Abstract
Streptococcus pyogenes, is an important human pathogen classified within the pyogenic group of streptococci, exclusively adapted to the human host. Our goal was to employ a comparative evolutionary approach to better understand the genomic events concomitant with S. pyogenes human adaptation. As part of ascertaining these events, we sequenced the genome of one of the potential sister species, the agricultural pathogen S. canis, and combined it in a comparative genomics reconciliation analysis with two other closely related species, Streptococcus dysgalactiae and Streptococcus equi, to determine the genes that were gained and lost during S. pyogenes evolution. Genome wide phylogenetic analyses involving 15 Streptococcus species provided convincing support for a clade of S. equi, S. pyogenes, S. dysgalactiae, and S. canis and suggested that the most likely S. pyogenes sister species was S. dysgalactiae. The reconciliation analysis identified 113 genes that were gained on the lineage leading to S. pyogenes. Almost half (46%) of these gained genes were phage associated and 14 showed significant matches to experimentally verified bacteria virulence factors. Subsequent to the origin of S. pyogenes, over half of the phage associated genes were involved in 90 different LGT events, mostly involving different strains of S. pyogenes, but with a high proportion involving the horse specific pathogen S. equi subsp. equi, with the directionality almost exclusively (86%) in the S. pyogenes to S. equi direction. Streptococcus agalactiae appears to have played an important role in the evolution of S. pyogenes with a high proportion of LGTs originating from this species. Overall the analysis suggests that S. pyogenes adaptation to the human host was achieved in part by (i) the integration of new virulence factors (e.g. speB, and the sal locus) and (ii) the construction of new regulation networks (e.g. rgg, and to some extent speB).
Highlights
Streptococcus pyogenes is a leading human pathogen responsible for illness ranging from mild skin and respiratory infections to life-threatening invasive, and post-infection diseases
Information is available regarding the genomic repertoire of S. pyogenes
We describe the genomic features that evolved since the divergence of S. pyogenes from its closest relatives, in an attempt to understand the molecular details associated with S. pyogenes development as a strict human pathogen
Summary
Streptococcus pyogenes is a leading human pathogen responsible for illness ranging from mild skin and respiratory infections (e.g. pharyngitis and impetigo) to life-threatening invasive (e.g. pneumonia, septicemia, streptococcal toxic shock syndrome, necrotizing fasciitis), and post-infection diseases (e.g. acute rheumatic fever, paediatric autoimmune neuropsychiatric disorders). Many different serotypes and strains have been described, with some being linked to particular disease. Strains causing necrotizing fasciitis are largely serotype M1 and M3 [1], while M18 is often linked to acute rheumatic fever [2], and M28 to puerperal sepsis [3]. The publications associated with these genomes have suggested links between lisogenic phages, and the virulence factors they are carrying, to specific diseases. A long and detailed list of S. pyogenes virulence factors is available S. pyogenes is unusual in that it is only found in humans
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