Bacterial cyclic diguanylate signaling networks sense temperature

• Published in: Nature communications Vol. 12; no. 1; p. 1986
• Main Authors: Almblad, Henrik, Randall, Trevor E., Liu, Fanny, Leblanc, Katherine, Groves, Ryan A., Kittichotirat, Weerayuth, Winsor, Geoffrey L., Fournier, Nicolas, Au, Emily, Groizeleau, Julie, Rich, Jacquelyn D., Lou, Yuefei, Granton, Elise, Jennings, Laura K., Singletary, Larissa A., Winstone, Tara M. L., Good, Nathan M., Bumgarner, Roger E., Hynes, Michael F., Singh, Manu, Stietz, Maria Silvina, Brinkman, Fiona S. L., Kumar, Ayush, Brassinga, Ann Karen Cornelia, Parsek, Matthew R., Tseng, Boo Shan, Lewis, Ian A., Yipp, Bryan G., MacCallum, Justin L., Harrison, Joe Jonathan
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 31.03.2021; Nature Publishing Group; Nature Portfolio
• Subjects: 38/5; 45/22; 45/23; 45/70; 631/326/41/2482; 631/326/421; 631/326/46; 631/45/612/1233; 64/11; 82/83; 96/1; 96/44; 96/95; Algorithms; Bacteria; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Biofilms; Biofilms - growth & development; Catalysis; Chemical synthesis; Chimeras; Chromatography, Liquid; Cyclic GMP - analogs & derivatives; Cyclic GMP - metabolism; Escherichia coli Proteins - genetics; Escherichia coli Proteins - metabolism; Gene Expression Regulation, Bacterial; Homology; Humanities and Social Sciences; Mass Spectrometry; Motility; multidisciplinary; Opportunist infection; Pathogens; Phosphorus-Oxygen Lyases - genetics; Phosphorus-Oxygen Lyases - metabolism; Protein folding; Pseudomonas aeruginosa; Pseudomonas aeruginosa - genetics; Pseudomonas aeruginosa - metabolism; Pseudomonas aeruginosa - physiology; Science; Science (multidisciplinary); Second Messenger Systems - physiology; Signal Transduction - physiology; Signaling; Temperature; Temperature dependence; Virulence
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-021-22176-2

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. Many bacteria use the second messenger cyclic diguanylate (c-di-GMP) to control motility, biofilm production and virulence. Here, the authors identify a thermosensitive enzyme that synthesizes c-di-GMP and modulates temperature-dependent motility, biofilm development and virulence in the opportunistic pathogen Pseudomonas aeruginosa .