Feed Restriction Modifies Intestinal Microbiota-Host Mucosal Networking in Chickens Divergent in Residual Feed Intake
ABSTRACT 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 clarif...
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American Society for Microbiology
2019
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oai:doaj.org-article:e49da414fdbd4e98ab0fbd6b2a1649752021-12-02T18:39:16ZFeed Restriction Modifies Intestinal Microbiota-Host Mucosal Networking in Chickens Divergent in Residual Feed Intake10.1128/mSystems.00261-182379-5077https://doaj.org/article/e49da414fdbd4e98ab0fbd6b2a1649752019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00261-18https://doaj.org/toc/2379-5077ABSTRACT 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.Barbara U. Metzler-ZebeliSina-Catherine SiegerstetterElizabeth MagowanPeadar G. LawlorRenée M. PetriNiamh E. O´ConnellQendrim ZebeliAmerican Society for Microbiologyarticlechickenfeed intake levelintestinal barrier functionintestinal microbiotaintestinal physiologyresidual feed intakeMicrobiologyQR1-502ENmSystems, Vol 4, Iss 1 (2019) |
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chicken feed intake level intestinal barrier function intestinal microbiota intestinal physiology residual feed intake Microbiology QR1-502 |
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chicken feed intake level intestinal barrier function intestinal microbiota intestinal physiology residual feed intake Microbiology QR1-502 Barbara U. Metzler-Zebeli Sina-Catherine Siegerstetter Elizabeth Magowan Peadar G. Lawlor Renée M. Petri Niamh E. O´Connell Qendrim Zebeli Feed Restriction Modifies Intestinal Microbiota-Host Mucosal Networking in Chickens Divergent in Residual Feed Intake |
description |
ABSTRACT 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. |
format |
article |
author |
Barbara U. Metzler-Zebeli Sina-Catherine Siegerstetter Elizabeth Magowan Peadar G. Lawlor Renée M. Petri Niamh E. O´Connell Qendrim Zebeli |
author_facet |
Barbara U. Metzler-Zebeli Sina-Catherine Siegerstetter Elizabeth Magowan Peadar G. Lawlor Renée M. Petri Niamh E. O´Connell Qendrim Zebeli |
author_sort |
Barbara U. Metzler-Zebeli |
title |
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_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_sort |
feed restriction modifies intestinal microbiota-host mucosal networking in chickens divergent in residual feed intake |
publisher |
American Society for Microbiology |
publishDate |
2019 |
url |
https://doaj.org/article/e49da414fdbd4e98ab0fbd6b2a164975 |
work_keys_str_mv |
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