Genomic and genetic analysis of Bordetella bacteriophages encoding reverse transcriptase-mediated tropism-switching cassettes

Minghsun Liu, Mari Gingery, Sergei R Doulatov, Yichin Liu, Asher Hodes, Stephen Baker, Paul Davis, Mark Simmonds, Carol Churcher, Karen Mungall, Michael A Quail, Andrew Preston, Eric T Harvill, Duncan J Maskell, Frederick A Eiserling, Julian Parkhill, Jeff F Miller

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Abstract

Liu et al. recently described a group of related temperate bacteriophages that infect Bordetella subspecies and undergo a unique template-dependent, reverse transcriptase-mediated tropism switching phenomenon (Liu et al., Science 295: 2091-2094, 2002). Tropism switching results from the introduction of single nucleotide substitutions at defined locations in the VR1 (variable region 1) segment of the mtd (major tropism determinant) gene, which determines specificity for receptors on host bacteria. In this report, we describe the complete nucleotide sequences of the 42.5- to 42.7-kb double-stranded DNA genomes of three related phage isolates and characterize two additional regions of variability. Forty-nine coding sequences were identified. Of these coding sequences, bbp36 contained VR2 (variable region 2), which is highly dynamic and consists of a variable number of identical 19-bp repeats separated by one of three 5-bp spacers, and bpm encodes a DNA adenine methylase with unusual site specificity and a homopolymer tract that functions as a hotspot for frameshift mutations. Morphological and sequence analysis suggests that these Bordetella phage are genetic hybrids of P22 and T7 family genomes, lending further support to the idea that regions encoding protein domains, single genes, or blocks of genes are readily exchanged between bacterial and phage genomes. Bordetella bacteriophages are capable of transducing genetic markers in vitro, and by using animal models, we demonstrated that lysogenic conversion can take place in the mouse respiratory tract during infection.
Original languageEnglish
Pages (from-to)1503-1517
Number of pages15
JournalJournal of Bacteriology
Volume186
Issue number5
DOIs
Publication statusPublished - 2004

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Bordetella
Tropism
RNA-Directed DNA Polymerase
Bacteriophages
Site-Specific DNA-Methyltransferase (Adenine-Specific)
Genome
Genes
Bacterial Genomes
Frameshift Mutation
Genetic Markers
Respiratory Tract Infections
Sequence Analysis
Nucleotides
Animal Models
Bacteria
DNA

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Genomic and genetic analysis of Bordetella bacteriophages encoding reverse transcriptase-mediated tropism-switching cassettes. / Liu, Minghsun; Gingery, Mari; Doulatov, Sergei R; Liu, Yichin; Hodes, Asher; Baker, Stephen; Davis, Paul; Simmonds, Mark; Churcher, Carol; Mungall, Karen; Quail, Michael A; Preston, Andrew; Harvill, Eric T; Maskell, Duncan J; Eiserling, Frederick A; Parkhill, Julian; Miller, Jeff F.

In: Journal of Bacteriology, Vol. 186, No. 5, 2004, p. 1503-1517.

Research output: Contribution to journalArticle

Liu, M, Gingery, M, Doulatov, SR, Liu, Y, Hodes, A, Baker, S, Davis, P, Simmonds, M, Churcher, C, Mungall, K, Quail, MA, Preston, A, Harvill, ET, Maskell, DJ, Eiserling, FA, Parkhill, J & Miller, JF 2004, 'Genomic and genetic analysis of Bordetella bacteriophages encoding reverse transcriptase-mediated tropism-switching cassettes', Journal of Bacteriology, vol. 186, no. 5, pp. 1503-1517. https://doi.org/10.1128/​JB.186.5.1503-1517.2004
Liu, Minghsun ; Gingery, Mari ; Doulatov, Sergei R ; Liu, Yichin ; Hodes, Asher ; Baker, Stephen ; Davis, Paul ; Simmonds, Mark ; Churcher, Carol ; Mungall, Karen ; Quail, Michael A ; Preston, Andrew ; Harvill, Eric T ; Maskell, Duncan J ; Eiserling, Frederick A ; Parkhill, Julian ; Miller, Jeff F. / Genomic and genetic analysis of Bordetella bacteriophages encoding reverse transcriptase-mediated tropism-switching cassettes. In: Journal of Bacteriology. 2004 ; Vol. 186, No. 5. pp. 1503-1517.
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AU - Liu, Yichin

AU - Hodes, Asher

AU - Baker, Stephen

AU - Davis, Paul

AU - Simmonds, Mark

AU - Churcher, Carol

AU - Mungall, Karen

AU - Quail, Michael A

AU - Preston, Andrew

AU - Harvill, Eric T

AU - Maskell, Duncan J

AU - Eiserling, Frederick A

AU - Parkhill, Julian

AU - Miller, Jeff F

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