Abstract
Production of the Panton-Valentine leukocidin (PVL) by Staphylococcus aureus is mediated via the genes lukS-PV and lukF-PV which are carried on bacteriophage ϕSa2. PVL is associated with S. aureus strains that cause serious infections and clones of community-associated methicillin-resistant S. aureus (CA-MRSA) that have additionally disseminated widely. In Western Australia (WA) the original CA-MRSA were PVL negative however, between 2005 and 2008, following the introduction of eight international PVL-positive CA-MRSA, PVL-positive WA CA-MRSA were found. There was concern that PVL bacteriophages from the international clones were transferring into the local clones, therefore a comparative study of PVL-carrying ϕSa2 prophage genomes from historic WA PVL-positive S. aureus and representatives of all PVL-positive CA-MRSA isolated in WA between 2005 and 2008 was performed. The prophages were classified into two genera and three PVL bacteriophage groups and had undergone many recombination events during their evolution. Comparative analysis of mosaic regions of selected bacteriophages using the Alignments of bacteriophage genomes (Alpha) aligner revealed novel recombinations and modules. There was heterogeneity in the chromosomal integration sites, the lysogeny regulation regions, the defence and DNA processing modules, the structural and packaging modules and the lukSF-PV genes. One WA CA-MRSA (WA518751) and one international clone (Korean Clone) have probably acquired PVL-carrying ϕSa2 in WA, however these clones did not disseminate in the community. Genetic heterogeneity made it impossible to trace the source of the PVL prophages in the other WA clones. Against this background of PVL prophage diversity, the sequence of one group, the ϕSa2USA/ϕSa2wa-st93 group, was remarkably stable over at least 20 years and associated with the highly virulent USA300 and ST93-IVa CA-MRSA lineages that have disseminated globally.
Highlights
Staphylococcus aureus is a pandemic pathogen that is part of the human microbiota [1]
In methicillin-sensitive S. aureus (MSSA) and community-associated methicillin-resistant S. aureus (CA-MRSA) the Panton-Valentine leukocidin (PVL) is a virulence factor that is carried on a bacteriophage known as φSa2 which is integrated into the chromosome as a prophage [2]
The prophage genomes had the organisation of Siphoviridae family Sfi21-like PVL viruses of the Caudovirales order and, according to the most recent staphylococcal bacteriophage classification criteria, were placed into two genera and three PVL bacteriophage groups (Table 2) [34,35,36]. φSa2wa-st22, -st59 and -st772 (76.1–76.7% nt identity) were placed into the 77likevirus genus of icosahedral-headed bacteriophage. φSa2wa-st22 and -st772 were group 1 PVL bacteriophage with 74.4% nt identity and φSa2wa-st59 was group 3. φSa2wa-st1, -st5, -st8, -st30, -st72, -st78, -st80, -st93, -st93mssa, -st121mssa and φSa2USA (74.2–100% nt identity) were 3alikevirus genus, prolate-headed group 2 PVL bacteriophage. φSa2wa-st5 was unusual in that it encoded type C DNA polymerase (Genbank: AUM57702) rather than type A (Fig 1)
Summary
Staphylococcus aureus is a pandemic pathogen that is part of the human microbiota [1]. Paramount to the success of S. aureus has been its ability to utilize mobile elements to acquire and disseminate antibiotic resistance, virulence and adaptive mechanisms amongst staphylococcal populations. In methicillin-sensitive S. aureus (MSSA) and community-associated methicillin-resistant S. aureus (CA-MRSA) the Panton-Valentine leukocidin (PVL) is a virulence factor that is carried on a bacteriophage known as φSa2 which is integrated into the chromosome as a prophage [2]. Many virulent strains of MSSA and CA-MRSA do not produce PVL, as the pathogen evolves it is evident that those that have disseminated to cause the greatest burden of infectious disease harbor the prophage [9]
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