Pseudomonas aeruginosa EftM Is a Thermoregulated Methyltransferase

J Biol Chem. 2016 Feb 12;291(7):3280-90. doi: 10.1074/jbc.M115.706853. Epub 2015 Dec 16.

Abstract

Pseudomonas aeruginosa is a Gram-negative opportunistic pathogen that trimethylates elongation factor-thermo-unstable (EF-Tu) on lysine 5. Lysine 5 methylation occurs in a temperature-dependent manner and is generally only seen when P. aeruginosa is grown at temperatures close to ambient (25 °C) but not at higher temperatures (37 °C). We have previously identified the gene, eftM (for EF-Tu-modifying enzyme), responsible for this modification and shown its activity to be associated with increased bacterial adhesion to and invasion of respiratory epithelial cells. Bioinformatic analyses predicted EftM to be a Class I S-adenosyl-l-methionine (SAM)-dependent methyltransferase. An in vitro methyltransferase assay was employed to show that, in the presence of SAM, EftM directly trimethylates EF-Tu. A natural variant of EftM, with a glycine to arginine substitution at position 50 in the predicted SAM-binding domain, lacks both SAM binding and enzyme activity. Mass spectrometry analysis of the in vitro methyltransferase reaction products revealed that EftM exclusively methylates at lysine 5 of EF-Tu in a distributive manner. Consistent with the in vivo temperature dependence of methylation of EF-Tu, preincubation of EftM at 37 °C abolished methyltransferase activity, whereas this activity was retained when EftM was preincubated at 25 °C. Irreversible protein unfolding at 37 °C was observed, and we propose that this instability is the molecular basis for the temperature dependence of EftM activity. Collectively, our results show that EftM is a thermolabile, SAM-dependent methyltransferase that directly trimethylates lysine 5 of EF-Tu in P. aeruginosa.

Keywords: EF-Tu; Pseudomonas aeruginosa (P. aeruginosa); S-adenosylmethionine (SAM); circular dichroism (CD); homology modeling; lysine methyltransferase; mass spectrometry (MS); translation elongation factor.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amino Acid Substitution
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Binding Sites
  • Computational Biology
  • Enzyme Stability
  • Isoenzymes / chemistry
  • Isoenzymes / genetics
  • Isoenzymes / metabolism
  • Lysine / metabolism
  • Methylation
  • Models, Molecular*
  • Mutation
  • Peptide Elongation Factor Tu / chemistry
  • Peptide Elongation Factor Tu / genetics
  • Peptide Elongation Factor Tu / metabolism*
  • Protein Conformation
  • Protein Methyltransferases / chemistry
  • Protein Methyltransferases / genetics
  • Protein Methyltransferases / metabolism*
  • Protein Processing, Post-Translational*
  • Protein Unfolding
  • Pseudomonas aeruginosa / enzymology*
  • Pseudomonas aeruginosa / growth & development
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / metabolism
  • S-Adenosylmethionine / metabolism*
  • Sequence Homology, Amino Acid
  • Substrate Specificity
  • Temperature

Substances

  • Bacterial Proteins
  • Isoenzymes
  • Recombinant Fusion Proteins
  • S-Adenosylmethionine
  • Protein Methyltransferases
  • Peptide Elongation Factor Tu
  • Lysine

Associated data

  • PDB/3BXO