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Research Article

Vibrio cholerae adapts to sessile and motile lifestyles by cyclic di-GMP regulation of cell shape

Nicolas L. Fernandez, View ORCID ProfileBrian Y. Hsueh, Nguyen T. Q. Nhu, View ORCID ProfileJoshua L. Franklin, View ORCID ProfileYann S. Dufour, and Christopher M. Waters
  1. aDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824

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PNAS November 17, 2020 117 (46) 29046-29054; first published November 2, 2020; https://doi.org/10.1073/pnas.2010199117
Nicolas L. Fernandez
aDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824
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Brian Y. Hsueh
aDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824
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  • ORCID record for Brian Y. Hsueh
Nguyen T. Q. Nhu
aDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824
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Joshua L. Franklin
aDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824
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  • ORCID record for Joshua L. Franklin
Yann S. Dufour
aDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824
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  • ORCID record for Yann S. Dufour
Christopher M. Waters
aDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824
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  • For correspondence: watersc3@msu.edu
  1. Edited by Caroline S. Harwood, University of Washington, Seattle, WA, and approved September 17, 2020 (received for review May 20, 2020)

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Significance

Form follows function is true of living organisms, including bacteria, as the shapes and morphology they adopt contribute to their biological characteristics. But whether bacteria can actively change their shape to adapt to their environment is less understood. Vibrio cholerae, the pathogenic bacterium responsible for the diarrheal disease cholera, adopts a characteristic “comma”-shaped cell morphology. Here we show that the intracellular signaling molecule, cyclic di-GMP, drives curved V. cholerae to adopt a straight cell morphology that is advantageous to a sessile biofilm lifestyle, while curved V. cholerae are better adapted for swimming. Our research provides a clear example of how bacteria can actively alter their form to impact function.

Abstract

The cell morphology of rod-shaped bacteria is determined by the rigid net of peptidoglycan forming the cell wall. Alterations to the rod shape, such as the curved rod, occur through manipulating the process of cell wall synthesis. The human pathogen Vibrio cholerae typically exists as a curved rod, but straight rods have been observed under certain conditions. While this appears to be a regulated process, the regulatory pathways controlling cell shape transitions in V. cholerae and the benefits of switching between rod and curved shape have not been determined. We demonstrate that cell shape in V. cholerae is regulated by the bacterial second messenger cyclic dimeric guanosine monophosphate (c-di-GMP) by posttranscriptionally repressing expression of crvA, a gene encoding an intermediate filament-like protein necessary for curvature formation in V. cholerae. This regulation is mediated by the transcriptional cascade that also induces production of biofilm matrix components, indicating that cell shape is coregulated with V. cholerae’s induction of sessility. During microcolony formation, wild-type V. cholerae cells tended to exist as straight rods, while genetically engineering cells to maintain high curvature reduced microcolony formation and biofilm density. Conversely, straight V. cholerae mutants have reduced swimming speed when using flagellar motility in liquid. Our results demonstrate regulation of cell shape in bacteria is a mechanism to increase fitness in planktonic and biofilm lifestyles.

  • cell shape
  • crvA
  • cyclic di-GMP
  • biofilm
  • motility

Footnotes

  • ↵1Present address: Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48103.

  • ↵2To whom correspondence may be addressed. Email: watersc3{at}msu.edu.
  • Author contributions: N.L.F., B.Y.H., N.T.Q.N., J.L.F., Y.S.D., and C.M.W. designed research; N.L.F., B.Y.H., and N.T.Q.N. performed research; N.L.F., B.Y.H., N.T.Q.N., J.L.F., Y.S.D., and C.M.W. analyzed data; and N.L.F., Y.S.D., and C.M.W. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • See online for related content such as Commentaries.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2010199117/-/DCSupplemental.

Data Availability.

All study data are included in the article and supporting information.

Published under the PNAS license.

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Vibrio cholerae adapts to sessile and motile lifestyles by cyclic di-GMP regulation of cell shape
Nicolas L. Fernandez, Brian Y. Hsueh, Nguyen T. Q. Nhu, Joshua L. Franklin, Yann S. Dufour, Christopher M. Waters
Proceedings of the National Academy of Sciences Nov 2020, 117 (46) 29046-29054; DOI: 10.1073/pnas.2010199117

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Vibrio cholerae adapts to sessile and motile lifestyles by cyclic di-GMP regulation of cell shape
Nicolas L. Fernandez, Brian Y. Hsueh, Nguyen T. Q. Nhu, Joshua L. Franklin, Yann S. Dufour, Christopher M. Waters
Proceedings of the National Academy of Sciences Nov 2020, 117 (46) 29046-29054; DOI: 10.1073/pnas.2010199117
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  • Straightening up for life in a biofilm
    - Nov 17, 2020
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