Multi-omics revealed the mechanism of feed efficiency in sheep by the combined action of the host and rumen microbiota

This study was conducted to investigate potential regulatory mechanisms of feed efficiency (FE) in sheep by linking rumen microbiota with its host by the multi-omics analysis. One hundred and ninety-eight hybrid female sheep (initial body weight = 30.88 ± 4.57 kg; 4-month-old) were selected as candi...

Full description

Saved in:
Bibliographic Details
Main Authors: Guangchen Zhou, Junda Li, Xuhui Liang, Bohua Yang, Ximeng He, Hongyu Tang, Hongran Guo, Gongwei Liu, Wenyuan Cui, Yulin Chen, Yuxin Yang
Format: Article
Language:English
Published: KeAi Communications Co., Ltd. 2024-09-01
Series:Animal Nutrition
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S240565452400057X
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850210026696736768
author Guangchen Zhou
Junda Li
Xuhui Liang
Bohua Yang
Ximeng He
Hongyu Tang
Hongran Guo
Gongwei Liu
Wenyuan Cui
Yulin Chen
Yuxin Yang
author_facet Guangchen Zhou
Junda Li
Xuhui Liang
Bohua Yang
Ximeng He
Hongyu Tang
Hongran Guo
Gongwei Liu
Wenyuan Cui
Yulin Chen
Yuxin Yang
author_sort Guangchen Zhou
collection DOAJ
description This study was conducted to investigate potential regulatory mechanisms of feed efficiency (FE) in sheep by linking rumen microbiota with its host by the multi-omics analysis. One hundred and ninety-eight hybrid female sheep (initial body weight = 30.88 ± 4.57 kg; 4-month-old) were selected as candidate sheep. Each test sheep was fed in an individual pen for 60 days, and the residual feed intake (RFI) was calculated. The ten candidate sheep with the highest RFI were divided into the Low-FE group, and the ten with the lowest RFI were divided into the High-FE group, all selected for sample collection. The RFI, average daily gain and average daily feed intake were highly significantly different between the two experimental groups (P < 0.05). Compared with Low-FE group, the insulin-like growth factor-1 and very low-density lipoprotein in serum and the propionate in rumen significantly increased in High-FE group (P < 0.01), but the acetate:propionate ratio in rumen significantly decreased in High-FE group (P = 0.034). Metagenomics revealed Selenomonas ruminantium, Selenomonas sp. and Faecalibacterium prausnitzii were key bacteria, and increased abundance of the genes encoding the enzymes for cellulose degradation and production of propionate in High-FE group. The results of proteomics and section showed the rumen papilla length and expression of carbonic anhydrase and Na+/K+-ATPase were significantly higher in High-FE group (P < 0.05). On the other hand, the acetyl-CoA content significantly increased in the liver of High-FE group (P = 0.002). The relative expression levels of insulin-like growth factor-1 and apolipoprotein A4 genes were significantly up-regulated in the liver of High-FE group (P < 0.05), but relative expression level of monoacylglycerol O-acyltransferase 3 gene was significantly down-regulated (P = 0.037). These findings provide the mechanism by which the collaborative interaction between rumen microbiota fermentation and host uptake and metabolism of fermentation products impacts feed efficiency traits in sheep.
format Article
id doaj-art-4635676129c643ddb7f5ce5c2080dda7
institution OA Journals
issn 2405-6545
language English
publishDate 2024-09-01
publisher KeAi Communications Co., Ltd.
record_format Article
series Animal Nutrition
spelling doaj-art-4635676129c643ddb7f5ce5c2080dda72025-08-20T02:09:52ZengKeAi Communications Co., Ltd.Animal Nutrition2405-65452024-09-011836737910.1016/j.aninu.2024.04.009Multi-omics revealed the mechanism of feed efficiency in sheep by the combined action of the host and rumen microbiotaGuangchen Zhou0Junda Li1Xuhui Liang2Bohua Yang3Ximeng He4Hongyu Tang5Hongran Guo6Gongwei Liu7Wenyuan Cui8Yulin Chen9Yuxin Yang10Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaCorresponding author.; Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaThis study was conducted to investigate potential regulatory mechanisms of feed efficiency (FE) in sheep by linking rumen microbiota with its host by the multi-omics analysis. One hundred and ninety-eight hybrid female sheep (initial body weight = 30.88 ± 4.57 kg; 4-month-old) were selected as candidate sheep. Each test sheep was fed in an individual pen for 60 days, and the residual feed intake (RFI) was calculated. The ten candidate sheep with the highest RFI were divided into the Low-FE group, and the ten with the lowest RFI were divided into the High-FE group, all selected for sample collection. The RFI, average daily gain and average daily feed intake were highly significantly different between the two experimental groups (P < 0.05). Compared with Low-FE group, the insulin-like growth factor-1 and very low-density lipoprotein in serum and the propionate in rumen significantly increased in High-FE group (P < 0.01), but the acetate:propionate ratio in rumen significantly decreased in High-FE group (P = 0.034). Metagenomics revealed Selenomonas ruminantium, Selenomonas sp. and Faecalibacterium prausnitzii were key bacteria, and increased abundance of the genes encoding the enzymes for cellulose degradation and production of propionate in High-FE group. The results of proteomics and section showed the rumen papilla length and expression of carbonic anhydrase and Na+/K+-ATPase were significantly higher in High-FE group (P < 0.05). On the other hand, the acetyl-CoA content significantly increased in the liver of High-FE group (P = 0.002). The relative expression levels of insulin-like growth factor-1 and apolipoprotein A4 genes were significantly up-regulated in the liver of High-FE group (P < 0.05), but relative expression level of monoacylglycerol O-acyltransferase 3 gene was significantly down-regulated (P = 0.037). These findings provide the mechanism by which the collaborative interaction between rumen microbiota fermentation and host uptake and metabolism of fermentation products impacts feed efficiency traits in sheep.http://www.sciencedirect.com/science/article/pii/S240565452400057XResidual feed intakeSheepMicrobial compositionRumen proteomeLiver transcriptomeMetabolite
spellingShingle Guangchen Zhou
Junda Li
Xuhui Liang
Bohua Yang
Ximeng He
Hongyu Tang
Hongran Guo
Gongwei Liu
Wenyuan Cui
Yulin Chen
Yuxin Yang
Multi-omics revealed the mechanism of feed efficiency in sheep by the combined action of the host and rumen microbiota
Animal Nutrition
Residual feed intake
Sheep
Microbial composition
Rumen proteome
Liver transcriptome
Metabolite
title Multi-omics revealed the mechanism of feed efficiency in sheep by the combined action of the host and rumen microbiota
title_full Multi-omics revealed the mechanism of feed efficiency in sheep by the combined action of the host and rumen microbiota
title_fullStr Multi-omics revealed the mechanism of feed efficiency in sheep by the combined action of the host and rumen microbiota
title_full_unstemmed Multi-omics revealed the mechanism of feed efficiency in sheep by the combined action of the host and rumen microbiota
title_short Multi-omics revealed the mechanism of feed efficiency in sheep by the combined action of the host and rumen microbiota
title_sort multi omics revealed the mechanism of feed efficiency in sheep by the combined action of the host and rumen microbiota
topic Residual feed intake
Sheep
Microbial composition
Rumen proteome
Liver transcriptome
Metabolite
url http://www.sciencedirect.com/science/article/pii/S240565452400057X
work_keys_str_mv AT guangchenzhou multiomicsrevealedthemechanismoffeedefficiencyinsheepbythecombinedactionofthehostandrumenmicrobiota
AT jundali multiomicsrevealedthemechanismoffeedefficiencyinsheepbythecombinedactionofthehostandrumenmicrobiota
AT xuhuiliang multiomicsrevealedthemechanismoffeedefficiencyinsheepbythecombinedactionofthehostandrumenmicrobiota
AT bohuayang multiomicsrevealedthemechanismoffeedefficiencyinsheepbythecombinedactionofthehostandrumenmicrobiota
AT ximenghe multiomicsrevealedthemechanismoffeedefficiencyinsheepbythecombinedactionofthehostandrumenmicrobiota
AT hongyutang multiomicsrevealedthemechanismoffeedefficiencyinsheepbythecombinedactionofthehostandrumenmicrobiota
AT hongranguo multiomicsrevealedthemechanismoffeedefficiencyinsheepbythecombinedactionofthehostandrumenmicrobiota
AT gongweiliu multiomicsrevealedthemechanismoffeedefficiencyinsheepbythecombinedactionofthehostandrumenmicrobiota
AT wenyuancui multiomicsrevealedthemechanismoffeedefficiencyinsheepbythecombinedactionofthehostandrumenmicrobiota
AT yulinchen multiomicsrevealedthemechanismoffeedefficiencyinsheepbythecombinedactionofthehostandrumenmicrobiota
AT yuxinyang multiomicsrevealedthemechanismoffeedefficiencyinsheepbythecombinedactionofthehostandrumenmicrobiota