Preliminary comparative genomics revealed pathogenic potential and international spread of Staphylococcus argenteus

Abstract

Background Staphylococcus argenteus and S. schweitzeri, were recently proposed as novel species within S. aureus complex (SAC). S. argenteus has been reported in many countries and can threaten human health. S. schweitzeri has not been associated with human infections, but has been isolated from non-human primates. Questions regarding the evolution of pathogenicity of these two species will remain elusive until an exploratory evolutionary framework is established.ResultsWe present genomic comparison analysis among members of SAC based on a pan-genome definition, which included 15 S. argenteus genomes (five newly sequenced), six S. schweitzeri genomes and 30 divergent S. aureus genomes. The three species had divergent core genomes and rare interspecific recombination was observed among the core genes. However, some subtypes of staphylococcal cassette chromosome mec (SCCmec) elements and prophages were present in different species. Of 111 tested virulence genes of S. aureus, 85 and 86 homologous genes were found in S. argenteus and S. schweitzeri, respectively. There was no difference in virulence gene content among the three species, but the sequence of most core virulence genes was divergent. Analysis of the agr locus and the genes in the capsular polysaccharides biosynthetic operon revealed that they both diverged before the speciation of SAC members. Furthermore, the widespread geographic distribution of S. argenteus, sequence type 2250, showed ambiguous biogeographical structure among geographically isolated populations, demonstrating an international spread of this pathogen.Conclusions S. argenteus has spread among several countries, and invasive infections and persistent carriage may be not limited to currently reported regions. S. argenteus probably had undergone a recent host adaption and can cause human infections with a similar pathogenic potential.Electronic supplementary materialThe online version of this article (10.1186/s12864-017-4149-9) contains supplementary material, which is available to authorized users.

Staphylococcus argenteus and Staphylococcus schweitzeri are cytotoxic to human cells in vitro due to high expression of alpha-hemolysin Hla

“…The S. argenteus clinical isolate RK308 has been described previously [18]. The S. argenteus type strain MSHR1132T (isolated from a human sample [11]), and the S. schweitzeri type strain FSA084T (isolated from a redtailed monkey in Gabon, Africa [7]) have been described previously [2] and were purchased from DSMZ, Braunschweig, Germany.…”

“…Sequences for isolates included in cytotoxicity assays and RNA expression analyses are available online in the GenBank database (http:// www.ncbi.nlm.nih.gov/Genbank/index.html) under the following accession numbers: S. argenteus RK308, LSFQ00000000; S. argenteus MSHR1132T, FR821777; S. schweitzeri FSA084T, CCEL00000000; S. aureus 1800T (DSM20231), AMYL00000000 and MRSA CCUG 35601, REGS00000000. For a complete list of all 116 sequenced S. argenteus isolates used to confirm the presence of the hla gene, please refer to [18]. Sequence alignments and phylogenetic analyses were done in CLC Main Workbench (Qiagen, Hilden, Germany) using standard program settings.…”

“…S. argenteus and S. schweitzeri have been shown to carry several toxin genes, such as staphylococcal enterotoxins sea, sec, and sed, hemolysins hla and hlb and Panton-Valentine leucocidin (pvl) [3,7,[15][16][17][18], although some studies have indicated a lower prevalence of these genes compared to S. aureus [3,17]. Using S. aureus-specific PCR primers, the majority of S. argenteus isolates were first shown to be PVLnegative [3].…”

“…Using S. aureus-specific PCR primers, the majority of S. argenteus isolates were first shown to be PVLnegative [3]. However, whole genome sequencing (WGS) later revealed both a nucleotide sequence similarity of only approximately 75% between S. argenteus and S. aureus in the pvl gene, and actually much higher prevalence of pvl among S. argenteus isolates [18]. Alpha-hemolysin (Hla) was the first staphylococcal exotoxin to be identified and belongs to the group of membrane-damaging toxins (reviewed in [19]), with a well-studied function and role in S. aureus virulence.…”

“…We previously characterized a clinical S. argenteus isolate (RK308) and, using WGS, were able to identify several toxin genes in the genome [18]. To further investigate the molecular mechanisms of S. argenteus virulence, we here studied the effect of this particular isolate on human cells in vitro and could show that, as opposed to S. aureus, S. argenteus was cytotoxic due to high levels of the secreted toxin Hla.…”