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A Look into the Melting Pot: The mecC-Harboring Region Is a Recombination Hot Spot in Staphylococcus stepanovicii.

ABSTRACT: INTRODUCTION:Horizontal gene transfer (HGT) is an important driver for resistance- and virulence factor accumulation in pathogenic bacteria such as Staphylococcus aureus. METHODS:Here, we have investigated the downstream region of the bacterial chromosomal attachment site (attB) for the staphylococcal cassette chromosome mec (SCCmec) element of a commensal mecC-positive Staphylococcus stepanovicii strain (IMT28705; ODD4) with respect to genetic composition and indications of HGT. S. stepanovicii IMT28705 was isolated from a fecal sample of a trapped wild bank vole (Myodes glareolus) during a screening study (National Network on "Rodent-Borne Pathogens") in Germany. Whole genome sequencing (WGS) of IMT28705 together with the mecC-negative type strain CM7717 was conducted in order to comparatively investigate the genomic region downstream of attB (GenBank accession no. KR732654 and KR732653). RESULTS:The bank vole isolate (IMT28705) harbors a mecC gene which shares 99.2% nucleotide (and 98.5% amino acid) sequence identity with mecC of MRSA_LGA251. In addition, the mecC-encoding region harbors the typical blaZ-mecC-mecR1-mecI structure, corresponding with the class E mec complex. While the sequences downstream of attB in both S. stepanovicii isolates (IMT28705 and CM7717) are partitioned by 15 bp direct repeats, further comparison revealed a remarkable low concordance of gene content, indicating a chromosomal "hot spot" for foreign DNA integration and exchange. CONCLUSION:Our data highlight the necessity for further research on transmission routes of resistance encoding factors from the environmental and wildlife resistome.

SUBMITTER: Semmler T

PROVIDER: S-EPMC4723332 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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A Look into the Melting Pot: The mecC-Harboring Region Is a Recombination Hot Spot in Staphylococcus stepanovicii.

Semmler Torsten T Harrison Ewan M EM Lübke-Becker Antina A Ulrich Rainer G RG Wieler Lothar H LH Guenther Sebastian S Stamm Ivonne I Hanssen Anne-Merethe AM Holmes Mark A MA Vincze Szilvia S Walther Birgit B

PloS one 20160122 1

<h4>Introduction</h4>Horizontal gene transfer (HGT) is an important driver for resistance- and virulence factor accumulation in pathogenic bacteria such as Staphylococcus aureus.<h4>Methods</h4>Here, we have investigated the downstream region of the bacterial chromosomal attachment site (attB) for the staphylococcal cassette chromosome mec (SCCmec) element of a commensal mecC-positive Staphylococcus stepanovicii strain (IMT28705; ODD4) with respect to genetic composition and indications of HGT. ...[more]

PMID: 26799070

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Project description:Staphylococcus pseudintermedius is a major canine pathogen but also occasionally colonizes and infects humans. Multidrug-resistant methicillin-resistant S. pseudintermedius (MDR MRSP) strains have emerged globally, making treatment and control of this pathogen challenging. Sequence type 71 (ST71), ST68, and ST45 are the most widespread and successful MDR MRSP clones. The potential genetic factors underlying the clonal success of these and other predominant clones remain unknown. Characterization of the pangenome, lineage-associated accessory genes, and genes acquired through horizontal gene transfer from other bacteria is important for identifying such factors. Here, we analyzed genome sequence data from 622 S. pseudintermedius isolates to investigate the evolution of pathogenicity across lineages. We show that the predominant clones carry one or more lineage-associated virulence genes. The gene encoding staphylococcal protein A (SpA), a key virulence factor involved in immune evasion and a potential vaccine antigen, is deleted in 62% of isolates. Most importantly, we have discovered that the spa locus is a hot spot for recombination and horizontal gene transfer in S. pseudintermedius, where genes related to restriction modification, prophage immunity, mercury resistance, and nucleotide and carbohydrate metabolism have been acquired in different lineages. Our study also establishes that ST45 is composed of two distinct sublineages that differ in their accessory gene content and virulence potential. Collectively, this study reports several previously undetected lineage-associated genetic factors that may have a role in the clonal success of the major MDR MRSP clones. These data provide a framework for future experimental studies on S. pseudintermedius pathogenesis and for developing novel therapeutics against this pathogen.IMPORTANCEStaphylococcus pseudintermedius is a major canine pathogen but can also occasionally infect humans. Identification of genetic factors contributing to the virulence and clonal success of multidrug-resistant S. pseudintermedius clones is critical for the development of therapeutics against this pathogen. Here, we characterized the genome sequences of a global collection of 622 S. pseudintermedius isolates. We show that all major clones, besides carrying core virulence genes, which are present in all strains, carry one or more lineage-specific genes. Many of these genes have been acquired from other bacterial species through a horizontal gene transfer mechanism. Importantly, we have discovered that the staphylococcal protein A gene (spa), a widely used marker for molecular typing of S. pseudintermedius strains and a potential vaccine candidate antigen, is deleted in 62% of strains. Furthermore, the spa locus in S. pseudintermedius acts as a reservoir to accumulate lineage-associated genes with adaptive functions.

Dataset Information

A Look into the Melting Pot: The mecC-Harboring Region Is a Recombination Hot Spot in Staphylococcus stepanovicii.

Publications

A Look into the Melting Pot: The mecC-Harboring Region Is a Recombination Hot Spot in Staphylococcus stepanovicii.

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