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Journal ArticleDOI

Global diversity and geography of soil fungi

28 Nov 2014-Science (American Association for the Advancement of Science)-Vol. 346, Iss: 6213, pp 1256688-1256688
TL;DR: 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 manyfungal groups exhibited distinct preferences for specific edaphic conditions (such as pH, calcium, or phosphorus).
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.

Summary (3 min read)

Introduction

  • Fungi are eukaryotic microorganisms that play fundamental ecological roles as decomposers, mutualists, or pathogens of plants and animals; they drive carbon cycling in forest soils, mediate mineral nutrition of plants, and alleviate carbon limitations of other soil organisms.
  • Such patterns suggest that the distribution of microbes reflects latitudinal variation in ecosystem nutrient dynamics (2) (3) (4) .
  • Richness of nearly all terrestrial and marine macro-organisms is negatively related to increasing latitude (5) -a pattern attributed to the combined effects of climate, niche conservatism, and rates of evolutionary radiation and extinction (6) .
  • Only a few of these biogeographic processes have been demonstrated for fungi at the local scale (9) .
  • Little is known about general patterns of fungal diversity or functional roles over large geographic scales.

Sample preparation

  • The authors collected 40 soil cores from natural communities in each of 365 sites across the world using a uniform sampling protocol (Fig. 1A ; Data S1).
  • Most plots (2500 m 2 ) were circular, but in steep mountain regions and densely forested areas, some plots were oblong.
  • The 40 soil cores taken in each site were pooled, coarse roots and stones removed, and a subset of the soil was air-dried at <35 °C.
  • PCR was performed using a mixture of six forward primers (in equimolar concentration) analogous to ITS3 and a degenerate reverse primer analogous to ITS4 (hereafter referred to as ITS4ngs).
  • Amplicons were purified with Exonuclease I and FastAP thermosensitive alkaline phosphatase enzymes (Thermo Scientific, Pittsburgh, PA USA).

Bioinformatics

  • Pyrosequencing on five half-plates resulted in 2,512,068 reads with a median length of 409 bases.
  • Chimera control was exercised through UCHIME 4.2 (www.drive5.com/uchime/).
  • The longest sequence of each Operational Taxonomic Unit (OTU), based on clustering at 98.0% sequence similarity, was selected as the representative for BLASTn searches (word size=7; penalties: gap=-1; gap extension=-2; match=1) against the International Nucleotide Sequence Databases Collaboration (INSDC: www.insdc.org) and UNITE (unite.ut.ee) databases.
  • For each query, the authors considered the 10 best-matching references to annotate their global sequences as accurately as possible.
  • As a rule, the authors considered evalues of BLASTn search results ˂e -50 reliable to assign sequences to the fungal kingdom, whereas those >e -20 were considered ´unknown´.

Statistical analyses

  • Estimates of the mean annual temperature (MAT), mean annual precipitation (MAP), soil moisture, and soil carbon at 30 arc second resolution were obtained from the WorldClim database (www.worldclim.org).
  • The authors further calculated the ratio of relative plant richness to fungal richness and fitted this ratio with latitude using polynomial functions to test the assumed uniformity of plant-to-fungal richness ratios at the global scale (1, 19, 20) .
  • To obtain coefficients of determination (cumulative R 2 adjusted ) and statistics (F pseudo and P-values) for each variable, components of the best models were forward selected.
  • The authors tested the differences among fungal taxonomic and functional groups for the occurrence frequency (number of sites detected) and latitudinal range of OTUs using a nonparametric Kruskal-Wallis test and Bonferroni-adjusted multiple comparisons among mean ranks.
  • The average latitudinal range was regressed with the latitude of study sites by polynomial model selection based on the AICc criterion.

Results and Discussion

  • The richness of Basidiomycota and its class Agaricomycetes were best explained by a positive response to soil Ca concentration (13.5% and 12.8%, respectively).
  • Spatial predictors were included in the best richness models of nearly all functional and phylogenetic groups (except Glomeromycota), indicating regional-or continental-scale differences in OTU richness (Fig. 1B ).
  • Compared to other tropical regions, richness of fungi was conspicuously lower in Africa, independent of biome type.
  • Among edaphic variables, soil pH and Ca concentration were typically the most important predictors of fungal OTU richness.
  • Ca is important for many physiological processes in plants and microorganisms and it influences the turnover rate of soil organic matter (31) .

Macroecological patterns

  • In general agreement with biogeographic patterns of plants, animals, and foliar endophytic fungi (5, 32) , the overall richness of soil fungi increased towards the equator (Fig. 3A ).
  • All of these phylogenetic groups originated >150 million years ago on the supercontinent Pangaea (33) and have had sufficient time for long-distance dispersal.
  • Adaptation to cold climate in younger fungal phyla has been suggested to explain differential latitudinal preferences among fungal groups (34) .
  • Their global analysis provided no support for this hypothesis (Fig. S9 ).
  • Instead, it revealed that ancient lineages are relatively more common in non-wooded ecosystems.

Relation of plant and fungal richness

  • Plant and fungal richness were positively correlated (Fig. S10 ), but plant richness explained no residual richness of fungi based on the best regression model (R 2 adj <0.01; P>0.05).
  • Strong phylogenetic signals in soil feedbacks, adaptive radiation, and negative density dependence (the Janzen-Connell hypothesis) have probably contributed to the pronounced richness of both plants and their pathogens at low latitudes (36, 37) .
  • The authors found that relative EcM host density had a strong influence on EcM fungal richness, suggesting that greater availability of colonizable roots in soil provides more carbon for EcM fungi and thereby yields greater species density and local-scale richness regardless of latitude.
  • Based on the function of fungi-to-plant richness ratio to latitude and latitudinal distribution of land, the authors calculated that fungal richness is overestimated by 1.5-and 2.5-fold based on constant temperate (45° latitude) and boreal (65° latitude) richness ratios, respectively.
  • Since richness estimates are calculated based on the frequency of the rarest species, the reliability of singleton data call into question biologically meaningful extrapolations (11) .

Community ecology

  • Variation partitioning analysis revealed that climatic, edaphic, and floristic variables (and their shared effects) are the strongest predictors for community composition of all fungi and most of their functional groups (Fig. S11 ).
  • The saprotroph community composition was most strongly explained by purely spatial variables.
  • More specifically, PET and soil pH explained 2.4% and 1.5%, respectively, of the variation in total fungal community composition (Table S3 ; Fig. S12 ).
  • PET contributed 3.8%, 2.8%, and 11.7% to community structure of saprotrophs, plant pathogens, and yeasts, respectively.
  • These results indicate that both environmental and spatial predictors generally have a minor influence on species-level composition of fungi at the global scale.

Global biogeography

  • Consistent with Rapoport's rule formulated for macro-organisms (24) and later applied to marine bacteria (48) , the mean latitudinal range of fungi strongly increased towards the poles (Fig. S13 ).
  • These results also suggest that a greater proportion of fungi are endemic within tropical rather than extra-tropical ecosystems.
  • Animal parasites were more widely distributed compared with all other groups, suggesting that there are many generalist OTUs with global distribution.
  • In spite of the large geographical distance separating them, paleo-and neotropical biogeographic regions clustered together (P=0.059).
  • Co-migration with hosts over Pleistocene land bridges (e.g., Beringia, Wallacea, Panamanian) and longdistance dispersal by spores appear to have played important roles in shaping current fungal distribution patterns (30, 43) .

Conclusions and perspectives

  • Climatic variables explained the greatest proportion of richness and community composition in fungal groups by exhibiting both direct and indirect effects through altered soil and floristic variables.
  • The strong driving climatic forces identified here open up concerns regarding the impact of climate change on the spread of disease (51) and the functional consequences of altered soil microorganism communities (52) .
  • The observed abrupt functional differences between fungal communities in forested and treeless ecosystems, despite spatial juxtaposition, suggests that plant life form and mycorrhizal associations determine soil biochemical processes 29 more than plant species per se.
  • Loss of tree cover and shrub encroachment resulting from drying and warming may thus have a marked impact on ecosystem functioning both aboveand belowground.
  • The authors results highlight how little insight the authors still have into natural microbial distribution patterns, and this undermines their ability to appraise the actual role of humans in shaping these biogeographic processes.

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Content maybe subject to copyright    Report

1
Global diversity and geography of soil fungi
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Leho Tedersoo
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*, Mohammad Bahram
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, Sergei Põlme
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, Urmas Kõljalg
2
, Nourou S. Yorou
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,
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Ravi Wijesundera
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, Luis Villarreal Ruiz
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, Aída M. Vasco-Palacios
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, Pham Quang Thu
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, Ave
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Suija
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, Matthew E. Smith
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, Cathy Sharp
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, Erki Saluveer
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, Alessandro Saitta
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, Miguel Rosas
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,
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Taavi Riit
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, David Ratkowsky
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, Karin Pritsch
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, Kadri Põldmaa
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, Meike Piepenbring
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,
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Cherdchai Phosri
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, Marko Peterson
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, Kaarin Parts
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, Kadri Pärtel
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, Eveli Otsing
2
, Eduardo
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Nouhra
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, André L. Njouonkou
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, R. Henrik Nilsson
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, Luis N. Morgado
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, Jordan Mayor
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,
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Tom W. May
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, Luiza Majuakim
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, D. Jean Lodge
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, Su See Lee
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, Karl-Henrik Larsson
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, Petr
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Kohout
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, Kentaro Hosaka
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, Indrek Hiiesalu
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, Terry W. Henkel
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, Helery Harend
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, Liang-dong
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Guo
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, Alina Greslebin
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, Gwen Grelet
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, Jozsef Geml
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, Genevieve Gates
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, William
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Dunstan
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, Chris Dunk
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, Rein Drenkhan
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, John Dearnaley
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, André De Kesel
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, Tan Dang
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,
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Xin Chen
34
, Franz Buegger
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, Francis Q. Brearley
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, Gregory Bonito
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, Sten Anslan
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, Sandra
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Abell
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, Kessy Abarenkov
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1
Natural History Museum, University of Tartu, Tartu, Estonia.
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Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia.
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Faculté d´Agronomie, Université de Parakou, Parakou, Benin.
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Department of Plant Sciences, University of Colombo, Colombo 3, Sri Lanka.
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Postgrado en Recursos Genéticos y Productividad-Genética, LARGEMBIO, Colegio de
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Postgraduados-LPI 6, México City, Mexico.
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The Fungal Biodiversity Centre, CBS-KNAW, Utrecht, The Netherlands.
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Vietnamese Academy of Forest Sciences, Hanoi, Vietnam.
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Department of Plant Pathology, University of Florida, Gainesville, Florida, USA.
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Natural History Museum, Bulawayo, Zimbabwe.
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Department of Agricultural and Forest Sciences, Università di Palermo, Palermo, Italy.
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11
Department of Mycology, Goethe University Frankfurt, Frankfurt am Main, Germany.
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12
Tasmanian Institute of Agriculture, Hobart, Tasmania, Australia.
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Institute of Soil Ecology, Helmholtz Zentrum München, Neuherberg, Germany.
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Department of Biology, Nakhon Phanom University, Nakhon Phanom, Thailand.
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Instituto Multidisciplinario de Biología Vegetal, Córdoba, Argentina.
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Department of Biological Sciences, University of Bamenda, Bambili, Cameroon.
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Department of Biological and Environmental Sciences, University of Gothenburg, Göteborg,
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Sweden.
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Naturalis Biodiversity Center, Leiden, The Netherlands.
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Department of Forest Ecology and Management, Swedish University of Agricultural
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Sciences, Umeå, Sweden.
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Royal Botanic Gardens Melbourne, Melbourne, Victoria, Australia.
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Institute for Tropical Biology and Conservation, University Malaysia Sabah, Sabah,
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Malaysia.
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Center for Forest Mycology Research, USDA-Forest Service, Luquillo, Puerto Rico.
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Forest Research Institute Malaysia, Kepong, Selangor, Malaysia.
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24
Natural History Museum, University of Oslo, Oslo, Norway.
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Department of Botany, National Museum of Nature and Science, Tsukuba, Japan.
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Department of Biological Sciences, Humboldt State University, Arcata, California, USA.
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State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences,
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Beijing, China.
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CONICET - Facultad de Cs. Naturales, Universidad Nacional de la Patagonia SJB, Esquel,
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Chubut, Argentina.
49
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Ecosystems and Global Change team, Landcare Research, Lincoln, New Zealand.
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30
School of Veterinary & Life Sciences, Murdoch University, Western Australia, Australia.
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31
Institute of Forestry and Rural Engineering, Estonian University of Life Sciences, Tartu,
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Estonia.
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32
Faculty of Health, Engineering and Sciences, University of Southern Queensland,
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Toowoomba, Queensland, Australia.
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33
Botanic Garden Meise, Meise, Belgium.
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34
College of Life Sciences, Zhejiag University, Hangzhou 310058, China.
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School of Science and the Environment, Manchester Metropolitan University, Manchester,
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United Kingdom.
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36
School of Marine and Tropical Biology, James Cook University, Cairns, Queensland,
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Australia.
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Equal contribution
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*Corresponding author. E-mail: leho.tedersoo@ut.ee
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Abstract
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Fungi play major roles in ecosystem processes, but the determinants of fungal diversity and
68
biogeographic patterns remain poorly understood. By using DNA metabarcoding data from
69
hundreds of globally distributed soil samples, we demonstrate that fungal richness is decoupled
70
from plant diversity. The plant-to-fungus richness ratio declines exponentially towards the
71
poles, indicating strong biases in previous fungal diversity estimates.
Climatic factors,
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followed by edaphic and spatial variables, constitute the best predictors of fungal richness and
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community composition at the global scale. Fungi follow general biogeographic patterns
74
related to latitudinal diversity gradients but with several notable exceptions. These findings
75
significantly advance our understanding of fungal diversity patterns at the global scale and
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permit integration of fungi into a general macro-ecological framework.
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One-sentence summary
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A massive, global-scale metagenomic study detects hotspots of fungal diversity and
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macroecological patterns, and indicates that plant and fungal diversity are uncoupled.
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INTRODUCTION: The kingdom Fungi is one of the most diverse groups of organisms on
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Earth and they are integral ecosystem agents that govern soil carbon cycling, plant nutrition,
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and pathology. Fungi are widely distributed in all terrestrial ecosystems, but the distribution of
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species, phyla, and functional groups has been poorly documented. Based on 365 global soil
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samples from natural ecosystems, we determined the main drivers and biogeographic patterns
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of fungal diversity and community composition.
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RATIONALE: We identified soil-inhabiting fungi using 454 pyrosequencing and comparison
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against taxonomically and functionally annotated sequence databases. Multiple regression
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models were used to disentangle the roles of climatic, spatial, edaphic, and floristic parameters
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on fungal diversity and community composition. Structural equation models were used to
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determine the direct and indirect effects of climate on fungal diversity, soil chemistry and
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vegetation. We also examined if fungal biogeographic patterns matched paradigms derived
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from plants and animals namely, that species’ latitudinal ranges increase towards the poles
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(Rapoport’s rule) and diversity increases towards the equator. Finally, we sought group-
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specific global biogeographic links among major biogeographic regions and biomes using a
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network approach and area-based clustering.
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RESULTS: Metabarcoding analysis of global soils revealed fungal richness estimates
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approaching the number of species recorded to date. Distance from equator and mean annual
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precipitation had the strongest effects on richness of fungi including most fungal taxonomic
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and functional groups. Diversity of most fungal groups peaked in tropical ecosystems, but
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ectomycorrhizal fungi and several fungal classes were most diverse in temperate or boreal
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ecosystems and many fungal groups exhibited distinct preferences for specific edaphic
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conditions (e.g. pH, calcium, phosphorus). Consistent with Rapoport´s rule, the geographic
108

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References
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Journal ArticleDOI
TL;DR: Among the regions of the ribosomal cistron, the internal transcribed spacer (ITS) region has the highest probability of successful identification for the broadest range of fungi, with the most clearly defined barcode gap between inter- and intraspecific variation.
Abstract: Six DNA regions were evaluated as potential DNA barcodes for Fungi, the second largest kingdom of eukaryotic life, by a multinational, multilaboratory consortium. The region of the mitochondrial cytochrome c oxidase subunit 1 used as the animal barcode was excluded as a potential marker, because it is difficult to amplify in fungi, often includes large introns, and can be insufficiently variable. Three subunits from the nuclear ribosomal RNA cistron were compared together with regions of three representative protein-coding genes (largest subunit of RNA polymerase II, second largest subunit of RNA polymerase II, and minichromosome maintenance protein). Although the protein-coding gene regions often had a higher percent of correct identification compared with ribosomal markers, low PCR amplification and sequencing success eliminated them as candidates for a universal fungal barcode. Among the regions of the ribosomal cistron, the internal transcribed spacer (ITS) region has the highest probability of successful identification for the broadest range of fungi, with the most clearly defined barcode gap between inter- and intraspecific variation. The nuclear ribosomal large subunit, a popular phylogenetic marker in certain groups, had superior species resolution in some taxonomic groups, such as the early diverging lineages and the ascomycete yeasts, but was otherwise slightly inferior to the ITS. The nuclear ribosomal small subunit has poor species-level resolution in fungi. ITS will be formally proposed for adoption as the primary fungal barcode marker to the Consortium for the Barcode of Life, with the possibility that supplementary barcodes may be developed for particular narrowly circumscribed taxonomic groups.

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Journal ArticleDOI
TL;DR: The results suggest that the structure of soil bacterial communities is predictable, to some degree, across larger spatial scales, and the effect of soil pH on bacterial community composition is evident at even relatively coarse levels of taxonomic resolution.
Abstract: Soils harbor enormously diverse bacterial populations, and soil bacterial communities can vary greatly in composition across space. However, our understanding of the specific changes in soil bacterial community structure that occur across larger spatial scales is limited because most previous work has focused on either surveying a relatively small number of soils in detail or analyzing a larger number of soils with techniques that provide little detail about the phylogenetic structure of the bacterial communities. Here we used a bar-coded pyrosequencing technique to characterize bacterial communities in 88 soils from across North and South America, obtaining an average of 1,501 sequences per soil. We found that overall bacterial community composition, as measured by pairwise UniFrac distances, was significantly correlated with differences in soil pH (r = 0.79), largely driven by changes in the relative abundances of Acidobacteria, Actinobacteria, and Bacteroidetes across the range of soil pHs. In addition, soil pH explains a significant portion of the variability associated with observed changes in the phylogenetic structure within each dominant lineage. The overall phylogenetic diversity of the bacterial communities was also correlated with soil pH (R2 = 0.50), with peak diversity in soils with near-neutral pHs. Together, these results suggest that the structure of soil bacterial communities is predictable, to some degree, across larger spatial scales, and the effect of soil pH on bacterial community composition is evident at even relatively coarse levels of taxonomic resolution.

3,151 citations


"Global diversity and geography of s..." refers background in this paper

  • ...The phenomenon of high cryptic diversity and low success in naming OTUs at the genus or species level have been found in other groups of soil microbes and invertebrates, emphasizing our poor overall knowledge of global soil biodiversity (27, 28)....

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Journal ArticleDOI
TL;DR: Soils collected across a long-term liming experiment were used to investigate the direct influence of pH on the abundance and composition of the two major soil microbial taxa, fungi and bacteria, and both the relative abundance and diversity of bacteria were positively related to pH.
Abstract: Soils collected across a long-term liming experiment (pH 4.0-8.3), in which variation in factors other than pH have been minimized, were used to investigate the direct influence of pH on the abundance and composition of the two major soil microbial taxa, fungi and bacteria. We hypothesized that bacterial communities would be more strongly influenced by pH than fungal communities. To determine the relative abundance of bacteria and fungi, we used quantitative PCR (qPCR), and to analyze the composition and diversity of the bacterial and fungal communities, we used a bar-coded pyrosequencing technique. Both the relative abundance and diversity of bacteria were positively related to pH, the latter nearly doubling between pH 4 and 8. In contrast, the relative abundance of fungi was unaffected by pH and fungal diversity was only weakly related with pH. The composition of the bacterial communities was closely defined by soil pH; there was as much variability in bacterial community composition across the 180-m distance of this liming experiment as across soils collected from a wide range of biomes in North and South America, emphasizing the dominance of pH in structuring bacterial communities. The apparent direct influence of pH on bacterial community composition is probably due to the narrow pH ranges for optimal growth of bacteria. Fungal community composition was less strongly affected by pH, which is consistent with pure culture studies, demonstrating that fungi generally exhibit wider pH ranges for optimal growth.

2,966 citations


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Journal ArticleDOI
TL;DR: All fungal species represented by at least two ITS sequences in the international nucleotide sequence databases are now given a unique, stable name of the accession number type, and the term ‘species hypothesis’ (SH) is introduced for the taxa discovered in clustering on different similarity thresholds.
Abstract: The nuclear ribosomal internal transcribed spacer (ITS) region is the formal fungal barcode and in most cases the marker of choice for the exploration of fungal diversity in environmental samples. Two problems are particularly acute in the pursuit of satisfactory taxonomic assignment of newly generated ITS sequences: (i) the lack of an inclusive, reliable public reference data set and (ii) the lack of means to refer to fungal species, for which no Latin name is available in a standardized stable way. Here, we report on progress in these regards through further development of the UNITE database (http://unite.ut.ee) for molecular identification of fungi. All fungal species represented by at least two ITS sequences in the international nucleotide sequence databases are now given a unique, stable name of the accession number type (e.g. Hymenoscyphus pseudoalbidus|GU586904|SH133781.05FU), and their taxonomic and ecological annotations were corrected as far as possible through a distributed, third-party annotation effort. We introduce the term ‘species hypothesis’ (SH) for the taxa discovered in clustering on different similarity thresholds (97–99%). An automatically or manually designated sequence is chosen to represent each such SH. These reference sequences are released (http://unite.ut.ee/repository.php) for use by the scientific community in, for example, local sequence similarity searches and in the QIIME pipeline. The system and the data will be updated automatically as the number of public fungal ITS sequences grows. We invite everybody in the position to improve the annotation or metadata associated with their particular fungal lineages of expertise to do so through the new Web-based sequence management system in UNITE.

2,605 citations


"Global diversity and geography of s..." refers background or methods in this paper

  • ...0% sequence similarity thresholds (12) as implemented in CD-Hit 4....

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  • ...0% similarity clustering of all fungal ITS sequences in publicly available databases (12)....

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  • ...0% similarity clusters that include third-party taxonomic andmetadata updates (12) as implemented in the PlutoF workbench (13)....

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Journal ArticleDOI
TL;DR: This analysis is the first to describe these general and significant patterns, which have important consequences for models aiming to explain the latitudinal gradient, which were weaker and less steep in freshwater than in marine or terrestrial environments and differed significantly between continents and habitat types.
Abstract: The decline of biodiversity with latitude has received great attention, but both the concise pattern and the causes of the gradient are under strong debate. Most studies of the latitudinal gradient comprise only one or few organism types and are often restricted to certain region or habitat types. To test for significant variation in the gradient between organisms, habitats, or regions, a meta-analysis was conducted on nearly 600 latitudinal gradients assembled from the literature. Each gradient was characterized by two effect sizes, strength (correlation coefficient) and slope, and additionally by 14 variables describing organisms, habitats, and regions. The analysis corroborated the high generality of the latitudinal diversity decline. Gradients on regional scales were significantly stronger and steeper than on local scales, and slopes also varied with sampling grain. Both strength and slope increased with organism body mass, and strength increased with trophic level. The body mass-effect size relation varied for ecto- versus homeotherm organisms and for different dispersal types, suggesting allometric effects on energy use and dispersal ability as possible mechanisms for the body mass effect. Latitudinal gradients were weaker and less steep in freshwater than in marine or terrestrial environments and differed significantly between continents and habitat types. The gradient parameters were not affected by hemisphere or the latitudinal range covered. This analysis is the first to describe these general and significant patterns, which have important consequences for models aiming to explain the latitudinal gradient.

1,623 citations


"Global diversity and geography of s..." refers background in this paper

  • ...fungi (5, 32), the overall richness of soil fungi increased toward the equator (Fig....

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  • ...Richness of nearly all terrestrial and marine macroorganisms is negatively related to increasing latitude (5)—a pattern attributed to the combined effects of climate, niche conservatism, and rates of evolutionary radiation and extinction (6)....

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