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Journal of Bacteriology, June 2005, p. 4095-4103, Vol. 187, No. 12
0021-9193/05/$08.00+0     doi:10.1128/JB.187.12.4095-4103.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Genomic Sequence and Receptor for the Vibrio cholerae Phage KSF-1{Phi}: Evolutionary Divergence among Filamentous Vibriophages Mediating Lateral Gene Transfer

Shah M. Faruque,1* Iftekhar Bin Naser,1 Kazutaka Fujihara,2 Pornphan Diraphat,3 Nityananda Chowdhury,1 M. Kamruzzaman,1 Firdausi Qadri,1 Shinji Yamasaki,2 A. N. Ghosh,4 and John J. Mekalanos5

Molecular Genetics Laboratory, International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka-1212, Bangladesh,1 Department of Veterinary Sciences, Graduate School of Agriculture and Biological Sciences, Osaka Prefecture University, Osaka 599-8531, Japan,2 Department of Microbiology, Faculty of Public Health, Mahidol University, Bangkok, Thailand,3 National Institute of Cholera and Enteric Diseases, Kolkata-700 010, India,4 Department of Microbiology and Molecular Genetics, Harvard Medical School, 200 Longwood Avenue, Boston, Massachusetts 021155

Received 30 August 2004/ Accepted 28 February 2005

KSF-1{Phi}, a novel filamentous phage of Vibrio cholerae, supports morphogenesis of the RS1 satellite phage by heterologous DNA packaging and facilitates horizontal gene transfer. We analyzed the genomic sequence, morphology, and receptor for KSF-1{Phi} infection, as well as its phylogenetic relationships with other filamentous vibriophages. While strains carrying the mshA gene encoding mannose-sensitive hemagglutinin (MSHA) type IV pilus were susceptible to KSF-1{Phi} infection, naturally occurring MSHA-negative strains and an mshA deletion mutant were resistant. Furthermore, D-mannose as well as a monoclonal antibody against MSHA inhibited infection of MSHA-positive strains by the phage, suggesting that MSHA is the receptor for KSF-1{Phi}. The phage genome comprises 7,107 nucleotides, containing 14 open reading frames, 4 of which have predicted protein products homologous to those of other filamentous phages. Although the overall genetic organization of filamentous phages appears to be preserved in KSF-1{Phi}, the genomic sequence of the phage does not have a high level of identity with that of other filamentous phages and reveals a highly mosaic structure. Separate phylogenetic analysis of genomic sequences encoding putative replication proteins, receptor-binding proteins, and Zot-like proteins of 10 different filamentous vibriophages showed different results, suggesting that the evolution of these phages involved extensive horizontal exchange of genetic material. Filamentous phages which use type IV pili as receptors were found to belong to different branches. While one of these branches is represented by CTX{Phi}, which uses the toxin-coregulated pilus as its receptor, at least four evolutionarily diverged phages share a common receptor MSHA, and most of these phages mediate horizontal gene transfer. Since MSHA is present in a wide variety of V. cholerae strains and is presumed to express in the environment, diverse filamentous phages using this receptor are likely to contribute significantly to V. cholerae evolution.

* Corresponding author. Mailing address: Molecular Genetics Laboratory, ICDDR,B, GPO Box 128, Dhaka-1000, Bangladesh. Phone: 880 2 9886464. Fax: 880 2 8812529. E-mail: faruque{at}icddrb.org.

Journal of Bacteriology, June 2005, p. 4095-4103, Vol. 187, No. 12
0021-9193/05/$08.00+0     doi:10.1128/JB.187.12.4095-4103.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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