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 co...

Full description

Bibliographic Details
Main Authors: 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
Format: Article
Language:English
Published: BMC 2018-05-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-018-4771-1
id doaj-976ad5caf5ff45bf9c49a21ce2b77595
record_format Article
collection DOAJ
language English
format Article
sources DOAJ
author 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
spellingShingle 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
Whole genome analysis reveals the diversity and evolutionary relationships between necrotic enteritis-causing strains of Clostridium perfringens
BMC Genomics
Clostridium perfringens
Necrotic enteritis
Capsule
Adhesion
Prophage
Genome
author_facet 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
author_sort Jake A. Lacey
title Whole genome analysis reveals the diversity and evolutionary relationships between necrotic enteritis-causing strains of Clostridium perfringens
title_short Whole genome analysis reveals the diversity and evolutionary relationships between necrotic enteritis-causing strains of Clostridium perfringens
title_full Whole genome analysis reveals the diversity and evolutionary relationships between necrotic enteritis-causing strains of Clostridium perfringens
title_fullStr Whole genome analysis reveals the diversity and evolutionary relationships between necrotic enteritis-causing strains of Clostridium perfringens
title_full_unstemmed Whole genome analysis reveals the diversity and evolutionary relationships between necrotic enteritis-causing strains of Clostridium perfringens
title_sort whole genome analysis reveals the diversity and evolutionary relationships between necrotic enteritis-causing strains of clostridium perfringens
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2018-05-01
description 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.
topic Clostridium perfringens
Necrotic enteritis
Capsule
Adhesion
Prophage
Genome
url http://link.springer.com/article/10.1186/s12864-018-4771-1
work_keys_str_mv AT jakealacey wholegenomeanalysisrevealsthediversityandevolutionaryrelationshipsbetweennecroticenteritiscausingstrainsofclostridiumperfringens
AT theodorerallnutt wholegenomeanalysisrevealsthediversityandevolutionaryrelationshipsbetweennecroticenteritiscausingstrainsofclostridiumperfringens
AT benvezina wholegenomeanalysisrevealsthediversityandevolutionaryrelationshipsbetweennecroticenteritiscausingstrainsofclostridiumperfringens
AT thithuhaovan wholegenomeanalysisrevealsthediversityandevolutionaryrelationshipsbetweennecroticenteritiscausingstrainsofclostridiumperfringens
AT thomasstent wholegenomeanalysisrevealsthediversityandevolutionaryrelationshipsbetweennecroticenteritiscausingstrainsofclostridiumperfringens
AT xiaoyanhan wholegenomeanalysisrevealsthediversityandevolutionaryrelationshipsbetweennecroticenteritiscausingstrainsofclostridiumperfringens
AT julianirood wholegenomeanalysisrevealsthediversityandevolutionaryrelationshipsbetweennecroticenteritiscausingstrainsofclostridiumperfringens
AT benwade wholegenomeanalysisrevealsthediversityandevolutionaryrelationshipsbetweennecroticenteritiscausingstrainsofclostridiumperfringens
AT anthonylkeyburn wholegenomeanalysisrevealsthediversityandevolutionaryrelationshipsbetweennecroticenteritiscausingstrainsofclostridiumperfringens
AT torstenseemann wholegenomeanalysisrevealsthediversityandevolutionaryrelationshipsbetweennecroticenteritiscausingstrainsofclostridiumperfringens
AT hongleichen wholegenomeanalysisrevealsthediversityandevolutionaryrelationshipsbetweennecroticenteritiscausingstrainsofclostridiumperfringens
AT volkerharing wholegenomeanalysisrevealsthediversityandevolutionaryrelationshipsbetweennecroticenteritiscausingstrainsofclostridiumperfringens
AT priscillaajohanesen wholegenomeanalysisrevealsthediversityandevolutionaryrelationshipsbetweennecroticenteritiscausingstrainsofclostridiumperfringens
AT denalyras wholegenomeanalysisrevealsthediversityandevolutionaryrelationshipsbetweennecroticenteritiscausingstrainsofclostridiumperfringens
AT robertjmoore wholegenomeanalysisrevealsthediversityandevolutionaryrelationshipsbetweennecroticenteritiscausingstrainsofclostridiumperfringens
_version_ 1725355990992289792
spelling doaj-976ad5caf5ff45bf9c49a21ce2b775952020-11-25T00:23:37ZengBMCBMC Genomics1471-21642018-05-0119112210.1186/s12864-018-4771-1Whole genome analysis reveals the diversity and evolutionary relationships between necrotic enteritis-causing strains of Clostridium perfringensJake A. Lacey0Theodore R. Allnutt1Ben Vezina2Thi Thu Hao Van3Thomas Stent4Xiaoyan Han5Julian I. Rood6Ben Wade7Anthony L. Keyburn8Torsten Seemann9Honglei Chen10Volker Haring11Priscilla A. Johanesen12Dena Lyras13Robert J. Moore14Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash UniversityCSIRO Biosecurity Flagship, Australian Animal Health LaboratoryInfection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash UniversityPoultry Cooperative Research Centre, University of New EnglandInfection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash UniversityInfection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash UniversityInfection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash UniversityCSIRO Biosecurity Flagship, Australian Animal Health LaboratoryCSIRO Biosecurity Flagship, Australian Animal Health LaboratoryInfection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash UniversityCSIRO Biosecurity Flagship, Australian Animal Health LaboratoryCSIRO Biosecurity Flagship, Australian Animal Health LaboratoryInfection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash UniversityInfection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash UniversityInfection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash UniversityAbstract 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.http://link.springer.com/article/10.1186/s12864-018-4771-1Clostridium perfringensNecrotic enteritisCapsuleAdhesionProphageGenome