The Acyl-Proteome of Syntrophus aciditrophicus Reveals Metabolic Relationships in Benzoate Degradation

John M Muroski; Janine Y Fu; Hong Hanh Nguyen; Neil Q Wofford; Housna Mouttaki; Kimberly L James; Michael J McInerney; Robert P Gunsalus; Joseph A Loo; Rachel R Ogorzalek Loo

doi:10.1016/j.mcpro.2022.100215

The Acyl-Proteome of Syntrophus aciditrophicus Reveals Metabolic Relationships in Benzoate Degradation

Mol Cell Proteomics. 2022 Apr;21(4):100215. doi: 10.1016/j.mcpro.2022.100215. Epub 2022 Feb 19.

Affiliations

¹ Department of Chemistry and Biochemistry, University of California, Los Angeles, California, USA.
² TRANSMED Co Ltd, Ho Chi Minh City, Vietnam.
³ Department of Microbiology and Plant Biology, University of Oklahoma, Norman, Oklahoma, USA.
⁴ Department of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles, Los Angeles, California, USA; UCLA-DOE Institute, University of California, Los Angeles, California, USA; UCLA Molecular Biology Institute, University of California, Los Angeles, California, USA.
⁵ Department of Chemistry and Biochemistry, University of California, Los Angeles, California, USA; UCLA-DOE Institute, University of California, Los Angeles, California, USA; UCLA Molecular Biology Institute, University of California, Los Angeles, California, USA; Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles, California, USA.
⁶ Department of Chemistry and Biochemistry, University of California, Los Angeles, California, USA; UCLA-DOE Institute, University of California, Los Angeles, California, USA; UCLA Molecular Biology Institute, University of California, Los Angeles, California, USA. Electronic address: rloo@mednet.ucla.edu.

Abstract

Syntrophus aciditrophicus is a model syntrophic bacterium that degrades fatty and aromatic acids into acetate, CO₂, formate, and H₂ that are utilized by methanogens and other hydrogen-consuming microbes. S. aciditrophicus benzoate degradation proceeds by a multistep pathway with many intermediate reactive acyl-coenzyme A species (RACS) that can potentially N^ε-acylate lysine residues. Herein, we describe the identification and characterization of acyl-lysine modifications that correspond to RACS in the benzoate degradation pathway. The amounts of modified peptides are sufficient to analyze the post-translational modifications without antibody enrichment, enabling a range of acylations located, presumably, on the most extensively acylated proteins throughout the proteome to be studied. Seven types of acyl modifications were identified, six of which correspond directly to RACS that are intermediates in the benzoate degradation pathway including 3-hydroxypimeloylation, a modification first identified in this system. Indeed, benzoate-degrading enzymes are heavily represented among the acylated proteins. A total of 125 sites were identified in 60 proteins. Functional deacylase enzymes are present in the proteome, indicating a potential regulatory system/mechanism by which S. aciditrophicus modulates acylation. Uniquely, N^ε-acyl-lysine RACS are highly abundant in these syntrophic bacteria, raising the compelling possibility that post-translational modifications modulate benzoate degradation in this and potentially other, syntrophic bacteria. Our results outline candidates for further study of how acylations impact syntrophic consortia.

Keywords: Syntrophus aciditrophicus; lysine acylation; sirtuins; syntrophs.

Publication types

Research Support, N.I.H., Extramural
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Bacteria / metabolism
Benzoates / metabolism
Deltaproteobacteria* / metabolism
Lysine / metabolism
Proteome* / metabolism

The Acyl-Proteome of Syntrophus aciditrophicus Reveals Metabolic Relationships in Benzoate Degradation

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