Vibrio cholerae adapts to sessile and motile lifestyles by cyclic di-GMP regulation of cell shape

Abstract

The cell morphology of rod-shaped bacteria is determined by the rigid net of peptidoglycan forming the cell wall. Alterations to the rod shape, such as the curved rod, occur through manipulating the process of cell wall synthesis. The human pathogen Vibrio cholerae typically exists as a curved rod, but straight rods have been observed under certain conditions. While this appears to be a regulated process, the regulatory pathways controlling cell shape transitions in V. cholerae and the benefits of switching between rod and curved shape have not been determined. We demonstrate that cell shape in V. cholerae is regulated by the bacterial second messenger cyclic dimeric guanosine monophosphate (c-di-GMP) by posttranscriptionally repressing expression of crvA, a gene encoding an intermediate filament-like protein necessary for curvature formation in V. cholerae. This regulation is mediated by the transcriptional cascade that also induces production of biofilm matrix components, indicating that cell shape is coregulated with V. cholerae’s induction of sessility. During microcolony formation, wild-type V. cholerae cells tended to exist as straight rods, while genetically engineering cells to maintain high curvature reduced microcolony formation and biofilm density. Conversely, straight V. cholerae mutants have reduced swimming speed when using flagellar motility in liquid. Our results demonstrate regulation of cell shape in bacteria is a mechanism to increase fitness in planktonic and biofilm lifestyles.

A Novel Gene vp0610 Negatively Regulates Biofilm Formation in Vibrio parahaemolyticus

“…VP0610 can inhibit the transcription of opaR, while OpaR and AphA are the two main density-dependent core regulators of quorum sensing. HapR, a master regulator in Vibrio cholerae, negatively regulates biofilm formation by suppressing c-di-GMP production (Fong and Yildiz, 2008;Krasteva et al, 2010;Kalia et al, 2013;Biswas et al, 2020;Fernandez et al, 2020), consistent with our results; the c-di-GMP production of the mutant was significantly lower than that of the WT, resulting in a rapid biofilm formation in the WT after 24 h but a slow biofilm formation of the mutant. Therefore, we conclude that VP0610 has an indirect promoting effect on c-di-GMP production.…”

Pseudomonas aeruginosa post‐translational responses to elevated c‐di‐GMP levels

“…Multiple diguanylate cyclase and phosphodiesterase domain-containing proteins (GGDEF and EAL/HD-GYP, respectively) modulate the level of the diffusible molecule bis-(3′-5′)-cyclic dimeric guanosine monophosphate (c-di-GMP) to induce specific cellular responses at the single-cell level in multiple bacterial species. Overall, it appears that high levels of c-di-GMP promote a sessile bacterial lifestyle, characterized by biofilm formation and aggregative behavior, whereas low levels of cdi-GMP promote motility and virulence factor synthesis (Fernandez et al, 2020;Hengge, 2009;Jenal & Malone, 2006;Jones et al, 2015;Römling et al, 2013;Simm et al, 2004;Valentini & Filloux, 2016;Zorraquino et al, 2013). Although much has been learned in recent years, we are still in the early stages of understanding the mechanisms of c-di-GMP recognition and subsequent regulation of cellular phenotypes.…”

Yin and Yang of Biofilm Formation and Cyclic di-GMP Signaling of the Gastrointestinal Pathogen <b><i>Salmonella enterica</i></b> Serovar Typhimurium

“…In this context, cyclic di-GMP can direct fundamental processes such as carbon source catabolism, respiration, cell division, and cell shape by affecting global molecular processes such as RNA turnover, proteolysis, protein acetylation, secretion, and the catalytic activity of biofilm matrix biosynthesis enzymes. This physiological and behavioral consequences have a wide impact not only in the clinical, industrial, and agricultural setting, but also shape the ecology in oceans and affect geochemical relevant global compounds and cycles, such as the denitrification cycle [ 19 , 20 , 21 , 22 , 23 ]. The conformational flexibility and the ability to form various types of oligomers and few amino acids sufficient to define binding make it challenging to predict the binding sites of cyclic di-GMP [ 5 , 24 ].…”