Characterization of N-Succinylation of L-Lysylphosphatidylglycerol in Bacillus subtilis Using Tandem Mass Spectrometry

J Am Soc Mass Spectrom. 2016 Oct;27(10):1606-13. doi: 10.1007/s13361-016-1455-4. Epub 2016 Aug 9.

Abstract

Phospholipids generally dominate in bacterial lipids. The negatively charged nature of phospholipids renders bacteria susceptible to cationic antibiotic peptides. In comparison with Gram-negative bacteria, Gram-positive bacteria in general have much less zwitterionic phosphatidylethanolamine. However, they are known for producing aminoacylated phosphatidylglycerol (PG), especially positively charged L-lysyl-PG, which is catalyzed by lysyl-PG synthase MprF, which appears to have a broad range of specificity for L-aminoacyl transfer RNAs. In addition, many Gram-positive bacteria also have a dlt-gene-coded D-alanylation pathway for lipoteichoic acids and wall teichoic acids covalently attached to a glycolipid or peptidoglycan. D-Alanylation also masks the dominant negative charge of the phosphate-rich polymers of teichoic acids. Using mass spectrometry, we have recently observed that precursor scans in negative mode for deprotonated amino acid fragments were most sensitive for ester-linked amino acids. Such a scan for precursors generating an m/z 145 lysyl anion revealed lysyl-PG as well as an additional species 100 m/z units greater than lysyl-PG. This unexpected species corresponded precisely to the expected mass of N-succinylated lysyl-PG. Tandem mass spectrometry revealed a precise match to the fragmentation pattern of this putative new species. PG, lysyl-PG, and N-succinyl-lysyl-PG may form a complete loop of charge reversal from -1 to +1 and then back to -1. Analogous charge reversal by N-succinylation of lysine residues in the bacterial as well as eukaryotic proteomes has been recently discovered as a major posttranslational modification. Such modification in bacterial lipids is possibly catalyzed by an enzyme homologous to the enzymes that modify lysine residues in proteins. Graphical Abstract ᅟ.

Keywords: Charge modulation; Lipid; Lysine succinylation; MS2; MS3; Mass Spectrometry; Phosphatidylglycerol; Phospholipid; lysyl-phosphatidylglycerol; succinyl-lysyl-phosphatidylglycerol.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aminoacyltransferases
  • Anti-Bacterial Agents
  • Bacillus subtilis*
  • Bacterial Proteins
  • Lysine / analysis*
  • Phosphatidylglycerols / analysis*
  • Staphylococcus aureus
  • Tandem Mass Spectrometry*

Substances

  • Anti-Bacterial Agents
  • Bacterial Proteins
  • Phosphatidylglycerols
  • lysylphosphatidylglycerol
  • Aminoacyltransferases
  • Lysine