A LysR-Type Transcriptional Regulator, RovM, Senses Nutritional Cues Suggesting that It Is Involved in Metabolic Adaptation of Yersinia pestis to the Flea Gut

PLoS One. 2015 Sep 8;10(9):e0137508. doi: 10.1371/journal.pone.0137508. eCollection 2015.

Abstract

Yersinia pestis has evolved as a clonal variant of Yersinia pseudotuberculosis to cause flea-borne biofilm-mediated transmission of the bubonic plague. The LysR-type transcriptional regulator, RovM, is highly induced only during Y. pestis infection of the flea host. RovM homologs in other pathogens regulate biofilm formation, nutrient sensing, and virulence; including in Y. pseudotuberculosis, where RovM represses the major virulence factor, RovA. Here the role that RovM plays during flea infection was investigated using a Y. pestis KIM6+ strain deleted of rovM, ΔrovM. The ΔrovM mutant strain was not affected in characteristic biofilm gut blockage, growth, or survival during single infection of fleas. Nonetheless, during a co-infection of fleas, the ΔrovM mutant exhibited a significant competitive fitness defect relative to the wild type strain. This competitive fitness defect was restored as a fitness advantage relative to the wild type in a ΔrovM mutant complemented in trans to over-express rovM. Consistent with this, Y. pestis strains, producing elevated transcriptional levels of rovM, displayed higher growth rates, and differential ability to form biofilm in response to specific nutrients in comparison to the wild type. In addition, we demonstrated that rovA was not repressed by RovM in fleas, but that elevated transcriptional levels of rovM in vitro correlated with repression of rovA under specific nutritional conditions. Collectively, these findings suggest that RovM likely senses specific nutrient cues in the flea gut environment, and accordingly directs metabolic adaptation to enhance flea gut colonization by Y. pestis.

MeSH terms

  • Animals
  • Bacterial Proteins / biosynthesis
  • Bacterial Proteins / genetics*
  • Biofilms / growth & development
  • Coinfection / genetics
  • Flea Infestations / genetics
  • Flea Infestations / pathology
  • Gene Expression Regulation, Bacterial
  • Humans
  • Insect Vectors / genetics
  • Insect Vectors / pathogenicity
  • Plague / genetics*
  • Plague / pathology
  • Plague / transmission
  • Siphonaptera / genetics
  • Siphonaptera / pathogenicity
  • Transcription Factors / biosynthesis
  • Transcription Factors / genetics*
  • Yersinia pestis / genetics*
  • Yersinia pestis / growth & development
  • Yersinia pestis / pathogenicity
  • Yersinia pseudotuberculosis / genetics
  • Yersinia pseudotuberculosis / pathogenicity

Substances

  • Bacterial Proteins
  • RovA protein, Yersinia
  • RovM protein, Yersinia pseudotuberculosis
  • Transcription Factors

Grant support

The authors have no support or funding to report.