Accumulation of Succinyl Coenzyme A Perturbs the Methicillin-Resistant Staphylococcus aureus (MRSA) Succinylome and Is Associated with Increased Susceptibility to Beta-Lactam Antibiotics

Campbell, Christopher; Fingleton, Claire; Zeden, Merve S.; Bueno, Emilio; Gallagher, Laura A.; Shinde, Dhananjay; Ahn, Jongsam; Olson, Heather M.; Fillmore, Thomas L.; Adkins, Joshua N.; Razvi, Fareha; Bayles, Kenneth W.; Fey, Paul D.; Thomas, Vinai C.; Cava, Felipe; Clair, Geremy C.; O’Gara, James P.; Torres, ed., Victor J.

doi:10.1128/mBio.00530-21

Title: Accumulation of Succinyl Coenzyme A Perturbs the Methicillin-Resistant Staphylococcus aureus (MRSA) Succinylome and Is Associated with Increased Susceptibility to Beta-Lactam Antibiotics

Journal Article · Tue Jun 29 00:00:00 EDT 2021 · mBio (Online)

DOI:https://doi.org/10.1128/mBio.00530-21· OSTI ID:1804130

^[1];

^[1]; Bueno, Emilio ^[2]; Gallagher, Laura A. ^[1]; Shinde, Dhananjay ^[3]; Ahn, Jongsam ^[3]; Olson, Heather M. ^[4]; Fillmore, Thomas L. ^[4]; Adkins, Joshua N. ^[4]; Razvi, Fareha ^[3]; Bayles, Kenneth W. ^[3];

^[3];

^[2];

^[4];

^[1]; Torres, ed., Victor J.

Microbiology, School of Natural Sciences, National University of Ireland, Galway, Ireland
MIMS-Molecular Infection Medicine Sweden, Molecular Biology Department, Umeå University, Umeå, Sweden
Department of Pathology and Microbiology, University of Nebraska Medical Center, Omaha, Nebraska, USA
Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA

Penicillin binding protein 2a (PBP2a)-dependent resistance to β-lactam antibiotics in methicillin-resistant Staphylococcus aureus (MRSA) is regulated by the activity of the tricarboxylic acid (TCA) cycle via a poorly understood mechanism. We report that mutations in sucC and sucD, but not other TCA cycle enzymes, negatively impact β-lactam resistance without changing PBP2a expression. Increased intracellular levels of succinyl coenzyme A (succinyl-CoA) in the sucC mutant significantly perturbed lysine succinylation in the MRSA proteome. Suppressor mutations in sucA or sucB, responsible for succinyl-CoA biosynthesis, reversed sucC mutant phenotypes. The major autolysin (Atl) was the most succinylated protein in the proteome, and increased Atl succinylation in the sucC mutant was associated with loss of autolytic activity. Although PBP2a and PBP2 were also among the most succinylated proteins in the MRSA proteome, peptidoglycan architecture and cross-linking were unchanged in the sucC mutant. These data reveal that perturbation of the MRSA succinylome impacts two interconnected cell wall phenotypes, leading to repression of autolytic activity and increased susceptibility to β-lactam antibiotics.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Institute of Allergy and Infectious Diseases (NIAID)

Grant/Contract Number:: AC05-76RLO 1830; AC05-76RL01830

OSTI ID:: 1804130

Alternate ID(s):: OSTI ID: 1959058

Report Number(s):: PNNL-SA-166791; e00530-21

Journal Information:: mBio (Online), Journal Name: mBio (Online) Vol. 12 Journal Issue: 3; ISSN 2150-7511

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
MRSA
TCA cycle
antibiotic resistance
beta-lactams
succinyl-CoA
succinylome

Title: Accumulation of Succinyl Coenzyme A Perturbs the Methicillin-Resistant Staphylococcus aureus (MRSA) Succinylome and Is Associated with Increased Susceptibility to Beta-Lactam Antibiotics

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