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Feed Restriction Modifies Intestinal Microbiota-Host Mucosal Networking in Chickens Divergent in Residual Feed Intake

Differences in chickens’ feed intake may be the underlying factor influencing feed-efficiency (FE)-associated variation in intestinal microbiota and physiology. In chickens eating the same amount of feed, quantitative feed restriction may create similar intestinal conditions and help clarify this ca...

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Autores principales: Metzler-Zebeli, Barbara U., Siegerstetter, Sina-Catherine, Magowan, Elizabeth, Lawlor, Peadar G., Petri, Renée M., O´Connell, Niamh E., Zebeli, Qendrim
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6351724/
https://www.ncbi.nlm.nih.gov/pubmed/30701192
http://dx.doi.org/10.1128/mSystems.00261-18
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author Metzler-Zebeli, Barbara U.
Siegerstetter, Sina-Catherine
Magowan, Elizabeth
Lawlor, Peadar G.
Petri, Renée M.
O´Connell, Niamh E.
Zebeli, Qendrim
author_facet Metzler-Zebeli, Barbara U.
Siegerstetter, Sina-Catherine
Magowan, Elizabeth
Lawlor, Peadar G.
Petri, Renée M.
O´Connell, Niamh E.
Zebeli, Qendrim
author_sort Metzler-Zebeli, Barbara U.
collection PubMed
description Differences in chickens’ feed intake may be the underlying factor influencing feed-efficiency (FE)-associated variation in intestinal microbiota and physiology. In chickens eating the same amount of feed, quantitative feed restriction may create similar intestinal conditions and help clarify this cause-and-effect relationship. This study investigated the effect of ad libitum versus restrictive feeding (85% of ad libitum) on ileal and cecal microbiota, concentrations of short-chain fatty acids, visceral organ size, intestinal morphology, permeability, and expression of genes related to nutrient uptake, barrier function, and innate immune response in broiler chickens with divergent residual feed intake (RFI; metric for FE). On day 30 posthatch, 28 low-RFI (good FE) and 29 high-RFI (poor FE) chickens across both feeding-level groups (n = 112) were selected. Supervised multigroup data integration and relevance network analyses showed that especially Lactobacillus (negative) in ileal digesta, Turicibacter (positive) in cecal digesta, and Enterobacteriaceae (positive) in both intestinal segments depended on chicken’s feed intake, whereas the level of Anaerotruncus in cecal digesta was most discriminative for high RFI. Moreover, shallower crypts and fewer goblet cells in ceca indicated host-related energy-saving mechanisms with low RFI, whereas greater tissue resistance suggested a stronger jejunal barrier function in low-RFI chickens. Values corresponding to feed intake level × RFI interactions indicated larger pancreas and lower levels of ileal and cecal short-chain fatty acids in restrictively fed high-RFI chickens than in the other 3 groups, suggesting host physiological adaptations to support greater energy and nutrient needs of high-RFI chickens compensating for the restricted feeding. IMPORTANCE The impact of the FE-associated differences in feed intake on intestinal bacterial and host physiological parameters has so far not been clarified. Understanding the underlying principles is essential for the development of cost-effective strategies to improve FE in chicken production. Under conditions of quantitative feed restriction, low- and high-RFI chickens ate the same amount of feed. Therefore, this research helps in distinguishing intestinal bacterial taxa and functions that were highly reliant on feed intake from those that were associated with physiological adaptations to RFI-associated differences in host nutritional needs and intestinal nutrient availability. This work provides a background for further research to assess manipulation of the intestinal microbiota, host physiology, and FE in chickens by dietary intervention.
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spelling pubmed-63517242019-01-30 Feed Restriction Modifies Intestinal Microbiota-Host Mucosal Networking in Chickens Divergent in Residual Feed Intake Metzler-Zebeli, Barbara U. Siegerstetter, Sina-Catherine Magowan, Elizabeth Lawlor, Peadar G. Petri, Renée M. O´Connell, Niamh E. Zebeli, Qendrim mSystems Research Article Differences in chickens’ feed intake may be the underlying factor influencing feed-efficiency (FE)-associated variation in intestinal microbiota and physiology. In chickens eating the same amount of feed, quantitative feed restriction may create similar intestinal conditions and help clarify this cause-and-effect relationship. This study investigated the effect of ad libitum versus restrictive feeding (85% of ad libitum) on ileal and cecal microbiota, concentrations of short-chain fatty acids, visceral organ size, intestinal morphology, permeability, and expression of genes related to nutrient uptake, barrier function, and innate immune response in broiler chickens with divergent residual feed intake (RFI; metric for FE). On day 30 posthatch, 28 low-RFI (good FE) and 29 high-RFI (poor FE) chickens across both feeding-level groups (n = 112) were selected. Supervised multigroup data integration and relevance network analyses showed that especially Lactobacillus (negative) in ileal digesta, Turicibacter (positive) in cecal digesta, and Enterobacteriaceae (positive) in both intestinal segments depended on chicken’s feed intake, whereas the level of Anaerotruncus in cecal digesta was most discriminative for high RFI. Moreover, shallower crypts and fewer goblet cells in ceca indicated host-related energy-saving mechanisms with low RFI, whereas greater tissue resistance suggested a stronger jejunal barrier function in low-RFI chickens. Values corresponding to feed intake level × RFI interactions indicated larger pancreas and lower levels of ileal and cecal short-chain fatty acids in restrictively fed high-RFI chickens than in the other 3 groups, suggesting host physiological adaptations to support greater energy and nutrient needs of high-RFI chickens compensating for the restricted feeding. IMPORTANCE The impact of the FE-associated differences in feed intake on intestinal bacterial and host physiological parameters has so far not been clarified. Understanding the underlying principles is essential for the development of cost-effective strategies to improve FE in chicken production. Under conditions of quantitative feed restriction, low- and high-RFI chickens ate the same amount of feed. Therefore, this research helps in distinguishing intestinal bacterial taxa and functions that were highly reliant on feed intake from those that were associated with physiological adaptations to RFI-associated differences in host nutritional needs and intestinal nutrient availability. This work provides a background for further research to assess manipulation of the intestinal microbiota, host physiology, and FE in chickens by dietary intervention. American Society for Microbiology 2019-01-29 /pmc/articles/PMC6351724/ /pubmed/30701192 http://dx.doi.org/10.1128/mSystems.00261-18 Text en Copyright © 2019 Metzler-Zebeli et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Metzler-Zebeli, Barbara U.
Siegerstetter, Sina-Catherine
Magowan, Elizabeth
Lawlor, Peadar G.
Petri, Renée M.
O´Connell, Niamh E.
Zebeli, Qendrim
Feed Restriction Modifies Intestinal Microbiota-Host Mucosal Networking in Chickens Divergent in Residual Feed Intake
title Feed Restriction Modifies Intestinal Microbiota-Host Mucosal Networking in Chickens Divergent in Residual Feed Intake
title_full Feed Restriction Modifies Intestinal Microbiota-Host Mucosal Networking in Chickens Divergent in Residual Feed Intake
title_fullStr Feed Restriction Modifies Intestinal Microbiota-Host Mucosal Networking in Chickens Divergent in Residual Feed Intake
title_full_unstemmed Feed Restriction Modifies Intestinal Microbiota-Host Mucosal Networking in Chickens Divergent in Residual Feed Intake
title_short Feed Restriction Modifies Intestinal Microbiota-Host Mucosal Networking in Chickens Divergent in Residual Feed Intake
title_sort feed restriction modifies intestinal microbiota-host mucosal networking in chickens divergent in residual feed intake
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6351724/
https://www.ncbi.nlm.nih.gov/pubmed/30701192
http://dx.doi.org/10.1128/mSystems.00261-18
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