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Parasites dominate hyperdiverse soil protist communities in Neotropical rainforests

Nature Ecology & Evolution volume 1, Article number: 0091 (2017) Cite this article

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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

  1. Department of Ecology, University of Kaiserslautern, Erwin-Schrödinger-Straße, Kaiserslautern, 67663, Germany

    Frédéric Mahé, Tobias Siemensmeyer, Isabelle Trautmann, Guillaume Lentendu & Micah Dunthorn

  2. CNRS, UMR 7144, Station Biologique de Roscoff, Place Georges Teissier, Roscoff Cedex, 29680, France

    Colomban de Vargas, Sarah Romac & Cédric Berney

  3. Sorbonne Universités, UPMC Université de Paris 06, UMR 7144, Station Biologique de Roscoff, Place Georges Teissier, Roscoff Cedex, 29680, France

    Colomban de Vargas, Sarah Romac & Cédric Berney

  4. Department of Life Sciences, The Natural History Museum London, Cromwell Road, London, SW7 5BD, UK

    David Bass

  5. Centre for Environment, Fisheries and Aquaculture Science, Barrack Road, The Nothe, Weymouth, Dorset, DT4 8UB, UK

    David Bass

  6. Heidelberg Institute for Theoretical Studies, Schloß-Wolfsbrunnenweg, Heidelberg, 69118, Germany

    Lucas Czech, Alexandros Stamatakis & Alexey Kozlov

  7. Institute for Theoretical Informatics, Karlsruhe Institute of Technology, Am Fasanengarten, Karlsruhe, 76128, Germany

    Alexandros Stamatakis

  8. Laboratory of Soil Biodiversity, Université de Neuchâtel, Rue Emile-Argand, Neuchâtel, 2000, Switzerland

    Enrique Lara, David Singer, Edward A. D. Mitchell & Christophe V. W. Seppey

  9. Department of Forest Ecology and Management, Swedish University of Agricultural Sciences, Skogsmarksgränd, Umeå, 90183, Sweden

    Jordan Mayor

  10. Department of Computer Science, Cornell University, Gates Hall, Ithaca, 14853, New York, USA

    John Bunge

  11. Department of Statistical Science, Cornell University, Malott Hall, Ithaca, 14853, New York, USA

    Sarah Sernaker

  12. Jardin Botanique de Neuchâtel, Pertuis-du-Sault, Neuchâtel, 2000, Switzerland

    Edward A. D. Mitchell

  13. Department of Biosciences, University of Oslo, Blindernveien, 0316, Oslo, Norway

    Elianne Egge

  14. Department of Plant Ecology and Systematics, University of Kaiserslautern, Erwin-Schrödinger-Straße, Kaiserslautern, 67663, Germany

    Rainer Wirth

  15. Instituto de Microbiología, Universidad San Francisco de Quito, Diego de Robles, Quito, Ecuador

    Gabriel Trueba

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  1. Frédéric Mahé
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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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Competing interests

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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