Global diversity and geography of soil fungi
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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4,116 citations
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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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...Nonetheless, the significant globalscale pH effect in several groups of fungi is consistent with the substantial influence of pH on the phylogenetic structure of soil fungal and bacterial communities in both local and continental scales (27, 45)....
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2,966 citations
"Global diversity and geography of s..." refers background in this paper
...Nonetheless, the significant globalscale pH effect in several groups of fungi is consistent with the substantial influence of pH on the phylogenetic structure of soil fungal and bacterial communities in both local and continental scales (27, 45)....
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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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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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