STM2209-STM2208 (opvAB): A Phase Variation Locus of Salmonella enterica Involved in Control of O-Antigen Chain Length

Ignacio Cota,Josep Casadesús,Anne Béatrice Blanc-Potard,Dipshikha Chakravortty

doi:10.1371/journal.pone.0036863

Ignacio Cota, Josep Casadesús + Show 2 more

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https://doi.org/10.1371/journal.pone.0036863

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Journal: PloS one	Publication Date: May 11, 2012
Citations: 82	License type: CC BY 4.0

Affiliation: Universidad de Sevilla, University of Montpellier

Abstract

STM2209 and STM2208 are contiguous loci annotated as putative protein-coding genes in the chromosome of Salmonella enterica. Lack of homologs in related Enterobacteria and low G+C content suggest that S. enterica may have acquired STM2209-STM2208 by horizontal transfer. STM2209 and STM2208 are co-transcribed from a promoter upstream STM2209, and their products are inner (cytoplasmic) membrane proteins. Analysis with the bacterial adenylate cyclase two-hybrid system suggests that STM2209 and STM2208 may interact. Expression of STM2209-STM2208 is subjected to phase variation in wild type Salmonella enterica serovar Typhimurium. Switching frequencies in LB medium are 6.1×10−5 (OFF→ON) and 3.7×10−2 (ON→OFF) per cell and generation. Lack of DNA adenine methylation locks STM2209-STM2208 in the ON state, and lack of the LysR-type factor OxyR locks STM2209-STM2208 in the OFF state. OxyR-dependent activation of STM2209-STM2208 expression is independent of the oxidation state of OxyR. Salmonella cultures locked in the ON state show alteration of O-antigen length in the lipopolysaccharide, reduced absorption of bacteriophage P22, impaired resistance to serum, and reduced proliferation in macrophages. Phenotypic heterogeneity generated by STM2209-STM2208 phase variation may thus provide defense against phages. In turn, formation of a subpopulation unable to proliferate in macrophages may restrain Salmonella spread in animal organs, potentially contributing to successful infection.

Highlights

Phase variation, the reversible switch of gene expression at high frequency (e. g., .1025 per cell and generation), is a common phenomenon in bacteria
This study describes a new phase variation locus in Salmonella enterica serovar Typhimurium
STM2209-STM2208 is a Salmonella-specific locus STM2209 and STM2208 are contiguous loci annotated as putative protein-coding genes in the chromosome of Salmonella enterica

Summary

Introduction

The reversible switch of gene expression at high frequency (e. g., .1025 per cell and generation), is a common phenomenon in bacteria (reviewed in [1,2]). The reversible switch of gene expression at high frequency A consequence of phase variation is phenotypic heterogeneity in clonal bacterial populations, a phenomenon of paramount relevance for bacterial survival in harsh environments. For instance, phenotypic heterogeneity in cell envelope components may facilitate immune evasion and modulation [2,3]. Classical examples of phase variation in pathogenic bacteria involve loci encoding surface-exposed proteins, cell appendixes such as fimbriae, pili, and flagella, and lipopolysaccharide modification functions [1,2,4,5]. Phase variation is not restricted to bacterial pathogens nor to loci that encode components of the cell surface [6,7]

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