The Vibrio Cholerae FlgM Homologue is an Anti-sigma28 Factor That is Secreted Through the Sheathed Polar Flagellum

Overview

Journal J Bacteriol

Publisher American Society for Microbiology

Specialty Microbiology

Date 2004 Jul 3

PMID 15231794

Citations 29

Authors

Nidia E Correa

Jeffrey R Barker

Karl E Klose

Affiliations

Soon will be listed here.

Abstract

Vibrio cholerae has a single polar sheathed flagellum that propels the cells of this bacterium. Flagellar synthesis, motility, and chemotaxis have all been linked to virulence in this human pathogen. V. cholerae expresses flagellar genes in a hierarchy consisting of sigma54- and sigma28-dependent transcription. In other bacteria, sigma28 transcriptional activity is controlled by an anti-sigma28 factor, FlgM. We demonstrate that the V. cholerae FlgM homologue (i) physically interacts with sigma28, (ii) has a repressive effect on some V. cholerae sigma28-dependent flagellar promoters, and (iii) is secreted through the polar sheathed flagellum, consistent with anti-sigma28 activity. Interestingly, FlgM does not have a uniform repressive effect on all sigma28-dependent promoters, as determined by measurement of sigma28-dependent transcription in cells either lacking FlgM (DeltaflgM) or incapable of secretion (DeltafliF). Further analysis of a DeltafliF strain revealed that this flagellar assembly block causes a decrease in class III (FlrC- and sigma54-dependent) and class IV (sigma28-dependent), but not class II (FlrA- and sigma54-dependent), flagellar transcription. V. cholerae flgM and fliA (encodes sigma28) mutants were only modestly affected in their ability to colonize the infant mouse intestine, a measure of virulence. Our results demonstrate that V. cholerae FlgM functions as an anti-sigma28 factor and that the sheathed flagellum is competent for secretion of nonstructural proteins.

Citing Articles

Interplay of two small RNAs fine-tunes hierarchical flagella gene expression in Campylobacter jejuni.

Konig F, Svensson S, Sharma C Nat Commun. 2024; 15(1):5240.

PMID: 38897989 PMC: 11187230. DOI: 10.1038/s41467-024-48986-8.

The cAMP Receptor Protein (CRP) of Regulates Its Bacterial Growth, Type II Secretion System, Flagellum Formation, Adhesion Genes, and Virulence.

Tian Z, Xiang F, Peng K, Qin Z, Feng Y, Huang B Animals (Basel). 2024; 14(3).

PMID: 38338079 PMC: 10854923. DOI: 10.3390/ani14030437.

Dps-dependent in vivo mutation enhances long-term host adaptation in Vibrio cholerae.

Luo M, Chen G, Yi C, Xue B, Yang X, Ma Y PLoS Pathog. 2023; 19(3):e1011250.

PMID: 36928244 PMC: 10104298. DOI: 10.1371/journal.ppat.1011250.

The Vibrio Polar Flagellum: Structure and Regulation.

Lloyd C, Klose K Adv Exp Med Biol. 2023; 1404:77-97.

PMID: 36792872 DOI: 10.1007/978-3-031-22997-8_5.

The Polar Flagellar Transcriptional Regulatory Network in Deviates from Canonical Species.

Petersen B, Liu M, Podicheti R, Yang A, Simpson C, Hemmerich C J Bacteriol. 2021; 203(20):e0027621.

PMID: 34339299 PMC: 8459767. DOI: 10.1128/JB.00276-21.

References

Karlinsey J, Tanaka S, Bettenworth V, Yamaguchi S, Boos W, Aizawa S . Completion of the hook-basal body complex of the Salmonella typhimurium flagellum is coupled to FlgM secretion and fliC transcription. Mol Microbiol. 2000; 37(5):1220-31. DOI: 10.1046/j.1365-2958.2000.02081.x. View

Young G, Schmiel D, Miller V . A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system. Proc Natl Acad Sci U S A. 1999; 96(11):6456-61. PMC: 26903. DOI: 10.1073/pnas.96.11.6456. View

Furuno M, Sato K, Kawagishi I, Homma M . Characterization of a flagellar sheath component, PF60, and its structural gene in marine Vibrio. J Biochem. 2000; 127(1):29-36. DOI: 10.1093/oxfordjournals.jbchem.a022580. View

Klose K . The suckling mouse model of cholera. Trends Microbiol. 2001; 8(4):189-91. DOI: 10.1016/s0966-842x(00)01721-2. View

Kim Y, McCarter L . Analysis of the polar flagellar gene system of Vibrio parahaemolyticus. J Bacteriol. 2000; 182(13):3693-704. PMC: 94540. DOI: 10.1128/JB.182.13.3693-3704.2000. View

Heidelberg J, Eisen J, Nelson W, Clayton R, Gwinn M, Dodson R . DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature. 2000; 406(6795):477-83. PMC: 8288016. DOI: 10.1038/35020000. View

Watnick P, Lauriano C, Klose K, Croal L, Kolter R . The absence of a flagellum leads to altered colony morphology, biofilm development and virulence in Vibrio cholerae O139. Mol Microbiol. 2001; 39(2):223-35. PMC: 2860545. DOI: 10.1046/j.1365-2958.2001.02195.x. View

Prouty M, Correa N, Klose K . The novel sigma54- and sigma28-dependent flagellar gene transcription hierarchy of Vibrio cholerae. Mol Microbiol. 2001; 39(6):1595-609. DOI: 10.1046/j.1365-2958.2001.02348.x. View

Lee S, Butler S, Camilli A . Selection for in vivo regulators of bacterial virulence. Proc Natl Acad Sci U S A. 2001; 98(12):6889-94. PMC: 34448. DOI: 10.1073/pnas.111581598. View

10.

Hava D, Camilli A . Isolation and characterization of a temperature-sensitive generalized transducing bacteriophage for Vibrio cholerae. J Microbiol Methods. 2001; 46(3):217-25. DOI: 10.1016/s0167-7012(01)00276-7. View

11.

Colland F, Rain J, Gounon P, Labigne A, Legrain P, de Reuse H . Identification of the Helicobacter pylori anti-sigma28 factor. Mol Microbiol. 2001; 41(2):477-87. DOI: 10.1046/j.1365-2958.2001.02537.x. View

12.

McCarter L . Polar flagellar motility of the Vibrionaceae. Microbiol Mol Biol Rev. 2001; 65(3):445-62, table of contents. PMC: 99036. DOI: 10.1128/MMBR.65.3.445-462.2001. View

13.

Frisk A, Jyot J, Arora S, Ramphal R . Identification and functional characterization of flgM, a gene encoding the anti-sigma 28 factor in Pseudomonas aeruginosa. J Bacteriol. 2002; 184(6):1514-21. PMC: 134903. DOI: 10.1128/JB.184.6.1514-1521.2002. View

14.

Josenhans C, Niehus E, Amersbach S, Horster A, Betz C, Drescher B . Functional characterization of the antagonistic flagellar late regulators FliA and FlgM of Helicobacter pylori and their effects on the H. pylori transcriptome. Mol Microbiol. 2002; 43(2):307-22. DOI: 10.1046/j.1365-2958.2002.02765.x. View

15.

Yonekura K, Maki-Yonekura S, Namba K . Growth mechanism of the bacterial flagellar filament. Res Microbiol. 2002; 153(4):191-7. DOI: 10.1016/s0923-2508(02)01308-6. View

16.

Macnab R . How bacteria assemble flagella. Annu Rev Microbiol. 2003; 57:77-100. DOI: 10.1146/annurev.micro.57.030502.090832. View

17.

Hendrixson D, DiRita V . Transcription of sigma54-dependent but not sigma28-dependent flagellar genes in Campylobacter jejuni is associated with formation of the flagellar secretory apparatus. Mol Microbiol. 2003; 50(2):687-702. DOI: 10.1046/j.1365-2958.2003.03731.x. View

18.

Dasgupta N, Wolfgang M, Goodman A, Arora S, Jyot J, Lory S . A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa. Mol Microbiol. 2003; 50(3):809-24. DOI: 10.1046/j.1365-2958.2003.03740.x. View

19.

Lauriano C, Ghosh C, Correa N, Klose K . The sodium-driven flagellar motor controls exopolysaccharide expression in Vibrio cholerae. J Bacteriol. 2004; 186(15):4864-74. PMC: 451641. DOI: 10.1128/JB.186.15.4864-4874.2004. View

20.

Mekalanos J, Collier R, Romig W . Enzymic activity of cholera toxin. II. Relationships to proteolytic processing, disulfide bond reduction, and subunit composition. J Biol Chem. 1979; 254(13):5855-61. View