SrrAB modulates Staphylococcus aureus cell death through regulation of cidABC transcription

Ian H. Windham, Sujata S. Chaudhari, Jeffrey L. Bose, Vinai Chittezham Thomas, Kenneth W Bayles

Research output: Contribution to journalArticle

11 Citations (Scopus)

Abstract

The death and lysis of a subpopulation in Staphylococcus aureus biofilm cells are thought to benefit the surviving population by releasing extracellular DNA, a critical component of the biofilm extracellular matrix. Although the means by which S. aureus controls cell death and lysis is not understood, studies implicate the role of the cidABC and lrgAB operons in this process. Recently, disruption of the srrAB regulatory locus was found to cause increased cell death during biofilm development, likely as a result of the sensitivity of this mutant to hypoxic growth. In the current study, we extended these findings by demonstrating that cell death in the ΔsrrAB mutant is dependent on expression of the cidABC operon. The effect of cidABC expression resulted in the generation of increased reactive oxygen species (ROS) accumulation and was independent of acetate production. Interestingly, consistently with previous studies, cidC-encoded pyruvate oxidase was found to be important for the generation of acetic acid, which initiates the cell death process. However, these studies also revealed for the first time an important role of the cidB gene in cell death, as disruption of cidB in the ΔsrrAB mutant background decreased ROS generation and cell death in a cidCindependent manner. The cidB mutation also caused decreased sensitivity to hydrogen peroxide, which suggests a complex role for this system in ROS metabolism. Overall, the results of this study provide further insight into the function of the cidABC operon in cell death and reveal its contribution to the oxidative stress response.

Original languageEnglish (US)
Pages (from-to)1114-1122
Number of pages9
JournalJournal of bacteriology
Volume198
Issue number7
DOIs
StatePublished - Jan 1 2016

Fingerprint

Staphylococcus aureus
Cell Death
Operon
Biofilms
Reactive Oxygen Species
Pyruvate Oxidase
Acetic Acid
Hydrogen Peroxide
Extracellular Matrix
Acetates
Oxidative Stress
Mutation
DNA
Growth
Population
Genes

ASJC Scopus subject areas

  • Microbiology
  • Molecular Biology

Cite this

SrrAB modulates Staphylococcus aureus cell death through regulation of cidABC transcription. / Windham, Ian H.; Chaudhari, Sujata S.; Bose, Jeffrey L.; Chittezham Thomas, Vinai; Bayles, Kenneth W.

In: Journal of bacteriology, Vol. 198, No. 7, 01.01.2016, p. 1114-1122.

Research output: Contribution to journalArticle

@article{fd68ee675eb247618b1e7c6e33848639,
title = "SrrAB modulates Staphylococcus aureus cell death through regulation of cidABC transcription",
abstract = "The death and lysis of a subpopulation in Staphylococcus aureus biofilm cells are thought to benefit the surviving population by releasing extracellular DNA, a critical component of the biofilm extracellular matrix. Although the means by which S. aureus controls cell death and lysis is not understood, studies implicate the role of the cidABC and lrgAB operons in this process. Recently, disruption of the srrAB regulatory locus was found to cause increased cell death during biofilm development, likely as a result of the sensitivity of this mutant to hypoxic growth. In the current study, we extended these findings by demonstrating that cell death in the ΔsrrAB mutant is dependent on expression of the cidABC operon. The effect of cidABC expression resulted in the generation of increased reactive oxygen species (ROS) accumulation and was independent of acetate production. Interestingly, consistently with previous studies, cidC-encoded pyruvate oxidase was found to be important for the generation of acetic acid, which initiates the cell death process. However, these studies also revealed for the first time an important role of the cidB gene in cell death, as disruption of cidB in the ΔsrrAB mutant background decreased ROS generation and cell death in a cidCindependent manner. The cidB mutation also caused decreased sensitivity to hydrogen peroxide, which suggests a complex role for this system in ROS metabolism. Overall, the results of this study provide further insight into the function of the cidABC operon in cell death and reveal its contribution to the oxidative stress response.",
author = "Windham, {Ian H.} and Chaudhari, {Sujata S.} and Bose, {Jeffrey L.} and {Chittezham Thomas}, Vinai and Bayles, {Kenneth W}",
year = "2016",
month = "1",
day = "1",
doi = "10.1128/JB.00954-15",
language = "English (US)",
volume = "198",
pages = "1114--1122",
journal = "Journal of Bacteriology",
issn = "0021-9193",
publisher = "American Society for Microbiology",
number = "7",

}

TY - JOUR

T1 - SrrAB modulates Staphylococcus aureus cell death through regulation of cidABC transcription

AU - Windham, Ian H.

AU - Chaudhari, Sujata S.

AU - Bose, Jeffrey L.

AU - Chittezham Thomas, Vinai

AU - Bayles, Kenneth W

PY - 2016/1/1

Y1 - 2016/1/1

N2 - The death and lysis of a subpopulation in Staphylococcus aureus biofilm cells are thought to benefit the surviving population by releasing extracellular DNA, a critical component of the biofilm extracellular matrix. Although the means by which S. aureus controls cell death and lysis is not understood, studies implicate the role of the cidABC and lrgAB operons in this process. Recently, disruption of the srrAB regulatory locus was found to cause increased cell death during biofilm development, likely as a result of the sensitivity of this mutant to hypoxic growth. In the current study, we extended these findings by demonstrating that cell death in the ΔsrrAB mutant is dependent on expression of the cidABC operon. The effect of cidABC expression resulted in the generation of increased reactive oxygen species (ROS) accumulation and was independent of acetate production. Interestingly, consistently with previous studies, cidC-encoded pyruvate oxidase was found to be important for the generation of acetic acid, which initiates the cell death process. However, these studies also revealed for the first time an important role of the cidB gene in cell death, as disruption of cidB in the ΔsrrAB mutant background decreased ROS generation and cell death in a cidCindependent manner. The cidB mutation also caused decreased sensitivity to hydrogen peroxide, which suggests a complex role for this system in ROS metabolism. Overall, the results of this study provide further insight into the function of the cidABC operon in cell death and reveal its contribution to the oxidative stress response.

AB - The death and lysis of a subpopulation in Staphylococcus aureus biofilm cells are thought to benefit the surviving population by releasing extracellular DNA, a critical component of the biofilm extracellular matrix. Although the means by which S. aureus controls cell death and lysis is not understood, studies implicate the role of the cidABC and lrgAB operons in this process. Recently, disruption of the srrAB regulatory locus was found to cause increased cell death during biofilm development, likely as a result of the sensitivity of this mutant to hypoxic growth. In the current study, we extended these findings by demonstrating that cell death in the ΔsrrAB mutant is dependent on expression of the cidABC operon. The effect of cidABC expression resulted in the generation of increased reactive oxygen species (ROS) accumulation and was independent of acetate production. Interestingly, consistently with previous studies, cidC-encoded pyruvate oxidase was found to be important for the generation of acetic acid, which initiates the cell death process. However, these studies also revealed for the first time an important role of the cidB gene in cell death, as disruption of cidB in the ΔsrrAB mutant background decreased ROS generation and cell death in a cidCindependent manner. The cidB mutation also caused decreased sensitivity to hydrogen peroxide, which suggests a complex role for this system in ROS metabolism. Overall, the results of this study provide further insight into the function of the cidABC operon in cell death and reveal its contribution to the oxidative stress response.

UR - http://www.scopus.com/inward/record.url?scp=84961125184&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84961125184&partnerID=8YFLogxK

U2 - 10.1128/JB.00954-15

DO - 10.1128/JB.00954-15

M3 - Article

C2 - 26811317

AN - SCOPUS:84961125184

VL - 198

SP - 1114

EP - 1122

JO - Journal of Bacteriology

JF - Journal of Bacteriology

SN - 0021-9193

IS - 7

ER -