Analysis of the complete genome sequences of Clostridium perfringens strains harbouring the binary enterotoxin BEC gene and comparative genomics of pCP13-like family plasmids
Abstract 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 compon...
| Main Authors: | , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2022-03-01
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| Series: | BMC Genomics |
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| Online Access: | https://doi.org/10.1186/s12864-022-08453-4 |
| _version_ | 1818776574907908096 |
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| author | Kengo Ueda Kazuki Kawahara Narumi Kimoto Yusuke Yamaguchi Kazuhiro Yamada Hiroya Oki Takuya Yoshida Shigeaki Matsuda Yuki Matsumoto Daisuke Motooka Kentaro Kawatsu Tetsuya Iida Shota Nakamura Tadayasu Ohkubo Shinya Yonogi |
| author_facet | Kengo Ueda Kazuki Kawahara Narumi Kimoto Yusuke Yamaguchi Kazuhiro Yamada Hiroya Oki Takuya Yoshida Shigeaki Matsuda Yuki Matsumoto Daisuke Motooka Kentaro Kawatsu Tetsuya Iida Shota Nakamura Tadayasu Ohkubo Shinya Yonogi |
| author_sort | Kengo Ueda |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-12-18T11:15:06Z |
| format | Article |
| id | doaj.art-2571f5031e4b4b7a8c4082535aacd3bf |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-12-18T11:15:06Z |
| publishDate | 2022-03-01 |
| publisher | BMC |
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| series | BMC Genomics |
| spelling | doaj.art-2571f5031e4b4b7a8c4082535aacd3bf2022-12-21T21:09:56ZengBMCBMC Genomics1471-21642022-03-0123111410.1186/s12864-022-08453-4Analysis of the complete genome sequences of Clostridium perfringens strains harbouring the binary enterotoxin BEC gene and comparative genomics of pCP13-like family plasmidsKengo Ueda0Kazuki Kawahara1Narumi Kimoto2Yusuke Yamaguchi3Kazuhiro Yamada4Hiroya Oki5Takuya Yoshida6Shigeaki Matsuda7Yuki Matsumoto8Daisuke Motooka9Kentaro Kawatsu10Tetsuya Iida11Shota Nakamura12Tadayasu Ohkubo13Shinya Yonogi14Laboratory of Biophysical Chemistry, Graduate School of Pharmaceutical Sciences, Osaka UniversityLaboratory of Biophysical Chemistry, Graduate School of Pharmaceutical Sciences, Osaka UniversityLaboratory of Biophysical Chemistry, Graduate School of Pharmaceutical Sciences, Osaka UniversityLaboratory of Biophysical Chemistry, Graduate School of Pharmaceutical Sciences, Osaka UniversityDepartment of Microbiology and Medical Zoology, Aichi Prefectural Institute of Public HealthDepartment of Infection Metagenomics, Genome Information Research Center, Research Institute for Microbial Diseases (RIMD), Osaka UniversityLaboratory of Biophysical Chemistry, Graduate School of Pharmaceutical Sciences, Osaka UniversityDepartment of Bacterial Infection, Research Institute for Microbial Disease (RIMD), Osaka UniversityDepartment of Infection Metagenomics, Genome Information Research Center, Research Institute for Microbial Diseases (RIMD), Osaka UniversityDepartment of Infection Metagenomics, Genome Information Research Center, Research Institute for Microbial Diseases (RIMD), Osaka UniversityDivision of Microbiology, Osaka Institute of Public HealthDepartment of Bacterial Infection, Research Institute for Microbial Disease (RIMD), Osaka UniversityDepartment of Infection Metagenomics, Genome Information Research Center, Research Institute for Microbial Diseases (RIMD), Osaka UniversityLaboratory of Biophysical Chemistry, Graduate School of Pharmaceutical Sciences, Osaka UniversityDepartment of Bacterial Infection, Research Institute for Microbial Disease (RIMD), Osaka UniversityAbstract 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.https://doi.org/10.1186/s12864-022-08453-4C. perfringensBinary enterotoxinHorizontal gene transferConjugative plasmidpCP13-like family plasmid |
| spellingShingle | Kengo Ueda Kazuki Kawahara Narumi Kimoto Yusuke Yamaguchi Kazuhiro Yamada Hiroya Oki Takuya Yoshida Shigeaki Matsuda Yuki Matsumoto Daisuke Motooka Kentaro Kawatsu Tetsuya Iida Shota Nakamura Tadayasu Ohkubo Shinya Yonogi Analysis of the complete genome sequences of Clostridium perfringens strains harbouring the binary enterotoxin BEC gene and comparative genomics of pCP13-like family plasmids BMC Genomics C. perfringens Binary enterotoxin Horizontal gene transfer Conjugative plasmid pCP13-like family plasmid |
| 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 | C. perfringens Binary enterotoxin Horizontal gene transfer Conjugative plasmid pCP13-like family plasmid |
| url | https://doi.org/10.1186/s12864-022-08453-4 |
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