Staphylococcus aureus CidC Is a Pyruvate:Menaquinone Oxidoreductase

Xinyan Zhang, Kenneth W Bayles, Sorin Luca

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Recent studies have revealed an important role for the Staphylococcus aureus CidC enzyme in cell death during the stationary phase and in biofilm development and have contributed to our understanding of the metabolic processes that are important in the induction of bacterial programmed cell death (PCD). To gain more insight into the characteristics of this enzyme, we performed an in-depth biochemical and biophysical analysis of its catalytic properties. In vitro experiments show that this flavoprotein catalyzes the oxidative decarboxylation of pyruvate to acetate and carbon dioxide. CidC efficiently reduces menadione, but not CoenzymeQ0, suggesting a specific role in the S. aureus respiratory chain. CidC exists as a monomer under neutral-pH conditions but tends to aggregate and bind to artificial lipid membranes at acidic pH, resulting in enhanced enzymatic activity. Unlike its Escherichia coli counterpart, PoxB, CidC does not appear to be activated by other amphiphiles like Triton X-100 or octyl β-d-glucopyranoside. In addition, only reduced CidC is protected from proteolytic cleavage by chymotrypsin, and unlike its homologues in other bacteria, protease treatment does not increase CidC enzymatic activity. Finally, CidC exhibits maximal activity at pH 5.5-5.8 and negligible activity at pH 7-8. The results of this study are consistent with a model in which CidC functions as a pyruvate:menaquinone oxidoreductase whose activity is induced at the cellular membrane during cytoplasmic acidification, a process previously shown to be important for the induction of bacterial PCD.

Original languageEnglish (US)
Pages (from-to)4819-4829
Number of pages11
JournalBiochemistry
Volume56
Issue number36
DOIs
StatePublished - Sep 12 2017

Fingerprint

Pyruvate Synthase
Vitamin K 2
Cell death
Pyruvic Acid
Staphylococcus aureus
Oxidoreductases
Cell Death
Vitamin K 3
Flavoproteins
Amphiphiles
Acidification
Octoxynol
Chymotrypsin
Biofilms
Enzymes
Membrane Lipids
Artificial Membranes
Carbon Dioxide
Escherichia coli
Decarboxylation

ASJC Scopus subject areas

  • Biochemistry

Cite this

Staphylococcus aureus CidC Is a Pyruvate:Menaquinone Oxidoreductase. / Zhang, Xinyan; Bayles, Kenneth W; Luca, Sorin.

In: Biochemistry, Vol. 56, No. 36, 12.09.2017, p. 4819-4829.

Research output: Contribution to journalArticle

Zhang, Xinyan ; Bayles, Kenneth W ; Luca, Sorin. / Staphylococcus aureus CidC Is a Pyruvate:Menaquinone Oxidoreductase. In: Biochemistry. 2017 ; Vol. 56, No. 36. pp. 4819-4829.
@article{b34ac09eedb443598e68733b159bd029,
title = "Staphylococcus aureus CidC Is a Pyruvate:Menaquinone Oxidoreductase",
abstract = "Recent studies have revealed an important role for the Staphylococcus aureus CidC enzyme in cell death during the stationary phase and in biofilm development and have contributed to our understanding of the metabolic processes that are important in the induction of bacterial programmed cell death (PCD). To gain more insight into the characteristics of this enzyme, we performed an in-depth biochemical and biophysical analysis of its catalytic properties. In vitro experiments show that this flavoprotein catalyzes the oxidative decarboxylation of pyruvate to acetate and carbon dioxide. CidC efficiently reduces menadione, but not CoenzymeQ0, suggesting a specific role in the S. aureus respiratory chain. CidC exists as a monomer under neutral-pH conditions but tends to aggregate and bind to artificial lipid membranes at acidic pH, resulting in enhanced enzymatic activity. Unlike its Escherichia coli counterpart, PoxB, CidC does not appear to be activated by other amphiphiles like Triton X-100 or octyl β-d-glucopyranoside. In addition, only reduced CidC is protected from proteolytic cleavage by chymotrypsin, and unlike its homologues in other bacteria, protease treatment does not increase CidC enzymatic activity. Finally, CidC exhibits maximal activity at pH 5.5-5.8 and negligible activity at pH 7-8. The results of this study are consistent with a model in which CidC functions as a pyruvate:menaquinone oxidoreductase whose activity is induced at the cellular membrane during cytoplasmic acidification, a process previously shown to be important for the induction of bacterial PCD.",
author = "Xinyan Zhang and Bayles, {Kenneth W} and Sorin Luca",
year = "2017",
month = "9",
day = "12",
doi = "10.1021/acs.biochem.7b00570",
language = "English (US)",
volume = "56",
pages = "4819--4829",
journal = "Biochemistry",
issn = "0006-2960",
publisher = "American Chemical Society",
number = "36",

}

TY - JOUR

T1 - Staphylococcus aureus CidC Is a Pyruvate:Menaquinone Oxidoreductase

AU - Zhang, Xinyan

AU - Bayles, Kenneth W

AU - Luca, Sorin

PY - 2017/9/12

Y1 - 2017/9/12

N2 - Recent studies have revealed an important role for the Staphylococcus aureus CidC enzyme in cell death during the stationary phase and in biofilm development and have contributed to our understanding of the metabolic processes that are important in the induction of bacterial programmed cell death (PCD). To gain more insight into the characteristics of this enzyme, we performed an in-depth biochemical and biophysical analysis of its catalytic properties. In vitro experiments show that this flavoprotein catalyzes the oxidative decarboxylation of pyruvate to acetate and carbon dioxide. CidC efficiently reduces menadione, but not CoenzymeQ0, suggesting a specific role in the S. aureus respiratory chain. CidC exists as a monomer under neutral-pH conditions but tends to aggregate and bind to artificial lipid membranes at acidic pH, resulting in enhanced enzymatic activity. Unlike its Escherichia coli counterpart, PoxB, CidC does not appear to be activated by other amphiphiles like Triton X-100 or octyl β-d-glucopyranoside. In addition, only reduced CidC is protected from proteolytic cleavage by chymotrypsin, and unlike its homologues in other bacteria, protease treatment does not increase CidC enzymatic activity. Finally, CidC exhibits maximal activity at pH 5.5-5.8 and negligible activity at pH 7-8. The results of this study are consistent with a model in which CidC functions as a pyruvate:menaquinone oxidoreductase whose activity is induced at the cellular membrane during cytoplasmic acidification, a process previously shown to be important for the induction of bacterial PCD.

AB - Recent studies have revealed an important role for the Staphylococcus aureus CidC enzyme in cell death during the stationary phase and in biofilm development and have contributed to our understanding of the metabolic processes that are important in the induction of bacterial programmed cell death (PCD). To gain more insight into the characteristics of this enzyme, we performed an in-depth biochemical and biophysical analysis of its catalytic properties. In vitro experiments show that this flavoprotein catalyzes the oxidative decarboxylation of pyruvate to acetate and carbon dioxide. CidC efficiently reduces menadione, but not CoenzymeQ0, suggesting a specific role in the S. aureus respiratory chain. CidC exists as a monomer under neutral-pH conditions but tends to aggregate and bind to artificial lipid membranes at acidic pH, resulting in enhanced enzymatic activity. Unlike its Escherichia coli counterpart, PoxB, CidC does not appear to be activated by other amphiphiles like Triton X-100 or octyl β-d-glucopyranoside. In addition, only reduced CidC is protected from proteolytic cleavage by chymotrypsin, and unlike its homologues in other bacteria, protease treatment does not increase CidC enzymatic activity. Finally, CidC exhibits maximal activity at pH 5.5-5.8 and negligible activity at pH 7-8. The results of this study are consistent with a model in which CidC functions as a pyruvate:menaquinone oxidoreductase whose activity is induced at the cellular membrane during cytoplasmic acidification, a process previously shown to be important for the induction of bacterial PCD.

UR - http://www.scopus.com/inward/record.url?scp=85029378745&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85029378745&partnerID=8YFLogxK

U2 - 10.1021/acs.biochem.7b00570

DO - 10.1021/acs.biochem.7b00570

M3 - Article

C2 - 28809546

AN - SCOPUS:85029378745

VL - 56

SP - 4819

EP - 4829

JO - Biochemistry

JF - Biochemistry

SN - 0006-2960

IS - 36

ER -