Comprehensive longitudinal microbiome analysis of the chicken cecum reveals a shift from competitive to environmental drivers and a window of opportunity for Campylobacter

Umer Zeeshan Ijaz, Lojika Sivaloganathan, Aaron McKenna, Anne Richmond, Carmel Kelly, Mark Linton, Alexandros Ch Stratakos, Ursula Lavery, Abdi Elmi, Brendan W. Wren, Nick Dorrell*, Nicolae Corcionivoschi, Ozan Gundogdu

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

23 Citations (Scopus)
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Abstract

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.

Original languageEnglish
Article number2452
JournalFrontiers in Microbiology
Volume9
Issue numberOCT
DOIs
Publication statusPublished - 15 Oct 2018

Bibliographical note

Funding Information:
The authors acknowledge research funding from Moy Park. UZI is funded by NERC Independent Research Fellowship (NE/L011956/1).

Publisher Copyright:
Copyright © 2018 Ijaz, Sivaloganathan, McKenna, Richmond, Kelly, Linton, Stratakos, Lavery, Elmi, Wren, Dorrell, Corcionivoschi and Gundogdu. 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.

Copyright:
Copyright 2020 Elsevier B.V., All rights reserved.

Keywords

  • Campylobacter
  • Chicken
  • Competitive exclusion
  • Diversity
  • Environmental filtering
  • Microbiome
  • Phylogenetic signal

ASJC Scopus subject areas

  • Microbiology
  • Microbiology (medical)

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