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Research Article

Carbon Source-Dependent Reprogramming of Anaerobic Metabolism in Staphylococcus aureus

Anne Troitzsch, Vu Van Loi, Karen Methling, Daniela Zühlke, Michael Lalk, Katharina Riedel, Jörg Bernhardt, Eslam M. Elsayed, Gert Bange, Haike Antelmann, Jan Pané-Farré
William W. Metcalf, Editor
Anne Troitzsch
aUniversity of Greifswald, Department of Microbial Physiology and Molecular Biology, Greifswald, Germany
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Vu Van Loi
bFreie Universität Berlin, Institute of Biology-Microbiology, Berlin, Germany
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Karen Methling
cUniversity of Greifswald, Institute for Biochemistry, Greifswald, Germany
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Daniela Zühlke
aUniversity of Greifswald, Department of Microbial Physiology and Molecular Biology, Greifswald, Germany
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Michael Lalk
cUniversity of Greifswald, Institute for Biochemistry, Greifswald, Germany
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Katharina Riedel
aUniversity of Greifswald, Department of Microbial Physiology and Molecular Biology, Greifswald, Germany
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Jörg Bernhardt
aUniversity of Greifswald, Department of Microbial Physiology and Molecular Biology, Greifswald, Germany
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Eslam M. Elsayed
dPhilipps University Marburg, Center for Synthetic Microbiology (SYNMIKRO), Marburg, Germany
ePhilipps University Marburg, Department of Chemistry, Marburg, Germany
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Gert Bange
dPhilipps University Marburg, Center for Synthetic Microbiology (SYNMIKRO), Marburg, Germany
ePhilipps University Marburg, Department of Chemistry, Marburg, Germany
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Haike Antelmann
bFreie Universität Berlin, Institute of Biology-Microbiology, Berlin, Germany
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Jan Pané-Farré
aUniversity of Greifswald, Department of Microbial Physiology and Molecular Biology, Greifswald, Germany
dPhilipps University Marburg, Center for Synthetic Microbiology (SYNMIKRO), Marburg, Germany
ePhilipps University Marburg, Department of Chemistry, Marburg, Germany
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William W. Metcalf
University of Illinois at Urbana Champaign
Roles: Editor
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DOI: 10.1128/JB.00639-20
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ABSTRACT

To be a successful pathogen, Staphylococcus aureus has to adapt its metabolism to the typically oxygen- and glucose-limited environment of the host. Under fermenting conditions and in the presence of glucose, S. aureus uses glycolysis to generate ATP via substrate-level phosphorylation and mainly lactic acid fermentation to maintain the redox balance by reoxidation of NADH equivalents. However, it is less clear how S. aureus proceeds under anoxic conditions and glucose limitation, likely representing the bona fide situation in the host. Using a combination of proteomic, transcriptional, and metabolomic analyses, we show that in the absence of an abundant glycolysis substrate, the available carbon source pyruvate is converted to acetyl coenzyme A (AcCoA) in a pyruvate formate-lyase (PflB)-dependent reaction to produce ATP and acetate. This process critically depends on derepression of the catabolite control protein A (CcpA), leading to upregulation of pflB transcription. Under these conditions, ethanol production is repressed to prevent wasteful consumption of AcCoA. In addition, our global and quantitative characterization of the metabolic switch prioritizing acetate over lactate fermentation when glucose is absent illustrates examples of carbon source-dependent control of colonization and pathogenicity factors.

IMPORTANCE Under infection conditions, S. aureus needs to ensure survival when energy production via oxidative phosphorylation is not possible, e.g., either due to the lack of terminal electron acceptors or by the inactivation of components of the respiratory chain. Under these conditions, S. aureus can switch to mixed-acid fermentation to sustain ATP production by substrate level phosphorylation. The drop in the cellular NAD+/NADH ratio is sensed by the repressor Rex, resulting in derepression of fermentation genes. Here, we show that expression of fermentation pathways is further controlled by CcpA in response to the availability of glucose to ensure optimal resource utilization under growth-limiting conditions. We provide evidence for carbon source-dependent control of colonization and virulence factors. These findings add another level to the regulatory network controlling mixed-acid fermentation in S. aureus and provide additional evidence for the lifestyle-modulating effect of carbon sources available to S. aureus.

FOOTNOTES

    • Received 17 November 2020.
    • Accepted 28 January 2021.
    • Accepted manuscript posted online 1 February 2021.
  • Supplemental material is available online only.

  • Copyright © 2021 American Society for Microbiology.

All Rights Reserved.

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Carbon Source-Dependent Reprogramming of Anaerobic Metabolism in Staphylococcus aureus
Anne Troitzsch, Vu Van Loi, Karen Methling, Daniela Zühlke, Michael Lalk, Katharina Riedel, Jörg Bernhardt, Eslam M. Elsayed, Gert Bange, Haike Antelmann, Jan Pané-Farré
Journal of Bacteriology Mar 2021, 203 (8) e00639-20; DOI: 10.1128/JB.00639-20

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Carbon Source-Dependent Reprogramming of Anaerobic Metabolism in Staphylococcus aureus
Anne Troitzsch, Vu Van Loi, Karen Methling, Daniela Zühlke, Michael Lalk, Katharina Riedel, Jörg Bernhardt, Eslam M. Elsayed, Gert Bange, Haike Antelmann, Jan Pané-Farré
Journal of Bacteriology Mar 2021, 203 (8) e00639-20; DOI: 10.1128/JB.00639-20
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KEYWORDS

Staphylococcus aureus
anaerobiosis
CcpA

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