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The Microbial Community of Tardigrades: Environmental Influence and Species Specificity of Microbiome Structure and Composition

  • Matteo Vecchi
  • Irene L.G. Newton
  • Michele Cesari
  • Lorena Rebecchi
  • Roberto Guidetti
Invertebrate Microbiology

Abstract

Symbiotic associations of metazoans with bacteria strongly influence animal biology since bacteria are ubiquitous and virtually no animal is completely free from them. Tardigrades are micrometazoans famous for their ability to undergo ametabolic states (cryptobiosis) but very little information is available on potential microbial associations. We characterized the microbiomes of six limnoterrestrial tardigrade species belonging to several phylogenetic lines in tandem with the microbiomes of their respective substrates. The experimental design enabled us to determine the effects of both the environment and the host genetic background on the tardigrade microbiome; we were able to define the microbial community of the same species sampled from different environments, and the communities of different species from the same environment. Our 16S rRNA gene amplicon approach indicated that the tardigrade microbiome is species-specific and well differentiated from the environment. Tardigrade species showed a much lower microbial diversity compared to their substrates, with only one significant exception. Forty-nine common OTUs (operational taxonomic units) were classified into six bacterial phyla, while four common OTUs were unclassified and probably represent novel bacterial taxa. Specifically, the tardigrade microbiome appears dominated by Proteobacteria and Bacteroidetes. Some OTUs were shared between different species from geographically distant samples, suggesting the associated bacteria may be widespread. Putative endosymbionts of tardigrades from the order Rickettsiales were identified. Our results indicated that like all other animals, tardigrades have their own microbiota that is different among species, and its assembly is determined by host genotype and environmental influences.

Keywords

Endosymbiont Microbiome Rickettsiales Symbiosis Tardigrada 

Notes

Acknowledgments

We thank Kristian Hassel (Norwegian University of Science and Technology, Trondheim, Norway) and Renzo Rabacchi (Museo Civico di Ecologia e Storia Naturale di Marano sul Panaro, Modena, Italy) for the taxonomic determination of mosses in sample S7 and lichens in samples S4 and S5, respectively. We thank K. Ingemar Jönsson (Kristianstad University, Kristianstad, Sweden) for kindly providing sample S6 and Mauro Mandrioli (University of Modena and Reggio Emilia, Modena, Italy) for providing some laboratory reagents. We additionally wish to thank Kathy B. Sheehan and MaryAnn Martin (Indiana University, USA) for their support during laboratory work. Finally, we thank the anonymous reviewers and the reviewer Diane Nelson for the constructive suggestions in order to improve the manuscript.

Authors’ Contributions

This work is a part of the Ph.D. thesis of M.V. M.V. and R.G. designed and conceived the experiments. M.V. and M.C. performed the laboratory work. M.V. and I.G.N. analyzed the data. I.G.N., L.R., and R.G. provided reagents, instruments, and funds. M.V. wrote the first draft of the manuscript. M.V., I.G.N., M.C., L.R., and R.G. participated in revising the manuscript.

Funding Information

This research was supported by the Italian “Programma Nazionale Ricerche in Antartide (PNRA)–Ministero dell’Istruzione dell’Università e della Ricerca (MIUR)” as part of the project “Evolutive and phylogeographic history of Antarctic organisms and responses by ecosystems to climatic and environmental changings” (PdR 2013 B1/01) and by the “Bando per il finanziamento di azioni di mobilità nell’ambito del Programma di collaborazione scientifica e culturale dell'Università degli Studi di Modena e Reggio Emilia con Università straniere convenzionate-2016” (University of Modena and Reggio Emilia, Modena, Italy).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

248_2017_1134_MOESM1_ESM.docx (2 mb)
ESM 1 (DOCX 2074 kb)
248_2017_1134_MOESM2_ESM.xlsx (88 kb)
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Authors and Affiliations

  1. 1.Department of Life SciencesUniversity of Modena and Reggio EmiliaModenaItaly
  2. 2.Department of BiologyIndiana UniversityBloomingtonUSA

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