Sau42I, a BcgI-like restriction–modification system encoded by the Staphylococcus aureus quadruple-converting phage π42

Dempsey, R.; Carroll, David J.; Kong, Huimin; Higgins, Lauren; Keane, C. T.; Coleman, David C.

doi:10.1099/mic.0.27646-0

Cited by 47 publications

(38 citation statements)

References 40 publications

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“…Prophage sequences encoding a putative RM system were identified in StauST398-5pro. Thus, the emerging CC398 isolates, all of which harbor StauST398-5pro, have a prophage-encoded RM system conferring strong protection against horizontal genetic transfer, similar to that described for the /42 prophage (Dempsey et al, 2005). This protection may confer a selective advantage over competing organisms in their environment.…”

Section: Discussionmentioning

confidence: 99%

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Analysis of prophages harbored by the human-adapted subpopulation of Staphylococcus aureus CC398

Mee-Marquet

Corvaglia

Valentin

et al. 2013

Infection, Genetics and Evolution

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a b s t r a c tStaphylococcus aureus clonal complex 398 is a livestock-associated pathogen that poses a worldwide threat because of its ability to colonize and infect both humans and animals. We used high-resolution whole-genome microarrays, prophage profiling, immune evasion cluster characterization and wholegenome sequencing to investigate the roles of prophages in the emerging human-adapted subpopulation of CC398 that has been associated with invasive infections in humans living in animal-free environments.We characterized one phage and two prophages specifically harbored by CC398 isolates belonging to the emerging subpopulation. We introduced the phage into permissive prophage-free isolates. We investigated the effects of lysogeny on the host ability to resist further phage infection and transformation, to acquire the capacity to invade human cells, and to express virulence factors encoded by prophages. We report evidence of a defective /MR11-like helper prophage, named StauST398-5pro, specifically associated with the emerging non-LA CC398 subpopulation. StauST398-5pro confers substantial protection against horizontal genetic transfer to its host. It interacts with a human-associated b-converting prophage encoding immune-modulating proteins such that virulence genes are expressed during stress situations.Our findings provide insight into the role of phages in the expression of virulence and in the spread of genetic information among new host-adapted S. aureus isolates. We demonstrate that functional prophage elements can condition host specificity and confer new virulence traits on emerging intra-species clones of bacteria.

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Section: Discussionmentioning

confidence: 99%

“…File Table 1). Lysogenization of the prophage-free isolate S124 with S100-/ lysate, containing the recombinant phage StauST398-1, resulted in resistance to a broad range of phages, similar to isolates lysogenized with the /42 prophage that encodes a powerful restriction modification (RM) system (Dempsey et al, 2005).…”

Section: Phage Resistancementioning

confidence: 99%

Analysis of prophages harbored by the human-adapted subpopulation of Staphylococcus aureus CC398

Mee-Marquet

Corvaglia

Valentin

et al. 2013

Infection, Genetics and Evolution

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“…As a consequence, S. aureus lineages carry a unique combination of core variable genes, suggesting only a vertical transmission of these genes (24). Additional R-M systems were described for S. aureus, some of which were shown to be phage encoded, which may also contribute to phage exclusion (7). In addition to the host restriction, the lysogenic immunity of a resident prophage may play a role in prevalence differences.…”

Section: Discussionmentioning

confidence: 99%

Diversity of Prophages in Dominant Staphylococcus aureus Clonal Lineages

et al. 2009

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Temperate bacteriophages play an important role in the pathogenicity of Staphylococcus aureus, for instance, by mediating the horizontal gene transfer of virulence factors. Here we established a classification scheme for staphylococcal prophages of the major Siphoviridae family based on integrase gene polymorphism. Seventy-one published genome sequences of staphylococcal phages were clustered into distinct integrase groups which were related to the chromosomal integration site and to the encoded virulence gene content. Analysis of three marker modules (lysogeny, tail, and lysis) for phage functional units revealed that these phages exhibit different degrees of genome mosaicism. The prevalence of prophages in a representative S. aureus strain collection consisting of 386 isolates of diverse origin was determined. By linking the phage content to dominant S. aureus clonal complexes we could show that the distribution of bacteriophages varied remarkably between lineages, indicating restriction-based barriers. A comparison of colonizing and invasive S. aureus strain populations revealed that hlb-converting phages were significantly more frequent in colonizing strains.Staphylococcus aureus asymptomatically colonizes the anterior nares of humans but also causes a wide spectrum of acute and chronic diseases. Most of the dissimilarity between S. aureus strains is due to the presence of mobile genetic elements such as plasmids, bacteriophages, pathogenicity islands, transposons, and insertion sequences (2,14,19,23). Many virulence factors are encoded on such mobile elements (3,6,17,26,27,35). In particular, bacteriophages play an important role in the pathogenicity of S. aureus either by carrying accessory virulence factors such as Panton-Valentine leukocidin (PVL) (encoded by the luk-PV operon), staphylokinase (encoded by sak), enterotoxin A (encoded by sea), and exfoliative toxin A (encoded by eta) or by interrupting chromosomal virulence genes such as those for ␤-hemolysin (hlb) and lipase (geh) upon insertion. Additionally, phages are the primary vehicle of lateral gene transfer between S. aureus strains, providing the species with the potential for broad genetic variation. We could show that phages increase the genome plasticity of S. aureus during infection, facilitating the adaptation of the pathogen to various host conditions (11,12).Despite the obvious importance of phages for the biology of S. aureus, epidemiological data on the prevalence of phages in this species are limited (28, 33). More than 80 genome sequences of staphylococcal bacteriophages and prophages are available in the public genome databases. Most published S. aureus phages belong to the Siphoviridae family of temperate, tailed bacterial viruses. Traditionally, S. aureus phages were characterized according to their lytic activity, morphology, and serological properties (1, 28). Today, the temperate phages in clinical S. aureus isolates can by identified with a multiplex PCR strategy, which is based on sequence differences between viral genes codin...

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“…It is well known that lysogenic bacteria are resistant to infection with homologous bacteriophages. In addition, a recent study by Dempsey et al (7) showed that 42 introduces a restriction modification system into its lysogen, making the bacterium resistant to all international basic S. aureus typing phages. Using these properties we studied whether the IEC variants were carried by related or different ␤C-s.…”

Section: Diversity Of Bacterial Strains Containing Iec Types a To Gmentioning

confidence: 99%

The Innate Immune Modulators Staphylococcal Complement Inhibitor and Chemotaxis Inhibitory Protein ofStaphylococcus aureusAre Located on β-Hemolysin-Converting Bacteriophages

Wamel¹,

Rooijakkers²,

Ruyken³

et al. 2006

J Bacteriol

491

458

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Two newly discovered immune modulators, chemotaxis inhibitory protein of Staphylococcus aureus (CHIPS)and staphylococcal complement inhibitor (SCIN), cluster on the conserved 3 end of ␤-hemolysin (hlb)-converting bacteriophages (␤C-s). Since these ␤C-s also carry the genes for the immune evasion molecules staphylokinase (sak) and enterotoxin A (sea), this 8-kb region at the 3 end of ␤C-represents an innate immune evasion cluster (IEC). By PCR and Southern analyses of 85 clinical Staphylococcus aureus strains and 5 classical laboratory strains, we show that 90% of S. aureus strains carry a ␤C-with an IEC. Seven IEC variants were discovered, carrying different combinations of chp, sak, or sea (or sep), always in the same 5-to-3 orientation and on the 3 end of a ␤C-. From most IEC variants we could isolate active bacteriophages by mitomycin C treatment, of which lysogens were generated in S. aureus R5 (broad phage host). All IEC-carrying bacteriophages integrated into hlb, as was measured by Southern blotting of R5 lysogens. Large quantities of the different bacteriophages were obtained by mitomycin C treatment of the lysogens, and bacteriophages were collected and used to reinfect all lysogenic R5 strains. In total, five lytic families were found. Furthermore, phage DNA was isolated and digested with EcoR1, revealing that one IEC variant can be found on different ␤I-s. In conclusion, the four human-specific innate immune modulators SCIN, CHIPS, SAK, and SEA form an IEC that is easily transferred among S. aureus strains by a diverse group of ␤-hemolysin-converting bacteriophages.Recently, we described two new innate immune modulators of Staphylococcus aureus: staphylococcal complement inhibitor (SCIN) and chemotaxis inhibitory protein of S. aureus (CHIPS). SCIN is a C3 convertase inhibitor, blocking the formation of C3b on the surface of the bacterium and the ability of human neutrophils to phagocytose S. aureus (25). CHIPS is a bacterial chemokine receptor modulator that specifically binds two chemokine receptors. CHIPS attenuates the response of the C5a receptor (C5aR) as well as the formylated peptide receptor of human neutrophils. This results in inhibition of neutrophil chemotaxis and activation in response to C5a and formylated peptides (6,10,20,21). Both SCIN and CHIPS are important virulence factors that protect S. aureus from innate immune defense systems.The SCIN (scn) and CHIPS (chp) genes are found in 6/7 and 3/7 sequenced S. aureus strains, respectively. Analyses of these sequenced genomes showed that both scn and chp are carried by ␤-hemolysin (hlb)-converting bacteriophages (␤C-s), formerly known as double-and triple-converting phages. Doubleconverting bacteriophages were earlier described to negatively convert ␤-hemolysin expression but simultaneously introduce the staphylokinase (SAK) gene. Triple conversion leads to ␤-hemolysin-negative and SAK-and staphylococcal enterotoxin A (SEA)-positive strains. 13 and 42 are examples of, respectively, double-and triple-converting bacteriophages. Both 13 and ...

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Sau42I, a BcgI-like restriction–modification system encoded by the Staphylococcus aureus quadruple-converting phage π42

Cited by 47 publications

References 40 publications

Analysis of prophages harbored by the human-adapted subpopulation of Staphylococcus aureus CC398

Analysis of prophages harbored by the human-adapted subpopulation of Staphylococcus aureus CC398

Diversity of Prophages in Dominant Staphylococcus aureus Clonal Lineages

The Innate Immune Modulators Staphylococcal Complement Inhibitor and Chemotaxis Inhibitory Protein ofStaphylococcus aureusAre Located on β-Hemolysin-Converting Bacteriophages

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