Mosaic ancestry, inter-species gene flow and genetic diversity of composite enterotoxigenic Staphylococcus epidermidis pathogenicity islands.

The
only known elements encoding enterotoxins in coagulase-negative staphylococci
(CoNS) are composite Staphylococcus
epidermidis pathogenicity islands (SePIs), including SePI and SeCI regions.
We investigated 1545 Staphylococcus spp. genomes using
whole genome MLST, and queried them for genes of staphylococcal enterotoxin
family and for 29 ORFs identified in prototype
SePI from S. epidermidis FRI909. Enterotoxin-encoding genes were
identified in 97% of S. aureus
genomes, in one S. argenteus genome and
in 9 S. epidermidis genomes. All enterotoxigenic S. epidermidis strains carried composite
SePI, encoding sec and sel enterotoxin genes, and were assigned to a discrete wgMLST
cluster also containing genomes with incomplete islands located in the same
region as complete SePI in enterotoxigenic strains. S. epidermidis strains without SeCI and SePI genes, and strains
with complete SeCI and no SePI genes, were identified but no strains were found
to carry only SePI and not SeCI genes. The systematic differences between SePI
and SeCI regions imply a lineage-specific pattern of inheritance and support independent
acquisition of the two elements in S. epidermidis.
We provided evidence of reticulate evolution of mobile elements that contain
elements with different putative ancestry, including composite SePI that contains genes found in other
CoNS (SeCI), as well as in S. aureus (SePI-like
elements). We conclude that SePI-associated
elements present in non-enterotoxigenic S.
epidermidis represent a scaffold associated with acquisition of virulence-associated
genes. Gene exchange between S. aureus
and S. epidermidis may promote
emergence of new pathogenic S. epidermidis clones.