Dimensions of biodiversity in the Earth mycobiome

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.

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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.

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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).

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Correspondence to Kabir G. Peay.

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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.

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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

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