Decoding the evolutionary history of ST30 Staphylococcus aureus: insights into a potentially silent MSSA bloodstream pathogen
BackgroundStaphylococcus aureus clonal complex 30 (CC30) is a historically significant pathogen affecting both hospital and community settings. The notable pandemic clones, phage-type 80/81 (PT80/81) and the Southwest Pacific clone (SWP) have spread internationally, contributing to significant morbi...
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Frontiers Media S.A.
2025-04-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2025.1522747/full |
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| author | Matheus Assis Côrtes Esteves Mariana Fernandes Carvalho Alice Slotfeldt Viana Caroline Lopes Martini Luis Guilherme Araújo Longo Luis Guilherme Araújo Longo Deborah Nascimento Santos Silva Adriana Lucia Pires Ferreira Bernadete Teixeira Ferreira-Carvalho Paul Joseph Planet Paul Joseph Planet Agnes Marie Sá Figueiredo Agnes Marie Sá Figueiredo |
| author_facet | Matheus Assis Côrtes Esteves Mariana Fernandes Carvalho Alice Slotfeldt Viana Caroline Lopes Martini Luis Guilherme Araújo Longo Luis Guilherme Araújo Longo Deborah Nascimento Santos Silva Adriana Lucia Pires Ferreira Bernadete Teixeira Ferreira-Carvalho Paul Joseph Planet Paul Joseph Planet Agnes Marie Sá Figueiredo Agnes Marie Sá Figueiredo |
| author_sort | Matheus Assis Côrtes Esteves |
| collection | DOAJ |
| description | BackgroundStaphylococcus aureus clonal complex 30 (CC30) is a historically significant pathogen affecting both hospital and community settings. The notable pandemic clones, phage-type 80/81 (PT80/81) and the Southwest Pacific clone (SWP) have spread internationally, contributing to significant morbidity and mortality. Despite their importance, research on the evolution of sequence type (ST) 30 has been limited, often focusing on a small number of strains or specific regions.MethodsIn this study, we analyzed over 500 ST30 genomes from diverse sources, including Brazilian strains sequenced by our team, using genomic, pangenomic, phylogenetic, and time-calibrated phylogenetic analyses.ResultsWe traced key evolutionary events, estimating that the specialization of PT80/81 and SWP occurred after a divergence around 1868, forming a group of PT80/81-related strains and another group formed by SWP-related strains. Our findings highlight major events involving gene acquisition and loss, as well as mobile genetic elements (MGE). Notably, PT80/81 lost most lpl genes during diversification, which may have restricted the circulation of related strains. Contemporary strains—defined as those that emerged in the 21st century—predominantly cluster within a group divided into three subgroups, including Brazilian strains that acquired a novel pathogenicity island. Also clustering within the contemporary group, most toxic shock syndrome toxin-1 (TSST-1)-producing strains are methicillin-susceptible S. aureus (MSSA) that have gained additional virulence traits, including sea, which enhance their adaptability and virulence.ConclusionOur study revises the evolutionary history of ST30 S. aureus uncovering critical pathoadaptive events that may explain its success. Additionally, our findings emphasize a neglected issue: the high prevalence of MSSA in hospital infections, particularly the silent circulation of TSST-1 producing strains, capable of causing severe infections. Robust surveillance studies to monitor these strains are crucial. |
| format | Article |
| id | doaj-art-7b4282dffbd94ff2b0a5e771b931cd55 |
| institution | DOAJ |
| issn | 1664-302X |
| language | English |
| publishDate | 2025-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj-art-7b4282dffbd94ff2b0a5e771b931cd552025-08-20T03:17:31ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-04-011610.3389/fmicb.2025.15227471522747Decoding the evolutionary history of ST30 Staphylococcus aureus: insights into a potentially silent MSSA bloodstream pathogenMatheus Assis Côrtes Esteves0Mariana Fernandes Carvalho1Alice Slotfeldt Viana2Caroline Lopes Martini3Luis Guilherme Araújo Longo4Luis Guilherme Araújo Longo5Deborah Nascimento Santos Silva6Adriana Lucia Pires Ferreira7Bernadete Teixeira Ferreira-Carvalho8Paul Joseph Planet9Paul Joseph Planet10Agnes Marie Sá Figueiredo11Agnes Marie Sá Figueiredo12Departamento de Microbiologia Médica, Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, BrazilDepartamento de Microbiologia Médica, Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, BrazilDepartamento de Microbiologia Médica, Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, BrazilDepartamento de Microbiologia Médica, Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, BrazilDepartamento de Microbiologia Médica, Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, BrazilFaculdade de Medicina, Instituto de Educação Médica (IDOMED), Universidade Estácio de Sá, Rio de Janeiro, RJ, BrazilDepartamento de Microbiologia Médica, Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, BrazilDiagnósticos da América S.A., Rio de Janeiro, RJ, BrazilDepartamento de Microbiologia Médica, Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, BrazilChildren’s Hospital of Philadelphia, Philadelphia, PA, United StatesPerelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United StatesDepartamento de Microbiologia Médica, Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, BrazilPrograma de Pós-Graduação em Patologia, Faculdade de Medicina, Universidade Federal Fluminense, Rio de Janeiro, RJ, BrazilBackgroundStaphylococcus aureus clonal complex 30 (CC30) is a historically significant pathogen affecting both hospital and community settings. The notable pandemic clones, phage-type 80/81 (PT80/81) and the Southwest Pacific clone (SWP) have spread internationally, contributing to significant morbidity and mortality. Despite their importance, research on the evolution of sequence type (ST) 30 has been limited, often focusing on a small number of strains or specific regions.MethodsIn this study, we analyzed over 500 ST30 genomes from diverse sources, including Brazilian strains sequenced by our team, using genomic, pangenomic, phylogenetic, and time-calibrated phylogenetic analyses.ResultsWe traced key evolutionary events, estimating that the specialization of PT80/81 and SWP occurred after a divergence around 1868, forming a group of PT80/81-related strains and another group formed by SWP-related strains. Our findings highlight major events involving gene acquisition and loss, as well as mobile genetic elements (MGE). Notably, PT80/81 lost most lpl genes during diversification, which may have restricted the circulation of related strains. Contemporary strains—defined as those that emerged in the 21st century—predominantly cluster within a group divided into three subgroups, including Brazilian strains that acquired a novel pathogenicity island. Also clustering within the contemporary group, most toxic shock syndrome toxin-1 (TSST-1)-producing strains are methicillin-susceptible S. aureus (MSSA) that have gained additional virulence traits, including sea, which enhance their adaptability and virulence.ConclusionOur study revises the evolutionary history of ST30 S. aureus uncovering critical pathoadaptive events that may explain its success. Additionally, our findings emphasize a neglected issue: the high prevalence of MSSA in hospital infections, particularly the silent circulation of TSST-1 producing strains, capable of causing severe infections. Robust surveillance studies to monitor these strains are crucial.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1522747/fullMRSAStaphylococcus aureus evolutionphage-type 80/81Southwest Pacific clonetoxic-shock syndrome toxin |
| spellingShingle | Matheus Assis Côrtes Esteves Mariana Fernandes Carvalho Alice Slotfeldt Viana Caroline Lopes Martini Luis Guilherme Araújo Longo Luis Guilherme Araújo Longo Deborah Nascimento Santos Silva Adriana Lucia Pires Ferreira Bernadete Teixeira Ferreira-Carvalho Paul Joseph Planet Paul Joseph Planet Agnes Marie Sá Figueiredo Agnes Marie Sá Figueiredo Decoding the evolutionary history of ST30 Staphylococcus aureus: insights into a potentially silent MSSA bloodstream pathogen Frontiers in Microbiology MRSA Staphylococcus aureus evolution phage-type 80/81 Southwest Pacific clone toxic-shock syndrome toxin |
| title | Decoding the evolutionary history of ST30 Staphylococcus aureus: insights into a potentially silent MSSA bloodstream pathogen |
| title_full | Decoding the evolutionary history of ST30 Staphylococcus aureus: insights into a potentially silent MSSA bloodstream pathogen |
| title_fullStr | Decoding the evolutionary history of ST30 Staphylococcus aureus: insights into a potentially silent MSSA bloodstream pathogen |
| title_full_unstemmed | Decoding the evolutionary history of ST30 Staphylococcus aureus: insights into a potentially silent MSSA bloodstream pathogen |
| title_short | Decoding the evolutionary history of ST30 Staphylococcus aureus: insights into a potentially silent MSSA bloodstream pathogen |
| title_sort | decoding the evolutionary history of st30 staphylococcus aureus insights into a potentially silent mssa bloodstream pathogen |
| topic | MRSA Staphylococcus aureus evolution phage-type 80/81 Southwest Pacific clone toxic-shock syndrome toxin |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2025.1522747/full |
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