Whole genome analysis of a livestock-associated methicillin-resistant Staphylococcus aureus ST398 isolate from a case of human endocarditis

Schijffelen, M.J.; Boel, C. H. E.; Strijp, Jos A. G. van; Fluit, Ad C.

doi:10.1186/1471-2164-11-376

Cited by 185 publications

(173 citation statements)

References 44 publications

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“…For livestock CC398 (sequenced by Schijffelen et al, 2010, andUhlemann et al, 2012), our study demonstrated that this clade has undergone a host transition from originally humans to animals, mainly pigs and calves (van Loo et al, 2007;Lewis et al, 2008). However, as the present study demonstrates, CC398 is also a pathogen of bovine IMI.…”

Section: Clonality Of Bovine Strains and Phylogeneticscontrasting

confidence: 40%

Bovine Staphylococcus aureus: Subtyping, evolution, and zoonotic transfer

Boss

Cosandey

Luini

et al. 2016

Journal of Dairy Science

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Staphylococcus aureus is globally one of the most important pathogens causing contagious mastitis in cattle. Previous studies using ribosomal spacer (RS)-PCR, however, demonstrated in Swiss cows that Staph. aureus isolated from bovine intramammary infections are genetically heterogeneous, with Staph. aureus genotype B (GTB) and GTC being the most prominent genotypes. Furthermore, Staph. aureus GTB was found to be contagious, whereas Staph. aureus GTC and all the remaining genotypes were involved in individual cow disease. In addition to RS-PCR, other methods for subtyping Staph. aureus are known, including spa typing and multilocus sequence typing (MLST). They are based on sequencing the spa and various housekeeping genes, respectively. The aim of the present study was to compare the 3 analytic methods using 456 strains of Staph. aureus isolated from milk of bovine intramammary infections and bulk tanks obtained from 12 European countries. Furthermore, the phylogeny of animal Staph. aureus was inferred and the zoonotic transfer of Staph. aureus between cattle and humans was studied. The analyzed strains could be grouped into 6 genotypic clusters, with CLB, CLC, and CLR being the most prominent ones. Comparing the 3 subtyping methods, RS-PCR showed the highest resolution, followed by spa typing and MLST. We found associations among the methods but in many cases they were unsatisfactory except for CLB and CLC. Cluster CLB was positive for clonal complex (CC)8 in 99% of the cases and typically positive for t2953; it is the cattle-adapted form of CC8. Cluster CLC was always positive for t529 and typically positive for CC705. For CLR and the remaining subtypes, links among the 3 methods were generally poor. Bovine Staph. aureus is highly clonal and a few clones predominate. Animal Staph. aureus always evolve from human strains, such that every human strain may be the ancestor of a novel animal-adapted strain. The zoonotic transfer of IMI-and milk-associated strains of Staph. aureus between cattle and humans seems to be very limited and different hosts are not considered as a source for mutual, spontaneous infections. Spillover events, however, may happen.

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Section: Clonality Of Bovine Strains and Phylogeneticscontrasting

confidence: 40%

Bovine Staphylococcus aureus: Subtyping, evolution, and zoonotic transfer

Boss

Cosandey

Luini

et al. 2016

Journal of Dairy Science

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“…However, phage endopeptidases, for example lysostaphin which is capable of degrading some human proteins, may affect mammalian tissues (Park et al, 1999). This possibility could be investigated with an animal model of endocarditis for example, as CC398 isolates have been associated with a human case of endocarditis in a highly immuno-compromised patient (Schijffelen et al, 2010). However, the two subgroups of isolates recovered from human invasive infections (those harboring StauST398-4pro and those harboring StauST398-4pro and StauST398-5pro) did not differ in their ability to invade human cells, suggesting that the StauST3985-pro prophage is not involved.…”

Section: Discussionmentioning

confidence: 99%

“…LA CC398 isolates commonly carry phages /2 and / 6 (Schijffelen et al, 2010;Hallin et al, 2011;McCarthy et al, 2011), or a /Avb prophage (Price et al, 2012). By contrast, isolates belonging to the human clade contain b-converting /3 prophage variants that encode two immune-modulating proteins (Goerke et al, 2006;McCarthy et al, 2011;Price et al, 2012;Uhleman et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Analysis of prophages harbored by the human-adapted subpopulation of Staphylococcus aureus CC398

Mee-Marquet

Corvaglia

Valentin

et al. 2013

Infection, Genetics and Evolution

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a b s t r a c tStaphylococcus aureus clonal complex 398 is a livestock-associated pathogen that poses a worldwide threat because of its ability to colonize and infect both humans and animals. We used high-resolution whole-genome microarrays, prophage profiling, immune evasion cluster characterization and wholegenome sequencing to investigate the roles of prophages in the emerging human-adapted subpopulation of CC398 that has been associated with invasive infections in humans living in animal-free environments.We characterized one phage and two prophages specifically harbored by CC398 isolates belonging to the emerging subpopulation. We introduced the phage into permissive prophage-free isolates. We investigated the effects of lysogeny on the host ability to resist further phage infection and transformation, to acquire the capacity to invade human cells, and to express virulence factors encoded by prophages. We report evidence of a defective /MR11-like helper prophage, named StauST398-5pro, specifically associated with the emerging non-LA CC398 subpopulation. StauST398-5pro confers substantial protection against horizontal genetic transfer to its host. It interacts with a human-associated b-converting prophage encoding immune-modulating proteins such that virulence genes are expressed during stress situations.Our findings provide insight into the role of phages in the expression of virulence and in the spread of genetic information among new host-adapted S. aureus isolates. We demonstrate that functional prophage elements can condition host specificity and confer new virulence traits on emerging intra-species clones of bacteria.

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“…Sequences within subfamilies shared 94 to 100% ANI, whereas sequences from different subfamilies shared 69 to 81% ANI. The S. aureus strains ED98 (25) and S0385 (26) each carried multiple subfamilies of ICE6013 (Fig. 5).…”

Section: Resultsmentioning

confidence: 99%

Transposase-Mediated Excision, Conjugative Transfer, and Diversity of ICE 6013 Elements in Staphylococcus aureus

et al. 2017

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ICE6013 represents one of two families of integrative conjugative elements (ICEs) identified in the pan-genome of the human and animal pathogen Staphylococcus aureus. Here we investigated the excision and conjugation functions of ICE6013 and further characterized the diversity of this element. ICE6013 excision was not significantly affected by growth, temperature, pH, or UV exposure and did not depend on recA. The IS30-like DDE transposase (Tpase; encoded by orf1 and orf2) of ICE6013 must be uninterrupted for excision to occur, whereas disrupting three of the other open reading frames (ORFs) on the element significantly affects the level of excision. We demonstrate that ICE6013 conjugatively transfers to different S. aureus backgrounds at frequencies approaching that of the conjugative plasmid pGO1. We found that excision is required for conjugation, that not all S. aureus backgrounds are successful recipients, and that transconjugants acquire the ability to transfer ICE6013. Sequencing of chromosomal integration sites in serially passaged transconjugants revealed a significant integration site preference for a 15-bp AT-rich palindromic consensus sequence, which surrounds the 3-bp target site that is duplicated upon integration. A sequence analysis of ICE6013 from different host strains of S. aureus and from eight other species of staphylococci identified seven divergent subfamilies of ICE6013 that include sequences previously classified as a transposon, a plasmid, and various ICEs. In summary, these results indicate that the IS30-like Tpase functions as the ICE6013 recombinase and that ICE6013 represents a diverse family of mobile genetic elements that mediate conjugation in staphylococci.IMPORTANCE Integrative conjugative elements (ICEs) encode the abilities to integrate into and excise from bacterial chromosomes and plasmids and mediate conjugation between bacteria. As agents of horizontal gene transfer, ICEs may affect bacterial evolution. ICE6013 represents one of two known families of ICEs in the pathogen Staphylococcus aureus, but its core functions of excision and conjugation are not well studied. Here, we show that ICE6013 depends on its IS30-like DDE transposase for excision, which is unique among ICEs, and we demonstrate the conjugative transfer and integration site preference of ICE6013. A sequence analysis revealed that ICE6013 has diverged into seven subfamilies that are dispersed among staphylococci.

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Whole genome analysis of a livestock-associated methicillin-resistant Staphylococcus aureus ST398 isolate from a case of human endocarditis

Cited by 185 publications

References 44 publications

Bovine Staphylococcus aureus: Subtyping, evolution, and zoonotic transfer

Bovine Staphylococcus aureus: Subtyping, evolution, and zoonotic transfer

Analysis of prophages harbored by the human-adapted subpopulation of Staphylococcus aureus CC398

Transposase-Mediated Excision, Conjugative Transfer, and Diversity of ICE 6013 Elements in Staphylococcus aureus

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