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      Emerging perspectives in the gut–muscle axis: The gut microbiota and its metabolites as important modulators of meat quality

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          Abstract

          Animal breeding has made great genetic progress in increasing carcass weight and meat yield in recent decades. However, these improvements have come at the expense of meat quality. As the demand for meat quantity continues to rise, the meat industry faces the great challenge of maintaining and even increasing product quality. Recent research, including traditional statistical analyses and gut microbiota regulation research, has demonstrated that the gut microbiome exerts a considerable effect on meat quality, which has become increasingly intriguing in farm animals. Microbial metabolites play crucial roles as substrates or signalling factors to distant organs, influencing meat quality either beneficially or detrimentally. Interventions targeting the gut microbiota exhibit excellent potential as natural ways to foster the conversion of myofibres and promote intramuscular fat deposition. Here, we highlight the emerging roles of the gut microbiota in various dimensions of meat quality. We focus particularly on the effects of the gut microbiota and gut‐derived molecules on muscle fibre metabolism and intramuscular fat deposition and attempt to summarize the potential underlying mechanisms.

          Abstract

          The gut microbiome exerts a considerable effect on meat quality, which has become increasingly intriguing in farm animals. Microbial metabolites play crucial roles as substrates or signaling factors to distant organs, influencing meat quality either beneficially or detrimentally. Interventions targeting the gut microbiota exhibit excellent potential as natural ways to foster the conversion of myofibers and promote intramuscular fat deposition.

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          Most cited references129

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          Environment dominates over host genetics in shaping human gut microbiota

          Human gut microbiome composition is shaped by multiple factors but the relative contribution of host genetics remains elusive. Here we examine genotype and microbiome data from 1,046 healthy individuals with several distinct ancestral origins who share a relatively common environment, and demonstrate that the gut microbiome is not significantly associated with genetic ancestry, and that host genetics have a minor role in determining microbiome composition. We show that, by contrast, there are significant similarities in the compositions of the microbiomes of genetically unrelated individuals who share a household, and that over 20% of the inter-person microbiome variability is associated with factors related to diet, drugs and anthropometric measurements. We further demonstrate that microbiome data significantly improve the prediction accuracy for many human traits, such as glucose and obesity measures, compared to models that use only host genetic and environmental data. These results suggest that microbiome alterations aimed at improving clinical outcomes may be carried out across diverse genetic backgrounds.
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            Butyrate Improves Insulin Sensitivity and Increases Energy Expenditure in Mice

            OBJECTIVE We examined the role of butyric acid, a short-chain fatty acid formed by fermentation in the large intestine, in the regulation of insulin sensitivity in mice fed a high-fat diet. RESEARCH DESIGN AND METHODS In dietary-obese C57BL/6J mice, sodium butyrate was administrated through diet supplementation at 5% wt/wt in the high-fat diet. Insulin sensitivity was examined with insulin tolerance testing and homeostasis model assessment for insulin resistance. Energy metabolism was monitored in a metabolic chamber. Mitochondrial function was investigated in brown adipocytes and skeletal muscle in the mice. RESULTS On the high-fat diet, supplementation of butyrate prevented development of insulin resistance and obesity in C57BL/6 mice. Fasting blood glucose, fasting insulin, and insulin tolerance were all preserved in the treated mice. Body fat content was maintained at 10% without a reduction in food intake. Adaptive thermogenesis and fatty acid oxidation were enhanced. An increase in mitochondrial function and biogenesis was observed in skeletal muscle and brown fat. The type I fiber was enriched in skeletal muscle. Peroxisome proliferator–activated receptor-γ coactivator-1α expression was elevated at mRNA and protein levels. AMP kinase and p38 activities were elevated. In the obese mice, supplementation of butyrate led to an increase in insulin sensitivity and a reduction in adiposity. CONCLUSIONS Dietary supplementation of butyrate can prevent and treat diet-induced insulin resistance in mouse. The mechanism of butyrate action is related to promotion of energy expenditure and induction of mitochondria function.
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              Mechanisms underlying the resistance to diet-induced obesity in germ-free mice.

              The trillions of microbes that colonize our adult intestines function collectively as a metabolic organ that communicates with, and complements, our own human metabolic apparatus. Given the worldwide epidemic in obesity, there is interest in how interactions between human and microbial metabolomes may affect our energy balance. Here we report that, in contrast to mice with a gut microbiota, germ-free (GF) animals are protected against the obesity that develops after consuming a Western-style, high-fat, sugar-rich diet. Their persistently lean phenotype is associated with increased skeletal muscle and liver levels of phosphorylated AMP-activated protein kinase (AMPK) and its downstream targets involved in fatty acid oxidation (acetylCoA carboxylase; carnitine-palmitoyltransferase). Moreover, GF knockout mice lacking fasting-induced adipose factor (Fiaf), a circulating lipoprotein lipase inhibitor whose expression is normally selectively suppressed in the gut epithelium by the microbiota, are not protected from diet-induced obesity. Although GF Fiaf-/- animals exhibit similar levels of phosphorylated AMPK as their wild-type littermates in liver and gastrocnemius muscle, they have reduced expression of genes encoding the peroxisomal proliferator-activated receptor coactivator (Pgc-1alpha) and enzymes involved in fatty acid oxidation. Thus, GF animals are protected from diet-induced obesity by two complementary but independent mechanisms that result in increased fatty acid metabolism: (i) elevated levels of Fiaf, which induces Pgc-1alpha; and (ii) increased AMPK activity. Together, these findings support the notion that the gut microbiota can influence both sides of the energy balance equation, and underscore the importance of considering our metabolome in a supraorganismal context.
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                Author and article information

                Contributors
                nyang@cau.edu.cn
                Journal
                Microb Biotechnol
                Microb Biotechnol
                10.1111/(ISSN)1751-7915
                MBT2
                Microbial Biotechnology
                John Wiley and Sons Inc. (Hoboken )
                1751-7915
                30 October 2023
                January 2024
                : 17
                : 1 ( doiID: 10.1111/mbt2.v17.1 )
                : e14361
                Affiliations
                [ 1 ] State Key Laboratory of Animal Biotech Breeding and Frontier Science Center for Molecular Design Breeding China Agricultural University Beijing China
                [ 2 ] National Engineering Laboratory for Animal Breeding and Key Laboratory of Animal Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs China Agricultural University Beijing China
                [ 3 ] Department of Animal Genetics and Breeding, College of Animal Science and Technology China Agricultural University Beijing China
                [ 4 ] Sanya Institute of China Agricultural University Hainan China
                Author notes
                [*] [* ] Correspondence

                Ning Yang, Department of Animal Genetics and Breeding, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China.

                Email: nyang@ 123456cau.edu.cn

                Author information
                https://orcid.org/0000-0002-0514-2847
                https://orcid.org/0000-0001-5772-3320
                Article
                MBT214361 MICROBIO-2023-323.R1
                10.1111/1751-7915.14361
                10832551
                37902307
                1db2cdd5-9ab7-423b-8090-29a243235519
                © 2023 The Authors. Microbial Biotechnology published by Applied Microbiology International and John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

                History
                : 30 September 2023
                : 21 July 2023
                : 11 October 2023
                Page count
                Figures: 3, Tables: 2, Pages: 18, Words: 13844
                Funding
                Funded by: National Natural Science Foundation of China , doi 10.13039/501100001809;
                Award ID: 32102535
                Funded by: National Key Research and Development Program of China , doi 10.13039/501100012166;
                Award ID: 2022YFF1000204
                Funded by: Key Research and Development Program of Hainan Province
                Award ID: ZDYF2023XDNY036
                Categories
                Mini Review
                Mini Reviews
                Custom metadata
                2.0
                January 2024
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.3.6 mode:remove_FC converted:01.02.2024

                Biotechnology
                Biotechnology

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