The complete genomes of Staphylococcus aureus bacteriophages 80 and 80α—Implications for the specificity of SaPI mobilization

Christie, Gail E.; Matthews, Avery; King, Darrin; Lane, Kristin D.; Olivarez, Nicholas P.; Tallent, Sandra M.; Gill, Steven R.; Novick, Richard P.

doi:10.1016/j.virol.2010.08.036

Cited by 71 publications

(87 citation statements)

References 56 publications

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“…The mutant phage titers were similar to the wildtype, showing that dut is not essential for phage viability (Table 3). The phages were then used to infect the SaPIbov1 tst::tetM -containing strain JP45 [42], the SaPI1 tst::tetM -containing strain ST1 [43] and the SaPI2 tst::tetM -containing strain ST23 [43]. Transducing titers (cfu/ml) of the resulting lysates were determined by infecting RN4220 followed by plating on GL agar with the inclusion of 5 μg/ml tetracycline.…”

Section: Resultsmentioning

confidence: 99%

The Type 2 dUTPase of Bacteriophage ϕNM1 Initiates Mobilization of Staphylococcus aureus Bovine Pathogenicity Island 1

Hill

Dokland

2016

Journal of Molecular Biology

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Staphylococcus aureus pathogenicity islands (SaPIs) are genetic elements that are mobilized by specific helper phages. The initial step in mobilization is the derepression of the SaPI by the interaction of a phage protein with the SaPI master repressor, Stl. Stl proteins are highly divergent between different SaPIs and respond to different phage-encoded derepressors. One such SaPI, SaPIbov1, is derepressed by the dUTPase (Dut) of bacteriophage 80α (Dut80α) and its phage ϕ11 homolog, Dut11. We previously showed that SaPIbov1 could also be mobilized by phage ϕNM1, even though its dut gene is not homologous with that of 80α. Here, we show that ϕNM1 dut encodes a type 2 dUTPase (DutNM1), which has an α-helical structure that is distinct from the type 1 trimeric, β-sheet structure of Dut80α. Deletion of dutNM1 abolishes the ability of ϕNM1 to mobilize SaPIbov1. Like Dut80α, DutNM1 forms a direct interaction with SaPIbov1 Stl both in vivo and in vitro, leading to inhibition of the dUTPase activity and Stl release from its target DNA. This work provides novel insights into the diverse mechanisms of genetic mobilization in S. aureus.

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Section: Resultsmentioning

confidence: 99%

The Type 2 dUTPase of Bacteriophage ϕNM1 Initiates Mobilization of Staphylococcus aureus Bovine Pathogenicity Island 1

Hill

Dokland

2016

Journal of Molecular Biology

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“…Although SaPIbov1 deletions and subclones have not been very informative in this respect, similar studies with SaPI2 clearly demonstrate the existence of a third interference mechanism. For these experiments, we used phage 80 rather than 80α, because phage 80 does not support the production of small SaPI particles (19) and is not inhibited by any of the ppi genes described above or by cpmAB sp2 (Fig. S4A and Fig.…”

Section: Resultsmentioning

confidence: 99%

Staphylococcal pathogenicity island interference with helper phage reproduction is a paradigm of molecular parasitism

Ram

Chen

Kumar

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

118

133

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Staphylococcal pathogenicity islands (SaPIs) carry superantigen and resistance genes and are extremely widespread in Staphylococcus aureus and in other Gram-positive bacteria. SaPIs represent a major source of intrageneric horizontal gene transfer and a stealth conduit for intergeneric gene transfer; they are phage satellites that exploit the life cycle of their temperate helper phages with elegant precision to enable their rapid replication and promiscuous spread. SaPIs also interfere with helper phage reproduction, blocking plaque formation, sharply reducing burst size and enhancing the survival of host cells following phage infection. Here, we show that SaPIs use several different strategies for phage interference, presumably the result of convergent evolution. One strategy, not described previously in the bacteriophage microcosm, involves a SaPI-encoded protein that directly and specifically interferes with phage DNA packaging by blocking the phage terminase small subunit. Another strategy involves interference with phage reproduction by diversion of the vast majority of virion proteins to the formation of SaPI-specific small infectious particles. Several SaPIs use both of these strategies, and at least one uses neither but possesses a third. Our studies illuminate a key feature of the evolutionary strategy of these mobile genetic elements, in addition to their carriage of important genes—interference with helper phage reproduction, which could ensure their transferability and long-term persistence.

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“…These proteins are related to the well-characterized and highly conserved tailassociated GP61 protein of the staphylococcal phage phiMR11. GP61 is thought to be involved in cell host lysis during phage adsorption (13,14,53,62). The GP61 homolog in StB12 is encoded by the three successive ORF64, ORF65, and ORF66 that are interrupted by two putative group I introns at positions 37063 to 37307 and 37542 to 37918.…”

Section: Resultsmentioning

confidence: 99%

Characterization of Novel Phages Isolated in Coagulase-Negative Staphylococci Reveals Evolutionary Relationships with Staphylococcus aureus Phages

et al. 2012

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Despite increasing interest in coagulase-negative staphylococci (CoNS), little information is available about their bacteriophages. We isolated and sequenced three novel temperate Siphoviridae phages (StB12, StB27, and StB20) from the CoNS Staphylococcus hominis and S. capitis species. The genome sizes are around 40 kb, and open reading frames (ORFs) are arranged in functional modules encoding lysogeny, DNA metabolism, morphology, and cell lysis. Bioinformatics analysis allowed us to assign a potential function to half of the predicted proteins. Structural elements were further identified by proteomic analysis of phage particles, and DNA-packaging mechanisms were determined. Interestingly, the three phages show identical integration sites within their host genomes. In addition to this experimental characterization, we propose a novel classification based on the analysis of 85 phage and prophage genomes, including 15 originating from CoNS. Our analysis established 9 distinct clusters and revealed close relationships between S. aureus and CoNS phages. Genes involved in DNA metabolism and lysis and potentially in phage-host interaction appear to be widespread, while structural genes tend to be cluster specific. Our findings support the notion of a possible reciprocal exchange of genes between phages originating from S. aureus and CoNS, which may be of crucial importance for pathogenesis in staphylococci.

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The complete genomes of Staphylococcus aureus bacteriophages 80 and 80α—Implications for the specificity of SaPI mobilization

Cited by 71 publications

References 56 publications

The Type 2 dUTPase of Bacteriophage ϕNM1 Initiates Mobilization of Staphylococcus aureus Bovine Pathogenicity Island 1

The Type 2 dUTPase of Bacteriophage ϕNM1 Initiates Mobilization of Staphylococcus aureus Bovine Pathogenicity Island 1

Staphylococcal pathogenicity island interference with helper phage reproduction is a paradigm of molecular parasitism

Characterization of Novel Phages Isolated in Coagulase-Negative Staphylococci Reveals Evolutionary Relationships with Staphylococcus aureus Phages

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