The genome sequence of Clostridium botulinum type C neurotoxin-converting phage and the molecular mechanisms of unstable lysogeny

Yoshihiko Sakaguchi, Tetsuya Hayashi, Ken Kurokawa, Keisuke Nakayama, Kenshiro Oshima, Yukako Fujinaga, Makoto Ohnishi, Eiichi Ohtsubo, Masahira Hattori, Keiji Oguma

Research output: Contribution to journalArticle

84 Citations (Scopus)

Abstract

Botulinum neurotoxins (BoNTXs) produced by Clostridium botulinum are among the most poisonous substances known. Of the seven types of BoNTXs, genes for type C1 and D toxins (BoNTX/C1 and D) are carried by bacteriophages. The gene for exoenzyme C3 also resides on these phages. Here, we present the complete genome sequence of c-st, a representative of BoNTX/C1-converting phages. The genome is a linear double-stranded DNA of 185,682 bp with 404-bp terminal direct repeats, the largest known temperate phage genome. We identified 198 potential protein-coding regions, including the genes for production of BoNTX/C1 and exoenzyme C3. Very exceptionally, as a viable bacteriophage, a number of insertion sequences were found on the c-st genome. By analyzing the molecular structure of the c-st genome in lysogens, we also found that it exists as a circular plasmid prophage. These features account for the unstable lysogeny of BoNTX phages, which has historically been called "pseudolysogeny." The PCR scanning analysis of other BoNTX/C1 and D phages based on the c-st sequence further revealed that BoNTX phages comprise a divergent phage family, probably generated by exchanging genomic segments among BoNTX phages and their relatives.

Original languageEnglish
Pages (from-to)17472-17477
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume102
Issue number48
DOIs
Publication statusPublished - 2005 Nov 29
Externally publishedYes

Fingerprint

Clostridium botulinum type C
Lysogeny
Neurotoxins
Bacteriophages
Genome
Clostridium botulinum
Genes
Prophages
Terminal Repeat Sequences
Nucleic Acid Repetitive Sequences
Insertional Mutagenesis
Molecular Structure
Open Reading Frames

Keywords

  • Bacteriophage
  • Botulinum neurotoxin
  • Insertion sequence
  • Plasmid prophage

ASJC Scopus subject areas

  • Genetics
  • General

Cite this

The genome sequence of Clostridium botulinum type C neurotoxin-converting phage and the molecular mechanisms of unstable lysogeny. / Sakaguchi, Yoshihiko; Hayashi, Tetsuya; Kurokawa, Ken; Nakayama, Keisuke; Oshima, Kenshiro; Fujinaga, Yukako; Ohnishi, Makoto; Ohtsubo, Eiichi; Hattori, Masahira; Oguma, Keiji.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 102, No. 48, 29.11.2005, p. 17472-17477.

Research output: Contribution to journalArticle

Sakaguchi, Yoshihiko ; Hayashi, Tetsuya ; Kurokawa, Ken ; Nakayama, Keisuke ; Oshima, Kenshiro ; Fujinaga, Yukako ; Ohnishi, Makoto ; Ohtsubo, Eiichi ; Hattori, Masahira ; Oguma, Keiji. / The genome sequence of Clostridium botulinum type C neurotoxin-converting phage and the molecular mechanisms of unstable lysogeny. In: Proceedings of the National Academy of Sciences of the United States of America. 2005 ; Vol. 102, No. 48. pp. 17472-17477.
@article{348604e04bf24f778f749c2b3debb333,
title = "The genome sequence of Clostridium botulinum type C neurotoxin-converting phage and the molecular mechanisms of unstable lysogeny",
abstract = "Botulinum neurotoxins (BoNTXs) produced by Clostridium botulinum are among the most poisonous substances known. Of the seven types of BoNTXs, genes for type C1 and D toxins (BoNTX/C1 and D) are carried by bacteriophages. The gene for exoenzyme C3 also resides on these phages. Here, we present the complete genome sequence of c-st, a representative of BoNTX/C1-converting phages. The genome is a linear double-stranded DNA of 185,682 bp with 404-bp terminal direct repeats, the largest known temperate phage genome. We identified 198 potential protein-coding regions, including the genes for production of BoNTX/C1 and exoenzyme C3. Very exceptionally, as a viable bacteriophage, a number of insertion sequences were found on the c-st genome. By analyzing the molecular structure of the c-st genome in lysogens, we also found that it exists as a circular plasmid prophage. These features account for the unstable lysogeny of BoNTX phages, which has historically been called {"}pseudolysogeny.{"} The PCR scanning analysis of other BoNTX/C1 and D phages based on the c-st sequence further revealed that BoNTX phages comprise a divergent phage family, probably generated by exchanging genomic segments among BoNTX phages and their relatives.",
keywords = "Bacteriophage, Botulinum neurotoxin, Insertion sequence, Plasmid prophage",
author = "Yoshihiko Sakaguchi and Tetsuya Hayashi and Ken Kurokawa and Keisuke Nakayama and Kenshiro Oshima and Yukako Fujinaga and Makoto Ohnishi and Eiichi Ohtsubo and Masahira Hattori and Keiji Oguma",
year = "2005",
month = "11",
day = "29",
doi = "10.1073/pnas.0505503102",
language = "English",
volume = "102",
pages = "17472--17477",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "48",

}

TY - JOUR

T1 - The genome sequence of Clostridium botulinum type C neurotoxin-converting phage and the molecular mechanisms of unstable lysogeny

AU - Sakaguchi, Yoshihiko

AU - Hayashi, Tetsuya

AU - Kurokawa, Ken

AU - Nakayama, Keisuke

AU - Oshima, Kenshiro

AU - Fujinaga, Yukako

AU - Ohnishi, Makoto

AU - Ohtsubo, Eiichi

AU - Hattori, Masahira

AU - Oguma, Keiji

PY - 2005/11/29

Y1 - 2005/11/29

N2 - Botulinum neurotoxins (BoNTXs) produced by Clostridium botulinum are among the most poisonous substances known. Of the seven types of BoNTXs, genes for type C1 and D toxins (BoNTX/C1 and D) are carried by bacteriophages. The gene for exoenzyme C3 also resides on these phages. Here, we present the complete genome sequence of c-st, a representative of BoNTX/C1-converting phages. The genome is a linear double-stranded DNA of 185,682 bp with 404-bp terminal direct repeats, the largest known temperate phage genome. We identified 198 potential protein-coding regions, including the genes for production of BoNTX/C1 and exoenzyme C3. Very exceptionally, as a viable bacteriophage, a number of insertion sequences were found on the c-st genome. By analyzing the molecular structure of the c-st genome in lysogens, we also found that it exists as a circular plasmid prophage. These features account for the unstable lysogeny of BoNTX phages, which has historically been called "pseudolysogeny." The PCR scanning analysis of other BoNTX/C1 and D phages based on the c-st sequence further revealed that BoNTX phages comprise a divergent phage family, probably generated by exchanging genomic segments among BoNTX phages and their relatives.

AB - Botulinum neurotoxins (BoNTXs) produced by Clostridium botulinum are among the most poisonous substances known. Of the seven types of BoNTXs, genes for type C1 and D toxins (BoNTX/C1 and D) are carried by bacteriophages. The gene for exoenzyme C3 also resides on these phages. Here, we present the complete genome sequence of c-st, a representative of BoNTX/C1-converting phages. The genome is a linear double-stranded DNA of 185,682 bp with 404-bp terminal direct repeats, the largest known temperate phage genome. We identified 198 potential protein-coding regions, including the genes for production of BoNTX/C1 and exoenzyme C3. Very exceptionally, as a viable bacteriophage, a number of insertion sequences were found on the c-st genome. By analyzing the molecular structure of the c-st genome in lysogens, we also found that it exists as a circular plasmid prophage. These features account for the unstable lysogeny of BoNTX phages, which has historically been called "pseudolysogeny." The PCR scanning analysis of other BoNTX/C1 and D phages based on the c-st sequence further revealed that BoNTX phages comprise a divergent phage family, probably generated by exchanging genomic segments among BoNTX phages and their relatives.

KW - Bacteriophage

KW - Botulinum neurotoxin

KW - Insertion sequence

KW - Plasmid prophage

UR - http://www.scopus.com/inward/record.url?scp=28444476607&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=28444476607&partnerID=8YFLogxK

U2 - 10.1073/pnas.0505503102

DO - 10.1073/pnas.0505503102

M3 - Article

C2 - 16287978

AN - SCOPUS:28444476607

VL - 102

SP - 17472

EP - 17477

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 48

ER -