TY - JOUR
T1 - The two-component system ChvGI maintains cell envelope homeostasis in Caulobacter crescentus
T2 - ChvGI-dependent cell envelope homeostasis
AU - Quintero Yanes, Alex Armando
AU - Mayard, Aurélie
AU - Hallez, Regis
N1 - Funding Information:
This work was supported by the Fonds de la Recherche Scientifique – FNRS (F.R.S. – FNRS) with a Welbio Starting Grant (WELBIO-CR-2019S-05) to RH. A.Q-Y. was supported by a postdoctoral fellowship from the University of Namur (UNamur). R.H. is a Research Associate of F.R.S. – FNRS. https://www.frs-fnrs.be/en/ The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We are grateful to Sean Crosson and Benjamin Stein for willingness to discuss and share data on their ChvGI-related projects. Also, we would like to thank members of the URBM of the University of Namur for their comments and suggestions on this project, especially Dr. Angéline Reboul for her comments and advices on the microscopy analysis, Jérôme Coppine for plasmids constructs and his help with phosphorylation assays, and members of the Hallez lab for their comments on the manuscript.
Publisher Copyright:
Copyright: © 2022 Quintero-Yanes et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
PY - 2022/12/8
Y1 - 2022/12/8
N2 - Two-component systems (TCS) are often used by bacteria to rapidly assess and respond to environmental changes. The ChvG/ChvI (ChvGI) TCS conserved in α-proteobacteria is known for regulating expression of genes related to exopolysaccharide production, viru- lence and growth. The sensor kinase ChvG autophosphorylates upon yet unknown signals and phosphorylates the response regulator ChvI to regulate transcription. Recent studies in Caulobacter crescentus showed that chv mutants are sensitive to vancomycin treatment and fail to grow in synthetic minimal media. In this work, we identified the osmotic imbalance as the main cause of growth impairment in synthetic minimal media. We also determined the ChvI regulon and found that ChvI regulates cell envelope architecture by controlling outer membrane, peptidoglycan assembly/recycling and inner membrane proteins. In addition, we found that ChvI phosphorylation is also activated upon antibiotic treatment with vancomycin. We also challenged chv mutants with other cell envelope related stress and found that treatment with antibiotics targeting transpeptidation of peptidoglycan during cell elongation impairs growth of the mutant. Finally, we observed that the sensor kinase ChvG relo- cates from a patchy-spotty distribution to distinctive foci after transition from complex to synthetic minimal media. Interestingly, this pattern of (re)location has been described for proteins involved in cell growth control and peptidoglycan synthesis upon osmotic shock. Overall, our data support that the ChvGI TCS is mainly used to monitor and respond to osmotic imbalances and damages in the peptidoglycan layer to maintain cell envelope homeostasis.
AB - Two-component systems (TCS) are often used by bacteria to rapidly assess and respond to environmental changes. The ChvG/ChvI (ChvGI) TCS conserved in α-proteobacteria is known for regulating expression of genes related to exopolysaccharide production, viru- lence and growth. The sensor kinase ChvG autophosphorylates upon yet unknown signals and phosphorylates the response regulator ChvI to regulate transcription. Recent studies in Caulobacter crescentus showed that chv mutants are sensitive to vancomycin treatment and fail to grow in synthetic minimal media. In this work, we identified the osmotic imbalance as the main cause of growth impairment in synthetic minimal media. We also determined the ChvI regulon and found that ChvI regulates cell envelope architecture by controlling outer membrane, peptidoglycan assembly/recycling and inner membrane proteins. In addition, we found that ChvI phosphorylation is also activated upon antibiotic treatment with vancomycin. We also challenged chv mutants with other cell envelope related stress and found that treatment with antibiotics targeting transpeptidation of peptidoglycan during cell elongation impairs growth of the mutant. Finally, we observed that the sensor kinase ChvG relo- cates from a patchy-spotty distribution to distinctive foci after transition from complex to synthetic minimal media. Interestingly, this pattern of (re)location has been described for proteins involved in cell growth control and peptidoglycan synthesis upon osmotic shock. Overall, our data support that the ChvGI TCS is mainly used to monitor and respond to osmotic imbalances and damages in the peptidoglycan layer to maintain cell envelope homeostasis.
UR - https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9731502/
UR - http://www.scopus.com/inward/record.url?scp=85143570802&partnerID=8YFLogxK
U2 - 10.1371/journal.pgen.1010465
DO - 10.1371/journal.pgen.1010465
M3 - Article
SN - 1553-7390
VL - 18
JO - PLoS Genetics
JF - PLoS Genetics
IS - 12
M1 - e1010465
ER -