Whole genome analysis reveals the diversity and evolutionary relationships between necrotic enteritis-causing strains of Clostridium perfringens

Jake A. Lacey, Theodore R. Allnutt, Ben Vezina, Thi Thu Hao Van, Thomas Stent, Xiaoyan Han, Julian I. Rood, Ben Wade, Anthony L. Keyburn, Torsten Seemann, Honglei Chen, Volker Haring, Priscilla A. Johanesen, Dena Lyras, Robert J. Moore

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Background: Clostridium perfringens causes a range of diseases in animals and humans including necrotic enteritis in chickens and food poisoning and gas gangrene in humans. Necrotic enteritis is of concern in commercial chicken production due to the cost of the implementation of infection control measures and to productivity losses. This study has focused on the genomic analysis of a range of chicken-derived C. perfringens isolates, from around the world and from different years. The genomes were sequenced and compared with 20 genomes available from public databases, which were from a diverse collection of isolates from chickens, other animals, and humans. We used a distance based phylogeny that was constructed based on gene content rather than sequence identity. Similarity between strains was defined as the number of genes that they have in common divided by their total number of genes. In this type of phylogenetic analysis, evolutionary distance can be interpreted in terms of evolutionary events such as acquisition and loss of genes, whereas the underlying properties (the gene content) can be interpreted in terms of function. We also compared these methods to the sequence-based phylogeny of the core genome. Results: Distinct pathogenic clades of necrotic enteritis-causing C. perfringens were identified. They were characterised by variable regions encoded on the chromosome, with predicted roles in capsule production, adhesion, inhibition of related strains, phage integration, and metabolism. Some strains have almost identical genomes, even though they were isolated from different geographic regions at various times, while other highly distant genomes appear to result in similar outcomes with regard to virulence and pathogenesis. Conclusions: The high level of diversity in chicken isolates suggests there is no reliable factor that defines a chicken strain of C. perfringens, however, disease-causing strains can be defined by the presence of netB-encoding plasmids. This study reveals that horizontal gene transfer appears to play a significant role in genetic variation of the C. perfringens chromosome as well as the plasmid content within strains.

Original languageEnglish
Article number379
Number of pages22
JournalBMC Genomics
Volume19
Issue number1
DOIs
Publication statusPublished - 22 May 2018

Keywords

  • Adhesion
  • Capsule
  • Clostridium perfringens
  • Genome
  • Necrotic enteritis
  • Pangenome
  • Prophage

Cite this

Lacey, Jake A. ; Allnutt, Theodore R. ; Vezina, Ben ; Van, Thi Thu Hao ; Stent, Thomas ; Han, Xiaoyan ; Rood, Julian I. ; Wade, Ben ; Keyburn, Anthony L. ; Seemann, Torsten ; Chen, Honglei ; Haring, Volker ; Johanesen, Priscilla A. ; Lyras, Dena ; Moore, Robert J. / Whole genome analysis reveals the diversity and evolutionary relationships between necrotic enteritis-causing strains of Clostridium perfringens. In: BMC Genomics. 2018 ; Vol. 19, No. 1.
@article{7db28e6658b94484bc61e21b96ed87cc,
title = "Whole genome analysis reveals the diversity and evolutionary relationships between necrotic enteritis-causing strains of Clostridium perfringens",
abstract = "Background: Clostridium perfringens causes a range of diseases in animals and humans including necrotic enteritis in chickens and food poisoning and gas gangrene in humans. Necrotic enteritis is of concern in commercial chicken production due to the cost of the implementation of infection control measures and to productivity losses. This study has focused on the genomic analysis of a range of chicken-derived C. perfringens isolates, from around the world and from different years. The genomes were sequenced and compared with 20 genomes available from public databases, which were from a diverse collection of isolates from chickens, other animals, and humans. We used a distance based phylogeny that was constructed based on gene content rather than sequence identity. Similarity between strains was defined as the number of genes that they have in common divided by their total number of genes. In this type of phylogenetic analysis, evolutionary distance can be interpreted in terms of evolutionary events such as acquisition and loss of genes, whereas the underlying properties (the gene content) can be interpreted in terms of function. We also compared these methods to the sequence-based phylogeny of the core genome. Results: Distinct pathogenic clades of necrotic enteritis-causing C. perfringens were identified. They were characterised by variable regions encoded on the chromosome, with predicted roles in capsule production, adhesion, inhibition of related strains, phage integration, and metabolism. Some strains have almost identical genomes, even though they were isolated from different geographic regions at various times, while other highly distant genomes appear to result in similar outcomes with regard to virulence and pathogenesis. Conclusions: The high level of diversity in chicken isolates suggests there is no reliable factor that defines a chicken strain of C. perfringens, however, disease-causing strains can be defined by the presence of netB-encoding plasmids. This study reveals that horizontal gene transfer appears to play a significant role in genetic variation of the C. perfringens chromosome as well as the plasmid content within strains.",
keywords = "Adhesion, Capsule, Clostridium perfringens, Genome, Necrotic enteritis, Pangenome, Prophage",
author = "Lacey, {Jake A.} and Allnutt, {Theodore R.} and Ben Vezina and Van, {Thi Thu Hao} and Thomas Stent and Xiaoyan Han and Rood, {Julian I.} and Ben Wade and Keyburn, {Anthony L.} and Torsten Seemann and Honglei Chen and Volker Haring and Johanesen, {Priscilla A.} and Dena Lyras and Moore, {Robert J.}",
year = "2018",
month = "5",
day = "22",
doi = "10.1186/s12864-018-4771-1",
language = "English",
volume = "19",
journal = "BMC Genomics",
issn = "1471-2164",
publisher = "BioMed Central",
number = "1",

}

Whole genome analysis reveals the diversity and evolutionary relationships between necrotic enteritis-causing strains of Clostridium perfringens. / Lacey, Jake A.; Allnutt, Theodore R.; Vezina, Ben; Van, Thi Thu Hao; Stent, Thomas; Han, Xiaoyan; Rood, Julian I.; Wade, Ben; Keyburn, Anthony L.; Seemann, Torsten; Chen, Honglei; Haring, Volker; Johanesen, Priscilla A.; Lyras, Dena; Moore, Robert J.

In: BMC Genomics, Vol. 19, No. 1, 379, 22.05.2018.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Whole genome analysis reveals the diversity and evolutionary relationships between necrotic enteritis-causing strains of Clostridium perfringens

AU - Lacey, Jake A.

AU - Allnutt, Theodore R.

AU - Vezina, Ben

AU - Van, Thi Thu Hao

AU - Stent, Thomas

AU - Han, Xiaoyan

AU - Rood, Julian I.

AU - Wade, Ben

AU - Keyburn, Anthony L.

AU - Seemann, Torsten

AU - Chen, Honglei

AU - Haring, Volker

AU - Johanesen, Priscilla A.

AU - Lyras, Dena

AU - Moore, Robert J.

PY - 2018/5/22

Y1 - 2018/5/22

N2 - Background: Clostridium perfringens causes a range of diseases in animals and humans including necrotic enteritis in chickens and food poisoning and gas gangrene in humans. Necrotic enteritis is of concern in commercial chicken production due to the cost of the implementation of infection control measures and to productivity losses. This study has focused on the genomic analysis of a range of chicken-derived C. perfringens isolates, from around the world and from different years. The genomes were sequenced and compared with 20 genomes available from public databases, which were from a diverse collection of isolates from chickens, other animals, and humans. We used a distance based phylogeny that was constructed based on gene content rather than sequence identity. Similarity between strains was defined as the number of genes that they have in common divided by their total number of genes. In this type of phylogenetic analysis, evolutionary distance can be interpreted in terms of evolutionary events such as acquisition and loss of genes, whereas the underlying properties (the gene content) can be interpreted in terms of function. We also compared these methods to the sequence-based phylogeny of the core genome. Results: Distinct pathogenic clades of necrotic enteritis-causing C. perfringens were identified. They were characterised by variable regions encoded on the chromosome, with predicted roles in capsule production, adhesion, inhibition of related strains, phage integration, and metabolism. Some strains have almost identical genomes, even though they were isolated from different geographic regions at various times, while other highly distant genomes appear to result in similar outcomes with regard to virulence and pathogenesis. Conclusions: The high level of diversity in chicken isolates suggests there is no reliable factor that defines a chicken strain of C. perfringens, however, disease-causing strains can be defined by the presence of netB-encoding plasmids. This study reveals that horizontal gene transfer appears to play a significant role in genetic variation of the C. perfringens chromosome as well as the plasmid content within strains.

AB - Background: Clostridium perfringens causes a range of diseases in animals and humans including necrotic enteritis in chickens and food poisoning and gas gangrene in humans. Necrotic enteritis is of concern in commercial chicken production due to the cost of the implementation of infection control measures and to productivity losses. This study has focused on the genomic analysis of a range of chicken-derived C. perfringens isolates, from around the world and from different years. The genomes were sequenced and compared with 20 genomes available from public databases, which were from a diverse collection of isolates from chickens, other animals, and humans. We used a distance based phylogeny that was constructed based on gene content rather than sequence identity. Similarity between strains was defined as the number of genes that they have in common divided by their total number of genes. In this type of phylogenetic analysis, evolutionary distance can be interpreted in terms of evolutionary events such as acquisition and loss of genes, whereas the underlying properties (the gene content) can be interpreted in terms of function. We also compared these methods to the sequence-based phylogeny of the core genome. Results: Distinct pathogenic clades of necrotic enteritis-causing C. perfringens were identified. They were characterised by variable regions encoded on the chromosome, with predicted roles in capsule production, adhesion, inhibition of related strains, phage integration, and metabolism. Some strains have almost identical genomes, even though they were isolated from different geographic regions at various times, while other highly distant genomes appear to result in similar outcomes with regard to virulence and pathogenesis. Conclusions: The high level of diversity in chicken isolates suggests there is no reliable factor that defines a chicken strain of C. perfringens, however, disease-causing strains can be defined by the presence of netB-encoding plasmids. This study reveals that horizontal gene transfer appears to play a significant role in genetic variation of the C. perfringens chromosome as well as the plasmid content within strains.

KW - Adhesion

KW - Capsule

KW - Clostridium perfringens

KW - Genome

KW - Necrotic enteritis

KW - Pangenome

KW - Prophage

UR - http://www.scopus.com/inward/record.url?scp=85047463408&partnerID=8YFLogxK

U2 - 10.1186/s12864-018-4771-1

DO - 10.1186/s12864-018-4771-1

M3 - Article

VL - 19

JO - BMC Genomics

JF - BMC Genomics

SN - 1471-2164

IS - 1

M1 - 379

ER -