Streptococcus suis serotype 4: a population with the potential pathogenicity in humans and pigs

Streptococcus suis is a major bacterial pathogen in pigs and an emerging zoonotic pathogen. Different S. suis serotypes exhibit diverse characteristics in population structure and pathogenicity. Surveillance data highlight the significance of S. suis serotype 4 (SS4) in swine streptococcusis, a path...

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Main Authors: Jinlu Zhu, Jianping Wang, Weiming Kang, Xiyan Zhang, Anusak Kerdsin, Huochun Yao, Han Zheng, Zongfu Wu
Format: Article
Language:English
Published: Taylor & Francis Group 2024-12-01
Series:Emerging Microbes and Infections
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Online Access:https://www.tandfonline.com/doi/10.1080/22221751.2024.2352435
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author Jinlu Zhu
Jianping Wang
Weiming Kang
Xiyan Zhang
Anusak Kerdsin
Huochun Yao
Han Zheng
Zongfu Wu
author_facet Jinlu Zhu
Jianping Wang
Weiming Kang
Xiyan Zhang
Anusak Kerdsin
Huochun Yao
Han Zheng
Zongfu Wu
author_sort Jinlu Zhu
collection DOAJ
description Streptococcus suis is a major bacterial pathogen in pigs and an emerging zoonotic pathogen. Different S. suis serotypes exhibit diverse characteristics in population structure and pathogenicity. Surveillance data highlight the significance of S. suis serotype 4 (SS4) in swine streptococcusis, a pathotype causing human infections. However, except for a few epidemiologic studies, the information on SS4 remains limited. In this study, we investigated the population structure, pathogenicity, and antimicrobial characteristics of SS4 based on 126 isolates, including one from a patient with septicemia. We discovered significant diversities within this population, clustering into six minimum core genome (MCG) groups (1, 2, 3, 4, 7-2, and 7-3) and five lineages. Two main clonal complexes (CCs), CC17 and CC94, belong to MCG groups 1 and 3, respectively. Numerous important putative virulence-associated genes are present in these two MCG groups, and 35.00% (7/20) of pig isolates from CC17, CC94, and CC839 (also belonging to MCG group 3) were highly virulent (mortality rate ≥ 80%) in zebrafish and mice, similar to the human isolate ID36054. Cytotoxicity assays showed that the human and pig isolates of SS4 strains exhibit significant cytotoxicity to human cells. Antimicrobial susceptibility testing showed that 95.83% of strains isolated from our labs were classified as multidrug-resistant. Prophages were identified as the primary vehicle for antibiotic resistance genes. Our study demonstrates the public health threat posed by SS4, expanding the understanding of SS4 population structure and pathogenicity characteristics and providing valuable information for its surveillance and prevention.
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spelling doaj-art-e19b84b661404eaf99b61676dd3dbccd2025-08-20T02:20:37ZengTaylor & Francis GroupEmerging Microbes and Infections2222-17512024-12-0113110.1080/22221751.2024.2352435Streptococcus suis serotype 4: a population with the potential pathogenicity in humans and pigsJinlu Zhu0Jianping Wang1Weiming Kang2Xiyan Zhang3Anusak Kerdsin4Huochun Yao5Han Zheng6Zongfu Wu7MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, People’s Republic of ChinaNational Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, People’s Republic of ChinaNational Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, People’s Republic of ChinaNational Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, People’s Republic of ChinaFaculty of Public Health, Kasetsart University Chalermphrakiat Sakon Nakhon Province Campus, Sakon Nakhon, ThailandMOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, People’s Republic of ChinaNational Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, People’s Republic of ChinaMOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, People’s Republic of ChinaStreptococcus suis is a major bacterial pathogen in pigs and an emerging zoonotic pathogen. Different S. suis serotypes exhibit diverse characteristics in population structure and pathogenicity. Surveillance data highlight the significance of S. suis serotype 4 (SS4) in swine streptococcusis, a pathotype causing human infections. However, except for a few epidemiologic studies, the information on SS4 remains limited. In this study, we investigated the population structure, pathogenicity, and antimicrobial characteristics of SS4 based on 126 isolates, including one from a patient with septicemia. We discovered significant diversities within this population, clustering into six minimum core genome (MCG) groups (1, 2, 3, 4, 7-2, and 7-3) and five lineages. Two main clonal complexes (CCs), CC17 and CC94, belong to MCG groups 1 and 3, respectively. Numerous important putative virulence-associated genes are present in these two MCG groups, and 35.00% (7/20) of pig isolates from CC17, CC94, and CC839 (also belonging to MCG group 3) were highly virulent (mortality rate ≥ 80%) in zebrafish and mice, similar to the human isolate ID36054. Cytotoxicity assays showed that the human and pig isolates of SS4 strains exhibit significant cytotoxicity to human cells. Antimicrobial susceptibility testing showed that 95.83% of strains isolated from our labs were classified as multidrug-resistant. Prophages were identified as the primary vehicle for antibiotic resistance genes. Our study demonstrates the public health threat posed by SS4, expanding the understanding of SS4 population structure and pathogenicity characteristics and providing valuable information for its surveillance and prevention.https://www.tandfonline.com/doi/10.1080/22221751.2024.2352435Streptococcus suis serotype 4population structurepathogenicityantimicrobial susceptibilityprophageintegrative and conjugative elements
spellingShingle Jinlu Zhu
Jianping Wang
Weiming Kang
Xiyan Zhang
Anusak Kerdsin
Huochun Yao
Han Zheng
Zongfu Wu
Streptococcus suis serotype 4: a population with the potential pathogenicity in humans and pigs
Emerging Microbes and Infections
Streptococcus suis serotype 4
population structure
pathogenicity
antimicrobial susceptibility
prophage
integrative and conjugative elements
title Streptococcus suis serotype 4: a population with the potential pathogenicity in humans and pigs
title_full Streptococcus suis serotype 4: a population with the potential pathogenicity in humans and pigs
title_fullStr Streptococcus suis serotype 4: a population with the potential pathogenicity in humans and pigs
title_full_unstemmed Streptococcus suis serotype 4: a population with the potential pathogenicity in humans and pigs
title_short Streptococcus suis serotype 4: a population with the potential pathogenicity in humans and pigs
title_sort streptococcus suis serotype 4 a population with the potential pathogenicity in humans and pigs
topic Streptococcus suis serotype 4
population structure
pathogenicity
antimicrobial susceptibility
prophage
integrative and conjugative elements
url https://www.tandfonline.com/doi/10.1080/22221751.2024.2352435
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