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Comprehensive Longitudinal Microbiome Analysis of the Chicken Cecum Reveals a Shift From Competitive to Environmental Drivers and a Window of Opportunity for Campylobacter

Chickens are a key food source for humans yet their microbiome contains bacteria that can be pathogenic to humans, and indeed potentially to chickens themselves. Campylobacter is present within the chicken gut and is the leading cause of bacterial foodborne gastroenteritis within humans worldwide. I...

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Autores principales: Ijaz, Umer Zeeshan, Sivaloganathan, Lojika, McKenna, Aaron, Richmond, Anne, Kelly, Carmel, Linton, Mark, Stratakos, Alexandros Ch., Lavery, Ursula, Elmi, Abdi, Wren, Brendan W., Dorrell, Nick, Corcionivoschi, Nicolae, Gundogdu, Ozan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6196313/
https://www.ncbi.nlm.nih.gov/pubmed/30374341
http://dx.doi.org/10.3389/fmicb.2018.02452
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author Ijaz, Umer Zeeshan
Sivaloganathan, Lojika
McKenna, Aaron
Richmond, Anne
Kelly, Carmel
Linton, Mark
Stratakos, Alexandros Ch.
Lavery, Ursula
Elmi, Abdi
Wren, Brendan W.
Dorrell, Nick
Corcionivoschi, Nicolae
Gundogdu, Ozan
author_facet Ijaz, Umer Zeeshan
Sivaloganathan, Lojika
McKenna, Aaron
Richmond, Anne
Kelly, Carmel
Linton, Mark
Stratakos, Alexandros Ch.
Lavery, Ursula
Elmi, Abdi
Wren, Brendan W.
Dorrell, Nick
Corcionivoschi, Nicolae
Gundogdu, Ozan
author_sort Ijaz, Umer Zeeshan
collection PubMed
description Chickens are a key food source for humans yet their microbiome contains bacteria that can be pathogenic to humans, and indeed potentially to chickens themselves. Campylobacter is present within the chicken gut and is the leading cause of bacterial foodborne gastroenteritis within humans worldwide. Infection can lead to secondary sequelae such as Guillain-Barré syndrome and stunted growth in children from low-resource areas. Despite the global health impact and economic burden of Campylobacter, how and when Campylobacter appears within chickens remains unclear. The lack of day to day microbiome data with replicates, relevant metadata, and a lack of natural infection studies have delayed our understanding of the chicken gut microbiome and Campylobacter. Here, we performed a comprehensive day to day microbiome analysis of the chicken cecum from day 3 to 35 (12 replicates each day; final n = 379). We combined metadata such as chicken weight and feed conversion rates to investigate what the driving forces are for the microbial changes within the chicken gut over time, and how this relates to Campylobacter appearance within a natural habitat setting. We found a rapidly increasing microbial diversity up to day 12 with variation observed both in terms of genera and abundance, before a stabilization of the microbial diversity after day 20. In particular, we identified a shift from competitive to environmental drivers of microbial community from days 12 to 20 creating a window of opportunity whereby Campylobacter can appear. Campylobacter was identified at day 16 which was 1 day after the most substantial changes in metabolic profiles observed. In addition, microbial variation over time is most likely influenced by the diet of the chickens whereby significant shifts in OTU abundances and beta dispersion of samples often corresponded with changes in feed. This study is unique in comparison to the most recent studies as neither sampling was sporadic nor Campylobacter was artificially introduced, thus the experiments were performed in a natural setting. We believe that our findings can be useful for future intervention strategies and help reduce the burden of Campylobacter within the food chain.
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spelling pubmed-61963132018-10-29 Comprehensive Longitudinal Microbiome Analysis of the Chicken Cecum Reveals a Shift From Competitive to Environmental Drivers and a Window of Opportunity for Campylobacter Ijaz, Umer Zeeshan Sivaloganathan, Lojika McKenna, Aaron Richmond, Anne Kelly, Carmel Linton, Mark Stratakos, Alexandros Ch. Lavery, Ursula Elmi, Abdi Wren, Brendan W. Dorrell, Nick Corcionivoschi, Nicolae Gundogdu, Ozan Front Microbiol Microbiology Chickens are a key food source for humans yet their microbiome contains bacteria that can be pathogenic to humans, and indeed potentially to chickens themselves. Campylobacter is present within the chicken gut and is the leading cause of bacterial foodborne gastroenteritis within humans worldwide. Infection can lead to secondary sequelae such as Guillain-Barré syndrome and stunted growth in children from low-resource areas. Despite the global health impact and economic burden of Campylobacter, how and when Campylobacter appears within chickens remains unclear. The lack of day to day microbiome data with replicates, relevant metadata, and a lack of natural infection studies have delayed our understanding of the chicken gut microbiome and Campylobacter. Here, we performed a comprehensive day to day microbiome analysis of the chicken cecum from day 3 to 35 (12 replicates each day; final n = 379). We combined metadata such as chicken weight and feed conversion rates to investigate what the driving forces are for the microbial changes within the chicken gut over time, and how this relates to Campylobacter appearance within a natural habitat setting. We found a rapidly increasing microbial diversity up to day 12 with variation observed both in terms of genera and abundance, before a stabilization of the microbial diversity after day 20. In particular, we identified a shift from competitive to environmental drivers of microbial community from days 12 to 20 creating a window of opportunity whereby Campylobacter can appear. Campylobacter was identified at day 16 which was 1 day after the most substantial changes in metabolic profiles observed. In addition, microbial variation over time is most likely influenced by the diet of the chickens whereby significant shifts in OTU abundances and beta dispersion of samples often corresponded with changes in feed. This study is unique in comparison to the most recent studies as neither sampling was sporadic nor Campylobacter was artificially introduced, thus the experiments were performed in a natural setting. We believe that our findings can be useful for future intervention strategies and help reduce the burden of Campylobacter within the food chain. Frontiers Media S.A. 2018-10-15 /pmc/articles/PMC6196313/ /pubmed/30374341 http://dx.doi.org/10.3389/fmicb.2018.02452 Text en Copyright © 2018 Ijaz, Sivaloganathan, McKenna, Richmond, Kelly, Linton, Stratakos, Lavery, Elmi, Wren, Dorrell, Corcionivoschi and Gundogdu. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Ijaz, Umer Zeeshan
Sivaloganathan, Lojika
McKenna, Aaron
Richmond, Anne
Kelly, Carmel
Linton, Mark
Stratakos, Alexandros Ch.
Lavery, Ursula
Elmi, Abdi
Wren, Brendan W.
Dorrell, Nick
Corcionivoschi, Nicolae
Gundogdu, Ozan
Comprehensive Longitudinal Microbiome Analysis of the Chicken Cecum Reveals a Shift From Competitive to Environmental Drivers and a Window of Opportunity for Campylobacter
title Comprehensive Longitudinal Microbiome Analysis of the Chicken Cecum Reveals a Shift From Competitive to Environmental Drivers and a Window of Opportunity for Campylobacter
title_full Comprehensive Longitudinal Microbiome Analysis of the Chicken Cecum Reveals a Shift From Competitive to Environmental Drivers and a Window of Opportunity for Campylobacter
title_fullStr Comprehensive Longitudinal Microbiome Analysis of the Chicken Cecum Reveals a Shift From Competitive to Environmental Drivers and a Window of Opportunity for Campylobacter
title_full_unstemmed Comprehensive Longitudinal Microbiome Analysis of the Chicken Cecum Reveals a Shift From Competitive to Environmental Drivers and a Window of Opportunity for Campylobacter
title_short Comprehensive Longitudinal Microbiome Analysis of the Chicken Cecum Reveals a Shift From Competitive to Environmental Drivers and a Window of Opportunity for Campylobacter
title_sort comprehensive longitudinal microbiome analysis of the chicken cecum reveals a shift from competitive to environmental drivers and a window of opportunity for campylobacter
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6196313/
https://www.ncbi.nlm.nih.gov/pubmed/30374341
http://dx.doi.org/10.3389/fmicb.2018.02452
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