Impaired respiration elicits SrrAB-dependent programmed cell lysis and biofilm formation in Staphylococcus aureus

  1. Ameya A Mashruwala
  2. Adriana Van De Guchte
  3. Jeffrey M Boyd  Is a corresponding author
  1. Rutgers University, United States

Abstract

Biofilms are communities of microorganisms attached to a surface or each other. Biofilm associated cells are the etiologic agents of recurrent Staphylococcus aureus infections. Infected human tissues are hypoxic or anoxic. S. aureus increases biofilm formation in response to hypoxia, but how this occurs is unknown. In the current study we report that oxygen influences biofilm formation in its capacity as a terminal electron acceptor for cellular respiration. Genetic, physiological, or chemical inhibition of respiratory processes elicited increased biofilm formation. Impaired respiration led to increased cell lysis via divergent regulation of two processes: increased expression of the AtlA murein hydrolase and decreased expression of wall-teichoic acids. The AltA-dependent release of cytosolic DNA contributed to increased biofilm formation. Further, cell lysis and biofilm formation were governed by the SrrAB two-component regulatory system. Data presented support a model wherein SrrAB-dependent biofilm formation occurs in response to the accumulation of reduced menaquinone.

Article and author information

Author details

  1. Ameya A Mashruwala

    Department of Biochemistry and Microbiology, Rutgers University, New Brunswick, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5583-4174
  2. Adriana Van De Guchte

    Department of Biochemistry and Microbiology, Rutgers University, New Brunswick, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jeffrey M Boyd

    Department of Biochemistry and Microbiology, Rutgers University, New Brunswick, United States
    For correspondence
    jmboyd@SEBS.rutgers.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7721-3926

Funding

U.S. Department of Agriculture (multistate project NE1048)

  • Jeffrey M Boyd

Rutgers University Busch Biomedical Grant

  • Jeffrey M Boyd

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

Reviewing Editor

  1. Michael S Gilmore, Harvard Medical School, United States

Version history

  1. Received: December 4, 2016
  2. Accepted: February 20, 2017
  3. Accepted Manuscript published: February 21, 2017 (version 1)
  4. Version of Record published: April 4, 2017 (version 2)

Copyright

© 2017, Mashruwala 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. Ameya A Mashruwala
  2. Adriana Van De Guchte
  3. Jeffrey M Boyd
(2017)
Impaired respiration elicits SrrAB-dependent programmed cell lysis and biofilm formation in Staphylococcus aureus
eLife 6:e23845.
https://doi.org/10.7554/eLife.23845

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https://doi.org/10.7554/eLife.23845

Further reading

  1. A shortage of oxygen causes the bacteria Staphylococcus aureus to form biofilms that protect it from antibiotics.

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