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Analysis of the complete genome sequences of Clostridium perfringens strains harbouring the binary enterotoxin BEC gene and comparative genomics of pCP13-like family plasmids

BACKGROUND: BEC-producing Clostridium perfringens is a causative agent of foodborne gastroenteritis. It was first reported in 2014, and since then, several isolates have been identified in Japan and the United Kingdom. The novel binary ADP-ribosylating toxin BEC, which consists of two components (BE...

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Autores principales: Ueda, Kengo, Kawahara, Kazuki, Kimoto, Narumi, Yamaguchi, Yusuke, Yamada, Kazuhiro, Oki, Hiroya, Yoshida, Takuya, Matsuda, Shigeaki, Matsumoto, Yuki, Motooka, Daisuke, Kawatsu, Kentaro, Iida, Tetsuya, Nakamura, Shota, Ohkubo, Tadayasu, Yonogi, Shinya
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8941779/
https://www.ncbi.nlm.nih.gov/pubmed/35321661
http://dx.doi.org/10.1186/s12864-022-08453-4
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author Ueda, Kengo
Kawahara, Kazuki
Kimoto, Narumi
Yamaguchi, Yusuke
Yamada, Kazuhiro
Oki, Hiroya
Yoshida, Takuya
Matsuda, Shigeaki
Matsumoto, Yuki
Motooka, Daisuke
Kawatsu, Kentaro
Iida, Tetsuya
Nakamura, Shota
Ohkubo, Tadayasu
Yonogi, Shinya
author_facet Ueda, Kengo
Kawahara, Kazuki
Kimoto, Narumi
Yamaguchi, Yusuke
Yamada, Kazuhiro
Oki, Hiroya
Yoshida, Takuya
Matsuda, Shigeaki
Matsumoto, Yuki
Motooka, Daisuke
Kawatsu, Kentaro
Iida, Tetsuya
Nakamura, Shota
Ohkubo, Tadayasu
Yonogi, Shinya
author_sort Ueda, Kengo
collection PubMed
description BACKGROUND: BEC-producing Clostridium perfringens is a causative agent of foodborne gastroenteritis. It was first reported in 2014, and since then, several isolates have been identified in Japan and the United Kingdom. The novel binary ADP-ribosylating toxin BEC, which consists of two components (BECa and BECb), is encoded on a plasmid that is similar to pCP13 and harbours a conjugation locus, called Pcp, encoding homologous proteins of the type 4 secretion system. Despite the high in vitro conjugation frequency of pCP13, its dissemination and that of related plasmids, including bec-harbouring plasmids, in the natural environment have not been characterised. This lack of knowledge has limited our understanding of the genomic epidemiology of bec-harbouring C. perfringens strains. RESULTS: In this study, we determined the complete genome sequences of five bec-harbouring C. perfringens strains isolated from 2009 to 2019. Each isolate contains a ~ 3.36 Mbp chromosome and 1–3 plasmids of either the pCW3-like family, pCP13-like family, or an unknown family, and the bec-encoding region in all five isolates was located on a ~ 54 kbp pCP13-like plasmid. Phylogenetic and SNP analyses of these complete genome sequences and the 211 assembled C. perfringens genomes in GenBank showed that although these bec-harbouring strains were split into two phylogenetic clades, the sequences of the bec-encoding plasmids were nearly identical (>99.81%), with a significantly smaller SNP accumulation rate than that of their chromosomes. Given that the Pcp locus is conserved in these pCP13-like plasmids, we propose a mechanism in which the plasmids were disseminated by horizontal gene transfer. Data mining showed that strains carrying pCP13-like family plasmids were unexpectedly common (58/216 strains) and widely disseminated among the various C. perfringens clades. Although these plasmids possess a conserved Pcp locus, their ‘accessory regions’ can accommodate a wide variety of genes, including virulence-associated genes, such as becA/becB and cbp2. These results suggest that this family of plasmids can integrate various foreign genes and is transmissible among C. perfringens strains. CONCLUSION: This study demonstrates the potential significance of pCP13-like plasmids, including bec-encoding plasmids, for the characterisation and monitoring of the dissemination of pathogenic C. perfringens strains. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08453-4.
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spelling pubmed-89417792022-03-24 Analysis of the complete genome sequences of Clostridium perfringens strains harbouring the binary enterotoxin BEC gene and comparative genomics of pCP13-like family plasmids Ueda, Kengo Kawahara, Kazuki Kimoto, Narumi Yamaguchi, Yusuke Yamada, Kazuhiro Oki, Hiroya Yoshida, Takuya Matsuda, Shigeaki Matsumoto, Yuki Motooka, Daisuke Kawatsu, Kentaro Iida, Tetsuya Nakamura, Shota Ohkubo, Tadayasu Yonogi, Shinya BMC Genomics Research BACKGROUND: BEC-producing Clostridium perfringens is a causative agent of foodborne gastroenteritis. It was first reported in 2014, and since then, several isolates have been identified in Japan and the United Kingdom. The novel binary ADP-ribosylating toxin BEC, which consists of two components (BECa and BECb), is encoded on a plasmid that is similar to pCP13 and harbours a conjugation locus, called Pcp, encoding homologous proteins of the type 4 secretion system. Despite the high in vitro conjugation frequency of pCP13, its dissemination and that of related plasmids, including bec-harbouring plasmids, in the natural environment have not been characterised. This lack of knowledge has limited our understanding of the genomic epidemiology of bec-harbouring C. perfringens strains. RESULTS: In this study, we determined the complete genome sequences of five bec-harbouring C. perfringens strains isolated from 2009 to 2019. Each isolate contains a ~ 3.36 Mbp chromosome and 1–3 plasmids of either the pCW3-like family, pCP13-like family, or an unknown family, and the bec-encoding region in all five isolates was located on a ~ 54 kbp pCP13-like plasmid. Phylogenetic and SNP analyses of these complete genome sequences and the 211 assembled C. perfringens genomes in GenBank showed that although these bec-harbouring strains were split into two phylogenetic clades, the sequences of the bec-encoding plasmids were nearly identical (>99.81%), with a significantly smaller SNP accumulation rate than that of their chromosomes. Given that the Pcp locus is conserved in these pCP13-like plasmids, we propose a mechanism in which the plasmids were disseminated by horizontal gene transfer. Data mining showed that strains carrying pCP13-like family plasmids were unexpectedly common (58/216 strains) and widely disseminated among the various C. perfringens clades. Although these plasmids possess a conserved Pcp locus, their ‘accessory regions’ can accommodate a wide variety of genes, including virulence-associated genes, such as becA/becB and cbp2. These results suggest that this family of plasmids can integrate various foreign genes and is transmissible among C. perfringens strains. CONCLUSION: This study demonstrates the potential significance of pCP13-like plasmids, including bec-encoding plasmids, for the characterisation and monitoring of the dissemination of pathogenic C. perfringens strains. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08453-4. BioMed Central 2022-03-23 /pmc/articles/PMC8941779/ /pubmed/35321661 http://dx.doi.org/10.1186/s12864-022-08453-4 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Ueda, Kengo
Kawahara, Kazuki
Kimoto, Narumi
Yamaguchi, Yusuke
Yamada, Kazuhiro
Oki, Hiroya
Yoshida, Takuya
Matsuda, Shigeaki
Matsumoto, Yuki
Motooka, Daisuke
Kawatsu, Kentaro
Iida, Tetsuya
Nakamura, Shota
Ohkubo, Tadayasu
Yonogi, Shinya
Analysis of the complete genome sequences of Clostridium perfringens strains harbouring the binary enterotoxin BEC gene and comparative genomics of pCP13-like family plasmids
title Analysis of the complete genome sequences of Clostridium perfringens strains harbouring the binary enterotoxin BEC gene and comparative genomics of pCP13-like family plasmids
title_full Analysis of the complete genome sequences of Clostridium perfringens strains harbouring the binary enterotoxin BEC gene and comparative genomics of pCP13-like family plasmids
title_fullStr Analysis of the complete genome sequences of Clostridium perfringens strains harbouring the binary enterotoxin BEC gene and comparative genomics of pCP13-like family plasmids
title_full_unstemmed Analysis of the complete genome sequences of Clostridium perfringens strains harbouring the binary enterotoxin BEC gene and comparative genomics of pCP13-like family plasmids
title_short Analysis of the complete genome sequences of Clostridium perfringens strains harbouring the binary enterotoxin BEC gene and comparative genomics of pCP13-like family plasmids
title_sort analysis of the complete genome sequences of clostridium perfringens strains harbouring the binary enterotoxin bec gene and comparative genomics of pcp13-like family plasmids
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8941779/
https://www.ncbi.nlm.nih.gov/pubmed/35321661
http://dx.doi.org/10.1186/s12864-022-08453-4
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