Progressive genome-wide introgression in agricultural Campylobacter coli

Samuel K. Sheppard, Xavier Didelot, Keith A. Jolley, Aaron E. Darling, Ben Pascoe, Guillaume Meric, David J. Kelly, Alison Cody, Frances M. Colles, Norval J. C. Strachan, Iain D. Ogden, Ken Forbes, Nigel P. French, Philip Carter, William G. Miller, Noel D. McCarthy, Robert Owen, Eva Litrup, Michael Egholm, Jason P. Affourtit & 4 others Stephen D. Bentley, Julian Parkhill, Martin C. J. Maiden, Daniel Falush

Research output: Contribution to journalArticle

67 Citations (Scopus)

Abstract

Hybridization between distantly related organisms can facilitate rapid adaptation to novel environments, but is potentially constrained by epistatic fitness interactions among cell components. The zoonotic pathogens Campylobacter coli and C. jejuni differ from each other by around 15% at the nucleotide level, corresponding to an average of nearly 40 amino acids per protein-coding gene. Using whole genome sequencing, we show that a single C. coli lineage, which has successfully colonized an agricultural niche, has been progressively accumulating C. jejuni DNA. Members of this lineage belong to two groups, the ST-828 and ST-1150 clonal complexes. The ST-1150 complex is less frequently isolated and has undergone a substantially greater amount of introgression leading to replacement of up to 23% of the C. coli core genome as well as import of novel DNA. By contrast, the more commonly isolated ST-828 complex bacteria have 10-11% introgressed DNA, and C. jejuni and nonagricultural C. coli lineages each have <2%. Thus, the C. coli that colonize agriculture, and consequently cause most human disease, have hybrid origin, but this cross-species exchange has so far not had a substantial impact on the gene pools of either C. jejuni or nonagricultural C. coli. These findings also indicate remarkable interchangeability of basic cellular machinery after a prolonged period of independent evolution.

Original languageEnglish
Pages (from-to)1051-1064
Number of pages14
JournalMolecular Ecology
Volume22
Issue number4
DOIs
Publication statusPublished - Feb 2013

Fingerprint

Campylobacter coli
introgression
genome
Genome
DNA
gene
machinery
import
niche
fitness
pathogen
amino acid
replacement
agriculture
Gene Pool
bacterium
protein
Campylobacter jejuni
Zoonoses
Cellular Structures

Keywords

  • Campylobacter coli
  • Campylobacter jejuni
  • DNA, Bacterial
  • Evolution, Molecular
  • Genome, Bacterial
  • Hybridization, Genetic
  • Likelihood Functions
  • Models, Genetic
  • Sequence Analysis, DNA

Cite this

Sheppard, S. K., Didelot, X., Jolley, K. A., Darling, A. E., Pascoe, B., Meric, G., ... Falush, D. (2013). Progressive genome-wide introgression in agricultural Campylobacter coli. Molecular Ecology, 22(4), 1051-1064. https://doi.org/10.1111/mec.12162

Progressive genome-wide introgression in agricultural Campylobacter coli. / Sheppard, Samuel K.; Didelot, Xavier; Jolley, Keith A.; Darling, Aaron E.; Pascoe, Ben; Meric, Guillaume; Kelly, David J.; Cody, Alison; Colles, Frances M.; Strachan, Norval J. C.; Ogden, Iain D.; Forbes, Ken; French, Nigel P.; Carter, Philip; Miller, William G.; McCarthy, Noel D.; Owen, Robert; Litrup, Eva; Egholm, Michael; Affourtit, Jason P.; Bentley, Stephen D.; Parkhill, Julian; Maiden, Martin C. J.; Falush, Daniel.

In: Molecular Ecology, Vol. 22, No. 4, 02.2013, p. 1051-1064.

Research output: Contribution to journalArticle

Sheppard, SK, Didelot, X, Jolley, KA, Darling, AE, Pascoe, B, Meric, G, Kelly, DJ, Cody, A, Colles, FM, Strachan, NJC, Ogden, ID, Forbes, K, French, NP, Carter, P, Miller, WG, McCarthy, ND, Owen, R, Litrup, E, Egholm, M, Affourtit, JP, Bentley, SD, Parkhill, J, Maiden, MCJ & Falush, D 2013, 'Progressive genome-wide introgression in agricultural Campylobacter coli', Molecular Ecology, vol. 22, no. 4, pp. 1051-1064. https://doi.org/10.1111/mec.12162
Sheppard, Samuel K. ; Didelot, Xavier ; Jolley, Keith A. ; Darling, Aaron E. ; Pascoe, Ben ; Meric, Guillaume ; Kelly, David J. ; Cody, Alison ; Colles, Frances M. ; Strachan, Norval J. C. ; Ogden, Iain D. ; Forbes, Ken ; French, Nigel P. ; Carter, Philip ; Miller, William G. ; McCarthy, Noel D. ; Owen, Robert ; Litrup, Eva ; Egholm, Michael ; Affourtit, Jason P. ; Bentley, Stephen D. ; Parkhill, Julian ; Maiden, Martin C. J. ; Falush, Daniel. / Progressive genome-wide introgression in agricultural Campylobacter coli. In: Molecular Ecology. 2013 ; Vol. 22, No. 4. pp. 1051-1064.
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AB - Hybridization between distantly related organisms can facilitate rapid adaptation to novel environments, but is potentially constrained by epistatic fitness interactions among cell components. The zoonotic pathogens Campylobacter coli and C. jejuni differ from each other by around 15% at the nucleotide level, corresponding to an average of nearly 40 amino acids per protein-coding gene. Using whole genome sequencing, we show that a single C. coli lineage, which has successfully colonized an agricultural niche, has been progressively accumulating C. jejuni DNA. Members of this lineage belong to two groups, the ST-828 and ST-1150 clonal complexes. The ST-1150 complex is less frequently isolated and has undergone a substantially greater amount of introgression leading to replacement of up to 23% of the C. coli core genome as well as import of novel DNA. By contrast, the more commonly isolated ST-828 complex bacteria have 10-11% introgressed DNA, and C. jejuni and nonagricultural C. coli lineages each have <2%. Thus, the C. coli that colonize agriculture, and consequently cause most human disease, have hybrid origin, but this cross-species exchange has so far not had a substantial impact on the gene pools of either C. jejuni or nonagricultural C. coli. These findings also indicate remarkable interchangeability of basic cellular machinery after a prolonged period of independent evolution.

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