Comparative analysis of prophages carried by human and animal-associated Staphylococcus aureus strains spreading across the European regions (original) (raw)

Staphylococcus aureus is a major human and animal pathogen although the animal-associated S. aureus can be a potential risk of human zoonoses. Acquisition of phage-related genomic islands determines the S. aureus species diversity. This study characterized and compared the genome architecture, distribution nature, and evolutionary relationship of 65 complete prophages carried by human and animal-associated S. aureus strains spreading across the European regions. The analyzed prophage genomes showed mosaic architecture with extensive variation in genome size. The phylogenetic analyses generated seven clades in which prophages of the animal-associated S. aureus scattered in all the clades. The S. aureus strains with the same SCCmec type, and clonal complex favored the harboring of similar prophage sequences and suggested that the frequency of phage-mediated horizontal gene transfer is higher between them. The presence of various virulence factors in prophages of animal-associated S. aureus suggested that these prophages could have more pathogenic potential than prophages of human-associated S. aureus. This study showed that the S. aureus phages are dispersed among the several S. aureus serotypes and around the European regions. Further, understanding the phage functional genomics is necessary for the phage-host interactions and could be used for tracing the S. aureus strains transmission. Staphylococcus aureus is a major human and animal pathogen, leading to cause severe hospital-acquired, community-acquired, and animal-acquired infections 1. S. aureus colonies in various ecological niches within human and animal hosts 2 and causing the diverse ranges of infections ranging from skin and soft tissue infections to life-threatening infections 3,4. The animal-associated S. aureus can be a potential risk of human zoonoses and a threat to human public health 5,6. The genomic plasticity of S. aureus facilitates the acquisition of the mobile genetic elements (MGEs) such as prophage, S. aureus pathogenic island (SaPIs), genomic islands (νSa), transposons, staphylococcal cassette chromosomes (SCCs), and plasmids, which have an array of genes encoding proteins involved in antibiotic resistance, virulence, and other contingency functions 7-9. Acquisition of prophages or phage-related genomic islands determine the diversity of the S. aureus species and contribute to a dramatic form of genetic adaptation to various host conditions 10. Based on the genome sequence and sizes of the S. aureus phages, phages can be grouped into three classes among Caudovirales order, viz., Podoviridae family belongs to class I with the smallest genome (< 20 kb), Siphoviridae family belongs to class II showing intermediate genome sizes (39-125 kb), and Myoviridae family belongs to class III with largest genome size (> 125 kb) 2,11. The genome of Siphoviridae family is composed of six functional modules viz., lysogeny, DNA replication, packaging, head, tail, and lysis 12. Prophage can be switched from a lysogenic state to a lytic state in response to the metabolic state or environmental stresses of the host 13. The expression of a specific phage repressor gene (cI) inhibits the