Genome Evolution of Invasive Methicillin-Resistant Staphylococcus aureus in the Americas
ABSTRACT Staphylococcus aureus causes a variety of debilitating and life-threatening diseases, and thus remains a challenging global health threat. S. aureus is remarkably diverse, yet only a minority of methicillin-resistant S. aureus (MRSA) clones have caused pandemic proportions of diseases. The...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-06-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.00201-22 |
| _version_ | 1818255480299978752 |
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| author | Joshua T. Smith Elissa M. Eckhardt Nicole B. Hansel Tahmineh Rahmani Eliato Isabella W. Martin Cheryl P. Andam |
| author_facet | Joshua T. Smith Elissa M. Eckhardt Nicole B. Hansel Tahmineh Rahmani Eliato Isabella W. Martin Cheryl P. Andam |
| author_sort | Joshua T. Smith |
| collection | DOAJ |
| description | ABSTRACT Staphylococcus aureus causes a variety of debilitating and life-threatening diseases, and thus remains a challenging global health threat. S. aureus is remarkably diverse, yet only a minority of methicillin-resistant S. aureus (MRSA) clones have caused pandemic proportions of diseases. The genetic drivers of the successful dissemination of some clones across wide geographical expanses remain poorly understood. We analyzed 386 recently published MRSA genomes from bloodstream infections sampled in North, Central, and South America from 2011 to 2018. Here, we show that MRSA-associated bloodstream infections were attributable to two genetically distinct lineages. One lineage consisted almost exclusively of sequence type (ST) 8, which emerged in 1964. A second lineage emerged in 1986 and consisted of STs 5, 105, and 231. The two lineages have simultaneously disseminated across geographically distant sites. Sublineages rapidly diverged within locations in the early 2000s. Their diversification was associated with independent acquisitions of unique variants of the mobile mecA-carrying chromosomal cassette and distinct repertoires of antimicrobial resistance genes. We show that the evolution and spread of invasive multidrug-resistant MRSA in the Americas was driven by transcontinental dissemination, followed by more recent establishment and divergence of local pathogen populations. Our study highlights the need for continued international surveillance of high-risk clones to control the global health threat of multidrug resistance. IMPORTANCE Bloodstream infections due to S. aureus cause significant patient morbidity and mortality worldwide, exacerbated by the emergence and spread of methicillin resistant S. aureus (MRSA). This study provides important insights on the evolution and long-distance geographic expansion of two distinct MRSA lineages that predominate in bloodstream infections in the past 5 decades. The success of these two lineages partly lies on their acquisition of a diverse set of antimicrobial resistance genes and of unique variants of the mobile genetic element SCCmec that carries the gene mecA conferring resistance to beta-lactams. High-risk antimicrobial resistant clones can therefore rapidly disseminate across long distances and establish within local communities within a short period of time. These results have important implications for global initiatives and local epidemiological efforts to monitor and control invasive MRSA infections and transcontinental spread of multidrug resistance. |
| first_indexed | 2024-12-12T17:12:32Z |
| format | Article |
| id | doaj.art-65264d8c4ca344e3ac1091b8bbed9590 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-12-12T17:12:32Z |
| publishDate | 2022-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-65264d8c4ca344e3ac1091b8bbed95902022-12-22T00:17:51ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-06-0110310.1128/spectrum.00201-22Genome Evolution of Invasive Methicillin-Resistant Staphylococcus aureus in the AmericasJoshua T. Smith0Elissa M. Eckhardt1Nicole B. Hansel2Tahmineh Rahmani Eliato3Isabella W. Martin4Cheryl P. Andam5Department of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, Durham, New Hampshire, USADartmouth-Hitchcock Medical Center and Dartmouth College Geisel School of Medicine, Lebanon, New Hampshire, USADartmouth-Hitchcock Medical Center and Dartmouth College Geisel School of Medicine, Lebanon, New Hampshire, USADepartment of Chemical Engineering, University of New Hampshire, Durham, New Hampshire, USADartmouth-Hitchcock Medical Center and Dartmouth College Geisel School of Medicine, Lebanon, New Hampshire, USADepartment of Biological Sciences, University at Albany, State University of New York, Albany, New York, USAABSTRACT Staphylococcus aureus causes a variety of debilitating and life-threatening diseases, and thus remains a challenging global health threat. S. aureus is remarkably diverse, yet only a minority of methicillin-resistant S. aureus (MRSA) clones have caused pandemic proportions of diseases. The genetic drivers of the successful dissemination of some clones across wide geographical expanses remain poorly understood. We analyzed 386 recently published MRSA genomes from bloodstream infections sampled in North, Central, and South America from 2011 to 2018. Here, we show that MRSA-associated bloodstream infections were attributable to two genetically distinct lineages. One lineage consisted almost exclusively of sequence type (ST) 8, which emerged in 1964. A second lineage emerged in 1986 and consisted of STs 5, 105, and 231. The two lineages have simultaneously disseminated across geographically distant sites. Sublineages rapidly diverged within locations in the early 2000s. Their diversification was associated with independent acquisitions of unique variants of the mobile mecA-carrying chromosomal cassette and distinct repertoires of antimicrobial resistance genes. We show that the evolution and spread of invasive multidrug-resistant MRSA in the Americas was driven by transcontinental dissemination, followed by more recent establishment and divergence of local pathogen populations. Our study highlights the need for continued international surveillance of high-risk clones to control the global health threat of multidrug resistance. IMPORTANCE Bloodstream infections due to S. aureus cause significant patient morbidity and mortality worldwide, exacerbated by the emergence and spread of methicillin resistant S. aureus (MRSA). This study provides important insights on the evolution and long-distance geographic expansion of two distinct MRSA lineages that predominate in bloodstream infections in the past 5 decades. The success of these two lineages partly lies on their acquisition of a diverse set of antimicrobial resistance genes and of unique variants of the mobile genetic element SCCmec that carries the gene mecA conferring resistance to beta-lactams. High-risk antimicrobial resistant clones can therefore rapidly disseminate across long distances and establish within local communities within a short period of time. These results have important implications for global initiatives and local epidemiological efforts to monitor and control invasive MRSA infections and transcontinental spread of multidrug resistance.https://journals.asm.org/doi/10.1128/spectrum.00201-22Staphylococcus aureusbloodstream infectioninvasivegenome evolutionmethicillin resistanceMRSA |
| spellingShingle | Joshua T. Smith Elissa M. Eckhardt Nicole B. Hansel Tahmineh Rahmani Eliato Isabella W. Martin Cheryl P. Andam Genome Evolution of Invasive Methicillin-Resistant Staphylococcus aureus in the Americas Microbiology Spectrum Staphylococcus aureus bloodstream infection invasive genome evolution methicillin resistance MRSA |
| title | Genome Evolution of Invasive Methicillin-Resistant Staphylococcus aureus in the Americas |
| title_full | Genome Evolution of Invasive Methicillin-Resistant Staphylococcus aureus in the Americas |
| title_fullStr | Genome Evolution of Invasive Methicillin-Resistant Staphylococcus aureus in the Americas |
| title_full_unstemmed | Genome Evolution of Invasive Methicillin-Resistant Staphylococcus aureus in the Americas |
| title_short | Genome Evolution of Invasive Methicillin-Resistant Staphylococcus aureus in the Americas |
| title_sort | genome evolution of invasive methicillin resistant staphylococcus aureus in the americas |
| topic | Staphylococcus aureus bloodstream infection invasive genome evolution methicillin resistance MRSA |
| url | https://journals.asm.org/doi/10.1128/spectrum.00201-22 |
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