Abstract

ABSTRACTThe Rcs phosphorelay and Psp (phage shock protein) systems are envelope stress responses that are highly conserved in gammaproteobacteria. The Rcs regulon was found to be strongly induced during metal deprivation of Salmonella enterica serovar Typhimurium lacking the Psp response. Nineteen genes activated by the RcsA-RcsB response regulator make up an operon responsible for the production of colanic acid capsular polysaccharide, which promotes biofilm development. Despite more than half a century of research, the physiological function of colanic acid has remained elusive. Here we show that Rcs-dependent colanic acid production maintains the transmembrane electrical potential and proton motive force in cooperation with the Psp response. Production of negatively charged exopolysaccharide covalently bound to the outer membrane may enhance the surface potential by increasing the local proton concentration. This provides a unifying mechanism to account for diverse Rcs/colanic acid-related phenotypes, including susceptibility to membrane-damaging agents and biofilm formation.

Highlights

  • The Rcs phosphorelay and Psp systems are envelope stress responses that are highly conserved in gammaproteobacteria

  • Research conducted over the 50 years since the discovery of colanic acid suggests that this exopolysaccharide plays an important role for bacteria living in biofilms

  • As the Psp response has been shown to preserve proton motive force (PMF) during extracytoplasmic stress [38, 44, 45], we evaluated a possible role for the Rcs stress response and colanic acid capsule biosynthesis in PMF maintenance

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Summary

Introduction

The Rcs phosphorelay and Psp (phage shock protein) systems are envelope stress responses that are highly conserved in gammaproteobacteria. Nineteen genes activated by the RcsA-RcsB response regulator make up an operon responsible for the production of colanic acid capsular polysaccharide, which promotes biofilm development. Production of negatively charged exopolysaccharide covalently bound to the outer membrane may enhance the surface potential by increasing the local proton concentration. This provides a unifying mechanism to account for diverse Rcs/colanic acid-related phenotypes, including susceptibility to membrane-damaging agents and biofilm formation. RcsA-RcsB-regulated genes are primarily involved in exopolysaccharide (EPS) production and include the 19-gene colanic acid capsular operon and the yjbEFGH operon, which encodes the biosynthesis of a distinct EPS [18, 19]. Genes regulated by RcsB independently of RcsA include ftsZ, osmC, and rprA [20,21,22]

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