Evolution of the <italic toggle="yes">Staphylococcus argenteus</italic> ST2250 Clone in Northeastern Thailand Is Linked with the Acquisition of Livestock-Associated Staphylococcal Genes
ABSTRACT Staphylococcus argenteus is a newly named species previously described as a divergent lineage of Staphylococcus aureus that has recently been shown to have a global distribution. Despite growing evidence of the clinical importance of this species, knowledge about its population epidemiology...
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| Format: | Article |
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American Society for Microbiology
2017-09-01
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| Series: | mBio |
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| Online Access: | https://journals.asm.org/doi/10.1128/mBio.00802-17 |
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| author | Danesh Moradigaravand Dorota Jamrozy Rafal Mostowy Annaliesa Anderson Emma K. Nickerson Janjira Thaipadungpanit Vanaporn Wuthiekanun Direk Limmathurotsakul Sarunporn Tandhavanant Chanthiwa Wikraiphat Gumphol Wongsuvan Nittaya Teerawattanasook Yaowaruk Jutrakul Nuttiya Srisurat Prajuab Chaimanee T. Eoin West Beth Blane Julian Parkhill Narisara Chantratita Sharon J. Peacock |
| author_facet | Danesh Moradigaravand Dorota Jamrozy Rafal Mostowy Annaliesa Anderson Emma K. Nickerson Janjira Thaipadungpanit Vanaporn Wuthiekanun Direk Limmathurotsakul Sarunporn Tandhavanant Chanthiwa Wikraiphat Gumphol Wongsuvan Nittaya Teerawattanasook Yaowaruk Jutrakul Nuttiya Srisurat Prajuab Chaimanee T. Eoin West Beth Blane Julian Parkhill Narisara Chantratita Sharon J. Peacock |
| author_sort | Danesh Moradigaravand |
| collection | DOAJ |
| description | ABSTRACT Staphylococcus argenteus is a newly named species previously described as a divergent lineage of Staphylococcus aureus that has recently been shown to have a global distribution. Despite growing evidence of the clinical importance of this species, knowledge about its population epidemiology and genomic architecture is limited. We used whole-genome sequencing to evaluate and compare S. aureus (n = 251) and S. argenteus (n = 68) isolates from adults with staphylococcal sepsis at several hospitals in northeastern Thailand between 2006 and 2013. The majority (82%) of the S. argenteus isolates were of multilocus sequence type 2250 (ST2250). S. aureus was more diverse, although 43% of the isolates belonged to ST121. Bayesian analysis suggested an S. argenteus ST2250 substitution rate of 4.66 (95% confidence interval [CI], 3.12 to 6.38) mutations per genome per year, which was comparable to the S. aureus ST121 substitution rate of 4.07 (95% CI, 2.61 to 5.55). S. argenteus ST2250 emerged in Thailand an estimated 15 years ago, which contrasts with the S. aureus ST1, ST88, and ST121 clades that emerged around 100 to 150 years ago. Comparison of S. argenteus ST2250 genomes from Thailand and a global collection indicated a single introduction into Thailand, followed by transmission to local and more distant countries in Southeast Asia and further afield. S. argenteus and S. aureus shared around half of their core gene repertoire, indicating a high level of divergence and providing strong support for their classification as separate species. Several gene clusters were present in ST2250 isolates but absent from the other S. argenteus and S. aureus study isolates. These included multiple exotoxins and antibiotic resistance genes that have been linked previously with livestock-associated S. aureus, consistent with a livestock reservoir for S. argenteus. These genes appeared to be associated with plasmids and mobile genetic elements and may have contributed to the biological success of ST2250. IMPORTANCE In this study, we used whole-genome sequencing to understand the genome evolution and population structure of a systematic collection of ST2250 S. argenteus isolates. A newly identified ancestral species of S. aureus, S. argenteus has become increasingly known as a clinically important species that has been reported recently across various countries. Our results indicate that S. argenteus has spread at a relatively rapid pace over the past 2 decades across northeastern Thailand and acquired multiple exotoxin and antibiotic resistance genes that have been linked previously with livestock-associated S. aureus. Our findings highlight the clinical importance and potential pathogenicity of S. argenteus as a recently emerging pathogen. |
| first_indexed | 2024-12-19T05:03:01Z |
| format | Article |
| id | doaj.art-917b84b41de2475b894f37ecfb1959a3 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-19T05:03:01Z |
| publishDate | 2017-09-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-917b84b41de2475b894f37ecfb1959a32022-12-21T20:35:02ZengAmerican Society for MicrobiologymBio2150-75112017-09-018410.1128/mBio.00802-17Evolution of the <italic toggle="yes">Staphylococcus argenteus</italic> ST2250 Clone in Northeastern Thailand Is Linked with the Acquisition of Livestock-Associated Staphylococcal GenesDanesh Moradigaravand0Dorota Jamrozy1Rafal Mostowy2Annaliesa Anderson3Emma K. Nickerson4Janjira Thaipadungpanit5Vanaporn Wuthiekanun6Direk Limmathurotsakul7Sarunporn Tandhavanant8Chanthiwa Wikraiphat9Gumphol Wongsuvan10Nittaya Teerawattanasook11Yaowaruk Jutrakul12Nuttiya Srisurat13Prajuab Chaimanee14T. Eoin West15Beth Blane16Julian Parkhill17Narisara Chantratita18Sharon J. Peacock19Wellcome Trust Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridgeshire, United KingdomWellcome Trust Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridgeshire, United KingdomDepartment of Infectious Disease Epidemiology, School of Public Health, Imperial College London, London, United KingdomPfizer Vaccine Research and Development, Pearl River, New York, USACambridge University Hospitals NHS Foundation Trust, Cambridge, United KingdomMahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, ThailandMahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, ThailandMahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, ThailandDepartment of Microbiology and Immunology, Faculty of Tropical Medicine, Mahidol University, Bangkok, ThailandDepartment of Microbiology and Immunology, Faculty of Tropical Medicine, Mahidol University, Bangkok, ThailandMahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, ThailandDepartment of Clinical Pathology, Sunpasitthiprasong Hospital, Ubon Ratchathani, ThailandDepartment of Clinical Pathology, Udon Thani Regional Hospital, Udon Thani, ThailandDepartment of Clinical Pathology, Khon Kaen Regional Hospital, Khon Kaen, ThailandSrinagarind Hospital, Faculty of Medicine, Khon Kaen University, Khon Kaen, ThailandDivision of Pulmonary and Critical Care Medicine, Department of Medicine, University of Washington, Seattle, Washington, USADepartment of Medicine, University of Cambridge, Cambridge, United KingdomWellcome Trust Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridgeshire, United KingdomDepartment of Microbiology and Immunology, Faculty of Tropical Medicine, Mahidol University, Bangkok, ThailandWellcome Trust Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridgeshire, United KingdomABSTRACT Staphylococcus argenteus is a newly named species previously described as a divergent lineage of Staphylococcus aureus that has recently been shown to have a global distribution. Despite growing evidence of the clinical importance of this species, knowledge about its population epidemiology and genomic architecture is limited. We used whole-genome sequencing to evaluate and compare S. aureus (n = 251) and S. argenteus (n = 68) isolates from adults with staphylococcal sepsis at several hospitals in northeastern Thailand between 2006 and 2013. The majority (82%) of the S. argenteus isolates were of multilocus sequence type 2250 (ST2250). S. aureus was more diverse, although 43% of the isolates belonged to ST121. Bayesian analysis suggested an S. argenteus ST2250 substitution rate of 4.66 (95% confidence interval [CI], 3.12 to 6.38) mutations per genome per year, which was comparable to the S. aureus ST121 substitution rate of 4.07 (95% CI, 2.61 to 5.55). S. argenteus ST2250 emerged in Thailand an estimated 15 years ago, which contrasts with the S. aureus ST1, ST88, and ST121 clades that emerged around 100 to 150 years ago. Comparison of S. argenteus ST2250 genomes from Thailand and a global collection indicated a single introduction into Thailand, followed by transmission to local and more distant countries in Southeast Asia and further afield. S. argenteus and S. aureus shared around half of their core gene repertoire, indicating a high level of divergence and providing strong support for their classification as separate species. Several gene clusters were present in ST2250 isolates but absent from the other S. argenteus and S. aureus study isolates. These included multiple exotoxins and antibiotic resistance genes that have been linked previously with livestock-associated S. aureus, consistent with a livestock reservoir for S. argenteus. These genes appeared to be associated with plasmids and mobile genetic elements and may have contributed to the biological success of ST2250. IMPORTANCE In this study, we used whole-genome sequencing to understand the genome evolution and population structure of a systematic collection of ST2250 S. argenteus isolates. A newly identified ancestral species of S. aureus, S. argenteus has become increasingly known as a clinically important species that has been reported recently across various countries. Our results indicate that S. argenteus has spread at a relatively rapid pace over the past 2 decades across northeastern Thailand and acquired multiple exotoxin and antibiotic resistance genes that have been linked previously with livestock-associated S. aureus. Our findings highlight the clinical importance and potential pathogenicity of S. argenteus as a recently emerging pathogen.https://journals.asm.org/doi/10.1128/mBio.00802-17genomic epidemiologyStaphylococcus argenteusStaphylococcus aureusantibiotic resistance |
| spellingShingle | Danesh Moradigaravand Dorota Jamrozy Rafal Mostowy Annaliesa Anderson Emma K. Nickerson Janjira Thaipadungpanit Vanaporn Wuthiekanun Direk Limmathurotsakul Sarunporn Tandhavanant Chanthiwa Wikraiphat Gumphol Wongsuvan Nittaya Teerawattanasook Yaowaruk Jutrakul Nuttiya Srisurat Prajuab Chaimanee T. Eoin West Beth Blane Julian Parkhill Narisara Chantratita Sharon J. Peacock Evolution of the <italic toggle="yes">Staphylococcus argenteus</italic> ST2250 Clone in Northeastern Thailand Is Linked with the Acquisition of Livestock-Associated Staphylococcal Genes mBio genomic epidemiology Staphylococcus argenteus Staphylococcus aureus antibiotic resistance |
| title | Evolution of the <italic toggle="yes">Staphylococcus argenteus</italic> ST2250 Clone in Northeastern Thailand Is Linked with the Acquisition of Livestock-Associated Staphylococcal Genes |
| title_full | Evolution of the <italic toggle="yes">Staphylococcus argenteus</italic> ST2250 Clone in Northeastern Thailand Is Linked with the Acquisition of Livestock-Associated Staphylococcal Genes |
| title_fullStr | Evolution of the <italic toggle="yes">Staphylococcus argenteus</italic> ST2250 Clone in Northeastern Thailand Is Linked with the Acquisition of Livestock-Associated Staphylococcal Genes |
| title_full_unstemmed | Evolution of the <italic toggle="yes">Staphylococcus argenteus</italic> ST2250 Clone in Northeastern Thailand Is Linked with the Acquisition of Livestock-Associated Staphylococcal Genes |
| title_short | Evolution of the <italic toggle="yes">Staphylococcus argenteus</italic> ST2250 Clone in Northeastern Thailand Is Linked with the Acquisition of Livestock-Associated Staphylococcal Genes |
| title_sort | evolution of the italic toggle yes staphylococcus argenteus italic st2250 clone in northeastern thailand is linked with the acquisition of livestock associated staphylococcal genes |
| topic | genomic epidemiology Staphylococcus argenteus Staphylococcus aureus antibiotic resistance |
| url | https://journals.asm.org/doi/10.1128/mBio.00802-17 |
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