Global biogeography of highly diverse protistan communities in soil

Bates, Scott T.; Clemente, José C.; Flores, Gilberto E.; Walters, William A.; Parfrey, Laura Wegener; Knight, Rob; Fierer, Noah

doi:10.1038/ismej.2012.147

Cited by 429 publications

(369 citation statements)

References 51 publications

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“…3). This pattern of dominating parasites contrasts with the prevailing view that soil protist communities are dominated by predators of bacteria 34 , although a considerable presence of protist predators of fungi and animals, as well as protist parasites, has been observed elsewhere [35][36][37][38][39][40][41] . These dominating protist parasites also potentially contribute to the high animal diversity in the rainforests by the same mechanisms that other parasites contribute to high tree diversity as hypothesized in the Janzen-Connell model 4,5 .…”

Section: Discussionmentioning

confidence: 66%

“…To put the 50,118,536 soil protist reads into a phylogenetic context, they were dereplicated into 10,567,804 strictly identical amplicons and placed onto a comprehensive eukaryotic reference tree. The corresponding multiple sequence alignment used to build this tree contained 512 full-length sequences from all major eukaryotic clades (see Supplementary Data 1 and 2 for GenBank accession numbers, sequences and clade assignments), based on the taxon sampling as summarized in a range of pan-eukaryotic phylogenomic studies reviewed in refs 61,62 , with a bias towards lineages known to occur in soils from environmental sequencing studies; for example, refs 35,37,38 . To reduce phylogenetic artefacts, only high quality, full-or near-full length 18S rRNA reads were selected, and reads that have previously been observed to form long branches were omitted.…”

Section: Stampa Plotsmentioning

confidence: 99%

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Parasites dominate hyperdiverse soil protist communities in Neotropical rainforests

et al. 2017

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High animal and plant richness in tropical rainforest communities has long intrigued naturalists. It is unknown if similar hyperdiversity patterns are reflected at the microbial scale with unicellular eukaryotes (protists). Here we show, using environmental metabarcoding of soil samples and a phylogeny-aware cleaning step, that protist communities in Neotropical rainforests are hyperdiverse and dominated by the parasitic Apicomplexa, which infect arthropods and other animals. These host-specific parasites potentially contribute to the high animal diversity in the forests by reducing population growth in a density-dependent manner. By contrast, too few operational taxonomic units (OTUs) of Oomycota were found to broadly drive high tropical tree diversity in a host-specific manner under the Janzen-Connell model. Extremely high OTU diversity and high heterogeneity between samples within the same forests suggest that protists, not arthropods, are the most diverse eukaryotes in tropical rainforests. Our data show that protists play a large role in tropical terrestrial ecosystems long viewed as being dominated by macroorganisms.S ince the works of early naturalists such as von Humboldt and Bonpland 1 , we have known that animal and plant communities in tropical rainforests are exceedingly species rich. For example, one hectare can contain more than 400 tree species 2 and one tree can harbour more than 40 ant species 3 . This hyperdiversity of trees has been partially explained by the Janzen-Connell model 4,5 , which hypothesizes that host-specific predators and parasites reduce plant population growth in a density-dependent manner 6,7 . Sampling up in the tree canopies and below on the ground has further led to the view that arthropods are the most diverse eukaryotes in tropical rainforests 8,9 .The focus on eukaryotic macroorganisms in these studies is primarily because they are familiar and readily observable to us. We do not know whether the less familiar and less readily observable protists-microbial eukaryotes that are not animals, plants or fungi 10 -inhabiting these same ecosystems exhibit similar diversity patterns. To evaluate if macroorganismic diversity patterns are reflected at the microbial scale with protists, we conducted an environmental DNA metabarcoding study by sampling soils in 279 locations in a variety of lowland Neotropical forest types in La Selva Biological Station, Costa Rica, Barro Colorado Island, Panama and Tiputini Biodiversity Station, Ecuador. This metabarcoding approach has the power to uncover known and new taxa on a massive scale 11 . By amplifying DNA extracted from the soils with broadly targeted primers for the V4 region of 18S rRNA and sequencing it using the Illumina MiSeq platform, we were able to detect most eukaryotic lineages, and assess the diversity and relative dominance of free-living and parasitic lineages.

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Section: Discussionmentioning

confidence: 66%

Section: Stampa Plotsmentioning

confidence: 99%

Parasites dominate hyperdiverse soil protist communities in Neotropical rainforests

et al. 2017

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“…We used the Internal Transcribed Spacer 2 (ITS2) as a locus for DNA metabarcoding, which offers higher resolution at species level compared with 18S rDNA (Bates et al, 2013) and provides less primer bias compared with mitochondrial cytochrome oxidase I across multiple eukaryote kingdoms (Deagle et al, 2014). PCR was carried out using a mixture of 11 modified ITS3ngs forward primers (in equimolar concentration) and a degenerate ITS4ngs reverse primer (Tedersoo et al, 2016;Supplementary Table S2).…”

Section: Molecular Methodsmentioning

confidence: 99%

“…There is an old assumption that free-living soil microbial eukaryotes do not face dispersal limitation (Finlay, 2002), but several molecular studies provide evidence for their biogeographic patterns (for example, Green et al, 2004;Bahram et al, 2013;Bates et al, 2013; but see Queloz et al, 2011). Recent findings also suggest that similarly to macro-organisms, microbes are influenced by neutral processes (for example, Cottenie 2005;Hájek et al, 2011;Astorga et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Stochastic distribution of small soil eukaryotes resulting from high dispersal and drift in a local environment

et al. 2015

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A central challenge in ecology is to understand the relative importance of processes that shape diversity patterns. Compared with aboveground biota, little is known about spatial patterns and processes in soil organisms. Here we examine the spatial structure of communities of small soil eukaryotes to elucidate the underlying stochastic and deterministic processes in the absence of environmental gradients at a local scale. Specifically, we focus on the fine-scale spatial autocorrelation of prominent taxonomic and functional groups of eukaryotic microbes. We collected 123 soil samples in a nested design at distances ranging from 0.01 to 64 m from three boreal forest sites and used 454 pyrosequencing analysis of Internal Transcribed Spacer for detecting Operational Taxonomic Units of major eukaryotic groups simultaneously. Among the main taxonomic groups, we found significant but weak spatial variability only in the communities of Fungi and Rhizaria. Within Fungi, ectomycorrhizas and pathogens exhibited stronger spatial structure compared with saprotrophs and corresponded to vegetation. For the groups with significant spatial structure, autocorrelation occurred at a very fine scale (o2 m). Both dispersal limitation and environmental selection had a weak effect on communities as reflected in negative or null deviation of communities, which was also supported by multivariate analysis, that is, environment, spatial processes and their shared effects explained on average o10% of variance. Taken together, these results indicate a random distribution of soil eukaryotes with respect to space and environment in the absence of environmental gradients at the local scale, reflecting the dominant role of drift and homogenizing dispersal.

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“…However, such studies have largely focused on individual groups (e.g. only bacteria), with far less attention paid to unicellular and multicellular eukaryotes despite increasing evidence that the diversity of soil fungi, protists and metazoa is likely far higher than often considered [14][15][16]. Indeed, there are few cross-domain assessments of below-ground diversity (but see [17,18]).…”

Section: Introductionmentioning

confidence: 99%

Biogeographic patterns in below-ground diversity in New York City's Central Park are similar to those observed globally

et al. 2014

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Soil biota play key roles in the functioning of terrestrial ecosystems, however, compared to our knowledge of above-ground plant and animal diversity, the biodiversity found in soils remains largely uncharacterized. Here, we present an assessment of soil biodiversity and biogeographic patterns across Central Park in New York City that spanned all three domains of life, demonstrating that even an urban, managed system harbours large amounts of undescribed soil biodiversity. Despite high variability across the Park, below-ground diversity patterns were predictable based on soil characteristics, with prokaryotic and eukaryotic communities exhibiting overlapping biogeographic patterns. Further, Central Park soils harboured nearly as many distinct soil microbial phylotypes and types of soil communities as we found in biomes across the globe (including arctic, tropical and desert soils). This integrated cross-domain investigation highlights that the amount and patterning of novel and uncharacterized diversity at a single urban location matches that observed across natural ecosystems spanning multiple biomes and continents.

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Global biogeography of highly diverse protistan communities in soil

Cited by 429 publications

References 51 publications

Parasites dominate hyperdiverse soil protist communities in Neotropical rainforests

Parasites dominate hyperdiverse soil protist communities in Neotropical rainforests

Stochastic distribution of small soil eukaryotes resulting from high dispersal and drift in a local environment

Biogeographic patterns in below-ground diversity in New York City's Central Park are similar to those observed globally

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