Abstract

Staphylococcus hominis is a commensal resident of human skin and an opportunistic pathogen. The species is subdivided into two subspecies, S. hominis subsp. hominis and S. hominis subsp. novobiosepticus, which are difficult to distinguish. To investigate the evolution and epidemiology of S. hominis, a total of 108 isolates collected from 10 countries over 40 years were characterized by classical phenotypic methods and genetic methods. One nonsynonymous mutation in gyrB, scored with a novel SNP typing assay, had a perfect association with the novobiocin-resistant phenotype. A multilocus sequence typing (MLST) scheme was developed from six housekeeping gene fragments, and revealed relatively high levels of genetic diversity and a significant impact of recombination on S. hominis population structure. Among the 40 sequence types (STs) identified by MLST, three STs (ST2, ST16 and ST23) were S. hominis subsp. novobiosepticus, and they distinguished between isolates from different outbreaks, whereas 37 other STs were S. hominis subsp. hominis, one of which was widely disseminated (ST1). A modified PCR assay was developed to detect the presence of ccrAB4 from the SCCmec genetic element. S. hominis subsp. novobiosepticus isolates were oxacillin-resistant and carriers of specific components of SCCmec (mecA class A, ccrAB3, ccrAB4, ccrC), whereas S. hominis subsp. hominis included both oxacillin-sensitive and -resistant isolates and a more diverse array of SCCmec components. Surprisingly, phylogenetic analyses indicated that S. hominis subsp. novobiosepticus may be a polyphyletic and, hence, artificial taxon. In summary, these results revealed the genetic diversity of S. hominis, the identities of outbreak-causing clones, and the evolutionary relationships between subspecies and clones. The pathogenic lifestyle attributed to S. hominis subsp. novobiosepticus may have originated on more than one occasion.

Highlights

  • Distinguishing commensal from pathogenic coagulase-negative staphylococci (CoNS) is a major challenge for clinical microbiology laboratories

  • Sixty-eight isolates were from three hospitals in the USA (Illinois, n = 26; Mississippi, n = 1; New York, n = 41), 17 isolates were from one hospital in Spain, including isolates from an outbreak among neonates and two isolates from adults that were not associated with the outbreak [17], five isolates were from a hospital outbreak among adults in Brazil [18], and isolates were selected to be diverse by geography (Argentina, n = 1; Colombia, n = 1; Italy, n = 1; Japan, n = 1; Portugal, n = 2; Mexico, n = 3; Tunisia, n = 7) and by their different XhoI pulsed-field gel electrophoresis (PFGE) patterns that were characterized according to Bouchami et al [30]

  • S. hominis was revealed by multilocus sequence typing (MLST) to be a genetically diverse species, relative to other staphylococci such as S. aureus and S. epidermidis, and recombination was shown to have a significant role in generating this diversity

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Summary

Introduction

Distinguishing commensal from pathogenic coagulase-negative staphylococci (CoNS) is a major challenge for clinical microbiology laboratories. The CoNS are part of the normal bacterial flora of human skin, from which they frequently contaminate clinical specimens, yet they have been increasingly isolated over the past 30 years from human infections associated with indwelling medical devices [1,2]. Gunn and Colwell [7] reported S. hominis to be the most common and phenotypically diverse staphylococcal species isolated from unpolluted marine environments. Nucleotide diversity, which is the average number of pairwise nucleotide differences per site, ranged from 0.002 to 0.021 for different loci and averaged 0.01 across sequence types (STs) (Table 3). This level of nucleotide diversity is Marker category.

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