Large mobile genetic elements carrying resistance genes that do not confer a fitness burden in healthcare-associated meticillin-resistant Staphylococcus aureus

Knight, Gwenan M.; Budd, Emma; Lindsay, Jodi A.

doi:10.1099/mic.0.068551-0

Cited by 22 publications

(20 citation statements)

References 61 publications

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“…We have also reported high levels of MGE and antibiotic resistance variation in hospital MRSA clones suggesting frequent movement into and out of isolates, possibly because resistances may have both a selective advantage and a fitness cost on the host bacterium in differing conditions (Knight et al 2012, 2013; Zhou et al 2013; Knoppel et al 2014). Taken together, this data suggest that MGE transfer and loss is common and the high level detected in vivo suggests that sampling studies may be underestimating the variety of mobilomes in populations.…”

Section: Discussionmentioning

confidence: 77%

Extensive Horizontal Gene Transfer during Staphylococcus aureus Co-colonization In Vivo

McCarthy

Loeffler

Witney

et al. 2014

Genome Biology and Evolution

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128

112

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Staphylococcus aureus is a commensal and major pathogen of humans and animals. Comparative genomics of S. aureus populations suggests that colonization of different host species is associated with carriage of mobile genetic elements (MGE), particularly bacteriophages and plasmids capable of encoding virulence, resistance, and immune evasion pathways. Antimicrobial-resistant S. aureus of livestock are a potential zoonotic threat to human health if they adapt to colonize humans efficiently. We utilized the technique of experimental evolution and co-colonized gnotobiotic piglets with both human- and pig-associated variants of the lineage clonal complex 398, and investigated growth and genetic changes over 16 days using whole genome sequencing. The human isolate survived co-colonization on piglets more efficiently than in vitro. During co-colonization, transfer of MGE from the pig to the human isolate was detected within 4 h. Extensive and repeated transfer of two bacteriophages and three plasmids resulted in colonization with isolates carrying a wide variety of mobilomes. Whole genome sequencing of progeny bacteria revealed no acquisition of core genome polymorphisms, highlighting the importance of MGE. Staphylococcus aureus bacteriophage recombination and integration into novel sites was detected experimentally for the first time. During colonization, clones coexisted and diversified rather than a single variant dominating. Unexpectedly, each piglet carried unique populations of bacterial variants, suggesting limited transmission of bacteria between piglets once colonized. Our data show that horizontal gene transfer occurs at very high frequency in vivo and significantly higher than that detectable in vitro.

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Section: Discussionmentioning

confidence: 77%

Extensive Horizontal Gene Transfer during Staphylococcus aureus Co-colonization In Vivo

McCarthy

Loeffler

Witney

et al. 2014

Genome Biology and Evolution

Self Cite

128

112

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“…Isolates belonging to CC8/ST8-t190-IID/IIE Ϯ SCC M1 predominated. Previous studies have demonstrated a reduced fitness associated with larger SCCmec elements (49,50), and we previously speculated that the potential fitness cost associated with carrying a large SCCmec-SCC composite island (CI) may have contributed to the decline of ST8-MRSA-IIA-IIE and SCC M1 (21) in Irish hospitals. However, the many resistance genes detected among isolates of this clone may also have contributed to its decline due to reduced fitness, but other lineage-specific factors may also have contributed (51).…”

Section: Discussionmentioning

confidence: 99%

Extensive Genetic Diversity Identified among Sporadic Methicillin-Resistant Staphylococcus aureus Isolates Recovered in Irish Hospitals between 2000 and 2012

Kinnevey

Shore

Brennan

et al. 2014

Antimicrob Agents Chemother

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e Clonal replacement of predominant nosocomial methicillin-resistant Staphylococcus aureus (MRSA) strains has occurred several times in Ireland during the last 4 decades. However, little is known about sporadically occurring MRSA in Irish hospitals or in other countries. Eighty-eight representative pvl-negative sporadic MRSA isolates recovered in Irish hospitals between 2000 and 2012 were investigated. These yielded unusual pulsed-field gel electrophoresis and antibiogram-resistogram typing patterns distinct from those of the predominant nosocomial MRSA clone, ST22-MRSA-IV, during the study period. Isolates were characterized by spa typing and DNA microarray profiling for multilocus sequence type (MLST) clonal complex (CC) and/or sequence type (ST) and SCCmec type assignment, as well as for detection of virulence and antimicrobial resistance genes. Conventional PCR-based SCCmec subtyping was undertaken when necessary. Extensive diversity was detected, including 38 spa types, 13 MLST-CCs (including 18 STs among 62 isolates assigned to STs), and 25 SCCmec types (including 2 possible novel SCCmec elements and 7 possible novel SCCmec subtypes). Fifty-four MLST-spa-SCCmec type combinations were identified. Overall, 68.5% of isolates were assigned to nosocomial lineages, with ST8-t190-MRSA-IID/IIE ؎ SCC M1 predominating (17.4%), followed by CC779/ST779-t878-MRSA-SCCmec-SCC-SCC CRISPR (7.6%) and CC22/ST22-t032-MRSA-IVh (5.4%). Community-associated clones, including CC1-t127/t386/t2279-MRSA-IV, CC59-t216-MRSA-V, CC8-t008-MRSA-IVa, and CC5-t002/t242-MRSA-IV/V, and putative animal-associated clones, including CC130-t12399-MRSA-XI, ST8-t064-MRSA-IVa, ST398-t011-MRSA-IVa, and CC6-t701-MRSA-V, were also identified. In total, 53.3% and 47.8% of isolates harbored genes for resistance to two or more classes of antimicrobial agents and two or more mobile genetic element-encoded virulence-associated factors, respectively. Effective ongoing surveillance of sporadic nosocomial MRSA is warranted for early detection of emerging clones and reservoirs of virulence, resistance, and SCCmec genes.

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“…A c c e p t e d M a n u s c r i p t 12 documented in Portugal, Singapore and Australia [25][26][27]. One feature that may contribute to its success is the SCCmec IV element that this clone carries, which has a lower fitness cost than the larger SCCmec elements such as SCCmec types II and III that were prevalent in earlier HA-MRSA clones [28]. In addition, some variants of CC22 HA-MRSA have acquired the PVL-associated genes, causing outbreaks among neonates in Australia [29] and the UK [30].…”

Section: Hospital-associated Meticillin-resistantmentioning

confidence: 99%

Genomic insights into the emergence and spread of international clones of healthcare-, community- and livestock-associated meticillin-resistant Staphylococcus aureus : Blurring of the traditional definitions

Bal

Coombs

Holden

et al. 2016

Journal of Global Antimicrobial Resistance

123

105

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Please cite this article as: Bal AM, Coombs GW, Holden MTG, Lindsay JA, Nimmo GR, Tattevin P, Skov RL, Genomic insights into the emergence and spread of international clones of healthcare-, community-and livestock-associated meticillinresistant Staphylococcus aureus: blurring of the traditional definitions, Journal of Global Antimicrobial Resistance (2010), http://dx.doi.org/10.1016/j.jgar. 2016.04.004 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.  Genomics-based diagnostic tools such as whole-genome sequencing are useful in providing rapid information in relation to epidemiology and outbreaks.

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Large mobile genetic elements carrying resistance genes that do not confer a fitness burden in healthcare-associated meticillin-resistant Staphylococcus aureus

Cited by 22 publications

References 61 publications

Extensive Horizontal Gene Transfer during Staphylococcus aureus Co-colonization In Vivo

Extensive Horizontal Gene Transfer during Staphylococcus aureus Co-colonization In Vivo

Extensive Genetic Diversity Identified among Sporadic Methicillin-Resistant Staphylococcus aureus Isolates Recovered in Irish Hospitals between 2000 and 2012

Genomic insights into the emergence and spread of international clones of healthcare-, community- and livestock-associated meticillin-resistant Staphylococcus aureus : Blurring of the traditional definitions

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