The Wsp system of <i>Pseudomonas aeruginosa</i> links surface sensing and cell envelope stress

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Significance

Bacteria must respond quickly to environmental changes to survive. One way bacteria can respond to environmental stress is by undergoing a lifestyle transition from individual, free-swimming cells to a surface-associated community called a biofilm characterized by aggregative growth. The opportunistic pathogen Pseudomonas aeruginosa uses the Wsp chemosensory system to sense an unknown surface-associated cue. Here we show that the Wsp system senses cell envelope stress, specifically conditions that promote unfolded or misregulated periplasmic and inner membrane proteins. This work provides direct evidence that cell envelope stress is an important feature of surface sensing in P. aeruginosa.

Abstract

Surface sensing is a critical process that promotes the transition to a biofilm lifestyle. Several surface-sensing mechanisms have been described for a range of species, most involving surface appendages, such as flagella and pili. Pseudomonas aeruginosa uses the Wsp chemosensory-like signal transduction pathway to sense surfaces and promote biofilm formation. The methyl-accepting chemotaxis protein WspA recognizes an unknown surface-associated signal and initiates a phosphorylation cascade that activates the diguanylate cyclase WspR. We conducted a screen for Wsp-activating compounds and found that chemicals that impact the cell envelope induce Wsp signaling, increase intracellular c-di-GMP levels, and can promote surface attachment. To isolate the Wsp system from other P. aeruginosa surface-sensing systems, we heterologously expressed it in Escherichia coli and found it sufficient for sensing surfaces and the chemicals identified in our screen. Using well-characterized reporters for different E. coli cell envelope stress responses, we then determined that Wsp sensitivity overlapped with multiple E. coli cell envelope stress-response systems. Using mutational and CRISPRi analysis, we found that misfolded proteins in the periplasm appear to be a major stimulus of the Wsp system. Finally, we show that surface attachment appears to have an immediate, observable effect on cell envelope integrity. Collectively, our results provide experimental evidence that cell envelope stress represents an important feature of surface sensing in P. aeruginosa.

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Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms.

P. K. Singh, A. L. Schaefer, M R Parsek … (2000)

The bacterium Pseudomonas aeruginosa permanently colonizes cystic fibrosis lungs despite aggressive antibiotic treatment. This suggests that P. aeruginosa might exist as biofilms--structured communities of bacteria encased in a self-produced polymeric matrix--in the cystic fibrosis lung. Consistent with this hypothesis, microscopy of cystic fibrosis sputum shows that P. aeruginosa are in biofilm-like structures. P. aeruginosa uses extracellular quorum-sensing signals (extracellular chemical signals that cue cell-density-dependent gene expression) to coordinate biofilm formation. Here we found that cystic fibrosis sputum produces the two principal P. aeruginosa quorum-sensing signals; however, the relative abundance of these signals was opposite to that of the standard P. aeruginosa strain PAO1 in laboratory broth culture. When P. aeruginosa sputum isolates were grown in broth, some showed quorum-sensing signal ratios like those of the laboratory strain. When we grew these isolates and PAO1 in a laboratory biofilm model, the signal ratios were like those in cystic fibrosis sputum. Our data support the hypothesis that P. aeruginosa are in a biofilm in cystic fibrosis sputum. Moreover, quorum-sensing signal profiling of specific P. aeruginosa strains may serve as a biomarker in screens to identify agents that interfere with biofilm development.

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Role of a highly conserved bacterial protein in outer membrane protein assembly.

Romé Voulhoux, Martine Bos, Jeroen Geurtsen … (2003)

After transport across the cytoplasmic membrane, bacterial outer membrane proteins are assembled into the outer membrane. Meningococcal Omp85 is a highly conserved protein in Gram-negative bacteria, and its homolog Toc75 is a component of the chloroplast protein-import machinery. Omp85 appeared to be essential for viability, and unassembled forms of various outer membrane proteins accumulated upon Omp85 depletion. Immunofluorescence microscopy revealed decreased surface exposure of outer membrane proteins, which was particularly apparent at the cell-division planes. Thus, Omp85 is likely to play a role in outer membrane protein assembly.

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Origins and diversification of a complex signal transduction system in prokaryotes.

Igor Zhulin, Kristin Wuichet (2009)

The molecular machinery that controls chemotaxis in bacteria is substantially more complex than any other signal transduction system in prokaryotes, and its origins and variability among living species are unknown. We found that this multiprotein "chemotaxis system" is present in most prokaryotic species and evolved from simpler two-component regulatory systems that control prokaryotic transcription. We discovered, through genomic analysis, signaling systems intermediate between two-component systems and chemotaxis systems. Evolutionary genomics established central and auxiliary components of the chemotaxis system. While tracing its evolutionary history, we also developed a classification scheme that revealed more than a dozen distinct classes of chemotaxis systems, enabling future predictive modeling of chemotactic behavior in unstudied species.

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Author and article information

Journal

Journal ID (nlm-ta): Proc Natl Acad Sci U S A

Journal ID (iso-abbrev): Proc Natl Acad Sci U S A

Journal ID (hwp): pnas

Journal ID (publisher-id): PNAS

Title: Proceedings of the National Academy of Sciences of the United States of America

Publisher: National Academy of Sciences

ISSN (Print): 0027-8424

ISSN (Electronic): 1091-6490

Publication date (Electronic): 27 April 2022

Publication date (Print): 3 May 2022

Publication date PMC-release: 27 April 2022

Volume: 119

Issue: 18

Electronic Location Identifier: e2117633119

Affiliations

[1] ^aDepartment of Microbiology, University of Washington School of Medicine , Seattle, WA 98109;

[2] ^bLaboratoire Matériaux, Polymères, Interfaces et Environnement Marin, Université de Toulon , 83041 Toulon, France;

[3] ^cGuangdong Province Sociomicrobiology Basic Science and Frontier Technology Research Team & Integrative Microbiology Research Center, South China Agricultural University , 510642 Guangzhou, China;

[4] ^dDepartment of Biological Sciences, University of Alberta , Edmonton, AB T6G 2R3, Canada;

[5] ^eDepartment of Microbiology, The Ohio State University , Columbus, OH 43210

Author notes

¹To whom correspondence may be addressed. Email: parsem@ 123456uw.edu .

Edited by Thomas Silhavy, Princeton University, Princeton, NJ; received September 24, 2021; accepted March 3, 2022

Author contributions: L.O., C.B., T.L.R., D.J.W., C.S.H., and M.R.P. designed research; L.O., Z.S., and J.E.D. performed research; C.B., Y.P., T.L.R., and C.S.H. contributed new reagents/analytic tools; L.O. analyzed data; and L.O. and M.R.P. wrote the paper.