A temperature-dependent translational switch controls biofilm development in Vibrio cholerae

Abstract

The gastrointestinal pathogen Vibrio cholerae frequently forms biofilms during its life cycle. Biofilm formation is vital for protection against environmental stresses and is thought to facilitate intestinal colonization. Adaptation to temperature is crucial for V. cholerae survival, as the pathogen is exposed to seasonal temperature variations in the aquatic environment, and temperature fluctuations during host-environment transitions. Here, we show that V. cholerae strains naturally lacking the master biofilm transcriptional regulator HapR are unable to develop colony rugosity at low temperatures. We find that BipA, a ribosome-associated GTPase, accounts for this temperature-dependent control of biofilm formation by repressing translation of the primary biofilm transcriptional activators VpsR and VpsT at low temperatures. In vitro studies demonstrate that low temperatures influence BipA structural conformation and decrease its sensitivity to proteolysis. Proteomic analyses reveal that BipA exerts temperature-dependent control over >200 proteins in V. cholerae involved in a multitude of cell processes, including biofilm assembly. Our study reveals a remarkable new facet of the complex V. cholerae biofilm regulatory cascade and suggests that combined transcriptional-translational control could be a common mechanism by which bacteria adapt to environmental flux.