Bacteriophage Predation Promotes Serovar Diversification in Listeria Monocytogenes

Mol Microbiol. 2015 Jul;97(1):33-46. doi: 10.1111/mmi.13009. Epub 2015 Apr 24.

Abstract

Listeria monocytogenes is a bacterial pathogen classified into distinct serovars (SVs) based on somatic and flagellar antigens. To correlate phenotype with genetic variation, we analyzed the wall teichoic acid (WTA) glycosylation genes of SV 1/2, 3 and 7 strains, which differ in decoration of the ribitol-phosphate backbone with N-acetylglucosamine (GlcNAc) and/or rhamnose. Inactivation of lmo1080 or the dTDP-l-rhamnose biosynthesis genes rmlACBD (lmo1081-1084) resulted in loss of rhamnose, whereas disruption of lmo1079 led to GlcNAc deficiency. We found that all SV 3 and 7 strains actually originate from a SV 1/2 background, as a result of small mutations in WTA rhamnosylation and/or GlcNAcylation genes. Genetic complementation of different SV 3 and 7 isolates using intact alleles fully restored a characteristic SV 1/2 WTA carbohydrate pattern, including antisera reactions and phage adsorption. Intriguingly, phage-resistant L. monocytogenes EGDe (SV 1/2a) isolates featured the same glycosylation gene mutations and were serotyped as SV 3 or 7 respectively. Again, genetic complementation restored both carbohydrate antigens and phage susceptibility. Taken together, our data demonstrate that L. monocytogenes SV 3 and 7 originate from point mutations in glycosylation genes, and we show that phage predation represents a major driving force for serovar diversification and evolution of L. monocytogenes.

MeSH terms

  • Acetylglucosamine / metabolism
  • Bacteriophages / genetics
  • Bacteriophages / physiology*
  • Cell Wall / chemistry*
  • Cell Wall / genetics
  • Cell Wall / metabolism
  • Genetic Complementation Test
  • Genetic Variation
  • Glycosylation
  • Listeria monocytogenes / classification*
  • Listeria monocytogenes / genetics
  • Listeria monocytogenes / virology*
  • Molecular Sequence Data
  • Nucleoside Diphosphate Sugars / genetics
  • Phenotype
  • Point Mutation
  • Rhamnose / metabolism
  • Serogroup
  • Serotyping
  • Teichoic Acids / genetics*
  • Teichoic Acids / metabolism
  • Thymine Nucleotides / genetics

Substances

  • Nucleoside Diphosphate Sugars
  • Teichoic Acids
  • Thymine Nucleotides
  • thymidine diphosphate rhamnose
  • Rhamnose
  • Acetylglucosamine

Associated data

  • GENBANK/AL591824