Abstract
The virulence of Staphylococcus aureus, in both human and animal hosts, is largely influenced by the acquisition of mobile genetic elements (MGEs). Most S. aureus strains carry a variety of MGEs, including three genomic islands (νSaα, νSaβ, νSaγ) that are diverse in virulence gene content but conserved within strain lineages. Although the mobilization of pathogenicity islands, phages and plasmids has been well studied, the mobilization of genomic islands is poorly understood. We previously demonstrated the mobilization of νSaβ by the adjacent temperate bacteriophage ϕSaBov from strain RF122. In this study, we demonstrate that ϕSaBov mediates the mobilization of νSaα and νSaγ, which are located remotely from ϕSaBov, mostly to recipient strains belonging to ST151. Phage DNA sequence analysis revealed that chromosomal DNA excision events from RF122 were highly specific to MGEs, suggesting sequence-specific DNA excision and packaging events rather than generalized transduction by a temperate phage. Disruption of the int gene in ϕSaBov did not affect phage DNA excision, packaging, and integration events. However, disruption of the terL gene completely abolished phage DNA packing events, suggesting that the primary function of temperate phage in the transfer of genomic islands is to allow for phage DNA packaging by TerL and that transducing phage particles are the actual vehicle for transfer. These results extend our understanding of the important role of bacteriophage in the horizontal transfer and evolution of genomic islands in S. aureus.
Highlights
Genetic variation of bacteria can be achieved through mutations, rearrangements and horizontal gene transfers and recombinations
To investigate the possibility that transducing phage particles induced from strain RF122 harbor genes uniquely associated with mobile genetic elements (MGEs), PCR was performed using phage DNA extracted from RF122 following mitomycin C treatment
Results of PCR revealed that transducing phage particles induced from RF122 harbor genes associated with MGEs including genomic islands νSaα, νSaβ, and νSaγ, SaPIbov1, SaPI122, and φSaBov (Fig 1B)
Summary
Genetic variation of bacteria can be achieved through mutations, rearrangements and horizontal gene transfers and recombinations. Genomic islands are relatively large segments of DNA ranging from 10 to 200 kb often integrated into tRNA gene clusters flanked by 16–20 bp direct repeats [3] They are recognized as discrete DNA segments acquired by horizontal gene transfer since they can differ from the rest of the chromosome in terms of GC content (%G+C) and codon usage [3, 5]. Staphylococcus aureus is a major pathogen that colonizes the skin and mucous membranes of humans and animals, causing diseases ranging from mild skin infections to severe invasive diseases such as necrotizing pneumonia, infective endocarditis, and osteomyelitis [6,7,8] The pathogenicity of this bacterium is largely influenced by the virulence genes carried on MGEs [9]. Our results showed that the genetic background of the host and recipient strains impact the ability and efficiency of transfer of MGEs mediated by bacteriophages, suggesting the presence of MGE-specific mechanisms of excision and integration from the donor and the recipient strains, respectively, in concert with functions from bacteriophages
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