Diversity of prophages in dominant Staphylococcus aureus clonal lineages

Abstract

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.

FIG. 1.

In silico analysis of the integrase groups, serogroups, holin groups, and virulence genes of 70 published staphylococcal bacteriophages of the class Siphoviridae. Integrase nucleotide sequences were aligned using the ClustalW algorithm. Identical serogroups and holin groups are color coded. Integrases of the serine recombinase-type family are shaded in gray.

FIG. 2.

Multiplex PCR detecting the Sa1int to Sa7int integrase genes in prototypic S. aureus strains.