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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,{dagger} Scott A. Beatson,1,{dagger} 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.

{dagger} 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.




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