Response of Vibrio cholerae to Low-Temperature Shifts: CspV Regulation of Type VI Secretion, Biofilm Formation, and Association with Zooplankton

Appl Environ Microbiol. 2016 Jun 30;82(14):4441-52. doi: 10.1128/AEM.00807-16. Print 2016 Jul 15.

Abstract

The ability to sense and adapt to temperature fluctuation is critical to the aquatic survival, transmission, and infectivity of Vibrio cholerae, the causative agent of the disease cholera. Little information is available on the physiological changes that occur when V. cholerae experiences temperature shifts. The genome-wide transcriptional profile of V. cholerae upon a shift in human body temperature (37°C) to lower temperatures, 15°C and 25°C, which mimic those found in the aquatic environment, was determined. Differentially expressed genes included those involved in the cold shock response, biofilm formation, type VI secretion, and virulence. Analysis of a mutant lacking the cold shock gene cspV, which was upregulated >50-fold upon a low-temperature shift, revealed that it regulates genes involved in biofilm formation and type VI secretion. CspV controls biofilm formation through modulation of the second messenger cyclic diguanylate and regulates type VI-mediated interspecies killing in a temperature-dependent manner. Furthermore, a strain lacking cspV had significant defects for attachment and type VI-mediated killing on the surface of the aquatic crustacean Daphnia magna Collectively, these studies reveal that cspV is a major regulator of the temperature downshift response and plays an important role in controlling cellular processes crucial to the infectious cycle of V. cholerae

Importance: Little is known about how human pathogens respond and adapt to ever-changing parameters of natural habitats outside the human host and how environmental adaptation alters dissemination. Vibrio cholerae, the causative agent of the severe diarrheal disease cholera, experiences fluctuations in temperature in its natural aquatic habitats and during the infection process. Furthermore, temperature is a critical environmental signal governing the occurrence of V. cholerae and cholera outbreaks. In this study, we showed that V. cholerae reprograms its transcriptome in response to fluctuations in temperature, which results in changes to biofilm formation and type VI secretion system activation. These processes in turn impact environmental survival and the virulence potential of this pathogen.

MeSH terms

  • Animals
  • Bacterial Adhesion
  • Bacterial Proteins / metabolism*
  • Biofilms / growth & development*
  • Cold Temperature*
  • Daphnia / microbiology
  • Gene Expression Profiling
  • Gene Expression Regulation, Bacterial*
  • Heat-Shock Proteins / metabolism*
  • Stress, Physiological
  • Survival Analysis
  • Type VI Secretion Systems / metabolism*
  • Vibrio cholerae / physiology
  • Vibrio cholerae / radiation effects*
  • Virulence
  • Zooplankton / growth & development*

Substances

  • Bacterial Proteins
  • CspV protein, Vibrio cholerae
  • Heat-Shock Proteins
  • Type VI Secretion Systems