ICESsuHN105, a Novel Multiple Antibiotic Resistant ICE in Streptococcus suis Serotype 5 Strain HN105

Streptococcussuis serotype 5, an emerging zoonosis bacterial pathogen, has been isolated from infections in both pigs and humans. In this study, we sequenced the first complete genome of a virulent, multidrug-resistant SS5 strain HN105. The strain HN105 displayed enhanced pathogenicity in zebrafish...

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Main Authors: Yinchu Zhu, Yue Zhang, Jiale Ma, Wenyang Dong, Xiaojun Zhong, Zihao Pan, Huochun Yao
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.00274/full
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author Yinchu Zhu
Yinchu Zhu
Yinchu Zhu
Yue Zhang
Yue Zhang
Yue Zhang
Jiale Ma
Jiale Ma
Jiale Ma
Wenyang Dong
Wenyang Dong
Wenyang Dong
Xiaojun Zhong
Xiaojun Zhong
Xiaojun Zhong
Zihao Pan
Zihao Pan
Zihao Pan
Huochun Yao
Huochun Yao
Huochun Yao
author_facet Yinchu Zhu
Yinchu Zhu
Yinchu Zhu
Yue Zhang
Yue Zhang
Yue Zhang
Jiale Ma
Jiale Ma
Jiale Ma
Wenyang Dong
Wenyang Dong
Wenyang Dong
Xiaojun Zhong
Xiaojun Zhong
Xiaojun Zhong
Zihao Pan
Zihao Pan
Zihao Pan
Huochun Yao
Huochun Yao
Huochun Yao
author_sort Yinchu Zhu
collection DOAJ
description Streptococcussuis serotype 5, an emerging zoonosis bacterial pathogen, has been isolated from infections in both pigs and humans. In this study, we sequenced the first complete genome of a virulent, multidrug-resistant SS5 strain HN105. The strain HN105 displayed enhanced pathogenicity in zebrafish and BABL/c mouse infection models. Comparative genome analysis identified a novel 80K integrative conjugative element (ICE), ICESsuHN105, as required for the multidrug resistance phenotype. Six corresponding antibiotic resistance genes in this ICE were identified, namely tet (O), tet (M), erm (two copies), aph, and spc. Phylogenetic analysis classified the element as a homolog of the ICESa2603 family, containing the typical family backbone and insertion DNA. DNA hybrids mediated by natural transformation between HN105 and ZY05719 verified the antibiotic resistant genes of ICESsuHN105 that could be transferred successfully, while they were dispersedly inserted with a single gene in different genomic locations of ZY05719(HN105) transformants. To further identify the horizontal transfer of ICESsuHN105 as a whole mobile genetic element, a circular intermediate form of ICESsuHN105 was detected by PCR. However, the effective conjugation using serotype 2 S. suis as recipients was not observed in current assays in vitro. Further studies confirmed the presence of the complete lantibiotic locus encoded in ICESsuHN105 that effectively inhibits the growth of other streptococci. In summary, this study demonstrated the presence of antibiotic resistance genes in ICE that are able to transfer between different clinical isolates and adapt to a broader range of Streptococcus serotype or species.
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spelling doaj.art-3cb87013a1c64af79e89012e5f5d29c02022-12-21T23:58:34ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-02-011010.3389/fmicb.2019.00274429596ICESsuHN105, a Novel Multiple Antibiotic Resistant ICE in Streptococcus suis Serotype 5 Strain HN105Yinchu Zhu0Yinchu Zhu1Yinchu Zhu2Yue Zhang3Yue Zhang4Yue Zhang5Jiale Ma6Jiale Ma7Jiale Ma8Wenyang Dong9Wenyang Dong10Wenyang Dong11Xiaojun Zhong12Xiaojun Zhong13Xiaojun Zhong14Zihao Pan15Zihao Pan16Zihao Pan17Huochun Yao18Huochun Yao19Huochun Yao20College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaOIE Reference Lab for Swine Streptococcosis, Nanjing, ChinaKey Laboratory of Animal Bacteriology, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, ChinaCollege of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaOIE Reference Lab for Swine Streptococcosis, Nanjing, ChinaKey Laboratory of Animal Bacteriology, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, ChinaCollege of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaOIE Reference Lab for Swine Streptococcosis, Nanjing, ChinaKey Laboratory of Animal Bacteriology, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, ChinaCollege of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaOIE Reference Lab for Swine Streptococcosis, Nanjing, ChinaKey Laboratory of Animal Bacteriology, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, ChinaCollege of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaOIE Reference Lab for Swine Streptococcosis, Nanjing, ChinaKey Laboratory of Animal Bacteriology, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, ChinaCollege of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaOIE Reference Lab for Swine Streptococcosis, Nanjing, ChinaKey Laboratory of Animal Bacteriology, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, ChinaCollege of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaOIE Reference Lab for Swine Streptococcosis, Nanjing, ChinaKey Laboratory of Animal Bacteriology, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, ChinaStreptococcussuis serotype 5, an emerging zoonosis bacterial pathogen, has been isolated from infections in both pigs and humans. In this study, we sequenced the first complete genome of a virulent, multidrug-resistant SS5 strain HN105. The strain HN105 displayed enhanced pathogenicity in zebrafish and BABL/c mouse infection models. Comparative genome analysis identified a novel 80K integrative conjugative element (ICE), ICESsuHN105, as required for the multidrug resistance phenotype. Six corresponding antibiotic resistance genes in this ICE were identified, namely tet (O), tet (M), erm (two copies), aph, and spc. Phylogenetic analysis classified the element as a homolog of the ICESa2603 family, containing the typical family backbone and insertion DNA. DNA hybrids mediated by natural transformation between HN105 and ZY05719 verified the antibiotic resistant genes of ICESsuHN105 that could be transferred successfully, while they were dispersedly inserted with a single gene in different genomic locations of ZY05719(HN105) transformants. To further identify the horizontal transfer of ICESsuHN105 as a whole mobile genetic element, a circular intermediate form of ICESsuHN105 was detected by PCR. However, the effective conjugation using serotype 2 S. suis as recipients was not observed in current assays in vitro. Further studies confirmed the presence of the complete lantibiotic locus encoded in ICESsuHN105 that effectively inhibits the growth of other streptococci. In summary, this study demonstrated the presence of antibiotic resistance genes in ICE that are able to transfer between different clinical isolates and adapt to a broader range of Streptococcus serotype or species.https://www.frontiersin.org/article/10.3389/fmicb.2019.00274/fullS. suis serotype 5comparative genomicsmulti-antibiotic resistanceintegrative and conjugative elementnatural transformationbacteriocin
spellingShingle Yinchu Zhu
Yinchu Zhu
Yinchu Zhu
Yue Zhang
Yue Zhang
Yue Zhang
Jiale Ma
Jiale Ma
Jiale Ma
Wenyang Dong
Wenyang Dong
Wenyang Dong
Xiaojun Zhong
Xiaojun Zhong
Xiaojun Zhong
Zihao Pan
Zihao Pan
Zihao Pan
Huochun Yao
Huochun Yao
Huochun Yao
ICESsuHN105, a Novel Multiple Antibiotic Resistant ICE in Streptococcus suis Serotype 5 Strain HN105
Frontiers in Microbiology
S. suis serotype 5
comparative genomics
multi-antibiotic resistance
integrative and conjugative element
natural transformation
bacteriocin
title ICESsuHN105, a Novel Multiple Antibiotic Resistant ICE in Streptococcus suis Serotype 5 Strain HN105
title_full ICESsuHN105, a Novel Multiple Antibiotic Resistant ICE in Streptococcus suis Serotype 5 Strain HN105
title_fullStr ICESsuHN105, a Novel Multiple Antibiotic Resistant ICE in Streptococcus suis Serotype 5 Strain HN105
title_full_unstemmed ICESsuHN105, a Novel Multiple Antibiotic Resistant ICE in Streptococcus suis Serotype 5 Strain HN105
title_short ICESsuHN105, a Novel Multiple Antibiotic Resistant ICE in Streptococcus suis Serotype 5 Strain HN105
title_sort icessuhn105 a novel multiple antibiotic resistant ice in streptococcus suis serotype 5 strain hn105
topic S. suis serotype 5
comparative genomics
multi-antibiotic resistance
integrative and conjugative element
natural transformation
bacteriocin
url https://www.frontiersin.org/article/10.3389/fmicb.2019.00274/full
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