Diaminopimelic Acid Amidation in Corynebacteriales: NEW INSIGHTS INTO THE ROLE OF LtsA IN PEPTIDOGLYCAN MODIFICATION

J Biol Chem. 2015 May 22;290(21):13079-94. doi: 10.1074/jbc.M115.642843. Epub 2015 Apr 6.

Abstract

A gene named ltsA was earlier identified in Rhodococcus and Corynebacterium species while screening for mutations leading to increased cell susceptibility to lysozyme. The encoded protein belonged to a huge family of glutamine amidotransferases whose members catalyze amide nitrogen transfer from glutamine to various specific acceptor substrates. We here describe detailed physiological and biochemical investigations demonstrating the specific role of LtsA protein from Corynebacterium glutamicum (LtsACg) in the modification by amidation of cell wall peptidoglycan diaminopimelic acid (DAP) residues. A morphologically altered but viable ΔltsA mutant was generated, which displays a high susceptibility to lysozyme and β-lactam antibiotics. Analysis of its peptidoglycan structure revealed a total loss of DAP amidation, a modification that was found in 80% of DAP residues in the wild-type polymer. The cell peptidoglycan content and cross-linking were otherwise not modified in the mutant. Heterologous expression of LtsACg in Escherichia coli yielded a massive and toxic incorporation of amidated DAP into the peptidoglycan that ultimately led to cell lysis. In vitro assays confirmed the amidotransferase activity of LtsACg and showed that this enzyme used the peptidoglycan lipid intermediates I and II but not, or only marginally, the UDP-MurNAc pentapeptide nucleotide precursor as acceptor substrates. As is generally the case for glutamine amidotransferases, either glutamine or NH4(+) could serve as the donor substrate for LtsACg. The enzyme did not amidate tripeptide- and tetrapeptide-truncated versions of lipid I, indicating a strict specificity for a pentapeptide chain length.

Keywords: Corynebacteriales; DAP amidation; antibiotics; bacterial metabolism; cell wall; enzyme; gene knockout; glutaminase; lysozyme; peptidoglycan.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amides / chemistry*
  • Amides / metabolism
  • Amino Acid Sequence
  • Anti-Bacterial Agents / pharmacology
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Blotting, Western
  • Cell Wall / metabolism
  • Cells, Cultured
  • Corynebacterium / genetics
  • Corynebacterium / growth & development
  • Corynebacterium / metabolism*
  • Diaminopimelic Acid / chemistry*
  • Diaminopimelic Acid / metabolism
  • Immunoenzyme Techniques
  • Microscopy, Electron, Transmission
  • Molecular Sequence Data
  • Muramidase / metabolism*
  • Mutation / genetics
  • Peptidoglycan / metabolism*
  • RNA, Messenger / genetics
  • Real-Time Polymerase Chain Reaction
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sequence Homology, Amino Acid
  • Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization
  • Transaminases / genetics
  • Transaminases / metabolism*

Substances

  • Amides
  • Anti-Bacterial Agents
  • Bacterial Proteins
  • Peptidoglycan
  • RNA, Messenger
  • Diaminopimelic Acid
  • Transaminases
  • glutamine-pyruvate aminotransferase
  • Muramidase