Epigenetic Control of Salmonella enterica O-Antigen Chain Length: A Tradeoff between Virulence and Bacteriophage Resistance

PLoS Genet. 2015 Nov 19;11(11):e1005667. doi: 10.1371/journal.pgen.1005667. eCollection 2015 Nov.

Abstract

The Salmonella enterica opvAB operon is a horizontally-acquired locus that undergoes phase variation under Dam methylation control. The OpvA and OpvB proteins form intertwining ribbons in the inner membrane. Synthesis of OpvA and OpvB alters lipopolysaccharide O-antigen chain length and confers resistance to bacteriophages 9NA (Siphoviridae), Det7 (Myoviridae), and P22 (Podoviridae). These phages use the O-antigen as receptor. Because opvAB undergoes phase variation, S. enterica cultures contain subpopulations of opvABOFF and opvABON cells. In the presence of a bacteriophage that uses the O-antigen as receptor, the opvABOFF subpopulation is killed and the opvABON subpopulation is selected. Acquisition of phage resistance by phase variation of O-antigen chain length requires a payoff: opvAB expression reduces Salmonella virulence. However, phase variation permits resuscitation of the opvABOFF subpopulation as soon as phage challenge ceases. Phenotypic heterogeneity generated by opvAB phase variation thus preadapts Salmonella to survive phage challenge with a fitness cost that is transient only.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacteriophages / genetics
  • Bacteriophages / pathogenicity
  • Genetic Fitness*
  • Lipopolysaccharides / chemistry
  • Lipopolysaccharides / genetics*
  • O Antigens / chemistry
  • O Antigens / genetics*
  • Salmonella enterica / genetics*
  • Salmonella enterica / pathogenicity
  • Salmonella enterica / virology
  • Site-Specific DNA-Methyltransferase (Adenine-Specific) / genetics
  • Virulence / genetics

Substances

  • Lipopolysaccharides
  • O Antigens
  • Dam methyltransferase
  • Site-Specific DNA-Methyltransferase (Adenine-Specific)

Grants and funding

This work was supported by grants BIO2013-44220-R (to JC) and BIO2013-46281-P (to FGdP) from the Ministerio de Economía e Innovación of Spain and the European Regional Fund. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.