Evolution of an agriculture-associated disease causing Campylobacter coli clade: evidence from national surveillance data in Scotland.

The common zoonotic pathogen Campylobacter coli is an important cause of bacterial gastroenteritis worldwide but its evolution is incompletely understood. Using multilocus sequence type (MLST) data of 7 housekeeping genes from a national survey of Campylobacter in Scotland (2005/6), and a combined p...

Full description

Saved in:
Bibliographic Details
Main Authors: Samuel K Sheppard, John F Dallas, Daniel J Wilson, Norval J C Strachan, Noel D McCarthy, Keith A Jolley, Frances M Colles, Ovidiu Rotariu, Iain D Ogden, Ken J Forbes, Martin C J Maiden
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2010-12-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0015708&type=printable
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849695058839732224
author Samuel K Sheppard
John F Dallas
Daniel J Wilson
Norval J C Strachan
Noel D McCarthy
Keith A Jolley
Frances M Colles
Ovidiu Rotariu
Iain D Ogden
Ken J Forbes
Martin C J Maiden
author_facet Samuel K Sheppard
John F Dallas
Daniel J Wilson
Norval J C Strachan
Noel D McCarthy
Keith A Jolley
Frances M Colles
Ovidiu Rotariu
Iain D Ogden
Ken J Forbes
Martin C J Maiden
author_sort Samuel K Sheppard
collection DOAJ
description The common zoonotic pathogen Campylobacter coli is an important cause of bacterial gastroenteritis worldwide but its evolution is incompletely understood. Using multilocus sequence type (MLST) data of 7 housekeeping genes from a national survey of Campylobacter in Scotland (2005/6), and a combined population genetic-phylogenetics approach, we investigated the evolutionary history of C. coli. Genealogical reconstruction of isolates from clinical infection, farm animals and the environment, revealed a three-clade genetic structure. The majority of farm animal, and all disease causing genotypes belonged to a single clade (clade 1) which had comparatively low synonymous sequence diversity, little deep branching genetic structure, and a higher number of shared alleles providing evidence of recent clonal decent. Calibration of the rate of molecular evolution, based on within-species genetic variation, estimated a more rapid rate of evolution than in traditional estimates. This placed the divergence of the clades at less than 2500 years ago, consistent with the introduction of an agricultural niche having had an effect upon the evolution of the C. coli clades. Attribution of clinical isolate genotypes to source, using an asymmetric island model, confirmed that strains from chicken and ruminants, and not pigs or turkeys, are the principal source of human C. coli infection. Taken together these analyses are consistent with an evolutionary scenario describing the emergence of agriculture-associated C. coli lineage that is an important human pathogen.
format Article
id doaj-art-65e152b577c24eb0adde0c77089e93a6
institution DOAJ
issn 1932-6203
language English
publishDate 2010-12-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj-art-65e152b577c24eb0adde0c77089e93a62025-08-20T03:19:53ZengPublic Library of Science (PLoS)PLoS ONE1932-62032010-12-01512e1570810.1371/journal.pone.0015708Evolution of an agriculture-associated disease causing Campylobacter coli clade: evidence from national surveillance data in Scotland.Samuel K SheppardJohn F DallasDaniel J WilsonNorval J C StrachanNoel D McCarthyKeith A JolleyFrances M CollesOvidiu RotariuIain D OgdenKen J ForbesMartin C J MaidenThe common zoonotic pathogen Campylobacter coli is an important cause of bacterial gastroenteritis worldwide but its evolution is incompletely understood. Using multilocus sequence type (MLST) data of 7 housekeeping genes from a national survey of Campylobacter in Scotland (2005/6), and a combined population genetic-phylogenetics approach, we investigated the evolutionary history of C. coli. Genealogical reconstruction of isolates from clinical infection, farm animals and the environment, revealed a three-clade genetic structure. The majority of farm animal, and all disease causing genotypes belonged to a single clade (clade 1) which had comparatively low synonymous sequence diversity, little deep branching genetic structure, and a higher number of shared alleles providing evidence of recent clonal decent. Calibration of the rate of molecular evolution, based on within-species genetic variation, estimated a more rapid rate of evolution than in traditional estimates. This placed the divergence of the clades at less than 2500 years ago, consistent with the introduction of an agricultural niche having had an effect upon the evolution of the C. coli clades. Attribution of clinical isolate genotypes to source, using an asymmetric island model, confirmed that strains from chicken and ruminants, and not pigs or turkeys, are the principal source of human C. coli infection. Taken together these analyses are consistent with an evolutionary scenario describing the emergence of agriculture-associated C. coli lineage that is an important human pathogen.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0015708&type=printable
spellingShingle Samuel K Sheppard
John F Dallas
Daniel J Wilson
Norval J C Strachan
Noel D McCarthy
Keith A Jolley
Frances M Colles
Ovidiu Rotariu
Iain D Ogden
Ken J Forbes
Martin C J Maiden
Evolution of an agriculture-associated disease causing Campylobacter coli clade: evidence from national surveillance data in Scotland.
PLoS ONE
title Evolution of an agriculture-associated disease causing Campylobacter coli clade: evidence from national surveillance data in Scotland.
title_full Evolution of an agriculture-associated disease causing Campylobacter coli clade: evidence from national surveillance data in Scotland.
title_fullStr Evolution of an agriculture-associated disease causing Campylobacter coli clade: evidence from national surveillance data in Scotland.
title_full_unstemmed Evolution of an agriculture-associated disease causing Campylobacter coli clade: evidence from national surveillance data in Scotland.
title_short Evolution of an agriculture-associated disease causing Campylobacter coli clade: evidence from national surveillance data in Scotland.
title_sort evolution of an agriculture associated disease causing campylobacter coli clade evidence from national surveillance data in scotland
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0015708&type=printable
work_keys_str_mv AT samuelksheppard evolutionofanagricultureassociateddiseasecausingcampylobactercolicladeevidencefromnationalsurveillancedatainscotland
AT johnfdallas evolutionofanagricultureassociateddiseasecausingcampylobactercolicladeevidencefromnationalsurveillancedatainscotland
AT danieljwilson evolutionofanagricultureassociateddiseasecausingcampylobactercolicladeevidencefromnationalsurveillancedatainscotland
AT norvaljcstrachan evolutionofanagricultureassociateddiseasecausingcampylobactercolicladeevidencefromnationalsurveillancedatainscotland
AT noeldmccarthy evolutionofanagricultureassociateddiseasecausingcampylobactercolicladeevidencefromnationalsurveillancedatainscotland
AT keithajolley evolutionofanagricultureassociateddiseasecausingcampylobactercolicladeevidencefromnationalsurveillancedatainscotland
AT francesmcolles evolutionofanagricultureassociateddiseasecausingcampylobactercolicladeevidencefromnationalsurveillancedatainscotland
AT ovidiurotariu evolutionofanagricultureassociateddiseasecausingcampylobactercolicladeevidencefromnationalsurveillancedatainscotland
AT iaindogden evolutionofanagricultureassociateddiseasecausingcampylobactercolicladeevidencefromnationalsurveillancedatainscotland
AT kenjforbes evolutionofanagricultureassociateddiseasecausingcampylobactercolicladeevidencefromnationalsurveillancedatainscotland
AT martincjmaiden evolutionofanagricultureassociateddiseasecausingcampylobactercolicladeevidencefromnationalsurveillancedatainscotland