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Journal of Bacteriology, November 2004, p. 7508-7520, Vol. 186, No. 22
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.22.7508-7520.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Evolutionary Dynamics of Insertion Sequences in Helicobacter pylori

Awdhesh Kalia,1 Asish K. Mukhopadhyay,1,{dagger} Giedrius Dailide,1 Yoshiyki Ito,1,2 Takeshi Azuma,2 Benjamin C. Y. Wong,3 and Douglas E. Berg1*

Department of Molecular Microbiology, Washington University School of Medicine, Saint Louis, Missouri,1 Second Department of Internal Medicine, Fukui Medical School, Fukui, Japan,2 Division of Gastroenterology, Department of Medicine, University of Hong Kong, Queen Mary Hospital, Hong Kong3

Received 21 April 2004/ Accepted 5 August 2004

Prokaryotic insertion sequence (IS) elements behave like parasites in terms of their ability to invade and proliferate in microbial gene pools and like symbionts when they coevolve with their bacterial hosts. Here we investigated the evolutionary history of IS605 and IS607 of Helicobacter pylori, a genetically diverse gastric pathogen. These elements contain unrelated transposase genes (orfA) and also a homolog of the Salmonella virulence gene gipA (orfB). A total of 488 East Asian, Indian, Peruvian, and Spanish isolates were screened, and 18 and 14% of them harbored IS605 and IS607, respectively. IS605 nucleotide sequence analysis (n = 42) revealed geographic subdivisions similar to those of H. pylori; the geographic subdivision was blurred, however, due in part to homologous recombination, as indicated by split decomposition and homoplasy tests (homoplasy ratio, 0.56). In contrast, the IS607 populations (n = 44) showed strong geographic subdivisions with less homologous recombination (homoplasy ratio, 0.2). Diversifying selection (ratio of nonsynonymous change to synonymous change, >>1) was evident in ~15% of the IS605 orfA codons analyzed but not in the IS607 orfA codons. Diversifying selection was also evident in ~2% of the IS605 orfB and ~10% of the IS607 orfB codons analyzed. We suggest that the evolution of these elements reflects selection for optimal transposition activity in the case of IS605 orfA and for interactions between the OrfB proteins and other cellular constituents that potentially contribute to bacterial fitness. Taken together, similarities in IS elements and H. pylori population genetic structures and evidence of adaptive evolution in IS elements suggest that there is coevolution between these elements and their bacterial hosts.

* Corresponding author. Mailing address: Box 8230, Department of Molecular Microbiology, 4940 Parkview Place, Washington University School of Medicine, Saint Louis, MO 63110. Phone: (314) 362-2772. Fax: (314) 362-1232. E-mail: berg{at}borcim.wustl.edu.

{dagger} Present address: National Institute for Cholera and Enteric Diseases, Kolkata, India.

Journal of Bacteriology, November 2004, p. 7508-7520, Vol. 186, No. 22
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.22.7508-7520.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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