Global diversity and geography of soil fungi
Assessing fungal diversity worldwide
Fungi are hyperdiverse but poorly known, despite their ecological and economic impacts. Tedersoo et al. collected nearly 15,000 topsoil samples from 365 sites worldwide and sequenced their genomes (see the Perspective by Wardle and Lindahl). Overall, they found a striking decline in fungal species richness with distance from the equator. For some specialist groups though, diversity depended more on the abundance of host plants than host diversity or geography. The findings reveal a huge gap between known and described species and the actual numbers of distinct fungi in the world's soils.
Science, this issue 10.1126/science.1256688; see also p. 1052
Structured Abstract
Introduction
The kingdom Fungi is one of the most diverse groups of organisms on Earth, and they are integral ecosystem agents that govern soil carbon cycling, plant nutrition, and pathology. Fungi are widely distributed in all terrestrial ecosystems, but the distribution of species, phyla, and functional groups has been poorly documented. On the basis of 365 global soil samples from natural ecosystems, we determined the main drivers and biogeographic patterns of fungal diversity and community composition.
Rationale
We identified soil-inhabiting fungi using 454 Life Sciences (Branford, CN) pyrosequencing and through comparison against taxonomically and functionally annotated sequence databases. Multiple regression models were used to disentangle the roles of climatic, spatial, edaphic, and floristic parameters on fungal diversity and community composition. Structural equation models were used to determine the direct and indirect effects of climate on fungal diversity, soil chemistry, and vegetation. We also examined whether fungal biogeographic patterns matched paradigms derived from plants and animals—namely, that species’ latitudinal ranges increase toward the poles (Rapoport’s rule) and diversity increases toward the equator. Last, we sought group-specific global biogeographic links among major biogeographic regions and biomes using a network approach and area-based clustering.
Results
Metabarcoding analysis of global soils revealed fungal richness estimates approaching the number of species recorded to date. Distance from equator and mean annual precipitation had the strongest effects on richness of fungi, including most fungal taxonomic and functional groups. Diversity of most fungal groups peaked in tropical ecosystems, but ectomycorrhizal fungi and several fungal classes were most diverse in temperate or boreal ecosystems, and many fungal groups exhibited distinct preferences for specific edaphic conditions (such as pH, calcium, or phosphorus). Consistent with Rapoport’s rule, the geographic range of fungal taxa increased toward the poles. Fungal endemicity was particularly strong in tropical regions, but multiple fungal taxa had cosmopolitan distribution.
Conclusions
Climatic factors, followed by edaphic and spatial patterning, are the best predictors of soil fungal richness and community composition at the global scale. Richness of all fungi and functional groups is causally unrelated to plant diversity, with the exception of ectomycorrhizal root symbionts, suggesting that plant-soil feedbacks do not influence the diversity of soil fungi at the global scale. The plant-to-fungi richness ratio declined exponentially toward the poles, indicating that current predictions—assuming globally constant ratios—overestimate fungal richness by 1.5- to 2.5-fold. Fungi follow similar biogeographic patterns as plants and animals, with the exception of several major taxonomic and functional groups that run counter to overall patterns. Strong biogeographic links among distant continents reflect relatively efficient long-distance dispersal compared with macro-organisms.
Abstract
Fungi play major roles in ecosystem processes, but the determinants of fungal diversity and biogeographic patterns remain poorly understood. Using DNA metabarcoding data from hundreds of globally distributed soil samples, we demonstrate that fungal richness is decoupled from plant diversity. The plant-to-fungus richness ratio declines exponentially toward the poles. Climatic factors, followed by edaphic and spatial variables, constitute the best predictors of fungal richness and community composition at the global scale. Fungi show similar latitudinal diversity gradients to other organisms, with several notable exceptions. These findings advance our understanding of global fungal diversity patterns and permit integration of fungi into a general macroecological framework.
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Supplementary Material
Summary
Figs. S1 to S17
Tables S1 to S3
Data Files S1 and S2
Resources
References and Notes
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Science
Volume 346 | Issue 6213
28 November 2014
28 November 2014
Copyright
Copyright © 2014, American Association for the Advancement of Science.
Submission history
Received: 29 May 2014
Accepted: 16 October 2014
Published in print: 28 November 2014
Acknowledgments
The sequence data and metadata are deposited in the Short Read Archive (accession SRP043706) and UNITE databases. Data used for analyses are available as supplementary materials, data files S1 and S2. We thank A. Corrales, H. Mann, D. Sveshnikov, F. O. P. Stefani, A. Voitk, and Y. Wu for supplying single soil samples; R. Puusepp, M. Haugas, and M. Nõukas for sample preparation; H. Kreft for providing interpolated plant diversity data; S. Jüris for designing the printed figure; M. I. Bidartondo, K. G. Peay, and three anonymous reviewers for constructive comments on the manuscript; and relevant institutions of multiple countries for issuing permissions for sampling and delivery. The bulk of this project was funded from Estonian Science Foundation grants 9286, 171PUT, and IUT20-30; EMP265; Frontiers in Biodiversity Research; European Research Council; and in part by numerous funding sources that facilitated co-author efforts in collecting and preprocessing samples.
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