studies have suggested that dispersal has an important role in both local community assembly and in generating large-scale biogeographical diversity patterns.

  • The identification of key functional traits is helping to make predictions about the newly discovered diversity of the mycobiome and decode its role in the health of plants, animals and ecosystems.

Abstract

Fungi represent a large proportion of the genetic diversity on Earth and fungal activity influences the structure of plant and animal communities, as well as rates of ecosystem processes. Large-scale DNA-sequencing datasets are beginning to reveal the dimensions of fungal biodiversity, which seem to be fundamentally different to bacteria, plants and animals. In this Review, we describe the patterns of fungal biodiversity that have been revealed by molecular-based studies. Furthermore, we consider the evidence that supports the roles of different candidate drivers of fungal diversity at a range of spatial scales, as well as the role of dispersal limitation in maintaining regional endemism and influencing local community assembly. Finally, we discuss the ecological mechanisms that are likely to be responsible for the high heterogeneity that is observed in fungal communities at local scales.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Functional diversity of the mycobiome.
Figure 2: Biogeography and emerging views of fungal diversity.
Figure 3: Community assembly and historical contingency.
Figure 4: Deconstructing structure–function relationships in fungal communities.

Similar content being viewed by others

References

  1. Arnold, A. E., Maynard, Z., Gilbert, G. S., Coley, P. D. & Kursar, T. A. Are tropical fungal endophytes hyperdiverse? Ecol. Lett. 3, 267–274 (2000).

    Google Scholar 

  2. Findley, K. et al. Topographic diversity of fungal and bacterial communities in human skin. Nature 498, 367–370 (2013). The first in-depth NGS study of the human mycobiome, which demonstrates substantial differences between the distribution of bacteria and fungi.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Talbot, J. M. et al. Endemism and functional convergence across the North American soil mycobiome. Proc. Natl Acad. Sci. USA 111, 6431–6346 (2014). This study contrasts regional differences in the composition of fungal species with the convergent production of extracellular enzymes, as evidence for high functional redundancy.

    Google Scholar 

  4. Tedersoo, L. et al. Global diversity and geography of soil fungi. Science 346, 1256688 (2014). The first global survey to show strong biogeographical patterns and variable latitudinal diversity gradients in fungi.

    PubMed  Google Scholar 

  5. Pion, M. et al. Bacterial farming by the fungus Morchella crassipes. Proc. Biol. Sci. 280, 20132242 (2013).

    PubMed  PubMed Central  Google Scholar 

  6. Remy, W., Taylor, T. N., Hass, H. & Kerp, H. Four-hundred-million-year-old vesicular arbuscular mycorrhizae. Proc. Natl Acad. Sci. USA 91, 11841–11843 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Floudas, D. et al. The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336, 1715–1719 (2012).

    CAS  PubMed  Google Scholar 

  8. Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323–329 (2006).

    CAS  PubMed  Google Scholar 

  9. Hohl, T. M., Rivera, A. & Pamer, E. G. Immunity to fungi. Curr. Opin. Immunol. 18, 465–472 (2006).

    CAS  PubMed  Google Scholar 

  10. Eastwood, D. C. et al. The plant cell wall-decomposing machinery underlies the functional diversity of forest fungi. Science 333, 762–765 (2011).

    CAS  PubMed  Google Scholar 

  11. Bagchi, R. et al. Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature 506, 85–88 (2014). This paper demonstrates the importance of fungal pathogens in maintaining the diversity of tropical rainforest trees.

    CAS  PubMed  Google Scholar 

  12. Taylor, J. W. & Berbee, M. L. Dating divergences in the Fungal Tree of Life: review and new analyses. Mycologia 98, 838–849 (2006).

    PubMed  Google Scholar 

  13. Treseder, K. K. & Lennon, J. T. Fungal traits that drive ecosystem dynamics on land. Microbiol. Mol. Biol. Rev. 79, 243–262 (2015). A study that identifies key functional traits for fungi and shows how they can be correlated with important ecological processes.

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Kittelmann, S. et al. Simultaneous amplicon sequencing to explore co-occurrence patterns of bacterial, archaeal and eukaryotic microorganisms in rumen microbial communities. PLoS ONE 8, e47879 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Herrera, C. M., Canto, A., Pozo, M. I. & Bazaga, P. Inhospitable sweetness: nectar filtering of pollinator-borne inocula leads to impoverished, phylogenetically clustered yeast communities. Proc. Biol. Sci. 277, 747–754 (2009).

    PubMed  PubMed Central  Google Scholar 

  16. Bass, D. et al. Yeast forms dominate fungal diversity in the deep oceans. Proc. Biol. Sci. 274, 3069–3077 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Zimmerman, N. B. & Vitousek, P. M. Fungal endophyte communities reflect environmental structuring across a Hawaiin landscape. Proc. Natl Acad. Sci. USA 109, 13022–13027 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Boddy, L. Saprotrophic cord-forming fungi: meeting the challenge of heterogeneous environments. Mycologia 91, 13–32 (1999).

    Google Scholar 

  19. Smith, M. L., Bruhn, J. N. & Anderson, J. B. The fungus Armillaria bulbosa is among the largest and oldest living organisms. Nature 356, 428–431 (1992).

    Google Scholar 

  20. Cosgrove, L., McGeechan, P. L., Robson, G. D. & Handley, P. S. Fungal communities associated with degradation of polyester polyurethane in soil. Appl. Environ. Microbiol. 73, 5817–5824 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Peay, K. G. Back to the future: natural history and the way forward in modern fungal ecology. Fungal Ecol. 12, 4–9 (2014).

    Google Scholar 

  22. Prosser, J. I. Dispersing misconceptions and identifying opportunities for the use of 'omics' in soil microbial ecology. Nat. Rev. Microbiol. 13, 439–446 (2015).

    CAS  PubMed  Google Scholar 

  23. Richards, T. A., Jones, M. D., Leonard, G. & Bass, D. Marine fungi: their ecology and molecular diversity. Ann. Rev. Mar. Sci. 4, 495–522 (2012).

    PubMed  Google Scholar 

  24. Qin, J. et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59–65 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Baldrian, P. et al. Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. ISME J. 6, 248–258 (2012).

    CAS  PubMed  Google Scholar 

  26. Smith, D. & Peay, K. Sequence depth, not PCR replication, improves ecological inference from next-generation DNA sequencing. PLoS ONE 9, e90234 (2014).

    PubMed  PubMed Central  Google Scholar 

  27. de Boer, W., Folman, L. B., Summerbell, R. C. & Boddy, L. Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol. Rev. 29, 795–811 (2005).

    CAS  Google Scholar 

  28. Bahram, M., Polme, S., Koljalg, U. & Tedersoo, L. A single European aspen (Populus tremula) tree individual may potentially harbour dozens of Cenococcum geophilum ITS genotypes and hundreds of species of ectomycorrhizal fungi. FEMS Microbiol. Ecol. 75, 313–320 (2011).

    CAS  PubMed  Google Scholar 

  29. Toju, H., Guimaraes, P. R., Olesen, J. M. & Thompson, J. N. Assembly of complex plant–fungus networks. Nat. Commun. 5, 5273 (2014).

    CAS  PubMed  Google Scholar 

  30. Jones, M. D. M. et al. Discovery of novel intermediate forms redefines the fungal tree of life. Nature 474, 200–203 (2011).

    CAS  PubMed  Google Scholar 

  31. Amend, A. S., Barshis, D. J. & Oliver, T. A. Coral-associated marine fungi form novel lineages and heterogeneous assemblages. ISME J. 6, 1291–1301 (2012).

    CAS  PubMed  Google Scholar 

  32. Amend, A. S. From dandruff to deep-sea vents: Malassezia-like fungi are ecologically hyper-diverse. PLoS Pathog. 10, e1004277 (2014).

    PubMed  PubMed Central  Google Scholar 

  33. Ghannoum, M. A. et al. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PloS Pathog. 6, e1000713 (2010).

    PubMed  PubMed Central  Google Scholar 

  34. Bisby, G. R. Geographical distribution of fungi. Bot. Rev. 9, 466–482 (1943).

    Google Scholar 

  35. Berkeley, M. J. in the Gardeners' Chronicle & Agricultural Gazette (London, 1863).

    Google Scholar 

  36. Baas-Becking, L. G. M. Geobiologie of inleiding tot de milieukunde (in Dutch) (W. P. van Stockum and Zoon, 1934).

    Google Scholar 

  37. Smith, M. E. et al. The ectomycorrhizal fungal community in a Neotropical forest dominated by the endemic dipterocarp Pakaraimaea dipterocarpacea. PLoS ONE 8, e55160 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Peay, K. G. et al. Lack of host specificity leads to independent assortment of dipterocarps and ectomycorrhizal fungi across a soil fertility gradient. Ecol. Lett. 18, 807–816 (2015).

    PubMed  Google Scholar 

  39. Bonito, G. et al. Historical biogeography and diversification of truffles in the Tuberaceae and their newly identified southern hemisphere sister lineage. PLoS ONE 8, e52765 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Peay, K. G., Schubert, M. G., Nguyen, N. H. & Bruns, T. D. Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol. Ecol. 16, 4122–4136 (2012).

    Google Scholar 

  41. Meiser, A., Balint, M. & Schmitt, I. Meta-analysis of deep-sequenced fungal communities indicates limited taxon sharing between studies and the presence of biogeographic patterns. New Phytol. 201, 623–635 (2014).

    CAS  PubMed  Google Scholar 

  42. Kõljalg, U. et al. Towards a unified paradigm for sequence-based identification of fungi. Mol. Ecol. 22, 5271–5277 (2013).

    PubMed  Google Scholar 

  43. Grantham, N. S. et al. Fungi identify the geographic origin of dust samples. PLoS ONE 10, e0122605 (2015).

    PubMed  PubMed Central  Google Scholar 

  44. Geml, J. in Biogeography of Microscopic Organisms: Is Everything Small Everywhere? (ed. Fontaneto, D.) (Cambridge Univ. Press, 2011).

    Google Scholar 

  45. Gibbons, S. M. et al. Evidence for a persistent microbial seedbank throughout the global ocean. Proc. Natl Acad. Sci. USA 110, 4651–4655 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Vincenot, L. et al. Extensive gene flow over Europe and possible speciation over Eurasia in the ectomycorrhizal basidiomycete Laccaria amethystina complex. Mol. Ecol. 21, 281–299 (2012).

    CAS  PubMed  Google Scholar 

  47. Davison, J. et al. Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349, 970–973 (2015).

    CAS  PubMed  Google Scholar 

  48. Bruns, T. D. & Taylor, J. W. Comment on “Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism”. Science 351, 826–826 (2016).

    CAS  PubMed  Google Scholar 

  49. Salgado-Salazar, C., Rossman, A. Y. & Chaverri, P. Not as ubiquitous as we thought: taxonomic crypsis, hidden diversity and cryptic speciation in the cosmopolitan fungus Thelonectria discophora (Nectriaceae, Hypocreales, Ascomycota). PLoS ONE 8, e76737 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Branco, S. et al. Genetic isolation between two recently diverged populations of a symbiotic fungus. Mol. Ecol. 24, 2747–2758 (2015).

    CAS  PubMed  Google Scholar 

  51. Matheny, P. B. et al. Out of the Palaeotropics? Historical biogeography and diversification of the cosmopolitan ectomycorrhizal mushroom family Inocybaceae. J. Biogeogr. 36, 577–592 (2009).

    Google Scholar 

  52. Sánchez-Ramírez, S., Tulloss, R. E., Amalfi, M., Moncalvo, J. M. & Carine, M. Palaeotropical origins, boreotropical distribution and increased rates of diversification in a clade of edible ectomycorrhizal mushrooms (Amanita section Caesareae). J. Biogeogr. 42, 351–363 (2015).

    Google Scholar 

  53. Moncalvo, J. M. & Buchanan, P. K. Molecular evidence for long distance dispersal across the Southern Hemisphere in the Ganoderma applanatum-australe species complex (Basidiomycota). Mycol. Res. 112, 425–436 (2008).

    CAS  PubMed  Google Scholar 

  54. Murat, C. et al. Polymorphism at the ribosomal DNA ITS and its relation to postglacial re-colonization routes of the Perigord truffle Tuber melanosporum. New Phytol. 164, 401–411 (2004).

    CAS  PubMed  Google Scholar 

  55. Kennedy, P. G., Garibay-Orijel, R., Higgins, L. M. & Angeles-Arguiz, R. Ectomycorrhizal fungi in Mexican Alnus forests support the host co-migration hypothesis and continental-scale patterns in phylogeography. Mycorrhiza 21, 559–568 (2011).

    PubMed  Google Scholar 

  56. Gaston, K. J. Global patterns in biodiversity. Nature 405, 220–227 (2000).

    CAS  PubMed  Google Scholar 

  57. MacArthur, R. H. & Wilson, E. O. The Theory of Island Biogeography (Princeton Univ. Press, 1967).

    Google Scholar 

  58. Amend, A., Samson, R., Seifert, K. & Bruns, T. Indoor fungal composition is geographically patterned and more diverse in temperate zones than in the tropics. Proc. Natl Acad. Sci. USA 107, 13748–13753 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Gilbert, G. S. & Webb, C. O. Phylogenetic signal in plant pathogen–host range. Proc. Natl Acad. Sci. USA 104, 4979–4983 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Kennedy, P. G., Izzo, A. D. & Bruns, T. D. There is high potential for the formation of common mycorrhizal networks between understorey and canopy trees in a mixed evergreen forest. J. Ecol. 91, 1071–1080 (2003).

    Google Scholar 

  61. Peay, K., Kennedy, P., Davies, S., Tan, S. & Bruns, T. Potential link between plant and fungal distributions in a dipterocarp rainforest: community and phylogenetic structure of tropical ectomycorrhizal fungi across a plant and soil ecotone. New Phytol. 185, 529–542 (2010).

    CAS  PubMed  Google Scholar 

  62. Crowther, T. W. et al. Untangling the fungal niche: the trait-based approach. Front. Microbiol. 5, 579 (2014).

    PubMed  PubMed Central  Google Scholar 

  63. Gilbert, G. S., Reynolds, D. R. & Bethancourt, A. The patchiness of epifoliar fungi in tropical forests: Host range, host abundance, and environment. Ecology 88, 575–581 (2007).

    PubMed  Google Scholar 

  64. Pellissier, L. et al. Soil fungal communities of grasslands are environmentally structured at a regional scale in the Alps. Mol. Ecol. 23, 4274–4290 (2014).

    CAS  PubMed  Google Scholar 

  65. Lindahl, B. D. et al. Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol. 173, 611–620 (2007).

    CAS  PubMed  Google Scholar 

  66. He, L., Liu, F., Karuppiah, V., Ren, Y. & Li, Z. Comparisons of the fungal and protistan communities among different marine sponge holobionts by pyrosequencing. Microb. Ecol. 67, 951–961 (2014).

    PubMed  Google Scholar 

  67. Tisthammer, K., Cobian, G. M. & Amend, A. S. Global biogeography of marine fungi is shapted by the environment. Fungal Ecol. 19, 39–46 (2016).

    Google Scholar 

  68. Coince, A. et al. Leaf and root-associated fungal assemblages do not follow similar elevational diversity patterns. PLoS ONE 9, e100668 (2014).

    PubMed  PubMed Central  Google Scholar 

  69. Parrent, J. L., Morris, W. F. & Vilgalys, R. CO2-enrichment and nutrient availability alter ectomycorrhizal fungal communities. Ecology 87, 2278–2287 (2006).

    PubMed  Google Scholar 

  70. Kennedy, P. G. & Bruns, T. D. Priority effects determine the outcome of ectomycorrhizal competition between two Rhizopogon species colonizing Pinus muricata seedlings. New Phytol. 166, 631–638 (2005).

    PubMed  Google Scholar 

  71. Fukami, T. et al. Assembly history dictates ecosystem functioning: evidence from wood decomposer communities. Ecol. Lett. 13, 675–684 (2010).

    PubMed  Google Scholar 

  72. Dickie, I. A., Fukami, T., Wilkie, J. P., Allen, R. B. & Buchanan, P. K. Do assembly history effects attenuate from species to ecosystem properties? A field test with wood inhabiting fungi. Ecol. Lett. 15, 133–141 (2012).

    PubMed  Google Scholar 

  73. Sterkenburg, E., Bahr, A., Brandström Durling, M., Clemmensen, K. E. & Lindahl, B. D. Changes in fungal communities along a boreal forest soil fertility gradient. New Phytol. 207, 1145–1158 (2015).

    PubMed  Google Scholar 

  74. Koide, R. T., Fernandez, C. & Malcolm, G. Determining place and process: functional traits of ectomycorrhizal fungi that affect both community structure and ecosystem function. New Phytol. 201, 433–439 (2014).

    PubMed  Google Scholar 

  75. Lilleskov, E. A., Hobbie, E. A. & Fahey, T. J. Ectomycorrhizal fungal taxa differing in response to nitrogen deposition also differ in pure culture organic nitrogen use and natural abundance of nitrogen isotopes. New Phytol. 154, 219–231 (2002).

    CAS  Google Scholar 

  76. Kohler, A. et al. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat. Genet. 47, 410–415 (2015). This paper illustrates the potential of using comparative genomics to identify the key evolutionary pressures and traits that are associated with fungal guilds.

    CAS  PubMed  Google Scholar 

  77. Ohm, R. A. et al. Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathog. 8, e1003037 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Riley, R. et al. Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. Proc. Natl Acad. Sci. USA 111, 9923–9928 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Talbot, J. M., Allison, S. D. & Treseder, K. K. Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct. Ecol. 22, 955–963 (2008).

    Google Scholar 

  80. Lindahl, B. D. & Tunlid, A. Ectomycorrhizal fungi — potential organic matter decomposers, yet not saprotrophs. New Phytol. 205, 1443–1447 (2015).

    CAS  PubMed  Google Scholar 

  81. Rineau, F. et al. Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus. ISME J. 7, 2010–2022 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Talbot, J. & Treseder, K. Controls over mycorrhizal uptake of organic nitrogen. Pedobiologia 53, 169–179 (2010).

    CAS  Google Scholar 

  83. Talbot, J. M., Martin, F., Kohler, A., Henrissat, B. & Peay, K. G. Functional guild classification predicts the enzymatic role of fungi in litter and soil biogeochemistry. Soil Biol. Biochem. 88, 441–456 (2015).

    CAS  Google Scholar 

  84. Burke, D. J., Smemo, K. A. & Hewins, C. R. Ectomycorrhizal fungi isolated from old-growth northern hardwood forest display variability in extracellular enzyme activity in the presence of plant litter. Soil Biol. Biochem. 68, 219–222 (2014).

    CAS  Google Scholar 

  85. Rineau, F. et al. The ectomycorrhizal fungus Paxillus involutus converts organic matter in plant litter using a trimmed brown-rot mechanism involving Fenton chemistry. Environ. Microbiol. 14, 1477–1487 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Shah, F. et al. Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors. New Phytol. 209, 1705–1719 (2016).

    CAS  PubMed  Google Scholar 

  87. Arnold, A. E. et al. Fungal endophytes limit pathogen damage in a tropical tree. Proc. Natl Acad. Sci. USA 100, 15649–15654 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Clay, K., Holah, J. & Rudgers, J. A. Herbivores cause a rapid increase in hereditary symbiosis and alter plant community composition. Proc. Natl Acad. Sci. USA 102, 12465–12470 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Marquez, L. M., Redman, R. S., Rodriguez, R. J. & Roossinck, M. J. A virus in a fungus in a plant: three-way symbiosis required for themal tolerance. Science 315, 513–515 (2007).

    CAS  PubMed  Google Scholar 

  90. Busby, P. E. et al. Leaf endophytes and Populus genotype affect severity of damage from the necrotrophic leaf pathogen, Drepanopeziza populi. Ecosphere 4, 1–12 (2013).

    Google Scholar 

  91. Busby, P. E., Peay, K. G. & Newcombe, G. Common foliar fungi of Populus trichocarpa modify Melampsora rust disease severity. New Phytol. 209, 1681–1692 (2015).

    PubMed  Google Scholar 

  92. Parfitt, D., Hunt, J., Dockrell, D., Rogers, H. J. & Boddy, L. Do all trees carry the seeds of their own destruction? PCR reveals numerous wood decay fungi latently present in sapwood of a wide range of angiosperm trees. Fungal Ecol. 3, 338–346 (2010).

    Google Scholar 

  93. Fukami, T., Bezemer, T. M., Mortimer, S. R. & van der Putten, W. H. Species divergence and trait convergence in experimental plant community assembly. Ecol. Lett. 8, 1283–1290 (2005).

    Google Scholar 

  94. Bodeker, I. T. et al. Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems. New Phytol. 203, 245–256 (2014).

    PubMed  Google Scholar 

  95. Talbot, J. M. et al. Independent roles of ectomycorrhizal and saprotrophic communities in soil organic matter decomposition. Soil Biol. Biochem. 57, 282–291 (2013).

    CAS  Google Scholar 

  96. Moeller, H. V., Peay, K. G. & Fukami, T. Ectomycorrhizal fungal traits reflect environmental conditions along a coastal California edaphic gradient. FEMS Microbiol. Ecol. 87, 797–806 (2014).

    CAS  PubMed  Google Scholar 

  97. Tedersoo, L., Sadam, A., Zambrano, M., Valencia, R. & Bahram, M. Low diversity and high host preference of ectomycorrhizal fungi in Western Amazonia, a neotropical biodiversity hotspot. ISME J. 4, 465–471 (2010).

    PubMed  Google Scholar 

  98. Smith, M. E., Henkel, T., Aime, M. C., Fremier, A. K. & Vilgalys, R. Ectomycorrhizal fungal diversity and community structure on three co-occurring leguminous canopy tree species in a Neotropical rainforest. New Phytol. 192, 699–712 (2011).

    PubMed  Google Scholar 

  99. Strickland, M. S. & Rousk, J. Considering fungal:bacterial dominance in soils — methods, controls, and ecosystem implications. Soil Biol. Biochem. 42, 1385–1395 (2010).

    CAS  Google Scholar 

  100. Rousk, J., Brookes, P. C. & Baath, E. Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl. Environ. Microbiol. 75, 1589–1596 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Peay, K., Dickie, I., Wardle, D., Bellingham, P. & Fukami, T. Rat invasion of islands alters fungal community structure, but not wood decomposition rates. Oikos 122, 258–264 (2012).

    Google Scholar 

  102. Hanson, C. A., Fuhrman, J. A., Horner-Devine, M. C. & Martiny, J. B. Beyond biogeographic patterns: processes shaping the microbial landscape. Nat. Rev. Microbiol. 10, 497–506 (2012).

    CAS  PubMed  Google Scholar 

  103. Martiny, J. B. H. et al. Microbial biogeography: putting microorganisms on the map. Nat. Rev. Microbiol. 4, 102–112 (2006).

    CAS  PubMed  Google Scholar 

  104. Fierer, N. & Jackson, R. B. The diversity and biogeography of soil bacterial communities. Proc. Natl Acad. Sci. USA 103, 626–631 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Lozupone, C. A. & Knight, R. Global patterns in bacterial diversity. Proc. Natl Acad. Sci. USA 104, 11436–11440 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  106. Rama, T. et al. Fungi ahoy! Diversity on marine wooden substrata in the high North. Fungal Ecol. 8, 46–58 (2014).

    Google Scholar 

  107. Hinchliff, C. E. et al. Synthesis of phylogeny and taxonomy into a comprehensive tree of life. Proc. Natl Acad. Sci. USA 112, 12764–12769 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  108. Costello, E. K. et al. Bacterial community variation in human body habitats across space and time. Science 326, 1694–1697 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  109. Brown, S. P. & Jumpponen, A. Contrasting primary successional trajectories of fungi and bacteria in retreating glacier soils. Mol. Ecol. 23, 481–497 (2014).

    PubMed  Google Scholar 

  110. Martiny, J. B. H., Eisen, J. A., Penn, K., Allison, S. D. & Horner-Devine, M. C. Drivers of bacterial β-diversity depend on spatial scale. Proc. Natl Acad. Sci. USA 108, 7850–7854 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. Polme, S. et al. Biogeography of ectomycorrhizal fungi associated with alders (Alnus spp.) in relation to biotic and abiotic variables at the global scale. New Phytol. 198, 1239–1249 (2013).

    CAS  PubMed  Google Scholar 

  112. Polme, S., Bahram, M., Koljalg, U. & Tedersoo, L. Global biogeography of Alnus-associated Frankia actinobacteria. New Phytol. 204, 979–988 (2014).

    PubMed  Google Scholar 

  113. Schoch, C. L. et al. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc. Natl Acad. Sci. USA 109, 6241–6246 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Hawksworth, D. The fungal dimension of biodiversity — magnitude, significance and conservation. Mycol. Res. 95, 641–655 (1991).

    Google Scholar 

  115. Taylor, D. L. et al. A first comprehensive census of fungi in soil reveals both hyperdiversity and fine-scale niche partitionning. Ecol. Monographs 84, 3–20 (2014).

    Google Scholar 

  116. May, R. A fondness for fungi. Nature 352, 475–476 (1991).

    Google Scholar 

  117. Prober, S. M. et al. Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecol. Lett. 18, 85–95 (2015).

    PubMed  Google Scholar 

  118. Fisher, M. C. et al. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194 (2012).

    CAS  PubMed  Google Scholar 

  119. Cui, L., Morris, A. & Ghedin, E. The human mycobiome in health and disease. Genome Med. 5, 63 (2013).

    PubMed  PubMed Central  Google Scholar 

  120. Huffnagle, G. B. & Noverr, M. C. The emerging world of the fungal microbiome. Trends Microbiol. 21, 334–341 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  121. Dowd, S. E. et al. Survey of fungi and yeast in polymicrobial infections in chronic wounds. J. Wound Care 20, 40–47 (2011).

    CAS  PubMed  Google Scholar 

  122. Nguyen, L. D. N., Viscogliosi, E. & Delhaes, L. The lung mycobiome: an emerging field of the human respiratory microbiome. Front. Microbiol. 6, 89 (2015).

    PubMed  PubMed Central  Google Scholar 

  123. Yafetto, L. et al. The fastest flights in nature: high speed spore discharge mechanisms among fungi. PLoS ONE 3, e3237 (2008).

    PubMed  PubMed Central  Google Scholar 

  124. Ingold, C. T. Fungal Spores: Their Liberation and Dispersal (Clarendon, 1971).

    Google Scholar 

  125. Norros, V., Penttilä, R., Suominen, M. & Ovaskainen, O. Dispersal may limit the occurrence of specialist wood decay fungi already at small spatial scales. Oikos 121, 961–974 (2012).

    Google Scholar 

  126. Peay, K. G. & Bruns, T. D. Spore dispersal of basidiomycete fungi at the landscape scale is driven by stochastic and deterministic processes and generates variability in plant–fungal interactions. New Phytol. 204, 180–191 (2014).

    PubMed  Google Scholar 

  127. Brown, J. K. M. & Hovmoller, M. S. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297, 537–541 (2002).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This manuscript was greatly improved by comments from A. Amend, B. Lindahl, N. Fierer, K. Treseder, J. Martiny and L. Tedersoo. K.G.P. received financial support from the US National Science Foundation (NSF) Division of Environmental Biology (DEB; grants 1249341 and 1249342).

Author information

Authors and Affiliations

  1. Department of Biology, Stanford University, Stanford, 94305, California, USA

    Kabir G. Peay

  2. Department of Plant Biology, University of Minnesota,

    Peter G. Kennedy

  3. Department of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, 55108, Minnesota, USA

    Peter G. Kennedy

  4. Department of Biology, Boston University, Boston, 02215, Massachusetts, USA

    Jennifer M. Talbot

Authors
  1. Kabir G. Peay
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter G. Kennedy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jennifer M. Talbot
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kabir G. Peay.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information S1 (table)

Supplementary information (XLS 57 kb)

Supplementary information S2 (box)

Supplemental Methods (PDF 195 kb)

PowerPoint slides

Glossary

Next-generation sequencing

(NGS). A set of DNA-sequencing platforms (including those produced by 454 and Illumina) that have increased sequencing output and decreased cost by orders of magnitude compared with Sanger sequencing.

Monophyletic

A group of organisms that consists of an ancestor and all of its descendants. Monophyly is the basis for modern taxonomy.

Osmotrophs

Organisms that rely on the uptake of dissolved organic compounds for their primary nutrition.

Chitin

A polymer of N-acetylglucosamine that is an important component of fungal cell walls.

Basidiomycota

One of the major phyla of the fungal kingdom, which includes some of the most dominant fungal species in natural systems and many key ectomycorrhizal and wood-decomposing taxa. Most fungal species that produce prominent mushrooms are from the Basidiomycota.

Mycorrhizal fungi

Fungi that are in symbiotic associations with plant roots, based on the exchange of photosynthates for soil nutrients, such as nitrogen and phosphorous.

Endophytic fungi

Fungi that live asymptomatically inside plant tissue.

Ectomycorrhizal fungi

Fungi engaged in a common form of mycorrhizal symbiosis that is characterized anatomically by fungal hyphae that wholly enclose the fine roots of the host. Ectomycorrhizal fungi evolved from several different lineages and many retain the decomposing abilities of their saprotrophic ancestors.

Ascomycota

One of the major phyla of the fungal kingdom. Some of the most dominant fungi in natural systems are found in this phylum, including many agriculturally important pathogens and most fungi that form lichen.

Rusts

A group of plant pathogens that are obligate biotrophs characterized by complex life cycles that involve several plant hosts. Rusts infect many agriculturally important crops, such as coffee, soybean and wheat, producing reddish-brown spores that give infected hosts the appearance of being rusty.

Glomeromycota

The phylum to which all arbuscular mycorrhizal fungi belong.

Ericoid mycorrhizal fungi

Fungi in a mycorrhizal symbiosis with certain members of the plant family Ericaceae that is characterized by the penetration of hair root cells and the formation of hyphal coils. Ericoid mycorrhizal fungi include diverse species from the Basidiomycota and Ascomycota phyla.

Gondwanan

Arising from Gondwana, the supercontinent that broke up approximately 180 million years ago and included parts of present day South America, Australia, New Zealand and Antarctica.

Cosmopolitan

In ecology, a very wide geographical distribution, often across several continents. Cosmopolitan taxa frequently traverse large dispersal barriers, such as oceans or mountains.

Endemism

In ecology, a restricted geographical distribution. Endemism can occur at a range of spatial scales, from a single lake or mountainside, to a continent.

Saprotroph

An organism that obtains nutrition from dead organic matter.

Arbuscular mycorrhizal fungi

Fungi in arbuscular mycorrhizal symbiosis with a plant host, which is the most common form of mycorrhizal symbiosis and is characterized by fungal hyphae that penetrate plant cell walls, where they form highly branched structures known as arbuscules. Arbuscular mycorrhizal fungi belong to a single monopyhyletic lineage and evolved with the earliest land plants.

Phylogeographical

Pertaining to the patterns of geographical distribution of phylogenetic lineages.

Beringia

An area of land that includes parts of present day Russia and Alaska and that formed a bridge connecting Asia and North America during the lower sea levels of the Pleistocene glacial periods.

Evapotranspiration

The sum of evaporation from the surface of the earth and plant transpiration.

Historical contingency

When the current state of an ecological community depends on the precise sequence of prior events. Historical contingency is contrasted with determinism, in which a single end state will occur regardless of past events.

Propagules

Any biological unit that is capable of propagating an organism in a new location. For fungi this may include sexual and asexual spores, as well as hyphal fragments.

Forest stands

A contiguous area of forest in which a characteristic species composition and demography enables it to be distinguished from other areas of forest.

Guilds

Groups of species that use similar ecological strategies to exploit a common resource. Species are grouped into guilds irrespective of whether they are taxonomically related.

White rot

Historic classification of certain wood-decomposing fungi. The classification is based on the white colour of the wood that is generated by the enrichment of cellulose that occurs when powerful oxidative enzymes that are produced by these fungi breakdown lignin.

Brown rot

Historic classification of certain wood-decomposing fungi. The classification is based on the brown colour of the wood that is generated by the ability of these fungi to extract polysaccharides while leaving behind lignin.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Peay, K., Kennedy, P. & Talbot, J. Dimensions of biodiversity in the Earth mycobiome. Nat Rev Microbiol 14, 434–447 (2016). https://doi.org/10.1038/nrmicro.2016.59

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro.2016.59

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing