Broiler chickens and early life programming: Microbiome transplant-induced cecal community dynamics and phenotypic effects.

The concept of successional trajectories describes how small differences in initial community composition can magnify through time and lead to significant differences in mature communities. For many animals, the types and sources of early-life exposures to microbes have been shown to have significan...

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Main Authors: Gustavo A Ramírez, Ella Richardson, Jory Clark, Jitendra Keshri, Yvonne Drechsler, Mark E Berrang, Richard J Meinersmann, Nelson A Cox, Brian B Oakley
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0242108
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spelling doaj-f8ea30226da74284bee06e487515c4752021-03-04T12:26:16ZengPublic Library of Science (PLoS)PLoS ONE1932-62032020-01-011511e024210810.1371/journal.pone.0242108Broiler chickens and early life programming: Microbiome transplant-induced cecal community dynamics and phenotypic effects.Gustavo A RamírezElla RichardsonJory ClarkJitendra KeshriYvonne DrechslerMark E BerrangRichard J MeinersmannNelson A CoxBrian B OakleyThe concept of successional trajectories describes how small differences in initial community composition can magnify through time and lead to significant differences in mature communities. For many animals, the types and sources of early-life exposures to microbes have been shown to have significant and long-lasting effects on the community structure and/or function of the microbiome. In modern commercial poultry production, chicks are reared as a single age cohort and do not directly encounter adult birds. This scenario is likely to initiate a trajectory of microbial community development that is significantly different than non-industrial settings where chicks are exposed to a much broader range of environmental and fecal inocula; however, the comparative effects of these two scenarios on microbiome development and function remain largely unknown. In this work, we performed serial transfers of cecal material through multiple generations of birds to first determine if serial transfers exploiting the ceca in vivo, rather than the external environment or artificial incubations, can produce a stable microbial community. Subsequently, we compared microbiome development between chicks receiving this passaged, i.e. host-selected, cecal material orally, versus an environmental inoculum, to test the hypothesis that the first exposure of newly hatched chicks to microbes determines early GI microbiome structure and may have longer-lasting effects on bird health and development. Cecal microbiome dynamics and bird weights were tracked for a two-week period, with half of the birds in each treatment group exposed to a pathogen challenge at 7 days of age. We report that: i) a relatively stable community was derived after a single passage of transplanted cecal material, ii) this cecal inoculum significantly but ephemerally altered community structure relative to the environmental inoculum and PBS controls, and iii) either microbiome transplant administered at day-of-hatch appeared to have some protective effects against pathogen challenge relative to uninoculated controls. Differentially abundant taxa identified across treatment types may inform future studies aimed at identifying strains associated with beneficial phenotypes.https://doi.org/10.1371/journal.pone.0242108
collection DOAJ
language English
format Article
sources DOAJ
author Gustavo A Ramírez
Ella Richardson
Jory Clark
Jitendra Keshri
Yvonne Drechsler
Mark E Berrang
Richard J Meinersmann
Nelson A Cox
Brian B Oakley
spellingShingle Gustavo A Ramírez
Ella Richardson
Jory Clark
Jitendra Keshri
Yvonne Drechsler
Mark E Berrang
Richard J Meinersmann
Nelson A Cox
Brian B Oakley
Broiler chickens and early life programming: Microbiome transplant-induced cecal community dynamics and phenotypic effects.
PLoS ONE
author_facet Gustavo A Ramírez
Ella Richardson
Jory Clark
Jitendra Keshri
Yvonne Drechsler
Mark E Berrang
Richard J Meinersmann
Nelson A Cox
Brian B Oakley
author_sort Gustavo A Ramírez
title Broiler chickens and early life programming: Microbiome transplant-induced cecal community dynamics and phenotypic effects.
title_short Broiler chickens and early life programming: Microbiome transplant-induced cecal community dynamics and phenotypic effects.
title_full Broiler chickens and early life programming: Microbiome transplant-induced cecal community dynamics and phenotypic effects.
title_fullStr Broiler chickens and early life programming: Microbiome transplant-induced cecal community dynamics and phenotypic effects.
title_full_unstemmed Broiler chickens and early life programming: Microbiome transplant-induced cecal community dynamics and phenotypic effects.
title_sort broiler chickens and early life programming: microbiome transplant-induced cecal community dynamics and phenotypic effects.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2020-01-01
description The concept of successional trajectories describes how small differences in initial community composition can magnify through time and lead to significant differences in mature communities. For many animals, the types and sources of early-life exposures to microbes have been shown to have significant and long-lasting effects on the community structure and/or function of the microbiome. In modern commercial poultry production, chicks are reared as a single age cohort and do not directly encounter adult birds. This scenario is likely to initiate a trajectory of microbial community development that is significantly different than non-industrial settings where chicks are exposed to a much broader range of environmental and fecal inocula; however, the comparative effects of these two scenarios on microbiome development and function remain largely unknown. In this work, we performed serial transfers of cecal material through multiple generations of birds to first determine if serial transfers exploiting the ceca in vivo, rather than the external environment or artificial incubations, can produce a stable microbial community. Subsequently, we compared microbiome development between chicks receiving this passaged, i.e. host-selected, cecal material orally, versus an environmental inoculum, to test the hypothesis that the first exposure of newly hatched chicks to microbes determines early GI microbiome structure and may have longer-lasting effects on bird health and development. Cecal microbiome dynamics and bird weights were tracked for a two-week period, with half of the birds in each treatment group exposed to a pathogen challenge at 7 days of age. We report that: i) a relatively stable community was derived after a single passage of transplanted cecal material, ii) this cecal inoculum significantly but ephemerally altered community structure relative to the environmental inoculum and PBS controls, and iii) either microbiome transplant administered at day-of-hatch appeared to have some protective effects against pathogen challenge relative to uninoculated controls. Differentially abundant taxa identified across treatment types may inform future studies aimed at identifying strains associated with beneficial phenotypes.
url https://doi.org/10.1371/journal.pone.0242108
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