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

Ani Qu, Jennifer M. Brulc, Melissa K. Wilson, Bibiana Law, James R. Theoret, Lynn A. Joens, Michael E. Konkel, Florent Angly, Elizabeth A. Dinsdale, Robert A. Edwards, Karen E. Nelson, Bryan A. White

Research output: Contribution to journalArticle

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Abstract

Background: 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 Compylobacter jejuni. Methodology/Principal Findings: 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. Conclusion/Significance: 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.

Original languageEnglish (US)
Article numbere2945
JournalPLoS One
Volume3
Issue number8
DOIs
StatePublished - Aug 13 2008

Fingerprint

Gene transfer
Metagenomics
Horizontal Gene Transfer
Cecum
Microbiota
cecum
Chickens
Genes
chickens
genes
Bacteroidetes
Pathogens
Ribosomal DNA
horizontal gene transfer
microbiome
Virulence
Transposases
virulence
Gene Components
animal well-being

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome. / Qu, Ani; Brulc, Jennifer M.; Wilson, Melissa K.; Law, Bibiana; Theoret, James R.; Joens, Lynn A.; Konkel, Michael E.; Angly, Florent; Dinsdale, Elizabeth A.; Edwards, Robert A.; Nelson, Karen E.; White, Bryan A.

In: PLoS One, Vol. 3, No. 8, e2945, 13.08.2008.

Research output: Contribution to journalArticle

Qu, A, Brulc, JM, Wilson, MK, Law, B, Theoret, JR, Joens, LA, Konkel, ME, Angly, F, Dinsdale, EA, Edwards, RA, Nelson, KE & White, BA 2008, 'Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome', PLoS One, vol. 3, no. 8, e2945. https://doi.org/10.1371/journal.pone.0002945
Qu, Ani ; Brulc, Jennifer M. ; Wilson, Melissa K. ; Law, Bibiana ; Theoret, James R. ; Joens, Lynn A. ; Konkel, Michael E. ; Angly, Florent ; Dinsdale, Elizabeth A. ; Edwards, Robert A. ; Nelson, Karen E. ; White, Bryan A. / Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome. In: PLoS One. 2008 ; Vol. 3, No. 8.
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