Characterization of integrative and conjugative elements carrying antibiotic resistance genes of Streptococcus suis isolated in China

Streptococcus suis, an emerging zoonotic pathogen, is important reservoirs of antibiotic resistance genes that play critical roles in the horizontal transfer of corresponding resistances. In the present study, 656 antibiotic resistance (AR) genes were detected in 154 of 155 genomes of S. suis strain...

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Main Authors: Jianping Wang, Kexin Qi, Xuemei Bai, Zongfu Wu, Weiming Kang, Pujun Liang, Han Zheng, Jianguo Xu
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-12-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.1074844/full
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author Jianping Wang
Kexin Qi
Xuemei Bai
Zongfu Wu
Weiming Kang
Pujun Liang
Pujun Liang
Han Zheng
Jianguo Xu
author_facet Jianping Wang
Kexin Qi
Xuemei Bai
Zongfu Wu
Weiming Kang
Pujun Liang
Pujun Liang
Han Zheng
Jianguo Xu
author_sort Jianping Wang
collection DOAJ
description Streptococcus suis, an emerging zoonotic pathogen, is important reservoirs of antibiotic resistance genes that play critical roles in the horizontal transfer of corresponding resistances. In the present study, 656 antibiotic resistance (AR) genes were detected in 154 of 155 genomes of S. suis strains isolated from the nasopharynx of slaughtered pigs and the lungs of diseased pigs in China. The AR genes were clustered into 11 categories, consisting of tetracycline, macrolides, lincosamide, streptogramin, aminoglycoside, trimethoprim, amphenicols, nucleoside, quinupristin/dalfopristin, glycopeptide, and oxazolidinones resistance genes. In order to investigate the transmission patterns of the AR genes, AR genes-associated the mobile genetic elements (MGEs) were extracted and investigated. Twenty ICEs, one defective ICE, one tandem ICE, and ten prophages were found, which mainly carried tetracycline, macrolides/lincosamides/streptogramin (MLS), and aminoglycosides resistance genes. Three types of DNA cargo with AR genes were integrated into specific sites of ICEs: integrative mobilizable elements (IMEs), cis-IMEs (CIMEs), and transposon Tn916. Obvious differences in AR gene categories were found among the three cargo types. IMEs mainly harbored tetracycline and MLS resistance genes. CIMEs mainly carried aminoglycoside resistance genes, while transposon Tn916 carried only the tet (M) gene. Nearly all AR genes in ICEs were carried by IMEs and CIMEs. IMEs were prevalent and were also detected in additional 29 S. suis genomes. The horizontal transfer of IMEs and CIMEs may play critical role in ICE evolution and AR gene transmission in the S. suis population. Our findings provide novel insights into the transmission patterns of AR genes and the evolutionary mechanisms of ICEs in S. suis.
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spelling doaj.art-61c84dd0460249eda409c77e5095ba052022-12-22T12:27:12ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-12-011310.3389/fmicb.2022.10748441074844Characterization of integrative and conjugative elements carrying antibiotic resistance genes of Streptococcus suis isolated in ChinaJianping Wang0Kexin Qi1Xuemei Bai2Zongfu Wu3Weiming Kang4Pujun Liang5Pujun Liang6Han Zheng7Jianguo Xu8State Key Laboratory of Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaState Key Laboratory of Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaState Key Laboratory of Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaOIE Reference Lab for Swine Streptococcosis, MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaState Key Laboratory of Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaState Key Laboratory of Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaNanxishan Hospital of Guangxi Zhuang Autonomous Region, Guilin, ChinaState Key Laboratory of Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaState Key Laboratory of Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaStreptococcus suis, an emerging zoonotic pathogen, is important reservoirs of antibiotic resistance genes that play critical roles in the horizontal transfer of corresponding resistances. In the present study, 656 antibiotic resistance (AR) genes were detected in 154 of 155 genomes of S. suis strains isolated from the nasopharynx of slaughtered pigs and the lungs of diseased pigs in China. The AR genes were clustered into 11 categories, consisting of tetracycline, macrolides, lincosamide, streptogramin, aminoglycoside, trimethoprim, amphenicols, nucleoside, quinupristin/dalfopristin, glycopeptide, and oxazolidinones resistance genes. In order to investigate the transmission patterns of the AR genes, AR genes-associated the mobile genetic elements (MGEs) were extracted and investigated. Twenty ICEs, one defective ICE, one tandem ICE, and ten prophages were found, which mainly carried tetracycline, macrolides/lincosamides/streptogramin (MLS), and aminoglycosides resistance genes. Three types of DNA cargo with AR genes were integrated into specific sites of ICEs: integrative mobilizable elements (IMEs), cis-IMEs (CIMEs), and transposon Tn916. Obvious differences in AR gene categories were found among the three cargo types. IMEs mainly harbored tetracycline and MLS resistance genes. CIMEs mainly carried aminoglycoside resistance genes, while transposon Tn916 carried only the tet (M) gene. Nearly all AR genes in ICEs were carried by IMEs and CIMEs. IMEs were prevalent and were also detected in additional 29 S. suis genomes. The horizontal transfer of IMEs and CIMEs may play critical role in ICE evolution and AR gene transmission in the S. suis population. Our findings provide novel insights into the transmission patterns of AR genes and the evolutionary mechanisms of ICEs in S. suis.https://www.frontiersin.org/articles/10.3389/fmicb.2022.1074844/fullStreptococcus suisantibiotic resistanceICEIMEsnf2 gene
spellingShingle Jianping Wang
Kexin Qi
Xuemei Bai
Zongfu Wu
Weiming Kang
Pujun Liang
Pujun Liang
Han Zheng
Jianguo Xu
Characterization of integrative and conjugative elements carrying antibiotic resistance genes of Streptococcus suis isolated in China
Frontiers in Microbiology
Streptococcus suis
antibiotic resistance
ICE
IME
snf2 gene
title Characterization of integrative and conjugative elements carrying antibiotic resistance genes of Streptococcus suis isolated in China
title_full Characterization of integrative and conjugative elements carrying antibiotic resistance genes of Streptococcus suis isolated in China
title_fullStr Characterization of integrative and conjugative elements carrying antibiotic resistance genes of Streptococcus suis isolated in China
title_full_unstemmed Characterization of integrative and conjugative elements carrying antibiotic resistance genes of Streptococcus suis isolated in China
title_short Characterization of integrative and conjugative elements carrying antibiotic resistance genes of Streptococcus suis isolated in China
title_sort characterization of integrative and conjugative elements carrying antibiotic resistance genes of streptococcus suis isolated in china
topic Streptococcus suis
antibiotic resistance
ICE
IME
snf2 gene
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.1074844/full
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