Bis-(3'-5')-cyclic dimeric GMP-linked quorum sensing controls swarming in Vibrio parahaemolyticus

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 108; no. 44; pp. 18079 - 18084
• Main Authors: Trimble, Michael J, McCarter, Linda L
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 01-11-2011; National Acad Sciences
• Subjects: Bacteria; Bifunctional enzymes; binding proteins; Binding sites; Biological Sciences; Cell density; Cells; coculture; Coculture techniques; Colonization; Cyclic GMP - analogs & derivatives; Cyclic GMP - metabolism; Enzymes; Gene expression; Gene expression regulation; Genes, Bacterial; Gram-negative bacteria; Intercellular signalling; Language; Luminescence; Pheromones; Plasmids; population size; Proteins; pyridoxal; Quorum Sensing; Second messengers; Signal Transduction; Survival; Swarming; Vibrio; Vibrio parahaemolyticus; Vibrio parahaemolyticus - genetics; Vibrio parahaemolyticus - physiology
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1113790108

Movement over and colonization of surfaces are important survival strategies for bacteria, and many find it advantageous to perform these activities as a group, using quorum sensing to sample population size and synchronize behavior. It is puzzling however, that swarming-proficient and virulent strains of Vibrio parahaemolyticus are silenced for the vibrio archetypal pathway of quorum sensing. Here we describe the S-signal, a pheromone that can be communicated between cells in coculture to regulate surface colonization. This signal was harvested in cell-free supernatants and demonstrated to stimulate swarming gene expression at low cell density. The S-signal was generated by the pyridoxal phosphate-dependent aminotransferase ScrA; signal reception required the periplasmic binding protein ScrB and the membrane-bound GGDEF-EAL domain-containing protein ScrC. ScrC is a bifunctional enzyme that has the ability to form and degrade the second messenger bis-(3'-5') cyclic dimeric GMP (c-di-GMP). ScrA in neighboring cells was able to alter the activity of ScrC in a ScrB-dependent manner, transforming ScrC’s repressing ability to inducing activity with respect to swarming. Conversely, cell–cell signaling repressed capsule gene expression. In summary, we report that quorum sensing can stimulate swarming in V. parahaemolyticus; it does so via an alternative pathway capable of generating an autoinducing signal that influences c-di-GMP, thereby expanding the lexicon and language of cell–cell communication.