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Parasites dominate hyperdiverse soil protist communities in Neotropical rainforests

Abstract

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.

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Figure 1: Similarity of protists to the taxonomic reference database.
Figure 2: Phylogenetic placement of Neotropical soil protist reads on a taxonomically unconstrained global eukaryotic tree.
Figure 3: Taxonomic identity and relative abundances of soil protist reads and OTUs in three Neotropical rainforests.

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Acknowledgements

We thank T. Stoeck, L. Katz, H. Kauserud, O. T. Lewis and D. Montagnes for helpful comments. Funding primarily came from: a Deutsche Forschungsgemeinschaft grant DU1319/1-1 to M.D.; the Klaus Tschira Foundation to L.C., A.S and A.K; and the French Government’s ‘Investissements d’Avenir’ program OCEANOMICS (ANR-11-BTBR-0008) to C.d.V., C.B. and S.R. Funding also came from: the Natural Environment Research Council grants NE/H000887/1 and NE/H009426/1 to D.B.; the National Science Foundation’s International Research Fellowship Program (OISE-1012703) and the Smithsonian Tropical Research Institute’s Fellowship program to J.M.; the Swiss National Science Foundation (310003A 143960); and the Swiss Federal Office for the Environment and Swiss National Science Foundation to E.L. and E.A.D.M. The authors gratefully acknowledge the Gauss Centre for Supercomputing e.V. (www.gauss-centre.eu) for funding this project by providing computing time on the GCS Supercomputer SuperMUC at the Leibniz Supercomputing Centre (www.lrz.de).

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Authors and Affiliations

Authors

Contributions

F.M. and M.D. conceived the project. F.M., C.d.V., J.M., T.S., S.R. and M.D. collected the samples. Sequencing was carried out by F.M., T.S., I.T., S.R and M.D. Data analysis was done by F.M., D.B., L.C., A.S., E.L., D.S., J.B., S.S., I.T., C.B., A.K., E.E. and M.D. The first draft of the manuscript was written by F.M., C.d.V., D.B., L.C., A.S. and M.D., and all authors contributed to discussing the results and editing the manuscript.

Corresponding author

Correspondence to Micah Dunthorn.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Methods, Supplementary References, Supplementary Figures 1–16, Supplementary Tables 1–3. (PDF 3214 kb)

Supplementary Code 1

Main computer code and sampling information. (XML 692 kb)

Supplementary Code 2

Additional computer code for phylogenetic placements. (HTML 896 kb)

Supplementary Data 1

GenBank references used in eukaryotic reference tree. (TXT 2380 kb)

Supplementary Data 2

GenBank accession numbers and clade assignments for eukaryotic reference tree. (XLSX 23 kb)

Supplementary Data 3

GenBank references used in Alveolata reference tree. (TXT 441 kb)

Supplementary Data 4

GenBank accession numbers and clade assignments for Alveolata reference tree. (XLSX 15 kb)

Supplementary Data 5

Comparison of constrained and unconstrained phylogenetic placements on the eukaryotic reference tree. (XLSX 27 kb)

Supplementary Data 6

Comparison of constrained and unconstrained phylogenetic placements on the Alveolata reference tree. (XLSX 25 kb)

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Mahé, F., de Vargas, C., Bass, D. et al. Parasites dominate hyperdiverse soil protist communities in Neotropical rainforests. Nat Ecol Evol 1, 0091 (2017). https://doi.org/10.1038/s41559-017-0091

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