Review
doi: 10.1038/nrmicro2393.The phage-related chromosomal islands of Gram-positive bacteria
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- PMID:20634809
- PMCID: PMC3522866
- DOI: 10.1038/nrmicro2393
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Review
The phage-related chromosomal islands of Gram-positive bacteria
Richard P Novick et al. Nat Rev Microbiol.2010 Aug.
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Abstract
The phage-related chromosomal islands (PRCIs) were first identified in Staphylococcus aureus as highly mobile, superantigen-encoding genetic elements known as the S. aureus pathogenicity islands (SaPIs). These elements are characterized by a specific set of phage-related functions that enable them to use the phage reproduction cycle for their own transduction and inhibit phage reproduction in the process. SaPIs produce many phage-like infectious particles; their streptococcal counterparts have a role in gene regulation but may not be infectious. These elements therefore represent phage satellites or parasites, not defective phages. In this Review, we discuss the shared genetic content of PRCIs, their life cycle and their ability to be transferred across large phylogenetic distances.
Figures
Genomes are aligned according to the prophage convention, with the integrase gene (int) at the left end. Genes are coloured according to their sequence and function:int andxis (excisionase) are yellow; transcription regulators are dark blue; replication genes (including the primase gene (pri) and the replication initiator gene (rep)) are purple; the replication origin (ori) is red; encapsidation genes are green, with the terminase small subunit gene (terS) in light green; superantigen and other accessory genes are pink; andpif (which functions in phage interference) is light blue. Genes encoding hypothetical proteins are orange.a | The gene organization ofStaphylococcus aureus pathogenicity islands (SaPIs).b | Putative phage-related chromosomal islands from genera other thanStaphylococcus. SaPIm1/n1 indicates SaPIn1 (fromS. aureus str. n315) and SaPIm1 (fromS. aureus str. mu50), which are essentially identical.
a |Staphylococcus aureus pathogenicity island (SaPI) induction by an SOS-induced helper prophage.attP andattS are the prophage and SaPI core attachment sequences, respectively;attB andattC are the prophage and SaPI core chromosomal attachment sequences, respectively. After induction and excision of the helper phage, phage dUTPase relieves the Stl-mediated repression of the SaPI, allowing production of SaPI proteins. SaPI excisionase (Xis) subsequently promotes the excision of the SaPI through a Campbell mechanism, restoring theattC andattS sites. Subsequent SaPI replication produces hundreds of copies in the form of a concatemer, which is cleaved by the terminase complex into individual copies and packed into phage particles consisting entirely of phage proteins but with a smaller head than the phage capsids, owing to the action of SaPI proteins.b | SaPI infection. Terminal redundancy allows the incoming SaPI DNA to circularize, after which the circular DNA is integrated at the chromosomalattC site by crossover with the SaPIattS site. This process requires the SaPI integrase. Stl silences the expression of SaPI genes, keeping the element integrated.c | Co-infection of a SaPI and a helper phage allows the SaPI DNA to be replicated prior to integration. The synthesis of phage proteins leads to the production of phage capsids, which are used to package the replicated SaPI DNA. As in parta, SaPI proteins affect the size of the capsids that are produced.
Lysates prepared fromStaphylococcus aureus strains carrying the relevantS. aureus pathogenicity island (SaPI) and/or helper phage were centrifuged, and the pellets were resuspended in buffer, applied to copper grids and negatively stained with uranyl acetate.a | Lysate from bacteria carrying phage 80α alone, containing a normal-sized capsids.b | Lysate from cells carrying phage 80α and SaPI1.c | Lysate from cells carrying phage 80α and SaPI1, showing both the large phage capsids and the small SaPI capsids.d | Lysate from cells carrying phage 80α and SaPIbov1ΔterS. Despite the absence of TerS, SaPIbov1 induces the formation of small capsids. L, large capsid; LP, large procapsid; S, small capsid; SP, small procapsid.
References
- Gogarten JP, Doolittle WF, Lawrence JG. Prokaryotic evolution in light of gene transfer. Mol. Biol. Evol. 2002;19:2226–2238. - PubMed
- Gillet Y, et al. Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet. 2002;359:753–759. - PubMed
- Novick RP. Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid. 2003;49:93–105. - PubMed
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