Metabolome and microbiome analysis revealed the effect mechanism of different feeding modes on the meat quality of Black Tibetan sheep

IntroductionBlack Tibetan sheep is one of the primitive sheep breeds in China that is famous for its great eating quality and nutrient value but with little attention to the relationship between feeding regimes and rumen metabolome along with its impact on the muscle metabolism and meat quality.Meth...

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Main Authors: Xue Zhang, Lijuan Han, Linsheng Gui, Sayed Haidar Abbas Raza, Shengzhen Hou, Baochun Yang, Zhiyou Wang, Ying Ma, Raafat T. M. Makhlof, Zamzam Alhuwaymil, Samah F. Ibrahim
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-01-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.1076675/full
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author Xue Zhang
Lijuan Han
Linsheng Gui
Sayed Haidar Abbas Raza
Sayed Haidar Abbas Raza
Shengzhen Hou
Baochun Yang
Zhiyou Wang
Ying Ma
Raafat T. M. Makhlof
Raafat T. M. Makhlof
Zamzam Alhuwaymil
Samah F. Ibrahim
author_facet Xue Zhang
Lijuan Han
Linsheng Gui
Sayed Haidar Abbas Raza
Sayed Haidar Abbas Raza
Shengzhen Hou
Baochun Yang
Zhiyou Wang
Ying Ma
Raafat T. M. Makhlof
Raafat T. M. Makhlof
Zamzam Alhuwaymil
Samah F. Ibrahim
author_sort Xue Zhang
collection DOAJ
description IntroductionBlack Tibetan sheep is one of the primitive sheep breeds in China that is famous for its great eating quality and nutrient value but with little attention to the relationship between feeding regimes and rumen metabolome along with its impact on the muscle metabolism and meat quality.MethodsThis study applies metabolomics-based analyses of muscles and 16S rDNA-based sequencing of rumen fluid to examine how feeding regimes influence the composition of rumen microbiota, muscle metabolism and ultimately the quality of meat from Black Tibetan sheep. Twenty-seven rams were randomly assigned to either indoor feeding conditions (SG, n = 9), pasture grazing with indoor feeding conditions (BG, n = 9) or pasture grazing conditions (CG, n = 9) for 120 days.ResultsThe results showed that, compared with BG and CG, SG improved the quality of Black Tibetan sheep mutton by preventing a decline in pH and increasing fat deposition to enhance the color, tenderness and water holding capacity (WHC) of the Longissimus lumborum (LL). Metabolomics and correlation analyses further indicated that the feeding regimes primarily altered amino acid, lipid and carbohydrate metabolism in muscles, thereby influencing the amino acid (AA) and fatty acid (FA) levels as well as the color, tenderness and WHC of the LL. Furthermore, SG increased the abundance of Christensenellaceae R-7 group, [Eubacterium] coprostanoligenes group, Methanobrevibacter, Ruminococcus 2 and Quinella, decreased the abundance of Lactobacillus, Prevotella 1 and Rikenellaceae RC9 gut group, and showed a tendency to decrease the abundance of Succinivibrio and Selenomonas 1. Interestingly, all of these microorganisms participated in the deposition of AAs and FAs and modified the levels of different metabolites involved in the regulation of meat quality (maltotriose, pyruvate, L-ascorbic acid, chenodeoxycholate, D-glucose 6-phosphate, glutathione, etc.).DiscussionOverall, the results suggest that feeding Black Tibetan sheep indoors with composite forage diet was beneficial to improve the mouthfeel of meat, its color and its nutritional value by altering the abundance of rumen bacteria which influenced muscle metabolism.
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spelling doaj.art-29701459104c4bac91a957d786459f062023-01-06T21:46:49ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-01-011310.3389/fmicb.2022.10766751076675Metabolome and microbiome analysis revealed the effect mechanism of different feeding modes on the meat quality of Black Tibetan sheepXue Zhang0Lijuan Han1Linsheng Gui2Sayed Haidar Abbas Raza3Sayed Haidar Abbas Raza4Shengzhen Hou5Baochun Yang6Zhiyou Wang7Ying Ma8Raafat T. M. Makhlof9Raafat T. M. Makhlof10Zamzam Alhuwaymil11Samah F. Ibrahim12Department of Animal Science, College of Agriculture and Animal Husbandry, Qinghai University, Xining, Qinghai, ChinaDepartment of Animal Science, College of Agriculture and Animal Husbandry, Qinghai University, Xining, Qinghai, ChinaDepartment of Animal Science, College of Agriculture and Animal Husbandry, Qinghai University, Xining, Qinghai, ChinaCollege of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi, ChinaSafety of Livestock and Poultry Products, College of Food Science, South China Agricultural University, Guangzhou, ChinaDepartment of Animal Science, College of Agriculture and Animal Husbandry, Qinghai University, Xining, Qinghai, ChinaDepartment of Animal Science, College of Agriculture and Animal Husbandry, Qinghai University, Xining, Qinghai, ChinaDepartment of Animal Science, College of Agriculture and Animal Husbandry, Qinghai University, Xining, Qinghai, ChinaDepartment of Animal Science, College of Agriculture and Animal Husbandry, Qinghai University, Xining, Qinghai, ChinaDepartment of Parasitology, Faculty of Medicine, Umm Al Qura University, Mecca, Saudi ArabiaDepartment of Parasitology, Faculty of Medicine, Minia University, Minya, EgyptOrganic Department, College of Science and Humanities at Al-Quway'iyah, Shaqra University, Shaqra, Saudi ArabiaDepartment of Clinical Sciences, College of Medicine, Princess Nourah bint Abdulrahman University, Riyadh, Saudi ArabiaIntroductionBlack Tibetan sheep is one of the primitive sheep breeds in China that is famous for its great eating quality and nutrient value but with little attention to the relationship between feeding regimes and rumen metabolome along with its impact on the muscle metabolism and meat quality.MethodsThis study applies metabolomics-based analyses of muscles and 16S rDNA-based sequencing of rumen fluid to examine how feeding regimes influence the composition of rumen microbiota, muscle metabolism and ultimately the quality of meat from Black Tibetan sheep. Twenty-seven rams were randomly assigned to either indoor feeding conditions (SG, n = 9), pasture grazing with indoor feeding conditions (BG, n = 9) or pasture grazing conditions (CG, n = 9) for 120 days.ResultsThe results showed that, compared with BG and CG, SG improved the quality of Black Tibetan sheep mutton by preventing a decline in pH and increasing fat deposition to enhance the color, tenderness and water holding capacity (WHC) of the Longissimus lumborum (LL). Metabolomics and correlation analyses further indicated that the feeding regimes primarily altered amino acid, lipid and carbohydrate metabolism in muscles, thereby influencing the amino acid (AA) and fatty acid (FA) levels as well as the color, tenderness and WHC of the LL. Furthermore, SG increased the abundance of Christensenellaceae R-7 group, [Eubacterium] coprostanoligenes group, Methanobrevibacter, Ruminococcus 2 and Quinella, decreased the abundance of Lactobacillus, Prevotella 1 and Rikenellaceae RC9 gut group, and showed a tendency to decrease the abundance of Succinivibrio and Selenomonas 1. Interestingly, all of these microorganisms participated in the deposition of AAs and FAs and modified the levels of different metabolites involved in the regulation of meat quality (maltotriose, pyruvate, L-ascorbic acid, chenodeoxycholate, D-glucose 6-phosphate, glutathione, etc.).DiscussionOverall, the results suggest that feeding Black Tibetan sheep indoors with composite forage diet was beneficial to improve the mouthfeel of meat, its color and its nutritional value by altering the abundance of rumen bacteria which influenced muscle metabolism.https://www.frontiersin.org/articles/10.3389/fmicb.2022.1076675/fullBlack Tibetan sheepfeeding regimesmeat quality16S rDNAmetabolomics
spellingShingle Xue Zhang
Lijuan Han
Linsheng Gui
Sayed Haidar Abbas Raza
Sayed Haidar Abbas Raza
Shengzhen Hou
Baochun Yang
Zhiyou Wang
Ying Ma
Raafat T. M. Makhlof
Raafat T. M. Makhlof
Zamzam Alhuwaymil
Samah F. Ibrahim
Metabolome and microbiome analysis revealed the effect mechanism of different feeding modes on the meat quality of Black Tibetan sheep
Frontiers in Microbiology
Black Tibetan sheep
feeding regimes
meat quality
16S rDNA
metabolomics
title Metabolome and microbiome analysis revealed the effect mechanism of different feeding modes on the meat quality of Black Tibetan sheep
title_full Metabolome and microbiome analysis revealed the effect mechanism of different feeding modes on the meat quality of Black Tibetan sheep
title_fullStr Metabolome and microbiome analysis revealed the effect mechanism of different feeding modes on the meat quality of Black Tibetan sheep
title_full_unstemmed Metabolome and microbiome analysis revealed the effect mechanism of different feeding modes on the meat quality of Black Tibetan sheep
title_short Metabolome and microbiome analysis revealed the effect mechanism of different feeding modes on the meat quality of Black Tibetan sheep
title_sort metabolome and microbiome analysis revealed the effect mechanism of different feeding modes on the meat quality of black tibetan sheep
topic Black Tibetan sheep
feeding regimes
meat quality
16S rDNA
metabolomics
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.1076675/full
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