Research Progress on Regulation Mechanism of Microbiota-gut-brain Axis in Livestock and Poultry
GENG Dan-Dan1,2, LI Xiao-Fan1,2, BI Yu-Lin2, JIANG Yong2, Wang Zhi-Xiu2, CHANG Guo-Bin1,2, CHEN Guo-Hong1,2, BAI Hao1,*
1 Joint International Research Laboratory of Agriculture and Agri-Product Safety, the Ministry of Education of China, Institutes of Agricultural Science and Technology Development, Yangzhou University, Yangzhou 225009, China; 2 College of Animal Science and Technology, Yangzhou University, Yangzhou 225009, China
Abstract：The microbiota-gut-brain axis (MGBA) is one of the most important physiological metabolic regulation mechanisms in animals. The gut microbiota plays a key role in the bidirectional response system mediated by the gut and the brain through neural and endocrine substances. Currently, there have been many reports on MGBA in the field of nutritional metabolism of livestock and poultry, while there are few studies on production and application and functional diseases of livestock and poultry. Based on the relationship between microorganisms and their metabolites and the host intestines, neuroendocrine system, and immune system, this article summarizes the research progress of livestock and poultry MGBA regulation, with a view to providing new ideas for the research and application of livestock and poultry MGBA, to achieving the purpose of scientific and efficient breeding, thereby improving the economic benefits and animal welfare of livestock and poultry and promoting the efficient and healthy development of the livestock and poultry breeding industry.
耿丹丹, 李潇凡, 毕瑜林, 江勇, 王志秀, 常国斌, 陈国宏, 白皓. 畜禽微生物-肠-脑轴调节机制研究进展[J]. 农业生物技术学报, 2023, 31(2): 404-415.
GENG Dan-Dan, LI Xiao-Fan, BI Yu-Lin, JIANG Yong, Wang Zhi-Xiu, CHANG Guo-Bin, CHEN Guo-Hong, BAI Hao. Research Progress on Regulation Mechanism of Microbiota-gut-brain Axis in Livestock and Poultry. 农业生物技术学报, 2023, 31(2): 404-415.
[1] 龚雪娜, 贾婷, 张浩, 等. 2021. 肠脑轴参与动物食欲的调节机制[J]. 生命的化学, 41(01): 61-67. (Gong X N, Jia T, Zhang H, et al.2021. The gut brain axis involved in the regulation of appetite in animals[J]. Chemistry of Life, 41(01): 61-67.) [2] 梁晶晶, 马冰洁, 静进. 2020. 微生物-肠-脑轴在孤独症谱系障碍中作用的研究进展[J]. 教育生物学杂志, 8(01): 74-78. (Liang J J, Ma B J, Jing J.2020. Advances in the role of microbiota-gut-brain axis in autism spectrum disorders[J]. Journal of Bio-education, 8(01): 74-78.) [3] 刘飞飞, 秦贵信, 姜海龙, 等. 2015. 脑-肠轴及其在动物摄食调控中的作用[J]. 畜牧兽医学报, 46(07): 1077-1083. (Liu F F, Qin G X, Jiang H L, et al.2015. Brain-gut axis and its role in feeding regulation in animals[J].Chinese Journal of Animal and Veterinary Sciences, 46(07): 1077-1083.) [4] 罗佳, 金锋. 2014. 肠道菌群影响宿主行为的研究进展[J]. 科学通报, 59(22): 2169-2190. (Luo J, Jin F.2014.Advances in studies on effects of gut microbiota on host behavior[J]. Chinese Science Bulletin, 59(22): 2169-2190.) [5] 彭会清, 贺莹, 欧阳丽君, 等. 2021. 短链脂肪酸在精神疾病中的研究进展[J]. 国际精神病学杂志, 48(04): 577-579. (Peng H Q, He Y, Ouyang L J, et al.2021. Progress of short chain fatty acids in psychiatric disorders[J].Journal of International Psychiatry, 48(04): 577-579.) [6] 王淑玲, 王后福, 盖叶顶, 等. 2019. 浅析反刍动物胃肠道微生物通过肠道—脑轴对宿主的影响[J]. 中国畜牧兽医, 46(12): 3598-3606. (Wang S L, Wang W F, Gaiye D, et al.2019. A brief analysis of the effect of gastrointestinal microorganisms on the host in ruminants through the intestine-brain axis[J].Chineseanimal Husbandry and Veterinary Medicine, 46(12): 3598-3606.) [7] 朱艳芝, 马文锋, 陈晓晨, 等. 2020. 色氨酸分解代谢及其在猪饲粮中的应用进展[J]. 动物营养学报, 32(03): 1019-1024. (Zhu Y Z, Ma W F, Chen X C, et al.2020. Tryptophan catabolism and its application in pig diet[J]. Chinese Journal of Animal Nutrition, 32(03): 1019-1024.) [8] 邹昕羽, Cheng H, 金美兰, 等. 2021. 微生物-肠-脑轴调控蛋鸡应激性异常行为的研究进展[J]. 动物营养学报, 33(04): 1859-1868. (Zou X Y, Cheng H, Jin M L, et al.2021. Research progress of microbiota-gut-brain axis regulating stress abnormal behavior in laying hens[J]. Chinese Journal of Animal Nutrition, 33(04): 1859-1868.) [9] Abbott C R, Monteiro M, Small C J, et al.2005. The inhibitory effects of peripheral administration of peptide YY(3-36) and glucagon-like peptide-1 on food intake are attenuated by ablation of the vagal-brainstem-hypothalamic pathway[J]. Brain Research, 1044(1): 127-131. [10] Ait-Belgnaoui A, Colom A, Braniste V, et al.2014. Probiotic gut effect prevents the chronic psychological stress-induced brain activity abnormality in mice[J]. Neurogastroenterology and Motility, 26(4): 510-520. [11] Bailey M T, Dowd S E, Galley J D, et al.2011. Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation[J]. Brain, Behavior, and Immunity, 25(3): 397-407. [12] Bansal T, Alaniz R C, Wood T K, et al.2010. The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation[J]. Proceedings of the National Academy of Sciences of the USA, 107(1): 228-233. [13] Batterham R L, Cowley M A, Small C J, et al.2002. Gut hormone PYY(3-36) physiologically inhibits food intake[J]. Nature, 418(6898): 650-654. [14] Bengmark S.2013. Gut microbiota, immune development and function[J]. Pharmacological Research, 69(1): 87-113. [15] Blevins J E, Stanley B G, Reidelberger R D.2000. Brain regions where cholecystokinin suppresses feeding in rats[J]. Brain Research, 860(1-2): 1-10. [16] Bravo J A, Forsythe P, Chew M V, et al.2011. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve[J]. Proceedings of the National Academy of Sciences of the USA, 108(38): 16050-16055. [17] Brown D G, Soto R, Yandamuri S, et al.2019. The microbiota protects from viral-induced neurologic damage through microglia-intrinsic TLR signaling[J]. Elife, 8: e47117. [18] Browning K N, Verheijden S, Boeckxstaens G E.2017. The vagus nerve in appetite regulation, mood, and intestinal inflammation[J]. Gastroenterology, 152(4): 730-744. [19] Butel M J.2014. Probiotics, gut microbiota and health[J]. Medecine et Maladies Infectieuses, 44(1): 1-8. [20] Calefi A S, da Silva Fonseca J G, Cohn D W, et al.2016. The gut-brain axis interactions during heat stress and avian necrotic enteritis[J]. Poultry Science, 95: 1005-1014. [21] Calefi A S, da Silva Fonseca J G, de Queiroz Nunes C A, et al.2019. Heat stress modulates brain monoamines and their metabolites production in broiler chickens co-infected with Clostridium perfringens type A and Eimeria spp[J]. Veterinary Sciences, 6(1): 4. [22] Camara M L, Corrigan F, Jaehne E J, et al.2015. Effects of centrally administered etanercept on behavior, microglia, and astrocytes in mice following a peripheral immune challenge[J]. Neuropsychopharmacology, 40(2): 502-512. [23] Carabotti M, Scirocco A, Maselli M A, et al.2015. The gut-brain axis: Interactions between enteric microbiota, central and enteric nervous systems[J]. Annals of Gastroenterology, 28(2): 203-209. [24] Chandra R, Liddle R A.2007. Cholecystokinin[J]. Current Opinion in Endocrinology, Diabetes, and Obesity, 14(1): 63-67. [25] Chimerel C, Emery E, Summers D K, et al.2014. Bacterial metabolite indole modulates incretin secretion from intestinal enteroendocrine L cells[J]. Cell Reports, 9(4): 1202-1208. [26] Cryan J F, O'Riordan K J, Cowan C S M, et al.2019. The microbiota-gut-brain axis[J]. Physiological Reviews, 99(4): 1877-2013. [27] Dürk T, Panther E, Müller T, et al.2005. 5-Hydroxytryptamine modulates cytokine and chemokine production in LPS-primed human monocytes via stimulation of different 5-HTR subtypes[J]. International Immunology, 17(5): 599-606. [28] Egerod K L, Petersen N, Timshel P N, et al.2018. Profiling of G protein-coupled receptors in vagal afferents reveals novel gut-to-brain sensing mechanisms[J]. Molecular Metabolism, 12: 62-75. [29] Farzi A, Fröhlich E E, Holzer P.2018. Gut microbiota and the neuroendocrine system[J]. Neurotherapeutics, 15(1):5-22. [30] Fleming S A, Monaikul S, Patsavas A J, et al.2019. Dietary polydextrose and galactooligosaccharide increase exploratory behavior, improve recognition memory, and alter neurochemistry in the young pig[J]. Nutritional Neuroscience, 22(7): 499-512. [31] Foster J A, Rinaman L, Cryan J F.2017. Stress & the gut-brain axis: Regulation by the microbiome[J]. Neurobiology of Stress, 7: 124-136. [32] Forsythe P, Bienenstock J, Kunze W A.2014. Vagal pathways for microbiome-brain-gut axis communication[J]. Advances in Experimental Medicine and Biology, 817: 115-133. [33] Furness J B.2000. Types of neurons in the enteric nervous system[J]. Journal of the Autonomic Nervous System, 81(1-3): 87-96. [34] Furness J B.2012. The enteric nervous system and neurogastroenterology[J]. Nature Reviews Gastroenterology & Hepatology, 9(5): 286-294. [35] Furness J B, Callaghan B P, Rivera L R, et al.2014. The enteric nervous system and gastrointestinal innervation: Integrated local and central control[J]. Advances in Experimental Medicine and Biology, 817: 39-71. [36] Furusawa Y, Obata Y, Fukuda S, et al.2013. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells[J]. Nature, 504(7480): 446-450. [37] Gasbarrini G, Bonvicini F, Gramenzi A.2016. Probiotics history[J]. Journal of Clinical Gastroenterology, 50(2): S116-S119. [38] Geng Z H, Zhu Y, Li Q L, et al.2022. Enteric nervous system: The bridge between the gut microbiota and neurological disorders[J]. Frontiers in Aging Neuroscience, 14:810483. [39] Goswami C, Iwasaki Y, Yada T.2018. Short chain fatty acids suppress food intake by activating vagal afferent neurons[J]. Journal of Nutritional Biochemistry, 57: 130-135. [40] Gunawardene A R, Corfe B M, Staton C A.2011. Classification and functions of enteroendocrine cells of the lower gastrointestinal tract[J]. International Journal of Experimental Pathology, 92(4): 219-231. [41] Hata T, Asano Y, Yoshihara K, et al.2017. Regulation of gut luminal serotonin by commensal microbiota in mice[J]. PLOS ONE, 12(7): e0180745. [42] Heanue T A, Shepherd I T, Burns A J.2016. Enteric nervous system development in avian and zebrafish models[J]. Developmental Biology, 417(2): 129-138. [43] Hillestad E M R, van der Meeren A, Nagaraja B H, et al.2022. Gut bless you: The microbiota-gut-brain axis in irritable bowel syndrome[J]. World Journal of Gastroenterology , 28(4):412-431. [44] Hiramatsu K.2020. Chicken intestinal L cells and glucagon-like peptide-1 secretion[J]. The Journal of Poultry Science, 57(1): 1-6. [45] Jaglin M, Rhimi M, Philippe C, et al.2018. Indole, a signaling molecule produced by the gut microbiota, negatively impacts emotional behaviors in rats[J]. Frontiers in Neuroscience, 12: 216. [46] Jiao A, Yu B, He J, et al.2020. Short chain fatty acids could prevent fat deposition in pigs via regulating related hormones and genes[J]. Food & Function, 11(2): 1845-1855. [47] Kennedy P J, Cryan J F, Dinan T G, et al.2017. Kynurenine pathway metabolism and the microbiota-gut-brain axis[J]. Neuropharmacology, 112(Pt B): 399-412. [48] Kimura I, Ozawa K, Inoue D, et al.2013. The gut microbiota suppresses insulin-mediated fat accumulation via the short-chain fatty acid receptor GPR43[J]. Nature Communications, 4: 1829. [49] Lacey J A, Stanley D, Keyburn A L, et al.2018. Clostridium perfringens-mediated necrotic enteritis is not influenced by the pre-existing microbiota but is promoted by large changes in the post-challenge microbiota[J]. Veterinary Microbiology, 227: 119-126. [50] La Fata G, Weber P, Mohajeri M H.2018. Probiotics and the gut immune system: Indirect regulation[J]. Probiotics and Antimicrobial Proteins, 10(1): 11-21. [51] Larraufie P, Martin-Gallausiaux C, Lapaque N, et al.2018. SCFAs strongly stimulate PYY production in human enteroendocrine cells[J]. Scientific Reports, 8(1): 74. [52] Latorre R, Sternini C, De Giorgio R, et al.2016. Enteroendocrine cells: A Review of their role in brain-gut communication[J]. Neurogastroenterology and Motility, 28(5): 620-630. [53] Liang G, Malmuthuge N, McFadden T B, et al.2014. Potential regulatory role of microRNAs in the development of bovine gastrointestinal tract during early life[J]. PLOS ONE, 9(3): e92592. [54] Liu Y, Sanderson D, Mian M F, et al.2021. Loss of vagal integrity disrupts immune components of the microbiota-gut-brain axis and inhibits the effect of Lactobacillus rhamnosus on behavior and the corticosterone stress response[J]. Neuropharmacology, 195: 108682. [55] Lyte M.2014. Microbial endocrinology: Host-microbiota neuroendocrine interactions influencing brain and behavior[J]. Gut Microbes, 5(3): 381-389. [56] Maranduba C M, De Castro S B, de Souza G T, et al. 2015. Intestinal microbiota as modulators of the immune system and neuroimmune system: Impact on the host health and homeostasis[J]. Journal of Immunology Research, 2015: 931574. [57] Martin C R, Osadchiy V, Kalani A, et al.2018. The brain-gut-microbiome axis[J]. Cellular and Molecular Gastroenterology and Hepatology, 6(2): 133-148. [58] Meimandipour A, Soleimani F A, Houshmand M, et al.2011. Effects of rough handling on short chain fatty acid production and gastrointestinal pH in broilers and modulatory role of Lactobacilli[J]. African Journal of Biotechnology, 10(74): 17030-17037. [59] Mindus C, van Staaveren N, Fuchs D, et al.2021. L. rhamnosus improves the immune response and tryptophan catabolism in laying hen pullets[J]. Scientific Reports, 11(1): 19538. [60] Moore R J.2016. Necrotic enteritis predisposing factors in broiler chickens[J]. Avian Pathology, 45(3): 275-281. [61] Nøhr M K, Pedersen M H, Gille A, et al.2013. GPR41/FFAR3 and GPR43/FFAR2 as cosensors for short-chain fatty acids in enteroendocrine cells vs FFAR3 in enteric neurons and FFAR2 in enteric leukocytes[J]. Endocrinology, 154(10): 3552-3564. [62] O'Mahony S M, Hyland N P, Dinan T G, et al.2011. Maternal separation as a model of brain-gut axis dysfunction[J]. Psychopharmacology, 214(1): 71-88. [63] Peng L, He Z, Chen W, et al.2007. Effects of butyrate on intestinal barrier function in a Caco-2 cell monolayer model of intestinal barrier[J]. Pediatric Research, 61(1): 37-41. [64] Poretsky R, Rodriguez-R L M, Luo C, et al.2014. Strengths and limitations of 16S rRNA gene amplicon sequencing in revealing temporal microbial community dynamics[J]. PLOS ONE, 9(4): e93827. [65] Ren W, Yin J, Xiao H, et al.2017. Intestinal microbiota-derived GABA mediates interleukin-17 expression during enterotoxigenic Escherichia coli Infection[J]. Frontiers in Immunology, 7: 685. [66] Rossi G, Pengo G, Caldin M, et al.2014. Comparison of microbiological, histological, and immunomodulatory parameters in response to treatment with either combination therapy with prednisone and metronidazole or probiotic VSL#3 strains in dogs with idiopathic inflammatory bowel disease[J]. PLOS ONE, 9(4): e94699. [67] Ruddick J P, Evans A K, Nutt D J, et al.2006. Tryptophan metabolism in the central nervous system: medical implications[J]. Expert Reviews in Molecular Medicine, 8(20): 1-27. [68] Salfen B E, Carroll J A, Keisler D H, et al.2004. Effects of exogenous ghrelin on feed intake, weight gain, behavior, and endocrine responses in weanling pigs[J]. Journal of Animal Science, 82(7): 1957-1966. [69] Sauleau P, Lapouble E, Val-Laillet D, et al.2009. The pig model in brain imaging and neurosurgery (review)[J]. Animal, 3(8): 1138-1151. [70] Savory C J, Gentle M J.1980. Intravenous injections of cholecystokinin and caerulein suppress food intake in domestic fowls[J]. Experientia, 36(10): 1191-1192. [71] Schalla M A, Stengel A.2018. The role of ghrelin in anorexia nervosa[J]. International Journal of Molecular Sciences, 19(7): 2117. [72] Shimizu S, Nakamachi T, Konno N, et al.2014. Orexin A enhances food intake in bullfrog larvae[J]. Peptides, 59: 79-82. [73] Sittipo P, Choi J, Lee S, et al.2022. The function of gut microbiota in immune-related neurological disorders: A review[J]. Journal of Neuroinflammation, 19(1):154. [74] Soret R, Chevalier J, De Coppet P, et al.2010. Short-chain fatty acids regulate the enteric neurons and control gastrointestinal motility in rats[J]. Gastroenterology, 138(5): 1772-1782. [75] Spencer N J, Hu H.2020. Enteric nervous system: Sensory transduction, neural circuits and gastrointestinal motility[J]. Nature Reviews Gastroenterology & Hepatology, 17(6): 338-351. [76] Strader A D, Woods S C.2005. Gastrointestinal hormones and food intake[J]. Gastroenterology, 128(1): 175-191. [77] Stracke J, Otten W, Tuchscherer A, et al.2017. Dietary tryptophan supplementation and affective state in pigs[J]. Journal of Veterinary Behavior, 20: 82-90. [78] Strandwitz P, Kim K H, Terekhova D, et al.2019. GABA-modulating bacteria of the human gut microbiota[J]. Nature Microbiology, 4(3):396-403. [79] Sudo N, Chida Y, Aiba Y, et al.2004. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice[J]. The Journal of Physiology, 558(Pt 1): 263-275. [80] Viladomiu M, Hontecillas R, Yuan L, et al.2013. Nutritional protective mechanisms against gut inflammation[J]. The Journal of Nutritional Biochemistry, 24(6): 929-939. [81] Villageliu D N, Lyte M.2017. Microbial endocrinology: Why the intersection of microbiology and neurobiology matters to poultry health[J]. Poultry Science, 96(8): 2501-2508. [82] Wang F B, Powley T L.2007. Vagal innervation of intestines: afferent pathways mapped with new en bloc horseradish peroxidase adaptation[J]. Cell and Tissue Research, 2007, 329(2): 221-230. [83] Wang H X, Wang Y P.2016. Gut microbiota-brain axis[J]. Chinese Medical Journal, 129(19): 2373-2380. [84] Wang S Z, Yu Y J, Adeli K.2020. Role of gut microbiota in neuroendocrine regulation of carbohydrate and lipid metabolism via the microbiota-gut-brain-liver axis[J]. Microorganisms, 8(4): 527. [85] Wang W C, Yan F F, Hu J Y, et al.2018. Supplementation of bacillus subtilis-based probiotic reduces heat stress-related behaviors and inflammatory response in broiler chickens[J]. Journal of Animal Science, 96(5): 1654-1666. [86] Wang Y, Du W, Lei K, et al.2017. Effects of dietary Bacillus licheniformis on gut physical barrier, immunity, and reproductive hormones of laying hens[J]. Probiotics Antimicrobial Proteins, 9(3): 292-299. [87] Yang X, Yu D, Xue L, et al.2020. Probiotics modulate the microbiota-gut-brain axis and improve memory deficits in aged SAMP8 mice[J]. Acta Pharmaceutica Sinica B, 10(3): 475-487. [88] Yelin I, Flett K B, Merakou C, et al.2019. Genomic and epidemiological evidence of bacterial transmission from probiotic capsule to blood in ICU patients[J]. Nature Medicine, 25(11): 1728-1732. [89] Yoo B B, Mazmanian S K.2017. The enteric network: Interactions between the immune and nervous systems of the gut[J]. Immunity, 46(6): 910-926. [90] Zhou L, Zhang M, Wang Y, et al.2018. Faecalibacterium prausnitzii produces butyrate to maintain Th17/Treg balance and to ameliorate colorectal colitis by inhibiting histone deacetylase 1[J]. Inflammatory Bowel Disease, 24: 1926-1940.
