The phage-related chromosomal islands of Gram-positive bacteria

Novick, Richard P.; Christie, Gail E.; Penadés, José R.

doi:10.1038/nrmicro2393

Cited by 347 publications

(384 citation statements)

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“…For example, in Vibrio cholerae the cholera toxin, a key virulence determinant, is encoded in the genome of the temperate phage ΦCTX 103 . As another example, Staphylococcus aureus pathogenicity islands (SaPIs) excise from the chromosome and replicate following induction by an infecting phage, and the SaPI DNA is packaged in modified phage particles and transferred to other S. aureus cells 104,105 and even to species from other genera 106 .…”

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Gene transfer agents: phage-like elements of genetic exchange

2012

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Horizontal gene transfer is important in the evolution of bacterial and archaeal genomes. An interesting genetic exchange process is carried out by diverse phage-like gene transfer agents (GTAs) that are found in a wide range of prokaryotes. Although GTAs resemble phages, they lack the hallmark capabilities that define typical phages, and they package random pieces of the producing cell's genome. In this Review, we discuss the defining characteristics of the GTAs that have been identified to date, along with potential functions for these agents and the possible evolutionary forces that act on the genes involved in their production.The prevalence of horizontal gene transfer (HGT), in which DNA is exchanged between closely or distantly related lineages, has altered the way we think about evolution 1,2 , having profound effects on our views of the evolutionary relationships among living organisms. It has caused a shift from a bifurcating 'tree of life' view to a 'net of life' or 'web of life' view [3][4][5] , in which "highways of gene sharing" (REF. 6) represent major connections, with genes (or DNA segments) viewed as "public goods, available for all organisms to integrate into their genomes" (REF. 7). HGT occurs within and between all three domains of life, and it has been estimated that 0.05-80% of genes in bacterial and archaeal genomes have been affected by HGT, depending on the analytical method used and the genome analysed [8][9][10] . Although HGT is widespread, it is not random: patterns of preferential gene exchange among specific groups of organisms that share ancestry or habitat have been * Present address. aslang@mun.ca; olgazh@dartmouth.edu; j.beatty@mail.ubc.ca Competing interests statementThe authors declare no competing financial interests. 6,9,11,12 . Such patterns are probably a consequence of existing barriers to HGT, which have been reviewed in detail elsewhere 13,14 . FURTHER INFORMATIONAlthough we have known about some HGT mechanisms for decades, novel processes that expand the existing repertoire of gene exchange methods are continually being identified. Transformation was the first mechanism of gene exchange to be discovered 15 , wherein DNA is taken up directly from the environment (reviewed elsewhere 16,17 ). In transduction, DNA transfer is mediated by viral particles (BOX 1). In conjugation, which was discovered in the 1940s 18 , DNA is transferred from a donor to a recipient cell during cell-to-cell contact; conjugation is used in the transfer of plasmids, transposons, integrons, and integrative and conjugative elements (ICEs) [19][20][21] . There are other modes of gene exchange that do not fit well into any of these three canonical mechanisms, including temporary cell fusion followed by chromosomal recombination and plasmid exchange 22 , intercellular connection through nanotubes 23 , and the release of membrane vesicles containing chromosomal, plasmid and phage DNA that can then merge with nearby cells 24 . In addition, a novel mechanism of gene transfer that has feature...

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Gene transfer agents: phage-like elements of genetic exchange

2012

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“…The Staphylococcus aureus pathogenicity islands (SaPIs) are the best-characterized members of the phage-inducible chromosomal island family of mobile genetic elements (MGEs; Novick et al, 2010). SaPIs are B15 kb mobile elements that encode virulence factors and are parasitic on specific temperate (helper) phages.…”

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Intra- and inter-generic transfer of pathogenicity island-encoded virulence genes by cos phages

et al. 2014

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Bacteriophage-mediated horizontal gene transfer is one of the primary driving forces of bacterial evolution. The pac-type phages are generally thought to facilitate most of the phage-mediated gene transfer between closely related bacteria, including that of mobile genetic elements-encoded virulence genes. In this study, we report that staphylococcal cos-type phages transferred the Staphylococcus aureus pathogenicity island SaPIbov5 to non-aureus staphylococcal species and also to different genera. Our results describe the first intra-and intergeneric transfer of a pathogenicity island by a cos phage, and highlight a gene transfer mechanism that may have important implications for pathogen evolution.

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“…Staphylococci are also likely to exchange genetic elements, possibly via generalized transduction, so they may acquire drug-resistant genes such as methicillin resistance. To the best of our knowledge, however, no direct evidence is available on intragenus generalized transduction in staphylococci (Novick et al, 2010).…”

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Intragenus generalized transduction in Staphylococcus spp. by a novel giant phage

et al. 2014

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Bacteriophage (phage)-mediated generalized transduction is expected to contribute to the emergence of drug-resistant staphylococcal clones in various environments. In this study, novel phage S6 was isolated from sewage and used to test generalized transduction in human-and animal-derived staphylococci. Phage S6 was a novel type of giant myophage, which possessed a DNA genome that contained uracil instead of thymine, and it could infect all of the tested staphylococcal species. The phage S6 appeared to be similar to the transducing phage PBS1, which infects Bacillus spp. Moreover, phage S6 facilitated the transduction of a plasmid in Staphylococcus aureus and from S. aureus to non-aureus staphylococcal species, as well as vice versa. Transduction of methicillin resistance also occurred in S. aureus. This is the first report of successful intragenus generalized transduction among staphylococci.

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The phage-related chromosomal islands of Gram-positive bacteria

Cited by 347 publications

References 40 publications

Gene transfer agents: phage-like elements of genetic exchange

Gene transfer agents: phage-like elements of genetic exchange

Intra- and inter-generic transfer of pathogenicity island-encoded virulence genes by cos phages

Intragenus generalized transduction in Staphylococcus spp. by a novel giant phage

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