Bacterial cyclic diguanylate signaling networks sense temperature
Henrik Almblad, Trevor E. Randall, Fanny Liu, Katherine Leblanc, Ryan A. Groves, Weerayuth Kittichotirat, Geoffrey L. Winsor, Nicolas Fournier, Emily Au, Julie Groizeleau, Jacquelyn D. Rich, Yuefei Lou, Elise Granton, Laura K. Jennings, Larissa A. Singletary, Tara M. L. Winstone, Nathan Good, Roger E. Bumgarner, Michael F. Hynes, Manu Singh, María Silvina Stietz, Fiona S. L. Brinkman, Ayush Kumar, Ann Karen C. Brassinga, Matthew R. Parsek, Boo Shan Tseng, Ian A. Lewis, Bryan G. Yipp, Justin L. MacCallum, Joe J. Harrison
Abstract
Many bacteria use the second messenger cyclic diguanylate (c-di-GMP) to control motility, biofilm production and virulence. Here, we identify a thermosensory diguanylate cyclase (TdcA) that modulates temperature-dependent motility, biofilm development and virulence in the opportunistic pathogen Pseudomonas aeruginosa. TdcA synthesizes c-di-GMP with catalytic rates that increase more than a hundred-fold over a ten-degree Celsius change. Analyses using protein chimeras indicate that heat-sensing is mediated by a thermosensitive Per-Arnt-SIM (PAS) domain. TdcA homologs are widespread in sequence databases, and a distantly related, heterologously expressed homolog from the Betaproteobacteria order Gallionellales also displayed thermosensitive diguanylate cyclase activity. We propose, therefore, that thermotransduction is a conserved function of c-di-GMP signaling networks, and that thermosensitive catalysis of a second messenger constitutes a mechanism for thermal sensing in bacteria.