Genomic analysis of Clostridium perfringens BEC/CPILE-positive, toxinotype D and e strains isolated from healthy children

Raymond Kiu; Kathleen Sim; Alex Shaw; Emma Cornwell; Derek Pickard; J. Simon Kroll; Lindsay J. Hall

doi:10.3390/toxins11090543

Genomic analysis of Clostridium perfringens BEC/CPILE-positive, toxinotype D and e strains isolated from healthy children

Raymond Kiu
, Kathleen Sim
, Alex Shaw
, Emma Cornwell
, Derek Pickard
, J. Simon Kroll
, Lindsay J. Hall^*

^*Corresponding author for this work

Microbes, Infection and Microbiomes

Research output: Contribution to journal › Article › peer-review

8 Citations (Scopus)

40 Downloads (Pure)

Abstract

Clostridium perfringens toxinotype D, toxinotype E, and gastroenteritis-linked BEC/CPILE-positive strains have never been reported in healthy children. We isolated, whole-genome sequenced and bioinformatically characterised three C. perfringens isolates-type D (IQ1), type E (IQ2) and BEC/CPILE-positive (IQ3), recovered from the stools of three healthy two-year-olds, which were further compared to 128 C. perfringens genomes available from NCBI. The analysis uncovered a previously under-described putative toxin gene alv (alveolysin) encoded by isolates IQ2 and IQ3, which appeared to be a clade-specific trait associated with strains from domestic animals. A plasmid analysis indicated that the iota-toxin was encoded on a near-intact previously described plasmid pCPPB-1 in type E strain IQ2. The BEC genes becA and becB were carried on a near-identical pCPOS-1 plasmid previously associated with Japanese gastroenteritis outbreaks. Furthermore, a close phylogenetic relatedness was inferred between the French C. perfringens type E isolates cp515.17 and newly sequenced IQ2, suggesting geographical links. This study describes novel C. perfringens isolates from healthy individuals which encode important toxin genes, indicating the potential spread of these veterinary and clinically important strains and mobile genetic elements, and highlights areas for future research.

Original language	English
Article number	543
Number of pages	14
Journal	Toxins
Volume	11
Issue number	9
DOIs	https://doi.org/10.3390/toxins11090543
Publication status	Published - 19 Sept 2019

Bibliographical note

Funding: This work was supported by a Wellcome Trust Investigator Award (100974/C/13/Z), and the Biotechnology and Biological Sciences Research Council (BBSRC); Institute Strategic Programme Gut Microbes and Health BB/R012490/1, and its constituent project(s) BBS/E/F/000PR10353 and BBS/E/F/000PR10356 to Lindsay J Hall; and by funding from the Winnicott Foundation and the National Institute for Health Research (NIHR) Biomedical Research Centre based at Imperial Healthcare National Health Service (NHS) Trust and Imperial College London (to J. Simon Kroll). Kathleen Sim was funded during this work by an NIHR Doctoral Research Fellowship [NIHR-DRF-2011-04-128]. This article presents independent research funded by the NIHR. The views expressed are those of the authors and not necessarily those of the NHS, NIHR, the Department of Health or other funders.

Acknowledgments: This research was supported in part by the NBI Computing infrastructure for Science (CiS) group through the provision of a High-Performance Computing (HPC) Cluster. We thank Shabhonam Caim for his computational assistance. We also thank the sequencing team at Wellcome Trust Sanger Institute for the sequencing work.

Publisher Copyright:
© 2019 by the authors.

Keywords

Binary toxins
Clostridium perfringens
Epsilon toxin
Genome analysis
Infants
Iota toxin
Whole genome sequencing

ASJC Scopus subject areas

Toxicology
Health, Toxicology and Mutagenesis

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Cite this

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title = "Genomic analysis of Clostridium perfringens BEC/CPILE-positive, toxinotype D and e strains isolated from healthy children",

abstract = "Clostridium perfringens toxinotype D, toxinotype E, and gastroenteritis-linked BEC/CPILE-positive strains have never been reported in healthy children. We isolated, whole-genome sequenced and bioinformatically characterised three C. perfringens isolates-type D (IQ1), type E (IQ2) and BEC/CPILE-positive (IQ3), recovered from the stools of three healthy two-year-olds, which were further compared to 128 C. perfringens genomes available from NCBI. The analysis uncovered a previously under-described putative toxin gene alv (alveolysin) encoded by isolates IQ2 and IQ3, which appeared to be a clade-specific trait associated with strains from domestic animals. A plasmid analysis indicated that the iota-toxin was encoded on a near-intact previously described plasmid pCPPB-1 in type E strain IQ2. The BEC genes becA and becB were carried on a near-identical pCPOS-1 plasmid previously associated with Japanese gastroenteritis outbreaks. Furthermore, a close phylogenetic relatedness was inferred between the French C. perfringens type E isolates cp515.17 and newly sequenced IQ2, suggesting geographical links. This study describes novel C. perfringens isolates from healthy individuals which encode important toxin genes, indicating the potential spread of these veterinary and clinically important strains and mobile genetic elements, and highlights areas for future research.",

keywords = "Binary toxins, Clostridium perfringens, Epsilon toxin, Genome analysis, Infants, Iota toxin, Whole genome sequencing",

author = "Raymond Kiu and Kathleen Sim and Alex Shaw and Emma Cornwell and Derek Pickard and Kroll, \{J. Simon\} and Hall, \{Lindsay J.\}",

note = "Funding: This work was supported by a Wellcome Trust Investigator Award (100974/C/13/Z), and the Biotechnology and Biological Sciences Research Council (BBSRC); Institute Strategic Programme Gut Microbes and Health BB/R012490/1, and its constituent project(s) BBS/E/F/000PR10353 and BBS/E/F/000PR10356 to Lindsay J Hall; and by funding from the Winnicott Foundation and the National Institute for Health Research (NIHR) Biomedical Research Centre based at Imperial Healthcare National Health Service (NHS) Trust and Imperial College London (to J. Simon Kroll). Kathleen Sim was funded during this work by an NIHR Doctoral Research Fellowship [NIHR-DRF-2011-04-128]. This article presents independent research funded by the NIHR. The views expressed are those of the authors and not necessarily those of the NHS, NIHR, the Department of Health or other funders. Acknowledgments: This research was supported in part by the NBI Computing infrastructure for Science (CiS) group through the provision of a High-Performance Computing (HPC) Cluster. We thank Shabhonam Caim for his computational assistance. We also thank the sequencing team at Wellcome Trust Sanger Institute for the sequencing work. Publisher Copyright: {\textcopyright} 2019 by the authors.",

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doi = "10.3390/toxins11090543",

language = "English",

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T1 - Genomic analysis of Clostridium perfringens BEC/CPILE-positive, toxinotype D and e strains isolated from healthy children

AU - Kiu, Raymond

AU - Sim, Kathleen

AU - Shaw, Alex

AU - Cornwell, Emma

AU - Pickard, Derek

AU - Kroll, J. Simon

AU - Hall, Lindsay J.

N1 - Funding: This work was supported by a Wellcome Trust Investigator Award (100974/C/13/Z), and the Biotechnology and Biological Sciences Research Council (BBSRC); Institute Strategic Programme Gut Microbes and Health BB/R012490/1, and its constituent project(s) BBS/E/F/000PR10353 and BBS/E/F/000PR10356 to Lindsay J Hall; and by funding from the Winnicott Foundation and the National Institute for Health Research (NIHR) Biomedical Research Centre based at Imperial Healthcare National Health Service (NHS) Trust and Imperial College London (to J. Simon Kroll). Kathleen Sim was funded during this work by an NIHR Doctoral Research Fellowship [NIHR-DRF-2011-04-128]. This article presents independent research funded by the NIHR. The views expressed are those of the authors and not necessarily those of the NHS, NIHR, the Department of Health or other funders. Acknowledgments: This research was supported in part by the NBI Computing infrastructure for Science (CiS) group through the provision of a High-Performance Computing (HPC) Cluster. We thank Shabhonam Caim for his computational assistance. We also thank the sequencing team at Wellcome Trust Sanger Institute for the sequencing work. Publisher Copyright: © 2019 by the authors.

PY - 2019/9/19

Y1 - 2019/9/19

N2 - Clostridium perfringens toxinotype D, toxinotype E, and gastroenteritis-linked BEC/CPILE-positive strains have never been reported in healthy children. We isolated, whole-genome sequenced and bioinformatically characterised three C. perfringens isolates-type D (IQ1), type E (IQ2) and BEC/CPILE-positive (IQ3), recovered from the stools of three healthy two-year-olds, which were further compared to 128 C. perfringens genomes available from NCBI. The analysis uncovered a previously under-described putative toxin gene alv (alveolysin) encoded by isolates IQ2 and IQ3, which appeared to be a clade-specific trait associated with strains from domestic animals. A plasmid analysis indicated that the iota-toxin was encoded on a near-intact previously described plasmid pCPPB-1 in type E strain IQ2. The BEC genes becA and becB were carried on a near-identical pCPOS-1 plasmid previously associated with Japanese gastroenteritis outbreaks. Furthermore, a close phylogenetic relatedness was inferred between the French C. perfringens type E isolates cp515.17 and newly sequenced IQ2, suggesting geographical links. This study describes novel C. perfringens isolates from healthy individuals which encode important toxin genes, indicating the potential spread of these veterinary and clinically important strains and mobile genetic elements, and highlights areas for future research.

AB - Clostridium perfringens toxinotype D, toxinotype E, and gastroenteritis-linked BEC/CPILE-positive strains have never been reported in healthy children. We isolated, whole-genome sequenced and bioinformatically characterised three C. perfringens isolates-type D (IQ1), type E (IQ2) and BEC/CPILE-positive (IQ3), recovered from the stools of three healthy two-year-olds, which were further compared to 128 C. perfringens genomes available from NCBI. The analysis uncovered a previously under-described putative toxin gene alv (alveolysin) encoded by isolates IQ2 and IQ3, which appeared to be a clade-specific trait associated with strains from domestic animals. A plasmid analysis indicated that the iota-toxin was encoded on a near-intact previously described plasmid pCPPB-1 in type E strain IQ2. The BEC genes becA and becB were carried on a near-identical pCPOS-1 plasmid previously associated with Japanese gastroenteritis outbreaks. Furthermore, a close phylogenetic relatedness was inferred between the French C. perfringens type E isolates cp515.17 and newly sequenced IQ2, suggesting geographical links. This study describes novel C. perfringens isolates from healthy individuals which encode important toxin genes, indicating the potential spread of these veterinary and clinically important strains and mobile genetic elements, and highlights areas for future research.

KW - Binary toxins

KW - Clostridium perfringens

KW - Epsilon toxin

KW - Genome analysis

KW - Infants

KW - Iota toxin

KW - Whole genome sequencing

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DO - 10.3390/toxins11090543

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C2 - 31546794

AN - SCOPUS:85072584646

SN - 2072-6651

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JO - Toxins

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ER -

Genomic analysis of Clostridium perfringens BEC/CPILE-positive, toxinotype D and e strains isolated from healthy children

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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