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Multi-scale ecological filters shape the crayfish microbiome

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Abstract

A general and practical understanding of the processes that drive microbiome assembly and structure are paramount to understanding organismal biology, health, and evolution. In this study of stream-dwelling crayfish, we conceptualized colonization of microbial symbionts as a series of ecological filters that operate at the environment, host, and host microsite levels, and identified key ecological processes at each level. A survey of Cambarus sciotensis in western Virginia, USA, showed that the local environment and host microsites interact to create complex patterns of microbial diversity and composition. An in situ experiment confirmed a prevailing effect of host microsite on microbial composition, and also showed that an ectosymbiotic worm (Annelida; Branchiobdellida) which feeds on biofilms and other symbionts had significant effects on microbial composition of the host carapace, but not gills. Bacterial communities of the carapace were taxonomically rich and even, and correlated with microbial communities of the ambient environment. Conversely, communities on gills were less diverse and dominated by two taxa with potential functional significance: Comamonadaceae and Chitinophagaceae. The bacterial communities of the gills appear to be tightly coupled to host biology, and those of the carapace are mostly determined by environmental context. Our work provides the first characterization of the crayfish microbiome and shows how multi-scale and experimental studies of symbiont community assembly provide valuable insights into how the animal microbiome is structured under conditions of natural complexity. Furthermore, this study demonstrates that metazoan symbiont taxa, i.e., the branchiobdellidans, can alter microbiome assembly and structure.

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Acknowledgments

We sincerely thank Michael J. Thomas and Mathew Hedin for their help in the field and laboratory. Allan Dickerman and the staff of the Virginia Tech Bioinformatics Institute were critical partners for high-throughput amplicon sequencing and analysis. This manuscript benefited greatly from thoughtful comments from Michelle A. Jusino and two anonymous reviewers. Funding was provided by the National Science Foundation (DEB-0949780 to BLB and DEB-0949823 to RPC), Virginia Tech Organismal Biology and Ecology Interdisciplinary Grants (to JS and KMG), and the Virginia Bioinformatics Institute and Fralin Life Science Institute Small Grants Program (to JS, KMG, JTL and BLB).

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Authors and Affiliations

  1. School of Forest Resources and Conservation, University of Florida, Gainesville, FL, 32603, USA

    James Skelton

  2. College of Life Sciences and Agriculture, University of New Hampshire, Durham, NH, 03824, USA

    Kevin M. Geyer

  3. Department of Biology, Indiana University, Bloomington, IN, 47405, USA

    Jay T. Lennon

  4. Department of Biology, Appalachian State University, 575 Rivers Street, Boone, NC, 28608, USA

    Robert P. Creed

  5. Department of Biological Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA, 24061, USA

    Bryan L. Brown

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Skelton, J., Geyer, K.M., Lennon, J.T. et al. Multi-scale ecological filters shape the crayfish microbiome. Symbiosis 72, 159–170 (2017). https://doi.org/10.1007/s13199-016-0469-9

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