Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome.

<h4>Background</h4>The complex microbiome of the ceca of chickens plays an important role in nutrient utilization, growth and well-being of these animals. Since we have a very limited understanding of the capabilities of most species present in the cecum, we investigated the role of the...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Ani Qu, Jennifer M Brulc, Melissa K Wilson, Bibiana F Law, James R Theoret, Lynn A Joens, Michael E Konkel, Florent Angly, Elizabeth A Dinsdale, Robert A Edwards, Karen E Nelson, Bryan A White
Formato: article
Lenguaje:EN
Publicado: Public Library of Science (PLoS) 2008
Materias:
R
Q
Acceso en línea:https://doaj.org/article/e830cc85acce49a0ab6648559c5f5090
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:e830cc85acce49a0ab6648559c5f5090
record_format dspace
spelling oai:doaj.org-article:e830cc85acce49a0ab6648559c5f50902021-11-25T06:11:13ZComparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome.1932-620310.1371/journal.pone.0002945https://doaj.org/article/e830cc85acce49a0ab6648559c5f50902008-08-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/18698407/?tool=EBIhttps://doaj.org/toc/1932-6203<h4>Background</h4>The complex microbiome of the ceca of chickens plays an important role in nutrient utilization, growth and well-being of these animals. Since we have a very limited understanding of the capabilities of most species present in the cecum, we investigated the role of the microbiome by comparative analyses of both the microbial community structure and functional gene content using random sample pyrosequencing. The overall goal of this study was to characterize the chicken cecal microbiome using a pathogen-free chicken and one that had been challenged with Campylobacter jejuni.<h4>Methodology/principal findings</h4>Comparative metagenomic pyrosequencing was used to generate 55,364,266 bases of random sampled pyrosequence data from two chicken cecal samples. SSU rDNA gene tags and environmental gene tags (EGTs) were identified using SEED subsystems-based annotations. The distribution of phylotypes and EGTs detected within each cecal sample were primarily from the Firmicutes, Bacteroidetes and Proteobacteria, consistent with previous SSU rDNA libraries of the chicken cecum. Carbohydrate metabolism and virulence genes are major components of the EGT content of both of these microbiomes. A comparison of the twelve major pathways in the SEED Virulence Subsystem (metavirulome) represented in the chicken cecum, mouse cecum and human fecal microbiomes showed that the metavirulomes differed between these microbiomes and the metavirulomes clustered by host environment. The chicken cecum microbiomes had the broadest range of EGTs within the SEED Conjugative Transposon Subsystem, however the mouse cecum microbiomes showed a greater abundance of EGTs in this subsystem. Gene assemblies (32 contigs) from one microbiome sample were predominately from the Bacteroidetes, and seven of these showed sequence similarity to transposases, whereas the remaining sequences were most similar to those from catabolic gene families.<h4>Conclusion/significance</h4>This analysis has demonstrated that mobile DNA elements are a major functional component of cecal microbiomes, thus contributing to horizontal gene transfer and functional microbiome evolution. Moreover, the metavirulomes of these microbiomes appear to associate by host environment. These data have implications for defining core and variable microbiome content in a host species. Furthermore, this suggests that the evolution of host specific metavirulomes is a contributing factor in disease resistance to zoonotic pathogens.Ani QuJennifer M BrulcMelissa K WilsonBibiana F LawJames R TheoretLynn A JoensMichael E KonkelFlorent AnglyElizabeth A DinsdaleRobert A EdwardsKaren E NelsonBryan A WhitePublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 3, Iss 8, p e2945 (2008)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Ani Qu
Jennifer M Brulc
Melissa K Wilson
Bibiana F Law
James R Theoret
Lynn A Joens
Michael E Konkel
Florent Angly
Elizabeth A Dinsdale
Robert A Edwards
Karen E Nelson
Bryan A White
Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome.
description <h4>Background</h4>The complex microbiome of the ceca of chickens plays an important role in nutrient utilization, growth and well-being of these animals. Since we have a very limited understanding of the capabilities of most species present in the cecum, we investigated the role of the microbiome by comparative analyses of both the microbial community structure and functional gene content using random sample pyrosequencing. The overall goal of this study was to characterize the chicken cecal microbiome using a pathogen-free chicken and one that had been challenged with Campylobacter jejuni.<h4>Methodology/principal findings</h4>Comparative metagenomic pyrosequencing was used to generate 55,364,266 bases of random sampled pyrosequence data from two chicken cecal samples. SSU rDNA gene tags and environmental gene tags (EGTs) were identified using SEED subsystems-based annotations. The distribution of phylotypes and EGTs detected within each cecal sample were primarily from the Firmicutes, Bacteroidetes and Proteobacteria, consistent with previous SSU rDNA libraries of the chicken cecum. Carbohydrate metabolism and virulence genes are major components of the EGT content of both of these microbiomes. A comparison of the twelve major pathways in the SEED Virulence Subsystem (metavirulome) represented in the chicken cecum, mouse cecum and human fecal microbiomes showed that the metavirulomes differed between these microbiomes and the metavirulomes clustered by host environment. The chicken cecum microbiomes had the broadest range of EGTs within the SEED Conjugative Transposon Subsystem, however the mouse cecum microbiomes showed a greater abundance of EGTs in this subsystem. Gene assemblies (32 contigs) from one microbiome sample were predominately from the Bacteroidetes, and seven of these showed sequence similarity to transposases, whereas the remaining sequences were most similar to those from catabolic gene families.<h4>Conclusion/significance</h4>This analysis has demonstrated that mobile DNA elements are a major functional component of cecal microbiomes, thus contributing to horizontal gene transfer and functional microbiome evolution. Moreover, the metavirulomes of these microbiomes appear to associate by host environment. These data have implications for defining core and variable microbiome content in a host species. Furthermore, this suggests that the evolution of host specific metavirulomes is a contributing factor in disease resistance to zoonotic pathogens.
format article
author Ani Qu
Jennifer M Brulc
Melissa K Wilson
Bibiana F Law
James R Theoret
Lynn A Joens
Michael E Konkel
Florent Angly
Elizabeth A Dinsdale
Robert A Edwards
Karen E Nelson
Bryan A White
author_facet Ani Qu
Jennifer M Brulc
Melissa K Wilson
Bibiana F Law
James R Theoret
Lynn A Joens
Michael E Konkel
Florent Angly
Elizabeth A Dinsdale
Robert A Edwards
Karen E Nelson
Bryan A White
author_sort Ani Qu
title Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome.
title_short Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome.
title_full Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome.
title_fullStr Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome.
title_full_unstemmed Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome.
title_sort comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome.
publisher Public Library of Science (PLoS)
publishDate 2008
url https://doaj.org/article/e830cc85acce49a0ab6648559c5f5090
work_keys_str_mv AT aniqu comparativemetagenomicsrevealshostspecificmetavirulomesandhorizontalgenetransferelementsinthechickencecummicrobiome
AT jennifermbrulc comparativemetagenomicsrevealshostspecificmetavirulomesandhorizontalgenetransferelementsinthechickencecummicrobiome
AT melissakwilson comparativemetagenomicsrevealshostspecificmetavirulomesandhorizontalgenetransferelementsinthechickencecummicrobiome
AT bibianaflaw comparativemetagenomicsrevealshostspecificmetavirulomesandhorizontalgenetransferelementsinthechickencecummicrobiome
AT jamesrtheoret comparativemetagenomicsrevealshostspecificmetavirulomesandhorizontalgenetransferelementsinthechickencecummicrobiome
AT lynnajoens comparativemetagenomicsrevealshostspecificmetavirulomesandhorizontalgenetransferelementsinthechickencecummicrobiome
AT michaelekonkel comparativemetagenomicsrevealshostspecificmetavirulomesandhorizontalgenetransferelementsinthechickencecummicrobiome
AT florentangly comparativemetagenomicsrevealshostspecificmetavirulomesandhorizontalgenetransferelementsinthechickencecummicrobiome
AT elizabethadinsdale comparativemetagenomicsrevealshostspecificmetavirulomesandhorizontalgenetransferelementsinthechickencecummicrobiome
AT robertaedwards comparativemetagenomicsrevealshostspecificmetavirulomesandhorizontalgenetransferelementsinthechickencecummicrobiome
AT karenenelson comparativemetagenomicsrevealshostspecificmetavirulomesandhorizontalgenetransferelementsinthechickencecummicrobiome
AT bryanawhite comparativemetagenomicsrevealshostspecificmetavirulomesandhorizontalgenetransferelementsinthechickencecummicrobiome
_version_ 1718414077672292352