Previous Article | Next Article 
Journal of Bacteriology, February 2005, p. 1430-1440, Vol. 187, No. 4
0021-9193/05/$08.00+0 doi:10.1128/JB.187.4.1430-1440.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.
The Flag-2 Locus, an Ancestral Gene Cluster, Is Potentially Associated with a Novel Flagellar System from Escherichia coli
Chuan-Peng Ren,1,
Scott A. Beatson,1,
Julian Parkhill,2 and
Mark J. Pallen1*
Bacterial Pathogenesis and Genomics Unit, Division of Immunity and Infection, Medical School, University of Birmingham, Birmingham,1
The Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, United Kingdom2
Received 2 September 2004/
Accepted 15 October 2004
Escherichia coli K-12 possesses two adjacent, divergent, promoterless flagellar genes, fhiA-mbhA, that are absent from Salmonella enterica. Through bioinformatics analysis, we found that these genes are remnants of an ancestral 44-gene cluster and are capable of encoding a novel flagellar system, Flag-2. In enteroaggregative E. coli strain 042, there is a frameshift in lfgC that is likely to have inactivated the system in this strain. Tiling path PCR studies showed that the Flag-2 cluster is present in 15 of 72 of the well-characterized ECOR strains. The Flag-2 system resembles the lateral flagellar systems of Aeromonas and Vibrio, particularly in its apparent dependence on RpoN. Unlike the conventional Flag-1 flagellin, the Flag-2 flagellin shows a remarkable lack of sequence polymorphism. The Flag-2 gene cluster encodes a flagellar type III secretion system (including a dedicated flagellar sigma-antisigma combination), thus raising the number of distinct type III secretion systems in Escherichia/Shigella to five. The presence of the Flag-2 cluster at identical sites in E. coli and its close relative Citrobacter rodentium, combined with its absence from S. enterica, suggests that it was acquired by horizontal gene transfer after the former two species diverged from Salmonella. The presence of Flag-2-like gene clusters in Yersinia pestis, Yersinia pseudotuberculosis, and Chromobacterium violaceum suggests that coexistence of two flagellar systems within the same species is more common than previously suspected. The fact that the Flag-2 gene cluster was not discovered in the first 10 Escherichia/Shigella genome sequences studied emphasizes the importance of maintaining an energetic program of genome sequencing for this important taxonomic group.
* Corresponding author. Mailing address: Bacterial Pathogenesis and Genomics Unit, Division of Immunity and Infection, Medical School, University of Birmingham, Birmingham, England B15 2TT. Phone: (44) 121 414 7163. Fax: (44) 121 414 3454. E-mail:
m.pallen{at}bham.ac.uk.
C.-P.R. and S.A.B. contributed equally to this study.
Journal of Bacteriology, February 2005, p. 1430-1440, Vol. 187, No. 4
0021-9193/05/$08.00+0 doi:10.1128/JB.187.4.1430-1440.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.
This article has been cited by other articles:
-
Fricke, W. F., Wright, M. S., Lindell, A. H., Harkins, D. M., Baker-Austin, C., Ravel, J., Stepanauskas, R.
(2008). Insights into the Environmental Resistance Gene Pool from the Genome Sequence of the Multidrug-Resistant Environmental Isolate Escherichia coli SMS-3-5. J. Bacteriol.
190: 6779-6794
[Abstract]
[Full Text]
-
Khan, M. A., Bouzari, S., Ma, C., Rosenberger, C. M., Bergstrom, K. S. B., Gibson, D. L., Steiner, T. S., Vallance, B. A.
(2008). Flagellin-Dependent and -Independent Inflammatory Responses following Infection by Enteropathogenic Escherichia coli and Citrobacter rodentium. Infect. Immun.
76: 1410-1422
[Abstract]
[Full Text]
-
Bresolin, G., Trcek, J., Scherer, S., Fuchs, T. M.
(2008). Presence of a functional flagellar cluster Flag-2 and low-temperature expression of flagellar genes in Yersinia enterocolitica W22703. Microbiology
154: 196-206
[Abstract]
[Full Text]
-
Liu, R., Ochman, H.
(2007). Origins of Flagellar Gene Operons and Secondary Flagellar Systems. J. Bacteriol.
189: 7098-7104
[Abstract]
[Full Text]
-
Poggio, S., Abreu-Goodger, C., Fabela, S., Osorio, A., Dreyfus, G., Vinuesa, P., Camarena, L.
(2007). A Complete Set of Flagellar Genes Acquired by Horizontal Transfer Coexists with the Endogenous Flagellar System in Rhodobacter sphaeroides. J. Bacteriol.
189: 3208-3216
[Abstract]
[Full Text]
-
Canals, R., Vilches, S., Wilhelms, M., Shaw, J. G., Merino, S., Tomas, J. M.
(2007). Non-structural flagella genes affecting both polar and lateral flagella-mediated motility in Aeromonas hydrophila. Microbiology
153: 1165-1175
[Abstract]
[Full Text]
-
Turner, S. M., Chaudhuri, R. R., Jiang, Z.-D., DuPont, H., Gyles, C., Penn, C. W., Pallen, M. J., Henderson, I. R.
(2006). Phylogenetic Comparisons Reveal Multiple Acquisitions of the Toxin Genes by Enterotoxigenic Escherichia coli Strains of Different Evolutionary Lineages. J. Clin. Microbiol.
44: 4528-4536
[Abstract]
[Full Text]
-
Kelly, M., Hart, E., Mundy, R., Marches, O., Wiles, S., Badea, L., Luck, S., Tauschek, M., Frankel, G., Robins-Browne, R. M., Hartland, E. L.
(2006). Essential Role of the Type III Secretion System Effector NleB in Colonization of Mice by Citrobacter rodentium. Infect. Immun.
74: 2328-2337
[Abstract]
[Full Text]
-
Canals, R., Altarriba, M., Vilches, S., Horsburgh, G., Shaw, J. G., Tomas, J. M., Merino, S.
(2006). Analysis of the Lateral Flagellar Gene System of Aeromonas hydrophila AH-3. J. Bacteriol.
188: 852-862
[Abstract]
[Full Text]
-
Chaudhuri, R. R., Pallen, M. J.
(2006). xBASE, a collection of online databases for bacterial comparative genomics. Nucleic Acids Res
34: D335-D337
[Abstract]
[Full Text]
-
Tominaga, A., Lan, R., Reeves, P. R.
(2005). Evolutionary Changes of the flhDC Flagellar Master Operon in Shigella Strains. J. Bacteriol.
187: 4295-4302
[Abstract]
[Full Text]