Comparative analysis of genomic characteristics, virulence and fitness of community-associated Staphylococcus aureus ST121 clone causing fatal diseases in China and other CA-MRSA clones

The increasing rate of community-associated Staphylococcus aureus (CA-SA) worldwide has aroused global public concern for decades. Although ST121 clone is one of the prevalent CA-SA in China, there is still limited knowledge about it. In this study, we conducted a genomic analysis of 28 CA-SA ST121...

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Main Authors: Wangxiao Zhou, Ye Jin, Gaoqin Teng, Weiwei Chen, Yunbo Chen, Qixia Luo, Yonghong Xiao
Format: Article
Language:English
Published: Taylor & Francis Group 2023-12-01
Series:Virulence
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Online Access:https://www.tandfonline.com/doi/10.1080/21505594.2023.2242547
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author Wangxiao Zhou
Ye Jin
Gaoqin Teng
Weiwei Chen
Yunbo Chen
Qixia Luo
Yonghong Xiao
author_facet Wangxiao Zhou
Ye Jin
Gaoqin Teng
Weiwei Chen
Yunbo Chen
Qixia Luo
Yonghong Xiao
author_sort Wangxiao Zhou
collection DOAJ
description The increasing rate of community-associated Staphylococcus aureus (CA-SA) worldwide has aroused global public concern for decades. Although ST121 clone is one of the prevalent CA-SA in China, there is still limited knowledge about it. In this study, we conducted a genomic analysis of 28 CA-SA ST121 isolates from severe bloodstream infection cases and 175 ST121 isolates from the public database. Phylogenetic analysis revealed the consistency and the complexity of global ST121 lineages, and suggested potential cross-country even cross-continental transmission of ST121 isolates. By investigating the virulence and fitness between ST121-CA-methicillin-resistant SA (CA-MRSA) and other CA-MRSA clones, we found that ST121-MRSA exhibits virulence comparable to the highly virulent USA300 clone, exceeding that of the predominant CA-MRSA lineage ST59 in China and the other American CA-MRSA clone MW2. Notably, based on analyses of virulence genes, eta, etb, edin-C and egc were only found in ST121, suggesting that the high virulence of ST121 may be attributed to the combination of these virulence factors encoded by mobile genetic elements. However, results of experiments in mice nasal and human alveolar epithelial cells showed that the colonization capacity of ST121 is much lower than that of other clones. Moreover, ST121-MRSA displayed much lower acid tolerance, suggesting that ST121-MRSA may not have such capacity to achieve the epidemiological success of other CA-MRSA clones and become the dominant lineage. Our findings expand current understanding of the epidemiology and pathogenicity of the hypervirulent ST121 clone, and highlight the importance of colonization capacity and environmental adaption in MRSA epidemiological success.
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spelling doaj-art-1896dcd45ca647858d29119fc62bf6232025-08-20T03:15:54ZengTaylor & Francis GroupVirulence2150-55942150-56082023-12-0114110.1080/21505594.2023.2242547Comparative analysis of genomic characteristics, virulence and fitness of community-associated Staphylococcus aureus ST121 clone causing fatal diseases in China and other CA-MRSA clonesWangxiao Zhou0Ye Jin1Gaoqin Teng2Weiwei Chen3Yunbo Chen4Qixia Luo5Yonghong Xiao6State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, National Clinical Research Center for Infectious Diseases, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, the First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, People’s Republic of ChinaState Key Laboratory for Diagnosis and Treatment of Infectious Diseases, National Clinical Research Center for Infectious Diseases, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, the First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, People’s Republic of ChinaDepartment of General Intensive Care Unit, The Second Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, Zhejiang, People’s Republic of ChinaDepartment of Laboratory Medicine, the First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, People’s Republic of ChinaState Key Laboratory for Diagnosis and Treatment of Infectious Diseases, National Clinical Research Center for Infectious Diseases, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, the First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, People’s Republic of ChinaState Key Laboratory for Diagnosis and Treatment of Infectious Diseases, National Clinical Research Center for Infectious Diseases, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, the First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, People’s Republic of ChinaState Key Laboratory for Diagnosis and Treatment of Infectious Diseases, National Clinical Research Center for Infectious Diseases, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, the First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, People’s Republic of ChinaThe increasing rate of community-associated Staphylococcus aureus (CA-SA) worldwide has aroused global public concern for decades. Although ST121 clone is one of the prevalent CA-SA in China, there is still limited knowledge about it. In this study, we conducted a genomic analysis of 28 CA-SA ST121 isolates from severe bloodstream infection cases and 175 ST121 isolates from the public database. Phylogenetic analysis revealed the consistency and the complexity of global ST121 lineages, and suggested potential cross-country even cross-continental transmission of ST121 isolates. By investigating the virulence and fitness between ST121-CA-methicillin-resistant SA (CA-MRSA) and other CA-MRSA clones, we found that ST121-MRSA exhibits virulence comparable to the highly virulent USA300 clone, exceeding that of the predominant CA-MRSA lineage ST59 in China and the other American CA-MRSA clone MW2. Notably, based on analyses of virulence genes, eta, etb, edin-C and egc were only found in ST121, suggesting that the high virulence of ST121 may be attributed to the combination of these virulence factors encoded by mobile genetic elements. However, results of experiments in mice nasal and human alveolar epithelial cells showed that the colonization capacity of ST121 is much lower than that of other clones. Moreover, ST121-MRSA displayed much lower acid tolerance, suggesting that ST121-MRSA may not have such capacity to achieve the epidemiological success of other CA-MRSA clones and become the dominant lineage. Our findings expand current understanding of the epidemiology and pathogenicity of the hypervirulent ST121 clone, and highlight the importance of colonization capacity and environmental adaption in MRSA epidemiological success.https://www.tandfonline.com/doi/10.1080/21505594.2023.2242547ST121community-associated infectionsgenomic analysishigh virulenceepidemiological success
spellingShingle Wangxiao Zhou
Ye Jin
Gaoqin Teng
Weiwei Chen
Yunbo Chen
Qixia Luo
Yonghong Xiao
Comparative analysis of genomic characteristics, virulence and fitness of community-associated Staphylococcus aureus ST121 clone causing fatal diseases in China and other CA-MRSA clones
Virulence
ST121
community-associated infections
genomic analysis
high virulence
epidemiological success
title Comparative analysis of genomic characteristics, virulence and fitness of community-associated Staphylococcus aureus ST121 clone causing fatal diseases in China and other CA-MRSA clones
title_full Comparative analysis of genomic characteristics, virulence and fitness of community-associated Staphylococcus aureus ST121 clone causing fatal diseases in China and other CA-MRSA clones
title_fullStr Comparative analysis of genomic characteristics, virulence and fitness of community-associated Staphylococcus aureus ST121 clone causing fatal diseases in China and other CA-MRSA clones
title_full_unstemmed Comparative analysis of genomic characteristics, virulence and fitness of community-associated Staphylococcus aureus ST121 clone causing fatal diseases in China and other CA-MRSA clones
title_short Comparative analysis of genomic characteristics, virulence and fitness of community-associated Staphylococcus aureus ST121 clone causing fatal diseases in China and other CA-MRSA clones
title_sort comparative analysis of genomic characteristics virulence and fitness of community associated staphylococcus aureus st121 clone causing fatal diseases in china and other ca mrsa clones
topic ST121
community-associated infections
genomic analysis
high virulence
epidemiological success
url https://www.tandfonline.com/doi/10.1080/21505594.2023.2242547
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