Recent Advances on Interaction and Regulation between Intestinal Microflora and Host Mucosal Immune System of Ruminants

  • DU Mei ,
  • LIANG Zeyi ,
  • ZHANG Jianbo ,
  • DING Xuezhi
Expand
  • 1. Key Laboratory of Yak Breeding Engineering, Lanzhou Institute of Husbandry and Pharmaceutical Sciences, Chinese Academy of Agricultural Sciences, Lanzhou 730050, China;
    2. Key Laboratory of Veterinary Pharmaceutical Development, Ministry of Agricultural and Rural Affairs, Lanzhou Institute of Husbandry and Pharmaceutical Sciences, Chinese Academy of Agricultural Sciences, Lanzhou 730050, China

Received date: 2020-10-09

  Online published: 2021-05-14

Supported by

 

Abstract

A large number of microorganisms interact with each other in ruminant intestines to realize the efficient utilization of feed nutrients. Normal and stable intestinal flora is an important guarantee for the health of the body, which play important roles on promote the development of intestinal morphology and structure, maintain normal immune function and resistance to exogenous pathogenic factors and so on. However, due to the complexity of livestock species, breeding environment, feed source and production target, it limits the research of ruminant intestinal microbiome and immune regulation to some extent, especially of the research on the regulation of intestinal flora to improve immunity based on exogenous measures is lagging behind. As everyone knows, ruminants are a "symbiotic population" composed of host organism and symbiotic microorganisms, its phenotypic traits are regulated by its own genes, also affected by "host second genome" digestive tract microorganisms. Therefore, this paper reviewed the related research results in recent years about the important role of ruminant intestinal bacteria in maintaining the integrity of host intestinal mucosal barrier, participating in Toll-like receptors (TLRs) recognition and promoting the development and differentiation of immune cells. Meanwhile, based on the different effects of exogenous regulation measures of intestinal flora on intestinal immune function, this paper summarized the related progress of probiotics and prebiotics targeted intervention to regulate the intestinal immune function of ruminants, so as to establish the references for intensive study in the interaction between intestinal bacteria and host intestinal immunity and provide scientific basis for the establishment of system in reducing antibiotics, green and healthy breeding of ruminants.

Cite this article

DU Mei , LIANG Zeyi , ZHANG Jianbo , DING Xuezhi . Recent Advances on Interaction and Regulation between Intestinal Microflora and Host Mucosal Immune System of Ruminants[J]. Chinese Journal of Animal Nutrition, 2021 , 33(5) : 2483 -2494 . DOI: 10.3969/j.issn.1006-267x.2021.05.009

References

[1] KAMADA N,SEO S U,CHEN G Y,et al.Role of the gut microbiota in immunity and inflammatory disease[J].Nature Reviews Immunology,2013,13(5):321-335.  
[2] ROOKS M G,GARRETT W S.Gut microbiota,metabolites and host immunity[J].Nature Reviews Immunology,2016,16(6):341-352.  
[3] 杨利娜,边高瑞,朱伟云.单胃动物肠道微生物菌群与肠道免疫功能的相互作用[J].微生物学报,2014,54(5):480-486. YANG L N,BIAN G R,ZHU W Y.Interactions between the monogastric animal gut microbiota and the intestinal immune function-a review[J].Acta Microbiologica Sinica,2014,54(5):480-486.(in Chinese)
[4] LIANG G X,MALMUTHUGE N,BAO H,et al.Transcriptome analysis reveals regional and temporal differences in mucosal immune system development in the small intestine of neonatal calves[J].BMC Genomics,2016,17:602.
[5] MA T,VILLOT C,RENAUD D,et al.Linking perturbations to temporal changes in diversity,stability,and compositions of neonatal calf gut microbiota:prediction of diarrhea[J].The ISME Journal,2020,14(9):2223-2235.  
[6] MA C,SUN Z,ZENG B H,et al.Cow-to-mouse fecal transplantations suggest intestinal microbiome as one cause of mastitis[J].Microbiome,2018,6:200.
[7] 袁续,葛盼,侯力月,等.牛副结核病诊断技术的研究进展[J].中国奶牛,2018(9):38-41. YUAN X,GE P,HOU L Y,et al.Research progression of diagnosis for bovine paratuberculosis[J].China Dairy Cattle,2018(9):38-41. (in Chinese)
[8] RODRIGUES R,GUERRA G,SOARES J,et al.Lactobacillus rhamnosus EM1107 in goat milk matrix modulates intestinal inflammation involving NF-κB p65 and SOCs-1 in an acid-induced colitis model[J].Journal of Functional Foods,2018,50:78-92.
[9] MAO S Y,ZHANG M L,LIU J H,et al.Characterising the bacterial microbiota across the gastrointestinal tracts of dairy cattle:membership and potential function[J].Scientific Reports,2015,5:16116.
[10] WANG J,FAN H,HAN Y,et al.Characterization of the microbial communities along the gastrointestinal tract of sheep by 454 pyroseqencing analysis[J].Asian-Australasian Journal of Animal Sciences,2017,30(1):100-110.
[11] THOETKIATTIKUL H,MHUANTONG W,LAOTHANACHAREON T,et al.Comparative analysis of microbial profiles in cow rumen fed with different dietary fiber by tagged 16S rRNA gene pyrosequencing[J].Current Microbiology,2013,67(2):130-137.  
[12] SPENCE C,WELLS W G,SMITH C J.Characterization of the primary starch utilization operon in the obligate anaerobe Bacteroides fragilis:regulation by carbon source and oxygen[J].Journal of Bacteriology,2006,188(13):4663-4672.  
[13] DONALDSON G P,LEE S M,MAZMANIAN S K.Gut biogeography of the bacterial microbiota[J].Nature Reviews Microbiology,2015,14(1):20-32.
[14] RAABIS S,LI W L,CERSOSIMO L.Effects and immune responses of probiotic treatment in ruminants[J].Veterinary Immunology and Immunopathology,2019,208:58-66.
[15] INGLIS G D,KALISCHUK L D,BUSZ H W,et al.Colonization of cattle intestines by Campylobacter jejuni and Campylobacter lanienae[J].Applied and Environmental Microbiology,2005,71(9):5145-5153.  
[16] JIAO J Z,ZHOU C S,GUAN L L,et al.Shifts in host mucosal innate immune function are associated with ruminal microbial succession in supplemental feeding and grazing goats at different ages[J].Frontiers in Microbiology,2017,8:1655.
[17] STANLEY K N,JONES K.Cattle and sheep farms as reservoirs of Campylobacter[J].Journal of Applied Microbiology,2010,94(Suppl.1):104S-113S.
[18] GARCIA J P,ADAMS V,BEINGESSER J,et al.Epsilon toxin is essential for the virulence of Clostridium perfringens type D infection in sheep,goats,and mice[J].Infection & Immunity,2013,81(7):2405-2414.  
[19] JIAO J Z,ZHANG X L,WANG M,et al.Linkages between epithelial microbiota and host transcriptome in the ileum during high-grain challenges:implications for gut homeostasis in goats[J].Journal of Agricultural and Food Chemistry,2018,67(1):551-561.
[20] CONSTABLE P D.Antimicrobial use in the treatment of calf diarrhea[J].Journal of Veterinary Internal Medicine,2010,18(1):8-17.
[21] HUWS S A,CREEVEY C J,OYAMA L B,et al.Addressing global ruminant agricultural challenges through understanding the rumen microbiome:past,present,and future[J].Frontiers in Microbiology,2018,9:2161.
[22] HOLMAN D B,GZYL K E.A meta-analysis of the bovine gastrointestinal tract microbiota[J].FEMS Microbiology Ecology,2019,95(6):fiz072.
[23] HENDERSON G,COX F,GANESH S,et al.Rumen microbial community composition varies with diet and host,but a core microbiome is found across a wide geographical range[J].Scientific Reports,2015,5:14567.
[24] 乐佳清,王佳堃.肠道对共生微生物的免疫耐受机制[J].动物营养学报,2017,29(5):1489-1497. LE J Q,WANG J K.Intestinal immune tolerance mechanism of symbiotic microorganisms[J].Chinese Journal of Animal Nutrition,2017,29(5):1489-1497. (in Chinese)
[25] CHASE C C L.Enteric immunity:happy gut,healthy animal[J].Veterinary Clinics of North America Food Animal Practice,2018,34(1):1-18.  
[26] O'HARA E,NEVES A L A,SONG Y,et al.The role of the gut microbiome in cattle production and health:driver or passenger?[J].Annual Review of Animal Biosciences,2020(8):199-220.
[27] KAWAI T,AKIRA S.The roles of TLRs,RLRs and NLRs in pathogen recognition[J].International Immunology,2009,21(4):317-337.  
[28] MALMUTHUGE N,GUAN L L.Understanding the gut microbiome of dairy calves:opportunities to improve early-life gut health[J].Journal of Dairy Science,2017,100(7):5996-6005.  
[29] LITTMAN D,PAMER E.Role of the commensal microbiota in normal and pathogenic host immune responses[J].Cell Host & Microbe,2011,10(4):311-323.  
[30] MUNIZ L R,KNOSP C,YERETSSIAN G.Intestinal antimicrobial peptides during homeostasis,infection,and disease[J].Frontiers in Immunology,2012,3:310.
[31] 李咏兰,邵艳红,王秀梅,等.绵羊β-防御素的发育表达和分布[J].中国兽医杂志,2008,44(1):3-4. LI Y L,SHAO Y H,WANG X M,et al.Developmental expression and distribution of sheep β-defensin[J].Chinese Journal of Veterinary Medicine,2008,44(1):3-4. (in Chinese)
[32] 刘传发,张良志,付海波,等.野牦牛和家牦牛粪便菌群与短链脂肪酸关系的研究[J].兽类学报,2019,39(1):1-7. LIU C F,ZHANG L Z,FU H B,et al.Relationship research between fecal microbes and short chain fatty acid between wild yak and domestic yak[J].Acta Theriologica Sinica,2019,39(1):1-7. (in Chinese)
[33] HAO Z,SHAO M X,HE H,et al.The dynamic distribution of small-tail han sheep microbiota across different intestinal segments[J].Frontiers in Microbiology,2018,9:32.
[34] BURGER-VAN PAASSEN N,VINCENT A,PUIMAN P J,et al.The regulation of intestinal mucin MUC2 expression by short-chain fatty acids:implications for epithelial protection[J].Biochemical Journal,2009,420(2):211-219.  
[35] SUNKARA L T,JIANG W Y,ZHANG G L.Modulation of antimicrobial host defense peptide gene expression by free fatty acids[J].PLoS One,2012,7(11):e49558.
[36] WANG H B,WANG P Y,XIN W,et al.Butyrate enhances intestinal epithelial barrier function via up-regulation of tight junction protein claudin-1 transcription[J].Digestive Diseases and Sciences,2012,57(12):3126-3135.  
[37] RAKOFF-NAHOUM S,PAGLINO J,ESLAMI-VARZANEH F,et al.Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis[J].Cell,2004,118(2):229-241.  
[38] CHANG Z L.Important aspects of Toll-like receptors,ligands and their signaling pathways[J].Inflammation Research,2010,59(10):791-808.  
[39] MALMUTHUGE N,LI M J,FRIES P,et al.Regional and age dependent changes in gene expression of Toll-like receptors and key antimicrobial defence molecules throughout the gastrointestinal tract of dairy calves[J].Veterinary Immunology and Immunopathology,2012,146(1):18-26.  
[40] LI C,WANG W M,LIU T,et al.Effect of early weaning on the intestinal microbiota and expression of genes related to barrier function in lambs[J].Frontiers in Microbiology,2018,9:1431.
[41] MALMUTHUGE N,LI M J,GOONEWARDENE L A,et al.Effect of calf starter feeding on gut microbial diversity and expression of genes involved in host immune responses and tight junctions in dairy calves during weaning transition[J].Journal of Dairy Science,2013,96(5):3189-3200.  
[42] ZHAN K,LIN M,LIU M M,et al.Establishment of primary bovine intestinal epithelial cell culture and clone method[J].In Vitro Cellular & Developmental Biology-Animal,2017,53(1):54-57.  
[43] CHIBA E,VILLENA J,HOSOYA S,et al.A newly established bovine intestinal epithelial cell line is effective for in vitro screening of potential antiviral immunobiotic microorganisms for cattle[J].Research in Veterinary Science,2012,93(2):688-694.  
[44] TAKANASHI N,TOMOSADA Y,VILLENA J,et al.Advanced application of bovine intestinal epithelial cell line for evaluating regulatory effect of lactobacilli against heat-killed enterotoxigenic Escherichia coli-mediated inflammation[J].BMC Microbiology,2013,13:54.
[45] CHARAVARYAMATH C,FRIES P,GOMIS S,et al.Mucosal changes in a long-term bovine intestinal segment model following removal of ingesta and microflora[J].Gut Microbes,2011,2(3):134-144.  
[46] JIAO J,LU Q,FORSTER R J,et al.Age and feeding system (supplemental feeding versus grazing) modulates colonic bacterial succession and host mucosal immune maturation in goats[J].Journal of Animal Science,2016,94(6):2506-2518.  
[47] LIU J H,BIAN G R,SUN D M,et al.Starter feeding supplementation alters colonic mucosal bacterial communities and modulates mucosal immune homeostasis in newborn lambs[J].Frontiers in Microbiology,2017,8:429.
[48] SOKOL H,PIGNEUR B,WATTERLOT L,et al.Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients[J].Proceedings of the National Academy of Sciences of the United States of America,2008,105(43):16731-16736.  
[49] OIKONOMOU G,TEIXEIRA A G V,FODITSCH C,et al.Fecal microbial diversity in pre-weaned dairy calves as described by pyrosequencing of metagenomic 16S rDNA.Associations of Faecalibacterium species with health and growth[J].PLoS One,2013,8(4):e63157.
[50] MALMUTHUGE N,LAING G X,GRIEBEL P J,et al.Taxonomic and functional compositions of the small intestinal microbiome in neonatal calves provide a framework for understanding early life gut health[J].Applied & Environmental Microbiology,2019,85(6):e02534.
[51] CHASE C,KAUSHIK C C R S.Mucosal immune system of cattle:all immune responses begin here[J].Veterinary Clinics of North America:Food Animal Practice,2019,35(3):431-451.  
[52] HARRIS T.Immunological effects of yeast products on pre-weaned dairy calves[D].Master's Thesis.Lubbock:Texas Tech University,2016.
[53] SOTO L P,ASTESANA D M,ZBRUN M V,et al.Probiotic effect on calves infected with salmonella dublin:haematological parameters and serum biochemical profile[J].Beneficial Microbes,2015,7(1):23-33.
[54] IRIANTO A,AUSTIN B.Probiotics in aquaculture[J].Journal of Fish Diseases,2002,25(11):633-642.  
[55] HARZALLAH D,BELHADJ H.Lactic acid bacteria as probiotics:characteristics,selection criteria and role in immunomodulation of human GI muccosal barrier[C]//KONGO M.Lactic acid bacteria-R & D for food,health and livestock purposes.[s.l.]:[s.n.],2013:197-216.
[56] UYENO Y,SHIGEMORI S,SHIMOSATO T.Effect of probiotics/prebiotics on cattle health and productivity[J].Microbes and Environments,2015,30(2):126-132.  
[57] CHUANG L,WU K G,PAI C,et al.Heat-killed cells of lactobacilli skew the immune response toward T helper 1 polarization in mouse splenocytes and dendritic cell-treated T cells[J].Journal of Agricultural and Food Chemistry,2007,55(26):11080-11086.  
[58] BERMÚDEZ-HUMARÁN L G.Lactococcus lactis as a live vector for mucosal delivery of therapeutic proteins[J].Human Vaccines,2009,5(4):264-267.  
[59] ISOLAURI E,SÜTAS Y,KANKAANPÄÄ P,et al.Probiotics:effects on immunity[J].The American Journal of Clinical Nutrition,2001,73(Suppl.2):444s-450s.
[60] 丑有财.复方女贞子和益生菌对犊牛生长性能和免疫功能的影响[D].硕士学位论文.哈尔滨:东北农业大学,2012. CHOU Y C.Study on the effect of compound nvzhenzi preparation and probiotics on growth performance and immunologic function in dairy calves[D].Master's Thesis.Harbin:Northeast Agriculture University,2012. (in Chinese)
[61] 刁其玉.微生物制剂在幼龄反刍动物营养与饲料中的应用[J].动物营养学报,2014,26(10):3159-3167. DIAO Q Y.Probiotics:application in nutrition and feed of young ruminants[J].Chinese Journal of Animal Nutrition,2014,26(10):3159-3167. (in Chinese)
[62] IZUDDIN W I,LOH T C,FOO H L,et al.Postbiotic L. plantarum RG14 improves ruminal epithelium growth,immune status and upregulates the intestinal barrier function in post-weaning lambs[J].Scientific Reports,2019,9:9938.
[63] RHAYAT L,MARESCA M,NICOLETTI C,et al.Effect of Bacillus subtilis strains on intestinal barrier function and inflammatory response[J].Other,2019,10:564.
[64] 程连平,贺濛初,夏晓冬,等.富硒酵母和枯草芽孢杆菌对湖羊羔羊生长性能、血清指标和消化功能的影响[J].动物营养学报,2018,30(8):3189-3198. CHENG L,HE M,XIA X,et al.Effects of selenium-enriched yeast and bacillus subtilis on growth performance,serum indices,digestive function of Hu lambs[J].Chinese Journal of Animal Nutrition,2018,30(8):3189-3198. (in Chinese)
[65] 范利霞.复合微生态制剂的研制及其对反刍动物免疫机能的影响[D].硕士学位论文.呼和浩特:内蒙古农业大学,2010. FAN L X.The development of composite probiotics on ruminant animals and immunity function[D].Master's Thesis.Hohhot:Inner Mongolia Agriculture University,2010. (in Chinese)
[66] 赵晓静.全营养保健代乳粉及甘露寡糖对犊牛代谢及生长发育影响的研究[D].硕士学位论文.保定:河北农业大学,2005. ZHAO X J.Effects of feeding early weaned calf with milk replacer and BIO-MOS on calf metabolism and growth[D].Master's Thesis.Baoding:Agricultural University of Hebei,2005. (in Chinese)
[67] SPRING P.Effects of mannanoligosaccharide on different cecal parameters and on cecal concentrations of enteric pathogens in poultry[D].Master's Thesis.Switzerland:ETH Zurich,1996.
[68] SAMANTA A K,SENANI S,KOLTE A P,et al.Effect of prebiotic on digestibility of total mixed ration[J].The Indian Veterinary Journal,2012,89(1):41-42.
[69] 杨立娜,吴凯为,朱力杰,等.益生元、多酚、蛋白质和多不饱和脂肪酸对肠道健康的影响[J].食品工业科技,2017,38(22):336-340. YANG L N,WU K W,ZHU L J,et al.Effect of prebiotics,phytochemicals,protein and polyunsaturated fatty acids on intestinal health[J].Science and Technology of Food Industry,2017,38(22):343-347. (in Chinese)
[70] DENMAN S E,TOMKINS N W,MCSWEENEY C S.Quantitation and diversity analysis of ruminal methanogenic populations in response to the antimethanogenic compound bromochloromethane[J].FEMS Microbiology Ecology,2007,62(3):313-322.  
[71] CASTRO M J.Calf intestinal health:assessment and dietary interventions for its improvement[J].Dissertations & Theses-Gradworks,2014,117(27):61-70.
[72] BORODY T J,KHORUTS A.Fecal microbiota transplantation and emerging applications[J].Nature Reviews Gastroenterology & Hepatology,2012,9(2):88-96.  
[73] MALMUTHUGE N,CHEN Y H,LIANG G X,et al.Heat-treated colostrum feeding promotes beneficial bacteria colonization in the small intestine of neonatal calves[J].Journal of Dairy Science,2015,98(11):8044-8053.  
[74] 王燕,滕晓晓,杨柠芝,等.粪菌移植法治疗非特异病原性羔羊腹泻的效果初报[J].畜牧兽医学报,2020,51(8):1878-1885. WANG Y,TENG X X,YANGN Z,et al.Preliminary report of the therapeutic effect of microbiota transplantation on non-specific pathogenic diarrhea in suckling lambs[J].Chinese Journal of Animal and Veterinary Sciences,2020,51(8):1878-1885. (in Chinese)
[75] 纪守坤.菌群移植调控奶牛瘤胃和肠道菌群及其生态学机理研究[D].博士学位论文.北京:中国农业大学,2018. SHOU K J.Reshaping gastrointestinal microbiota of cows with microbiota transplantation and it's ecological mechanism[D].Ph.D.Thesis.Beijing:China Agricultural University.2018. (in Chinese)
[76] 吴兆海.粪菌移植对被动免疫失败犊牛肠道屏障功能及肠道菌群构建的影响[D].博士学位论文.北京:中国农业大学,2018. WU Z H.Effects of fecal microbiota transplantation on intestinal barrier function and microbiota establishment in calves with failure of passive immune transfer[D].Ph.D.Thesis.Beijing:China Agricultural University.2018. (in Chinese)
[77] FISCHER A J,SONG Y,HE Z,et al.Effect of delaying colostrum feeding on passive transfer and intestinal bacterial colonization in neonatal male Holstein calves[J].Journal of Dairy Science,2018,101(4):3099-3109.  
[78] MALDONADO-GOMEZ M X,LEE H,BARILE D,et al.Adherence inhibition of enteric pathogens to epithelial cells by bovine colostrum fractions[J].International Dairy Journal,2015,40:24-32
[79] 姚军虎,申静.瘤胃可降解淀粉:决定反刍动物消化道健康与养分利用的关键日粮因子[J].饲料工业,2020,41(8):1-7. YAO J H,S J.Rumen degradable starch regulate the gut health and nutrient utilization in ruminants[J].Siliao Gongye,2020,41(8):1-7. (in Chinese)
[80] TAO S Y,DUANMU Y,DONG H B,et al.High concentrate diet induced mucosal injuries by enhancing epithelial apoptosis and inflammatory response in the hindgut of goats[J].PLoS One,2014,9(10):e111596.
[81] JIAO J Z,WU J,WANG M,et al.Rhubarb supplementation promotes intestinal mucosal innate immune homeostasis through modulating intestinal epithelial microbiota in goat kids[J].Journal of Agricultural & Food Chemistry,2018,66(4):1047-1057.  
[82] BONELLI F,TURINI L,SARRI G,et al.Oral administration of chestnut tannins to reduce the duration of neonatal calf diarrhea[J].BMC Veterinary Research,2018,14:227.
[83] 李俊才.黄芪多糖对犊牛健康和血液抗氧化指标的影响[D].硕士学位论文.洛阳:河南科技大学,2019. LI J C.Effects of astragalus polysaccharides on health and antioxidant capacity of calves[D].Master's Thesis.Luoyang:Henan University of Science and Technology,2019. (in Chinese)
Outlines

/