Temperature affects c-di-GMP signalling and biofilm formation in Vibrio cholerae

Environ Microbiol. 2015 Nov;17(11):4290-305. doi: 10.1111/1462-2920.12799. Epub 2015 Mar 25.

Abstract

Biofilm formation is crucial to the environmental survival and transmission of Vibrio cholerae, the facultative human pathogen responsible for the disease cholera. During its infectious cycle, V. cholerae experiences fluctuations in temperature within the aquatic environment and during the transition between human host and aquatic reservoirs. In this study, we report that biofilm formation is induced at low temperatures through increased levels of the signalling molecule, cyclic diguanylate (c-di-GMP). Strains harbouring in frame deletions of all V. cholerae genes that are predicted to encode diguanylate cyclases (DGCs) or phosphodiesterases (PDEs) were screened for their involvement in low-temperature-induced biofilm formation and Vibrio polysaccharide gene expression. Of the 52 mutants tested, deletions of six DGCs and three PDEs were found to affect these phenotypes at low temperatures. Unlike wild type, a strain lacking all six DGCs did not exhibit a low-temperature-dependent increase in c-di-GMP, indicating that these DGCs are required for temperature modulation of c-di-GMP levels. We also show that temperature modulates c-di-GMP levels in a similar fashion in the Gram-negative pathogen Pseudomonas aeruginosa but not in the Gram-positive pathogen Listeria monocytogenes. This study uncovers the role of temperature in environmental regulation of biofilm formation and c-di-GMP signalling.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Biofilms / growth & development*
  • Cholera / microbiology
  • Cholera / transmission*
  • Cyclic GMP / analogs & derivatives*
  • Cyclic GMP / metabolism
  • Escherichia coli Proteins / genetics
  • Humans
  • Listeria monocytogenes / growth & development
  • Listeria monocytogenes / metabolism
  • Phosphoric Diester Hydrolases / genetics
  • Phosphorus-Oxygen Lyases / genetics
  • Pseudomonas aeruginosa / growth & development
  • Pseudomonas aeruginosa / metabolism
  • Sequence Deletion / genetics
  • Signal Transduction / physiology
  • Temperature*
  • Vibrio cholerae / genetics
  • Vibrio cholerae / growth & development*
  • Vibrio cholerae / metabolism

Substances

  • Escherichia coli Proteins
  • bis(3',5')-cyclic diguanylic acid
  • Phosphoric Diester Hydrolases
  • Phosphorus-Oxygen Lyases
  • diguanylate cyclase
  • Cyclic GMP