Genomic evolution and virulence association of Clostridioides difficile sequence type 37 (ribotype 017) in China

Clostridioides difficile sequence type (ST) 37 (ribotype 017) is one of the most prevalent genotypes circulating in China. However, its genomic evolution and virulence determinants were rarely explored. Whole-genome sequencing, phylogeographic and phylogenetic analyses were conducted for C. difficil...

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Main Authors: Xingxing Xu, Yuo Luo, Huan Chen, Xiaojun Song, Qiao Bian, Xianjun Wang, Qian Liang, Jianhong Zhao, Chunhui Li, Guangzhong Song, Jun Yang, Lingli Sun, Jianmin Jiang, Huanying Wang, Bo Zhu, Guangyong Ye, Liang Chen, Yi-Wei Tang, Dazhi Jin
Format: Article
Language:English
Published: Taylor & Francis Group 2021-01-01
Series:Emerging Microbes and Infections
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Online Access:https://www.tandfonline.com/doi/10.1080/22221751.2021.1943538
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author Xingxing Xu
Yuo Luo
Huan Chen
Xiaojun Song
Qiao Bian
Xianjun Wang
Qian Liang
Jianhong Zhao
Chunhui Li
Guangzhong Song
Jun Yang
Lingli Sun
Jianmin Jiang
Huanying Wang
Bo Zhu
Guangyong Ye
Liang Chen
Yi-Wei Tang
Dazhi Jin
author_facet Xingxing Xu
Yuo Luo
Huan Chen
Xiaojun Song
Qiao Bian
Xianjun Wang
Qian Liang
Jianhong Zhao
Chunhui Li
Guangzhong Song
Jun Yang
Lingli Sun
Jianmin Jiang
Huanying Wang
Bo Zhu
Guangyong Ye
Liang Chen
Yi-Wei Tang
Dazhi Jin
author_sort Xingxing Xu
collection DOAJ
description Clostridioides difficile sequence type (ST) 37 (ribotype 017) is one of the most prevalent genotypes circulating in China. However, its genomic evolution and virulence determinants were rarely explored. Whole-genome sequencing, phylogeographic and phylogenetic analyses were conducted for C. difficile ST37 isolates. The 325 ST37 genomes from six continents, including North America (n = 66), South America (n = 4), Oceania (n = 7), Africa (n = 9), Europe (n = 138) and Asia (n = 101), were clustered into six major lineages, with region-dependent distributions, harbouring an array of antibiotic-resistance genes. The ST37 strains from China were divided into four distinct sublineages, showing five importation times and international sources. Isolates associated with severe infections exhibited significantly higher toxin productions, tcdB mRNA levels, and sporulation capacities (P < 0.001). Kyoto Encyclopedia of Genes and Genomes analysis showed 10 metabolic pathways were significantly enriched in the mutations among isolates associated with severe CDI (P < 0.05). Gene mutations in glycometabolism, amino acid metabolism and biosynthesis virtually causing instability in protein activity were correlated positively to the transcription of tcdR and negatively to the expression of toxin repressor genes, ccpA and codY. In summary, our study firstly presented genomic insights into genetic characteristics and virulence association of C. difficile ST37 in China. Gene mutations in certain important metabolic pathways are associated with severe symptoms and correlated with higher virulence in C. difficile ST37 isolates.
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spelling doaj-art-fb5a3e1bb6474f9f839d522b6df72ef82025-08-20T02:30:45ZengTaylor & Francis GroupEmerging Microbes and Infections2222-17512021-01-011011331134510.1080/22221751.2021.1943538Genomic evolution and virulence association of Clostridioides difficile sequence type 37 (ribotype 017) in ChinaXingxing Xu0Yuo Luo1Huan Chen2Xiaojun Song3Qiao Bian4Xianjun Wang5Qian Liang6Jianhong Zhao7Chunhui Li8Guangzhong Song9Jun Yang10Lingli Sun11Jianmin Jiang12Huanying Wang13Bo Zhu14Guangyong Ye15Liang Chen16Yi-Wei Tang17Dazhi Jin18Department of Clinical Laboratory, Women’s Hospital, Zhejiang University School of Medicine, Hangzhou, People’s Republic of ChinaSchool of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, AustraliaKey Laboratory of Microorganism technology and bioinformatics research of Zhejiang Province, Hangzhou, People’s Republic of ChinaCentre of Laboratory Medicine, Zhejiang Provincial People’s Hospital, People’s Hospital of Hangzhou Medical College, Hangzhou, People’s Republic of ChinaZhejiang Provincial Center for Disease Control and Prevention, Hangzhou, People’s Republic of ChinaDepartment of Laboratory Medicine, Hangzhou First People’s Hospital, Hangzhou, People’s Republic of ChinaKey Laboratory of Microorganism technology and bioinformatics research of Zhejiang Province, Hangzhou, People’s Republic of ChinaDepartment of Clinical Microbiology, Second Hospital of Hebei Medical University, Hebei Provincial Center for Clinical Laboratories, Shijiazhuang, People’s Republic of ChinaInfection Control Center, Xiangya Hospital of Central South University, Changsha, People’s Republic of ChinaSchool of Laboratory Medicine, Hangzhou Medical College, Hangzhou, People’s Republic of ChinaSchool of Laboratory Medicine, Hangzhou Medical College, Hangzhou, People’s Republic of ChinaKey Laboratory of Microorganism technology and bioinformatics research of Zhejiang Province, Hangzhou, People’s Republic of ChinaZhejiang Provincial Center for Disease Control and Prevention, Hangzhou, People’s Republic of ChinaKey Laboratory of Microorganism technology and bioinformatics research of Zhejiang Province, Hangzhou, People’s Republic of ChinaDepartment of Clinical Laboratory, Women’s Hospital, Zhejiang University School of Medicine, Hangzhou, People’s Republic of ChinaDepartment of Clinical Laboratory, Women’s Hospital, Zhejiang University School of Medicine, Hangzhou, People’s Republic of ChinaCenter for Discovery and Innovation, Hackensack Meridian Health, Nutley, NJ, USACepheid, Danaher Diagnostic Platform, Shanghai, People’s Republic of ChinaSchool of Laboratory Medicine, Hangzhou Medical College, Hangzhou, People’s Republic of ChinaClostridioides difficile sequence type (ST) 37 (ribotype 017) is one of the most prevalent genotypes circulating in China. However, its genomic evolution and virulence determinants were rarely explored. Whole-genome sequencing, phylogeographic and phylogenetic analyses were conducted for C. difficile ST37 isolates. The 325 ST37 genomes from six continents, including North America (n = 66), South America (n = 4), Oceania (n = 7), Africa (n = 9), Europe (n = 138) and Asia (n = 101), were clustered into six major lineages, with region-dependent distributions, harbouring an array of antibiotic-resistance genes. The ST37 strains from China were divided into four distinct sublineages, showing five importation times and international sources. Isolates associated with severe infections exhibited significantly higher toxin productions, tcdB mRNA levels, and sporulation capacities (P < 0.001). Kyoto Encyclopedia of Genes and Genomes analysis showed 10 metabolic pathways were significantly enriched in the mutations among isolates associated with severe CDI (P < 0.05). Gene mutations in glycometabolism, amino acid metabolism and biosynthesis virtually causing instability in protein activity were correlated positively to the transcription of tcdR and negatively to the expression of toxin repressor genes, ccpA and codY. In summary, our study firstly presented genomic insights into genetic characteristics and virulence association of C. difficile ST37 in China. Gene mutations in certain important metabolic pathways are associated with severe symptoms and correlated with higher virulence in C. difficile ST37 isolates.https://www.tandfonline.com/doi/10.1080/22221751.2021.1943538Clostridioides difficileST37whole genome sequencingphylogenysevere CDI
spellingShingle Xingxing Xu
Yuo Luo
Huan Chen
Xiaojun Song
Qiao Bian
Xianjun Wang
Qian Liang
Jianhong Zhao
Chunhui Li
Guangzhong Song
Jun Yang
Lingli Sun
Jianmin Jiang
Huanying Wang
Bo Zhu
Guangyong Ye
Liang Chen
Yi-Wei Tang
Dazhi Jin
Genomic evolution and virulence association of Clostridioides difficile sequence type 37 (ribotype 017) in China
Emerging Microbes and Infections
Clostridioides difficile
ST37
whole genome sequencing
phylogeny
severe CDI
title Genomic evolution and virulence association of Clostridioides difficile sequence type 37 (ribotype 017) in China
title_full Genomic evolution and virulence association of Clostridioides difficile sequence type 37 (ribotype 017) in China
title_fullStr Genomic evolution and virulence association of Clostridioides difficile sequence type 37 (ribotype 017) in China
title_full_unstemmed Genomic evolution and virulence association of Clostridioides difficile sequence type 37 (ribotype 017) in China
title_short Genomic evolution and virulence association of Clostridioides difficile sequence type 37 (ribotype 017) in China
title_sort genomic evolution and virulence association of clostridioides difficile sequence type 37 ribotype 017 in china
topic Clostridioides difficile
ST37
whole genome sequencing
phylogeny
severe CDI
url https://www.tandfonline.com/doi/10.1080/22221751.2021.1943538
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