Staphylococcus aureus CC398: Host Adaptation and Emergence of Methicillin Resistance in Livestock

Price, Lance B.; Stegger, Marc; Hasman, Henrik; Aziz, Maliha; Larsen, Jesper; Andersen, Paal Skytt; Pearson, Talima; Waters, Andrew E.; Foster, Jeffrey T.; Schupp, James; Gillece, John D.; Driebe, Elizabeth M.; Liu, Cindy M.; Springer, Burkhard; Zdovc, Irena; Battisti, Antonio; Franco, Alessia; Żmudzki, J.; Schwarz, Štefan; Butaye, Patrick; Jouy, Éric; Pomba, Constança; Porrero, M. Concepción; Ruimy, Raymond; Smith, Tara C.; Robinson, D. Ashley; Weese, J. Scott; Arriola, Carmen Sofia; Yu, Fei; Laurent, François; Keim, Paul; Skov, Robert; Aarestrup, Frank Møller

doi:10.1128/mbio.00520-12

Cited by 198 publications

(357 citation statements)

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“…An analysis of the MGEs of 22 representative isolates, including 35 prophages, provided insights into the ongoing evolution of this human-adapted subpopulation of ST398 isolates. As expected, the core genomes of representative BSI isolates from the 9-year-period cohort were highly similar, confirming that this ST398 subpopulation probably emerged recently [11]. However, with the exception of φ3-prophages, which are generally considered as a signature of human niche adaptation [37] and carried by most BSI isolates, the accessory gene pool differed considerably between these isolates.…”

Section: Discussionsupporting

confidence: 74%

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Messages from the first International Conference on Clinical Metagenomics (ICCMg)

Ruppé

Schrenzel²

2017

Microbes and Infection

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Background: It has been suggested that prophages in the ST398 S. aureus clone are responsible for expanding ST398's spectrum of action and increasing its ability to cause human infections. We carried out the first characterization of the various prophages carried by 76 ST398 bloodstream infection (BSI) isolates obtained over 9 years of observation. Results: Whole-genome sequencing of 22 representative isolates showed (1) the presence of the φ3-prophage and diverse genetic features typical of animal-associated isolates (i.e., SCCmec XI element, Tn916 transposon and non φ3-prophages) in a majority of BSI isolates, (2) one BSI isolate devoid of the φ3-prophage but otherwise similar to an animal-infecting isolate, (3) 35 prophages carrying numerous genes previously associated with virulence or immune evasion in animal models of staphylococcal infections. The analysis of prophage content in all 76 BSI isolates showed an increasing prevalence of polylysogeny over time. Overall, over the course of the last 10 years, the BSI isolates appear to have acquired increasing numbers of genetic features previously shown to contribute to bacterial adaptation and virulence in animal models of staphylococcal infections. Conclusions: We hypothesize that lysogeny has played a significant role in increasing the ability of the ST398 clone to cause infections in humans. Our findings highlight the risk that the ST398 lineage will increase its threat to public health by continuing to acquire virulence and/or multiple antibiotic-resistance genes from hospitalassociated clones of Staphylococcus aureus.

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Section: Discussionsupporting

confidence: 74%

“…Therefore, this "clonal" population differs drastically in terms of phenotypic features. Some studies have suggested a key role for prophages in the epidemiological changes currently taking place in this lineage [8,11,12]. However, the prophages carried by the human-adapted isolates remain poorly characterized.…”

Section: Introductionmentioning

confidence: 99%

Messages from the first International Conference on Clinical Metagenomics (ICCMg)

Ruppé

Schrenzel²

2017

Microbes and Infection

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“…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). These proteins are the staphylococcal complement inhibitor, SCIN, that prevents opsonophagocytosis and killing of S. aureus by human neutrophils; and the chemotaxis inhibitory protein of S. aureus, CHIPS.…”

Section: Introductionmentioning

confidence: 99%

“…Microarrays and whole-genome sequencing approaches applied to a large number of CC398 isolates distinguished two clades within the CC398 lineage (Price et al, 2012;Uhleman et al, 2012;McCarthy et al, 2011): the classical LA clade, isolates of which have long been responsible for frequent and transient colonization, and rare infections, of farmers and veterinarians (Huijsdens et al, 2006); and a human clade. This human clade is comprised of two subpopulations: the ancestral human subpopulation, and the emerging human-adapted non-LA CC398 subpopulation that has recently and increasingly been causing invasive infections worldwide in humans living in animal-free environments (Price et al, 2012;Valentin-Domelier et al, 2011;Jimenez et al, 2011;Stegger et al, 2010), and that readily colonize and spread between humans (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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“…[89][90][91] Bacteria hosted by animals can reach humans through direct contact, food and/or the environment. 92 Non-therapeutic use of antimicrobials in animals for growth promotion has been associated with high levels of AMR in the animal reservoir. This situation has occurred in many countries and is well-documented.…”

Section: Case Study 2: Antibiotic Prescription In China: Systemic Andmentioning

confidence: 99%

Exploring the evidence base for national and regional policy interventions to combat resistance

et al. 2016

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Staphylococcus aureus CC398: Host Adaptation and Emergence of Methicillin Resistance in Livestock

Cited by 198 publications

References 0 publications

Messages from the first International Conference on Clinical Metagenomics (ICCMg)

Messages from the first International Conference on Clinical Metagenomics (ICCMg)

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

Exploring the evidence base for national and regional policy interventions to combat resistance

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