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Global Diversity and Geography of Soil Fungi

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Global Diversity and Geography of Soil Fungi RESEARCH animals—namely, that species’ latitudinal RESEARCH ARTICLE SUMMARY ranges increase toward the poles (Rapo- port’s rule) and diversity increases toward FUNGAL BIOGEOGRAPHY the equator. Last, we sought group-specific global biogeographic links among major bio- geographic regions and biomes using a net- Global diversity and geography work approach and area-based clustering. of soil fungi RESULTS: Metabarcoding analysis of global soils revealed fungal richness esti- Leho Tedersoo,*† Mohammad Bahram,† Sergei Põlme, Urmas Kõljalg, Nourou S. Yorou, mates approaching the number of species Ravi Wijesundera, Luis Villarreal Ruiz, Aída M. Vasco-Palacios, Pham Quang Thu, recorded to date. Distance from equator Ave Suija, Matthew E. Smith, Cathy Sharp, Erki Saluveer, Alessandro Saitta, and mean annual precipitation had the Miguel Rosas, Taavi Riit, David Ratkowsky, Karin Pritsch, Kadri Põldmaa, strongest effects on rich- Meike Piepenbring, Cherdchai Phosri, Marko Peterson, Kaarin Parts, Kadri Pärtel, ON OUR WEB SITE ness of fungi, including Eveli Otsing, Eduardo Nouhra, André L. Njouonkou, R. Henrik Nilsson, Luis N. Morgado, Read the full article most fungal taxonomic Jordan Mayor, Tom W. May, Luiza Majuakim, D. Jean Lodge, Su See Lee, at http://dx.doi and functional groups. Karl-Henrik Larsson, Petr Kohout, Kentaro Hosaka, Indrek Hiiesalu, Terry W. Henkel, .org/10.1126/ Diversity of most fun- Helery Harend, Liang-dong Guo, Alina Greslebin, Gwen Grelet, Jozsef Geml, science.1256688 gal groups peaked in Genevieve Gates, William Dunstan, Chris Dunk, Rein Drenkhan, John Dearnaley, tropical ecosystems, but André De Kesel, Tan Dang, Xin Chen, Franz Buegger, Francis Q. Brearley, ectomycorrhizal fungi and several fungal Gregory Bonito, Sten Anslan, Sandra Abell, Kessy Abarenkov classes were most diverse in temperate or boreal ecosystems, and many fungal groups INTRODUCTION: The kingdom Fungi RATIONALE: We identified soil-inhabiting exhibited distinct preferences for specific is one of the most diverse groups of fungi using 454 Life Sciences (Branford, edaphic conditions (such as pH, calcium, organisms on Earth, and they are integral CN) pyrosequencing and through compari- or phosphorus). Consistent with Rapoport’s ecosystem agents that govern soil carbon son against taxonomically and functionally rule, the geographic range of fungal taxa in- cycling, plant nutrition, and pathology. annotated sequence databases. Multiple re- creased toward the poles. Fungal endemicity Fungi are widely distributed in all terres- gression models were used to disentangle was particularly strong in tropical regions, trial ecosystems, but the distribution of the roles of climatic, spatial, edaphic, and but multiple fungal taxa had cosmopolitan species, phyla, and functional groups has floristic parameters on fungal diversity and distribution. been poorly documented. On the basis community composition. Structural equa- of 365 global soil samples from nat- tion models were used to determine the CONCLUSIONS: Climatic factors, followed ural ecosystems, we determined direct and indirect effects of climate by edaphic and spatial patterning, are the the main drivers and biogeo- on fungal diversity, soil chemistry, best predictors of soil fungal richness and graphic patterns of fungal and vegetation. We also exam- community composition at the global scale. diversity and commu- ined whether fungal biogeo- Richness of all fungi and functional groups nity composition. graphic patterns matched is causally unrelated to plant diversity, with p a r a d i g m s d e r i v e d the exception of ectomycorrhizal root symbi- f r o m p l a n t s a n d onts, suggesting that plant-soil feedbacks do not influence the diversity of soil fungi at the global scale. The plant-to-fungi richness ra- tio declined exponentially toward the poles, indicating that current predictions—assum- ing globally constant ratios—overestimate fungal richness by 1.5- to 2.5-fold. Fungi fol- low 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. ■ RELATED ITEMS IN SCIENCE D. A. Wardle and B. D. Lindahl, Disentangling the global mycobiome. Science 346, 1052–1053 (2014). DOI: 10.1126/science.aaa1185 Direct and indirect ef ects of climatic and edaphic variables on plant and fungal richness. Line thickness corresponds to the relative strength of the relationships between the variables The list of author affiliations is available in the full article online. that af ect species richness. Dashed lines indicate negative relationships. MAP, mean annual *Corresponding author. E-mail: [email protected] †These authors contributed equally to this work. precipitation; Fire, time since last f re; Dist. equator, distance from the equator; Ca, soil calcium Cite this article as: L. Tedersoo et al., Science 346, 1256688 concentration; P, soil phosphorus concentration; pH, soil pH. (2014). DOI: 10.1126/science.1256688 1078 28 NOVEMBER 2014 • VOL 346 ISSUE 6213 sciencemag.org SCIENCE Published by AAAS RESEARCH ◥ soils or those with high clay concentrations and RESEARCH ARTICLE hardpans. Third, differences among soil horizons may be masked by other variables across large geographic scales (10). The 40 soil cores taken in FUNGAL BIOGEOGRAPHY each site were pooled, coarse roots and stones were removed, and a subset of the soil was air- dried at <35°C. Dried soil was stored in zip-lock Global diversity and geography plastic bags with silica gel in order to minimize humidity during transit. In the laboratory, we ground dried soil into fine powder using bead of soil fungi beating. We extracted DNA from 2.0 g of soil using 1 † 2† 1 2 Leho Tedersoo, * Mohammad Bahram, Sergei Põlme, Urmas Kõljalg, the PowerMax Soil DNA Isolation kit (MoBio, 3 4 5 6 Nourou S. Yorou, Ravi Wijesundera, Luis Villarreal Ruiz, Aída M. Vasco-Palacios, Carlsbad, CA) following manufacturer’sinstruc- 7 2 8 9 2 Pham Quang Thu, Ave Suija, Matthew E. Smith, Cathy Sharp, Erki Saluveer, tions. We performed polymerase chain reaction 10 11 2 12 13 Alessandro Saitta, Miguel Rosas, Taavi Riit, David Ratkowsky, Karin Pritsch, (PCR) using a mixture of six forward primers (in 2 11 14 2 Kadri Põldmaa, Meike Piepenbring, Cherdchai Phosri, Marko Peterson, equimolar concentration) analogous to ITS3 and Kaarin Parts,2 Kadri Pärtel,2 Eveli Otsing,2 Eduardo Nouhra,15 André L. Njouonkou,16 a degenerate reverse primer analogous to ITS4 R. Henrik Nilsson,17 Luis N. Morgado,18 Jordan Mayor,19 Tom W. May,20 (hereafter referred to as ITS4ngs). We shortened Luiza Majuakim,21 D. Jean Lodge,22 Su See Lee,23 Karl-Henrik Larsson,24 Petr Kohout,2 and modified forward and reverse primers to Kentaro Hosaka,25 Indrek Hiiesalu,2 Terry W. Henkel,26 Helery Harend,2 27 28 29 18 12 Liang-dong Guo, Alina Greslebin, Gwen Grelet, Jozsef Geml, Genevieve Gates, 1Natural History Museum, University of Tartu, Tartu, Estonia. William Dunstan,30 Chris Dunk,19 Rein Drenkhan,31 John Dearnaley,32 André De Kesel,33 2Institute of Ecology and Earth Sciences, University of 3 7 34 13 35 20 Tartu, Tartu, Estonia. Faculté d´Agronomie, Université de Tan Dang, Xin Chen, Franz Buegger, Francis Q. Brearley, Gregory Bonito, 4 2 36 1 Parakou, Parakou, Benin. Department of Plant Sciences, Sten Anslan, Sandra Abell, Kessy Abarenkov University of Colombo, Colombo 3, Sri Lanka. 5Postgrado en Recursos Genéticos y Productividad-Genética, LARGEMBIO, Colegio de Postgraduados–Líneas Prioritarias de Fungi play major roles in ecosystem processes, but the determinants of fungal diversity and 6 biogeographic patterns remain poorly understood. Using DNA metabarcoding data from Investigación 6, México City, Mexico. The Fungal Biodiversity Centre, Centraalbureau voor Schimmelcultures–Royal hundreds of globally distributed soil samples, we demonstrate that fungal richness is decoupled Netherlands Academy of Arts and Sciences, Utrecht, from plant diversity.The plant-to-fungus richness ratio declines exponentially toward the poles. Netherlands. 7Vietnamese Academy of Forest Sciences, Hanoi, Vietnam. 8Department of Plant Pathology, University Climatic factors, followed by edaphic and spatial variables, constitute the best predictors of 9 fungal richness and community composition at the global scale. Fungi show similar latitudinal of Florida, Gainesville, FL, USA. Natural History Museum, Bulawayo, Zimbabwe. 10Department of Agricultural and diversity gradients to other organisms, with several notable exceptions.These findings advance Forest Sciences, Università di Palermo, Palermo, Italy. our understanding of global fungal diversity patterns and permit integration of fungi into a 11Department of Mycology, Goethe University Frankfurt, 12 general macroecological framework. Frankfurt am Main, Germany. Tasmanian Institute of Agriculture, Hobart, Tasmania, Australia. 13Institute of Soil ungi are eukaryotic microorganisms that geographic scales. We used a global data set to Ecology, Helmholtz Zentrum München, Neuherberg, Germany. 14Department of Biology, Nakhon Phanom University, play fundamental ecological roles as decom- disentangle the roles of climatic, edaphic, floris- Nakhon Phanom, Thailand. 15Instituto Multidisciplinario de posers, mutualists, or pathogens of plants tic, and spatial variables governing global-scale Biología Vegetal, Córdoba, Argentina. 16Department of and animals; they drive carbon
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