Abstract
Staphylococcus aureus is a major cause of human and animal infections. Bacteriophage are a class of mobile genetic element (MGE) that carry virulence genes and disseminate them horizontally, including Panton–Valentine leukocidin (PVL), the immune evasion cluster (IEC) associated with human specificity, and enterotoxin A the major toxin associated with food poisoning. S. aureus isolates group into major clonal complex (CC) lineages that largely evolve independently due to possession of different restriction–modification (RM) systems. We aimed to better understand the horizontal and vertical transmission dynamics of virulence and resistance genes by bacteriophage by using (i) bioinformatic approaches to analyze bacteriophage genomes from the first 79 sequenced S. aureus isolates and (ii) S. aureus microarrays to analyze the distribution of bacteriophage and virulence genes in S. aureus isolates from a broader range of lineages. The distribution of eight bacteriophage families was highly variable but lineage associated. Nevertheless, there was evidence of frequent acquisition and loss and not just vertical transmission. Most bacteriophage genes were dispensable, and extensive mosaicism was seen. Surprisingly, virulence genes were tightly associated with specific phage families. This data suggests S. aureus bacteriophage evolve rapidly, and the horizontal gene transfer (HGT) of virulence genes encoded by bacteriophage is restricted by bacteriophage family and the lineage of the host bacterium, delaying the evolution of fully resistant and virulent strains.
Highlights
Staphylococcus aureus is a frequent colonizer of humans and mammals and a prevalent cause of skin and hospital associated infections
Staphylococcus aureus prophage carry important genes that impact on the ability to colonize the human nose, and to cause disease
It is interesting to consider why the bacterium has evolved to carry these genes on a mobile genetic elements (MGEs) and not to systematically incorporate them into the stable regions of the chromosome
Summary
Staphylococcus aureus is a frequent colonizer of humans and mammals and a prevalent cause of skin and hospital associated infections. Of further concern is the emergence of fully vancomycin resistant S. aureus (VRSA), reducing our options to prevent and treat severe MRSA infections (Weigel et al, 2003). The adaptation and evolution of these S. aureus is largely due to the acquisition of mobile genetic elements (MGEs) that carry virulence and resistance genes. Such MGEs include bacteriophage, staphylococcal cassette chromosomes (SCCs), plasmids, S. aureus pathogenicity islands (SaPIs), and transposons that can move between bacteria by horizontal gene transfer (HGT) mechanisms (Lindsay, 2010; Malachowa and DeLeo, 2010). The dissemination of MGEs through S. aureus populations is concerning as they can alter the pathogenicity, resistance, and host range of bacteria generating strains that cause novel clinical challenges
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