Host-selected mutations converging on a global regulator drive an adaptive leap by bacteria to symbiosis

  1. Molly Sabrina Pankey
  2. Randi L Foxall
  3. Ian M Ster
  4. Lauren A Perry
  5. Brian M Schuster
  6. Rachel A Donner
  7. Matthew Coyle
  8. Vaughn S Cooper
  9. Cheryl A Whistler  Is a corresponding author
  1. University of New Hampshire, United States
  2. University of Pittsburgh School of Medicine, United States

Abstract

Host immune and physical barriers protect against pathogens but also impede the establishment of essential symbiotic partnerships. To reveal mechanisms by which beneficial organisms adapt to circumvent host defenses, we experimentally evolved ecologically distinct bioluminescent Vibrio fischeri through Euprymna scolopes squid light organs. Serial squid passaging of bacteria produced eight distinct mutations in the binK sensor kinase gene that conferred an exceptional selective advantage demonstrated through both empirical and theoretical analysis. Squid-adaptive binK alleles promoted colonization and immune evasion that was mediated by cell-associated matrices including symbiotic polysaccharide (Syp) and cellulose. binK variation also altered quorum sensing, raising the threshold for luminescence induction. Preexisting coordinate regulation of symbiosis traits by BinK presented an efficient solution where altered BinK function was the key to unlock multiple colonization barriers. These results identify a genetic basis for microbial adaptability and underscore the importance of hosts as selective agents that shape emergent symbiont populations.

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Article and author information

Author details

  1. Molly Sabrina Pankey

    Department of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7061-9613
  2. Randi L Foxall

    Department of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Ian M Ster

    Department of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Lauren A Perry

    Department of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Brian M Schuster

    Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Rachel A Donner

    Department of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Matthew Coyle

    Department of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Vaughn S Cooper

    Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Cheryl A Whistler

    Department of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, Durham, United States
    For correspondence
    cheryl.whistler@unh.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2301-2069

Funding

National Science Foundation (IOS-1258099)

  • Vaughn S Cooper
  • Cheryl A Whistler

U.S. Department of Agriculture (216015)

  • Cheryl A Whistler

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

Reviewing Editor

  1. Edward G Ruby, University of Hawaii, United States

Publication history

  1. Received: December 19, 2016
  2. Accepted: April 23, 2017
  3. Accepted Manuscript published: April 27, 2017 (version 1)
  4. Version of Record published: June 9, 2017 (version 2)

Copyright

© 2017, Pankey 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. Molly Sabrina Pankey
  2. Randi L Foxall
  3. Ian M Ster
  4. Lauren A Perry
  5. Brian M Schuster
  6. Rachel A Donner
  7. Matthew Coyle
  8. Vaughn S Cooper
  9. Cheryl A Whistler
(2017)
Host-selected mutations converging on a global regulator drive an adaptive leap by bacteria to symbiosis
eLife 6:e24414.
https://doi.org/10.7554/eLife.24414

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