Exercise influences fatty acids in the longissimus dorsi muscle of Sunit lambs and improves dressing percentage by affecting digestion, absorption, and lipid metabolism
Main Article Content
Keywords
lamb, absorption, slaughter performance, short-chain fatty acids, fatty acid
Abstract
The transition from grazing to captive rearing resulted in a significant decline in meat quality. To enhance the quality of meat from captive sheep, we examined the impact of exercise on Sunit lambs. The lambs, with similar body weight and aged 3 months underwent a 90-day period of thought-driven exercise. At the end of the exercise period, we collected colonic contents, epithelial tissues, and the longissimus dorsi muscle, and recorded slaughter performance. Exercise was found to have a significant impact on the content of short-chain fatty acids in the colon. Additionally, it generally reduced the mRNA expression of fatty acid absorption transporter genes in the colonic epithelium and lipid metabolism-related genes in the longissimus dorsi muscle. Furthermore, exercise significantly affected the content of fatty acids in the longissimus dorsi muscle of Sunit lambs, and increased its dressing percentage. Exercise influences the composition of fatty acids of the longissimus dorsi muscle and improves dressing percentage by affecting the digestion, absorption, and metabolism of lipids in Sunit lambs. This could be profitable for the livestock industry, and could alter the nutrition and flavor of lamb meat.
References
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Rebec, G.V., Koceja, D.M., and Bunner, K. D., 2022. Measuring movement in health and disease. Brain Research Bulletin 181: 167–174. 10.1016/j.brainresbull.2022.01.021
Samuel, B.S., Shaito, A., Motoike, T., Rey, F.E., Backhed, F., Manchester, J.K., et al. 2008. Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41. Proceedings of the National Academy of Sciences 105(43): 16767–16772. 10.1073/pnas.0808567105
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Spence, J.R., Lauf, R., and Shroyer, N.F., 2011. Vertebrate intestinal endoderm development. Developmental Dynamics 240(3): 501–520. 10.1002/dvdy.22540
Stahl, A., 2004. A current review of fatty acid transport proteins (SLC27). Pflügers Archives 447(5): 722–727. 10.1007/s00424-003-1106-z
Stojanović, O., Altirriba, J., Rigo, D., Spiljar, M., Evrard, E., Roska, B., et al. 2021. Dietary excess regulates absorption and surface of gut epithelium through intestinal PPARα. Nature Communications 12(1): 7031. 10.1038/s41467-021-27133-7
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Teng, Y., Wang, Y., Tian, Y., Chen, Y.Y., Guan, W.Y., Piao, C.H., et al. 2020. Lactobacillus plantarum LP104 ameliorates hyperlipidemia induced by AMPK pathways in C57BL/6N mice fed high-fat diet. Journal of Functional Foods 64: 103665. 10.1016/j.jff.2019.103665
Tolhurst, G., Heffron, H., Lam, Y.S., Parker, H.E., Habib, A.M., Diakogiannaki, E., et al. 2012. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the g-protein–coupled receptor FFAR2. Diabetes 61(2): 364–371. 10.2337/db11-1019
Volpi-Lagreca, G., Gelid, L.F., Alende, M., Bressan, E.R., Pordomingo, A.B., and Pordomingo, A.J., 2021. Effect of placement weight and days on feed on feedlot cattle performance and carcass traits. Livestock Science 244: 104392. 10.1016/j.livsci.2020.104392
von Eckardstein, A., Nordestgaard, B.G., Remaley, A.T., and Catapano, A.L., 2023. High-density lipoprotein revisited: biological functions and clinical relevance. European Heart Journal 44(16): 1394–1407. 10.1093/eurheartj/ehac605
Wang, B., Luo, Y., Wang, Y., Wang, D., Hou, Y., Yao, D., et al. 2021. Rumen bacteria and meat fatty acid composition of Sunit sheep reared under different feeding regimens in China. Journal of the Science of Food and Agriculture 101(3): 1100–1110. 10.1002/jsfa.10720
Wang, D., Tang, G., Yu, J., Li, Y., Feng, L., Liu, H., et al. 2023. Microbial enterotypes shape the divergence in gut fermentation, host metabolism and growth rate of young goats. Microbiology Spectrum 11(1): e04818–e04822. 10.1128/spectrum.04818-22
Wen, K., Zhao, M.M., Liu, L., Khogali, M.K., Geng, T.Y., Wang, H.R., et al. 2021. Thiamine modulates intestinal morphological structure and microbiota under subacute ruminal acidosis induced by a high-concentrate diet in Saanen goats. Animal 15(10): 100370. 10.1016/j.animal.2021.100370
Wrzosek, L., Miquel, S., Noordine, M.-L., Bouet, S., Chevalier-Curt, M.J., Robert, V., et al. 2013. Bacteroides thetaiotaomicron and Faecalibacterium prausnitziiinfluence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent. BMC Biology 11(1): 61. 10.1186/1741-7007-11-61
Wang, Y.C., Wangm X., Li, J.Z., Huang, P.F., Li, Y.L., Ding, X.Q., Huangm J., et al., 2023. The impact of lactating Hu sheep’s dietary protein levels on lactation performance, progeny growth and rumen development. Animal Biotechnology 34(6): 1919–1930. 10.1080/10495398.2022.2058006
Yang, J.J., Pham, M.T., Rahim, A.R., Chuang, T.-H., Hsieh, M.-F., and Huang, C.-M., 2020. Mouse abdominal fat depots reduced by butyric acid-producing leuconostoc mesenteroides. Microorganisms 8(8): 1180. 10.3390/microorganisms8081180
Yao, D., Su, R., Zhang, Y., Wang, B., Hou, Y., Luo, Y., et al. 2022. Impact of dietary Lactobacillus supplementation on intramuscular fat deposition and meat quality of Sunit sheep. Journal of Food Biochemistry 46(8): e14207.
Ye, Z., Cao, C., Li, Q., Xu, Y.J., Liu, Y., 2020. Different dietary lipid consumption affects the serum lipid profiles, colonic short chain fatty acid composition and the gut health of Sprague Dawley rats. Food Res Int. 132: 109117. 10.1016/j.foodres.2020.109117.
Li, Z.C., Liu, D.H., Gu, R.C., Qiao, Y., Jin, Q., Zhang, Y.J., et al. 2023. Fecal microbiota transplantation in obesity metabolism: A meta analysis and systematic review. Diabetes Res Clin Pract 202: 110803. 10.1016/j.diabres.2023.110803.
Zha, A., Tan, B., Wang, J., Qi, M., Deng, Y., Li, R., et al. 2023. Dietary supplementation modified attapulgite promote intestinal epithelial barrier and regulate intestinal microbiota composition to prevent diarrhea in weaned piglets. International Immunopharmacology 117: 109742. 10.1016/j.intimp.2023.109742
Zheng, L., Kelly, C.J., Battista, K.D., Schaefer, R., Lanis, J.M., Alexeev, E.E., et al. 2017. Microbial-derived butyrate promotes epithelial barrier function through IL-10 receptor–dependent repression of claudin-2. Journal of Immunology 199(8): 2976–2984. 10.4049/jimmunol.1700105
Zimmermann, P., and Curtis, N., 2019. The effect of antibiotics on the composition of the intestinal microbiota–a systematic review. Journal of Infection 79(6): 471–489. 10.1016/j.jinf.2019.10.008
Dias, B.V., Gomes, S.V., da Cruz Castro, M.L., Carvalho, L.C.F., Breguez, G.S., de Souza, D.M.S., et al. 2022. EPA/DHA and linseed oil have different effects on liver and adipose tissue in rats fed with a high-fat diet. Prostaglandins & Other Lipid Mediators 159: 106622. 10.1016/j.prostaglandins.2022.106622
Du, E., Guo, W., Zhao, N., Chen, F., Fan, Q., Zhang, W., et al. 2022. Effects of diets with various levels of forage rape (Brassica napus) on growth performance, carcass traits, meat quality and rumen microbiota of Hu lambs. Journal of the Science of Food and Agriculture 102(3): 1281–1291. 10.1002/jsfa.11466
Dunne, P.G., Monahan, F.J., and Moloney, A.P., 2011. Current perspectives on the darker beef often reported from extensively managed cattle: does physical activity play a significant role? Livestock Science 142(1–3): 1–22.
Fu, J., Wang, Y., Tan, S., and Wang, J., 2021. Effects of banana resistant starch on the biochemical indexes and intestinal flora of obese rats induced by a high-fat diet and their correlation analysis. Frontiers in Bioengineering and Biotechnology 9: 575724. 10.3389/fbioe.2021.575724
Gangnat, I.D.M., Leiber, F., Dufey, P.A., Silacci, P., Kreuzer, M., and Berard, J., 2017. Physical activity, forced by steep pastures, affects muscle characteristics and meat quality of suckling beef calves. Cambridge University Press, Cambridge UK, p. 2.
Haghikia, A., Zimmermann, F., Schumann, P., Jasina, A., Roessler, J., Schmidt, D., et al. 2022. Propionate attenuates atherosclerosis by immune-dependent regulation of intestinal cholesterol metabolism. European Heart Journal 43(6): 518–533. 10.1093/eurheartj/ehab644
Hayashi, Y., Lee-Okada, H.-C., Nakamura, E., Tada, N., Yokomizo, T., Fujiwara, Y., et al. 2021. Ablation of fatty acid desaturase 2 (FADS2) exacerbates hepatic triacylglycerol and cholesterol accumulation in polyunsaturated fatty acid-depleted mice. FEBS Letters 595(14): 1920–1932. 10.1002/1873-3468.14134
Hou, Y., Su, L., Su, R., Luo, Y., Wang, B., Yao, D., et al. 2020. Effect of feeding regimen on meat quality, MyHC isoforms, AMPK, and PGC-1α genes expression in the biceps femoris muscle of Mongolia sheep. Food Science & Nutrition 8(5): 2262–2270. 10.1002/fsn3.1494
Hu, B., Ye, C., Leung, E.L.-H., Zhu, L., Hu, H., Zhang, Z., et al. 2020. Bletilla striata oligosaccharides improve metabolic syndrome through modulation of gut microbiota and intestinal metabolites in high fat diet-fed mice. Pharmacological Research, 159: 104942. 10.1016/j.phrs.2020.104942
Hughes, R. L., and Holscher, H. D., 2021. Fueling gut microbes: a review of the interaction between diet, exercise, and the gut microbiota in athletes. Advances in Nutrition 12(6): 2190–2215. 10.1093/advances/nmab077
Izuddin, W.I., Loh, T.C., Samsudin, A.A., Foo, H.L., Humam, A.M., and Shazali, N., 2019. Effects of post-biotic supplementation on growth performance, ruminal fermentation and microbial profile, blood metabolite and GHR, IGF-1 and MCT-1 gene expression in post-weaning lambs. BMC Veterinary Research 15(1): 315. 10.1186/s12917-019-2064-9
Jang, H.J., Kim, D.M., Kim, K.B., Park, J.W., Choi, J.Y., Oh, J.H., et al. 2017. Analysis of metabolomic patterns in thoroughbreds before and after exercise. Asian-Australasian Journal of Animal Sciences 30(11): 1633–1642. 10.5713/ajas.17.0167
Joo, S.T., Kim, G.D., Hwang, Y.H., and Ryu, Y.C., 2013. Control of fresh meat quality through manipulation of muscle fiber characteristics. Meat Science, 95(4): 828–836. 10.1016/j.meatsci.2013.04.044
Koh, A., De Vadder, F., Kovatcheva-Datchary, P., and Bäckhed, F., 2016. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell 165(6): 1332–1345. 10.1016/j.cell.2016.05.041
Larqué, E., Demmelmair, H., Klingler, M., De Jonge, S., Bondy, B., and Koletzko, B., 2006. Expression pattern of fatty acid transport protein-1 (FATP-1), FATP-4 and heart-fatty acid binding protein (H-FABP) genes in human term placenta. Early Human Development 82(10): 697–701. 10.1016/j.earlhumdev.2006.02.001
Ma, Y., Han, L., Zhang, S., Zhang, X., Hou, S., Gui, L., et al. 2023. Insight into the differences of meat quality between Qinghai white Tibetan sheep and black Tibetan sheep from the perspective of metabolomics and rumen microbiota. Food Chemistry: X 19: 100843. 10.1016/j.fochx.2023.100843
Mann, S., Beedie, C., and Jimenez, A., 2014. Differential effects of aerobic exercise, resistance training and combined exercise modalities on cholesterol and the lipid profile: review, synthesis and recommendations. Sports Medicine 44(2): 211–221. 10.1007/s40279-013-0110-5
Matsumoto, M., Inoue, R., Tsukahara, T., Ushida, K., Chiji, H., Matsubara, N., et al. 2008. Voluntary running exercise alters microbiota composition and increases n-butyrate concentration in the rat cecum. Bioscience, Biotechnology and Biochemistry, 72(2): 572–576. 10.1271/bbb.70474
Michal, J.J., Zhang, Z.W., Gaskins, C.T., and Jiang, Z., 2006. The bovine fatty acid binding protein 4 gene is significantly associated with marbling and subcutaneous fat depth in Wagyu×Limousin F2 crosses. Animal Genetics 37(4): 400–402. 10.1111/j.1365-2052.2006.01464.x
Quiroga, R., Nistal, E., Estébanez, B., Porras, D., Juárez-Fernández, M., Martínez-Flórez, S., et al. 2020. Exercise training modulates the gut microbiota profile and impairs inflammatory signaling pathways in obese children. Experimental & Molecular Medicine 52(7): 1048–1061. 10.1038/s12276-020-0459-0
Rebec, G.V., Koceja, D.M., and Bunner, K. D., 2022. Measuring movement in health and disease. Brain Research Bulletin 181: 167–174. 10.1016/j.brainresbull.2022.01.021
Samuel, B.S., Shaito, A., Motoike, T., Rey, F.E., Backhed, F., Manchester, J.K., et al. 2008. Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41. Proceedings of the National Academy of Sciences 105(43): 16767–16772. 10.1073/pnas.0808567105
Semeraro, M.D., Almer, G., Kaiser, M., Zelzer, S., Meinitzer, A., Scharnagl, H., et al. 2022. The effects of long-term moderate exercise and western-type diet on oxidative/nitrosative stress, serum lipids and cytokines in female Sprague Dawley rats. European Journal of Nutrition 61(1): 255–268. 10.1007/s00394-021-02639-4
Spence, J.R., Lauf, R., and Shroyer, N.F., 2011. Vertebrate intestinal endoderm development. Developmental Dynamics 240(3): 501–520. 10.1002/dvdy.22540
Stahl, A., 2004. A current review of fatty acid transport proteins (SLC27). Pflügers Archives 447(5): 722–727. 10.1007/s00424-003-1106-z
Stojanović, O., Altirriba, J., Rigo, D., Spiljar, M., Evrard, E., Roska, B., et al. 2021. Dietary excess regulates absorption and surface of gut epithelium through intestinal PPARα. Nature Communications 12(1): 7031. 10.1038/s41467-021-27133-7
Tazoe, H., Otomo, Y., Kaji, I., Tanaka, R., and Kuwahara, A., 2008. Roles of short-chain fatty acids receptors, GPR41 and GPR43 on colonic functions. Journal of Physiology & Pharmacology 59(Suppl 2): 251–262.
Teng, Y., Wang, Y., Tian, Y., Chen, Y.Y., Guan, W.Y., Piao, C.H., et al. 2020. Lactobacillus plantarum LP104 ameliorates hyperlipidemia induced by AMPK pathways in C57BL/6N mice fed high-fat diet. Journal of Functional Foods 64: 103665. 10.1016/j.jff.2019.103665
Tolhurst, G., Heffron, H., Lam, Y.S., Parker, H.E., Habib, A.M., Diakogiannaki, E., et al. 2012. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the g-protein–coupled receptor FFAR2. Diabetes 61(2): 364–371. 10.2337/db11-1019
Volpi-Lagreca, G., Gelid, L.F., Alende, M., Bressan, E.R., Pordomingo, A.B., and Pordomingo, A.J., 2021. Effect of placement weight and days on feed on feedlot cattle performance and carcass traits. Livestock Science 244: 104392. 10.1016/j.livsci.2020.104392
von Eckardstein, A., Nordestgaard, B.G., Remaley, A.T., and Catapano, A.L., 2023. High-density lipoprotein revisited: biological functions and clinical relevance. European Heart Journal 44(16): 1394–1407. 10.1093/eurheartj/ehac605
Wang, B., Luo, Y., Wang, Y., Wang, D., Hou, Y., Yao, D., et al. 2021. Rumen bacteria and meat fatty acid composition of Sunit sheep reared under different feeding regimens in China. Journal of the Science of Food and Agriculture 101(3): 1100–1110. 10.1002/jsfa.10720
Wang, D., Tang, G., Yu, J., Li, Y., Feng, L., Liu, H., et al. 2023. Microbial enterotypes shape the divergence in gut fermentation, host metabolism and growth rate of young goats. Microbiology Spectrum 11(1): e04818–e04822. 10.1128/spectrum.04818-22
Wen, K., Zhao, M.M., Liu, L., Khogali, M.K., Geng, T.Y., Wang, H.R., et al. 2021. Thiamine modulates intestinal morphological structure and microbiota under subacute ruminal acidosis induced by a high-concentrate diet in Saanen goats. Animal 15(10): 100370. 10.1016/j.animal.2021.100370
Wrzosek, L., Miquel, S., Noordine, M.-L., Bouet, S., Chevalier-Curt, M.J., Robert, V., et al. 2013. Bacteroides thetaiotaomicron and Faecalibacterium prausnitziiinfluence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent. BMC Biology 11(1): 61. 10.1186/1741-7007-11-61
Wang, Y.C., Wangm X., Li, J.Z., Huang, P.F., Li, Y.L., Ding, X.Q., Huangm J., et al., 2023. The impact of lactating Hu sheep’s dietary protein levels on lactation performance, progeny growth and rumen development. Animal Biotechnology 34(6): 1919–1930. 10.1080/10495398.2022.2058006
Yang, J.J., Pham, M.T., Rahim, A.R., Chuang, T.-H., Hsieh, M.-F., and Huang, C.-M., 2020. Mouse abdominal fat depots reduced by butyric acid-producing leuconostoc mesenteroides. Microorganisms 8(8): 1180. 10.3390/microorganisms8081180
Yao, D., Su, R., Zhang, Y., Wang, B., Hou, Y., Luo, Y., et al. 2022. Impact of dietary Lactobacillus supplementation on intramuscular fat deposition and meat quality of Sunit sheep. Journal of Food Biochemistry 46(8): e14207.
Ye, Z., Cao, C., Li, Q., Xu, Y.J., Liu, Y., 2020. Different dietary lipid consumption affects the serum lipid profiles, colonic short chain fatty acid composition and the gut health of Sprague Dawley rats. Food Res Int. 132: 109117. 10.1016/j.foodres.2020.109117.
Li, Z.C., Liu, D.H., Gu, R.C., Qiao, Y., Jin, Q., Zhang, Y.J., et al. 2023. Fecal microbiota transplantation in obesity metabolism: A meta analysis and systematic review. Diabetes Res Clin Pract 202: 110803. 10.1016/j.diabres.2023.110803.
Zha, A., Tan, B., Wang, J., Qi, M., Deng, Y., Li, R., et al. 2023. Dietary supplementation modified attapulgite promote intestinal epithelial barrier and regulate intestinal microbiota composition to prevent diarrhea in weaned piglets. International Immunopharmacology 117: 109742. 10.1016/j.intimp.2023.109742
Zheng, L., Kelly, C.J., Battista, K.D., Schaefer, R., Lanis, J.M., Alexeev, E.E., et al. 2017. Microbial-derived butyrate promotes epithelial barrier function through IL-10 receptor–dependent repression of claudin-2. Journal of Immunology 199(8): 2976–2984. 10.4049/jimmunol.1700105
Zimmermann, P., and Curtis, N., 2019. The effect of antibiotics on the composition of the intestinal microbiota–a systematic review. Journal of Infection 79(6): 471–489. 10.1016/j.jinf.2019.10.008
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