Spontaneous body wall contractions stabilize the fluid microenvironment that shapes host-microbe associations

  1. Janna C Nawroth
  2. Christoph Giez
  3. Alexander Klimovich
  4. Eva Kanso  Is a corresponding author
  5. Thomas CG Bosch  Is a corresponding author
  1. Helmholtz Munich, Germany
  2. Kiel University, Germany
  3. University of Southern California, United States

Abstract

The freshwater polyp Hydra is a popular biological model system; however, we still do not understand one of its most salient behaviours, the generation of spontaneous body wall contractions. Here, by applying experimental fluid dynamics analysis and mathematical modelling, we provide functional evidence that spontaneous contractions of body walls enhance the transport of chemical compounds from and to the tissue surface where symbiotic bacteria reside. Experimentally, a reduction in the frequency of spontaneous body wall contractions is associated with a changed composition of the colonizing microbiota. Together, our findings suggest that spontaneous body wall contractions create an important fluid transport mechanism that (1) may shape and stabilize specific host-microbe associations and (2) create fluid microhabitats that may modulate the spatial distribution of the colonizing microbes. This mechanism may be more broadly applicable to animal-microbe interactions since research has shown that rhythmic spontaneous contractions in the gastrointestinal tracts are essential for maintaining normal microbiota.

Data availability

All data presented in the main manuscript and supplemental figures is publicly available at NCBI Bioproject PRJNA842888The 16S rRNA sequencing raw data are deposited at the SRA and are available under the project ID PRJNA842888.

The following data sets were generated

Article and author information

Author details

  1. Janna C Nawroth

    Helmholtz Pioneer Campus, Helmholtz Munich, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Christoph Giez

    Zoological Institute, Kiel University, Kiel, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Alexander Klimovich

    Zoological Institute, Kiel University, Kiel, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1764-0613
  4. Eva Kanso

    Aerospace and Mechanical Engineering, University of Southern California, Los Angeles, United States
    For correspondence
    kanso@usc.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0336-585X
  5. Thomas CG Bosch

    Zoological Institute, Kiel University, Kiel, Germany
    For correspondence
    tbosch@zoologie.uni-kiel.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9488-5545

Funding

Deutsche Forschungsgemeinschaft (CRC 1182 Origin and Function of Metaorganisms"")

  • Janna C Nawroth
  • Christoph Giez
  • Alexander Klimovich
  • Eva Kanso
  • Thomas CG Bosch

Deutsche Forschungsgemeinschaft (CRC 1461 Neurotronics: Bio-Inspired Information Pathways"")

  • Thomas CG Bosch

Deutsche Forschungsgemeinschaft (CRC 1461 Neurotronics: Bio-Inspired Information Pathways"")

  • Alexander Klimovich

National Institutes of Health (grant 1 R01 HL 15362201-A)

  • Janna C Nawroth
  • Christoph Giez
  • Alexander Klimovich
  • Eva Kanso

National Science Foundation (INSPIRE grant 1608744)

  • Janna C Nawroth
  • Christoph Giez
  • Alexander Klimovich
  • Eva Kanso

National Science Foundation (RAISE grant)

  • Eva Kanso

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Raymond E Goldstein, University of Cambridge, United Kingdom

Version history

  1. Received: September 22, 2022
  2. Preprint posted: December 2, 2022 (view preprint)
  3. Accepted: June 30, 2023
  4. Accepted Manuscript published: July 3, 2023 (version 1)
  5. Version of Record published: August 2, 2023 (version 2)

Copyright

© 2023, Nawroth et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Janna C Nawroth
  2. Christoph Giez
  3. Alexander Klimovich
  4. Eva Kanso
  5. Thomas CG Bosch
(2023)
Spontaneous body wall contractions stabilize the fluid microenvironment that shapes host-microbe associations
eLife 12:e83637.
https://doi.org/10.7554/eLife.83637

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https://doi.org/10.7554/eLife.83637

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