Site-Specific Recombination Links the Evolution of P2-like Coliphages and Pathogenic Enterobacteria

Abstract

The genome of the tailed temperate coliphage P2 (Myoviridae) contains some genes that probably are horizontally transferred additions to the genome. One of these genes, the Z/fun gene, was recently found intact in the genome of Neisseria meningitidis. We have investigated the presence of P2-like phages, and the genetic variation at the position corresponding to the phage P2 Z/fun locus, in the Escherichia coli reference collection (ECOR). P2-like phages are common in E. coli since they are present in about 30% of the ECOR strains. Hybridizations and PCR amplifications indicate that the overall variation among these phages is small. Amplification of the region corresponding to the phage P2 Z/fun locus in 11 prophages revealed that this is a multivariable locus. Sequencing of the region resulted in 10 completely different sequences but with a similar high AT-content as the Z/fun gene. All sequences contained at least one open reading frame with good transcription and translation signals. All sequences were also surrounded by a highly similar, previously undiscovered, inverted repeat (IR). We also found this IR in genetically unstable regions in pathogenic enterobacteria. This demonstrates that P2-like phages are important factors in the evolution of bacteria, not only because they carry a diversity of lysogenic conversion genes but also because they can act as vectors for single genes. The genes found between the IRs have unknown functions, and only a few clearly similar genes have been found in other bacteria.

Phages and the Evolution of Bacterial Pathogens: from Genomic Rearrangements to Lysogenic Conversion

“…8B and C). Similar observations have been made with dairy phages (35), and a recent study of moron gene cassettes in P2-like phages from E. coli lends further support to this notion (170). The moron gene cassettes were highly diverse in length, DNA sequence, and encoded gene products.…”

“…8C). Therefore, these gene cassettes could travel between phages by homologous recombination (170). Which recombination systems might facilitate module exchange by homologous recombination?…”

Identification of a Gene Encoding a Functional Reverse Transcriptase within a Highly Variable Locus in the P2-Like Coliphages

“…At the region equivalent to the P2 Z/fun gene, i.e., the Z region, which is located between the well-conserved tail genes G and F I , these P2-like prophages have been shown to contain different gene cassettes surrounded by a highly similar inverted repeat, indicating a site-specific integration event. Similar inverted repeats, spacing other genes, can be found in genetically unstable regions in pathogenic enterobacteria (19). The tin and old genes are located at the right end of the P2 genetic map close to the cos site.…”

Evolution of a Self-Inducible Cytolethal Distending Toxin Type V-Encoding Bacteriophage from Escherichia coli O157:H7 to Shigella sonnei

“…P2-like prophages seem to be quite common in E. coli but also seem to be distributed among other proteobacteria of the gamma subgroup (29). The genomes of phages HP1 and HP2 in Haemophilus influenzae (30), ⌽CTX in Pseudomonas aeruginosa (31), and K139 in Vibrio cholerae (32) have all been sequenced and shown to be P2-like with respect to genome organization as well as nucleotide sequence.…”