REVIEW

Research Progress on Early Colonization Characteristics and Regulation of Gut Microbiota in Young Rabbits

  • ZHU Yuanting ,
  • GUO Haiying ,
  • ZHOU Jun ,
  • ZUO Yong
Expand
  • College of Life Science, Sichuan Normal University, Chengdu 610000, China

Received date: 2021-07-18

  Online published: 2022-02-15

Abstract

In weaning period, the gut microbial structure of young rabbits is easily disordered, which causes incidence of diarrhea resulting in vast numbers of deaths, seriously hindering the development of rabbit breeding industry. Therefore, it is extremely important to establish a healthy and stable intestinal flora for reducing the incidence of diarrhea in rabbits. This review systematically summarizes the research progress of early colonization and regulation of gut microbiota in young rabbits, in order to provide theoretical reference for relieving and preventing diarrhea in young rabbits.

Cite this article

ZHU Yuanting , GUO Haiying , ZHOU Jun , ZUO Yong . Research Progress on Early Colonization Characteristics and Regulation of Gut Microbiota in Young Rabbits[J]. Chinese Journal of Animal Nutrition, 2022 , 34(2) : 689 -699 . DOI: 10.3969/j.issn.1006-267x.2022.02.002

References

[1] CULLERE M, DALLE ZOTTE A.Rabbit meat production and consumption:state of knowledge and future perspectives[J].Meat Science, 2018, 143:137-146.
[2] CHEN H J, YANG W Y, WANG C Y.The review on structure of intestinal flora at different growth stages of rabbits[C]//2017 International Conference on Medicine Sciences and Bioengineering, Pennsylvani, USA:DEStech Publications, Inc., 2017:245-253.
[3] KYLIE J.An investigation into the fecal microbiota of domestic rabbits(Oryctolagus cuniculus) and factors influencing its composition[D].Guelph:University of Guelph, 2016:1-141.
[4] BEAUMONT M, PAËS C, MUSSARD E, et al.Gut microbiota derived metabolites contribute to intestinal barrier maturation at the suckling-to-weaning transition[J].Gut Microbes, 2020, 11(5):1268-1286.  
[5] 任传帅.寒地獭兔肠道菌群定植的初步研究[D].硕士学位论文.哈尔滨:东北农业大学, 2016. REN C S.Preliminary research on the colonization of gut flora in cold region Rex rabbits[D].Master's Thesis.Harbin:Northeast Agricultural University, 2016.(in Chinese)
[6] FANG S M, CHEN X, PAN J H, et al.Dynamic distribution of gut microbiota in meat rabbits at different growth stages and relationship with average daily gain (ADG)[J].BMC Microbiology, 2020, 20(1):116.
[7] 郭海勇, 单晓枫, 吴静, 等.家兔胚胎胃肠道细菌分离及16S rRNA基因序列分析[J].中国预防兽医学报, 2012, 34(12):967-971. GUO H Y, SHAN X F, WU J, et al.Isolation and 16S rRNA gene sequence analysis of gastrointestinal bacteria in the rabbit embryos[J].Chinese Journal of Preventive Veterinary Medicine, 2012, 34(12):967-971.(in Chinese)
[8] PADILHA M T, LICOIS D, GIDENNE T, et al.Relationships between microflora and caecal fermentation in rabbits before and after weaning[J].Reproduction, Nutrition, Development, 1995, 35(4):375-386.  
[9] 许宇静.断奶幼兔盲肠微生物多样性研究及两种添加剂组合对肉兔肠道健康的影响[D].硕士学位论文.杨凌:西北农林科技大学, 2015. XU Y J.Study of caecal microbial diversity of post-weaning rabbits and effects of two compound additives on intestine health of meat rabbits[D].Master's Thesis.Yangling:Northwest A&F University, 2015.(in Chinese)
[10] COMBES S, MICHELLAND R J, MONTEILS V, et al.Postnatal development of the rabbit caecal microbiota composition and activity[J].FEMS Microbiology Ecology, 2011, 77(3):680-689.  
[11] COMBES S, GIDENNE T, CAUQUIL L, et al.Coprophagous behavior of rabbit pups affects implantation of cecal microbiota and health status[J].Journal of Animal Science, 2014, 92(2):652-665.  
[12] CROWLEY E J, KING J M, WILKINSON T, et al.Comparison of the microbial population in rabbits and Guinea pigs by next generation sequencing[J].PloS One, 2017, 12(2):e0165779.
[13] CARABAÑO R, PIQUER J, MENOYO D, et al.The digestive system of the rabbit[M]//DE BLAS C, WISEMAN J.Nutrition of the Rabbit.Cambridge:CABI Publishing, 2010:1-18.
[14] PASCUAL J J.Early weaning of young rabbits:a review[J].World Rabbit Science, 2010, 9(4):165-170.
[15] FORTUN-LAMOTHE L, BOULLIER S.A review on the interactions between gut microflora and digestive mucosal immunity.Possible ways to improve the health of rabbits[J].Livestock Science, 2007, 107(1):1-18.  
[16] PADILHA M T, LICOIS D, GIDENNE T, et al.Caecal microflora and fermentation pattern in exclusively milk-fed young rabbits[J].Reproduction, Nutrition, Development, 1999, 39(2):223-230.  
[17] ORENGO J, GIDENNE T.Feeding behaviour and caecotrophy in the young rabbit before weaning:an approach by analysing the digestive contents[J].Applied Animal Behaviour Science, 2007, 102(1/2):106-118.
[18] SIDDIQI M Z, SRINIVASAN S, PARK H Y, et al.Exploration and characterization of novel glycoside hydrolases from the whole genome of Lactobacillus ginsenosidimutans and enriched production of minor ginsenoside Rg3(S) by a recombinant enzymatic process[J].Biomolecules, 2020, 10(2):288.
[19] YANG C L, MI L, HU X L, et al.Investigation into Host selection of the cecal acetogen population in rabbits after weaning[J].PloS One, 2016, 11(7):e0158768.
[20] 杨睿, 黎春秀, 付利芝, 等.不同日龄家兔肠道微生物群落结构[J].中国兽医学报, 2017, 37(9):1693-1698. YANG R, LI C X, FU L Z, et al.Intestinal microbial community structure changes and analysis in the growth of weaning young rabbits[J].Chinese Journal of Veterinary Science, 2017, 37(9):1693-1698.(in Chinese)
[21] MATTIOLI S, DAL BOSCO A, COMBES S, et al.Dehydrated alfalfa and fresh grass supply in young rabbits:effect on performance and caecal microbiota biodiversity[J].Animals, 2019, 9(6):341.
[22] 齐聪岩, 李红亚, 王树香, 等.发酵玉米秸秆对獭兔生长性能的影响及其促生长机理的研究[J].中国畜牧兽医, 2017, 44(7):2003-2008. QI C Y, LI H Y, WANG S X, et al.Effect of fermented corn stalks on growth performance and the growth promotion mechanism in otter rabbit[J].China Animal Husbandry & Veterinary Medicine, 2017, 44(7):2003-2008.(in Chinese)
[23] DABBOU S, FERROCINO I, KOVITVADHI A, et al.Bilberry pomace in rabbit nutrition:effects on growth performance, apparent digestibility, caecal traits, bacterial community and antioxidant status[J].Animal, 2019, 13(1):53-63.  
[24] 武帅.花生秧添加比例对肉兔颗粒饲料加工品质、生产性能和盲肠菌群的影响[D].硕士学位论文.沈阳:沈阳农业大学, 2019. WU S.Effect of the level of peanut vine addition on the processing quality, production performance and cecal flora of meat rabbit pellets[D].Master's Thesis.Shenyang:Shenyang Agricultural University, 2019.(in Chinese)
[25] FENG Y, DUAN C J, PANG H, et al.Cloning and identification of novel cellulase genes from uncultured microorganisms in rabbit cecum and characterization of the expressed cellulases[J].Applied Microbiology and Biotechnology, 2007, 75(2):319-328.  
[26] CHEN S Y, DENG F L, JIA X B, et al.Gut microbiota profiling with differential tolerance against the reduced dietary fibre level in rabbit[J].Scientific Reports, 2019, 9(1):288.
[27] TROCINO A, ALONSO J G, CARABAÑO R, et al.A Meta-analysis on the role of soluble fibre in diets for growing rabbits[J].World Rabbit Science, 2013, 21(1):1-15.
[28] WU Z Y, ZHOU H L, LI F C, et al.Effect of dietary fiber levels on bacterial composition with age in the cecum of meat rabbits[J].MicrobiologyOpen, 2019, 8(5):e00708.
[29] GÓMEZ-CONDE M S, DE ROZAS A P, BADIOLA I, et al.Effect of neutral detergent soluble fibre on digestion, intestinal microbiota and performance in twenty five day old weaned rabbits[J].Livestock Science, 2009, 125(2/3):192-198.
[30] GÓMEZ-CONDE M S, GARCÍA J, CHAMORRO S, et al.Neutral detergent-soluble fiber improves gut barrier function in twenty-five-day-old weaned rabbits[J].Journal of Animal Science, 2007, 85(12):3313-3321.  
[31] CHAO H Y, LI F C.Effect of level of fibre on performance and digestion traits in growing rabbits[J].Animal Feed Science and Technology, 2008, 144(3/4):279-291.
[32] 朱岩丽.日粮纤维/淀粉对生长肉兔生长、免疫、肠道菌群的影响及肠道蛋白质组学初探[D].博士学位论文.泰安:山东农业大学, 2013. ZHU Y L.The effect of dietary fiber/starch on growing rabbits' growth, immune response, intestinal bacterial community composition and intestinal proteomics study[D].Ph.D.Thesis.Tai'an:Shandong Agricultural University, 2013.(in Chinese)
[33] TAZZOLI M, TROCINO A, BIROLO M, et al.Optimizing feed efficiency and nitrogen excretion in growing rabbits by increasing dietary energy with high-starch, high-soluble fibre, low-insoluble fibre supply at low protein levels[J].Livestock Science, 2015, 172:59-68.
[34] ZHU Y L, WANG C Y, LI F C.Impact of dietary fiber/starch ratio in shaping caecal microbiota in rabbits[J].Canadian Journal of Microbiology, 2015, 61(10):771-784.  
[35] ZHU Y, SUN Y, WANG C, et al.Impact of dietary fibre:starch ratio in shaping caecal Archaea revealed in rabbits[J].Journal of Animal Physiology and Animal Nutrition, 2017, 101(4):635-640.  
[36] CHAMORRO S, GÓMEZ-CONDE M S, PÉREZ DE ROZAS A M, et al.Effect on digestion and performance of dietary protein content and of increased substitution of lucerne hay with soya-bean protein concentrate in starter diets for young rabbits[J].Animal, 2007, 1(5):651-659.  
[37] TROCINO A, FRAGKIADAKIS M, MAJOLINI D, et al.Soluble fibre, starch and protein level in diets for growing rabbits:effects on digestive efficiency and productive traits[J].Animal Feed Science and Technology, 2013, 180(1/2/3/4):73-82.
[38] NEIS E P J G, DEJONG C H C, RENSEN S S.The role of microbial amino acid metabolism in host metabolism[J].Nutrients, 2015, 7(4):2930-2946.  
[39] CARABAÑO R, BADIOLA I, CHAMORRO S, et al.New trends in rabbit feeding:influence of nutrition on intestinal health[J].Spanish Journal of Agricultural Research, 2008, 6:15-25.
[40] SUN X M, SHEN J L, LIU C, et al.L-arginine and N-carbamoylglutamic acid supplementation enhance young rabbit growth and immunity by regulating intestinal microbial community[J].Asian-Australasian Journal of Animal Sciences, 2019, 33(1):166-176.
[41] ZENG X F, HUANG Z M, ZHANG F R, et al.Oral administration of N-carbamylglutamate might improve growth performance and intestinal function of suckling piglets[J].Livestock Science, 2015, 181:242-248.
[42] DAI Z L, LI X L, XI P B, et al.Regulatory role for L-arginine in the utilization of amino acids by pig small-intestinal bacteria[J].Amino Acids, 2012, 43(1):233-244.  
[43] DE VRIES M C, VAUGHAN E E, KLEEREBEZEM M, et al.Lactobacillus plantarum-survival, functional and potential probiotic properties in the human intestinal tract[J].International Dairy Journal, 2006, 16(9):1018-1028.  
[44] WANG C, ZHU Y, LI F, et al.The effect of lactobacillus isolates on growth performance, immune response, intestinal bacterial community composition of growing Rex rabbits[J].Journal of Animal Physiology and Animal Nutrition, 2017, 101(5):e1-e13.
[45] SHEN X M, CUI H X, XU X R.Orally administered Lactobacillus casei exhibited several probiotic properties in artificially suckling rabbits[J].Asian-Australasian Journal of Animal Sciences, 2019, 33(8):1352-1359.
[46] PHUOC T L, JAMIKORN U.Effects of probiotic supplement (Bacillus subtilis and Lactobacillus acidophilus) on feed efficiency, growth performance, and microbial population of weaning rabbits[J].Asian-Australasian Journal of Animal Sciences, 2017, 30(2):198-205.
[47] POGÁNY SIMONOVÁ M, LAUKOVÁ A, CHRASTINOVÁ L', et al.Enterococcus faecium CCM7420, bacteriocin PPB CCM7420 and their effect in the digestive tract of rabbits[J].Czech Journal of Animal Science, 2009, 54(8):376-386.  
[48] POGÁNY SIMONOVÁ M, LAUKOVÁ A, ŽITÑAN R, et al.Effect of rabbit-origin enterocin-producing probiotic strain Enterococcus faecium CCM7420 application on growth performance and gut morphometry in rabbits[J].Czech Journal of Animal Science, 2015, 60(11):509-512.
[49] ZHOU Y, NI X, WEN B, et al.Appropriate dose of Lactobacillus buchneri supplement improves intestinal microbiota and prevents diarrhoea in weaning Rex rabbits[J].Beneficial Microbes, 2018, 9(3):401-416.  
[50] 宋强, 陈仕毅, 贾先波, 等.不同组合芽孢杆菌制剂对肉兔生长性能的影响[C]//中国畜牧兽医学会养兔学分会成立大会暨第一届学术交流大会论文集, 合肥:中国畜牧兽医学会养兔学分会筹委会, 2015:36-36. SONG Q, CHEN S Y, JIA X B, et al.Effects of different combinations of Bacillus preparation on growth performance of meat rabbits[C]//Proceedings of the Inaugural Meeting and the First Academic Exchange Meeting of Rabbit Breeding Branch of Chinese Association of Animal Science and Veterinary Medicine, Hefei:Rabbit Breeding Branch of Chinese Association of Animal Science and Veterinary Medicine, 2015:36-36.(in Chinese)
[51] GUO M J, WU F H, HAO G G, et al.Bacillus subtilis improves immunity and disease resistance in rabbits[J].Frontiers in Immunology, 2017, 8:354.
[52] LUO R, ZHANG J, ZHANG X Y, et al.Bacillus subtilis HH2 ameliorates TNBS-induced colitis by modulating gut microbiota composition and improving intestinal barrier function in rabbit model[J].Journal of Functional Foods, 2020, 74:104167.
[53] LIU L, ZENG D, YANG M Y, et al.Probiotic Clostridium butyricum improves the growth performance, immune function, and gut microbiota of weaning Rex rabbits[J].Probiotics and Antimicrobial Proteins, 2019, 11(4):1278-1292.  
[54] SHEHU B M, AYO J, AYANWALE B, et al.Growth performance and nutrient digestibility of weaned rabbits fed diets supplemented with varying levels of baker's yeast(Saccharomyces cerevisiae)[J].International Journal of Agriculture and Rural Development, 2014, 17(1):1619-1627.
[55] 李晓颖, 李凤娟, 王静, 等.益生菌对肉仔兔生产性能及肠道菌群的影响[J].饲料与畜牧, 2014(3):48-50. LI X Y, LI F J, WANG J, et al.Effects of probiotics on performance and intestinal microflora of young rabbits[J].Animal Agriculture, 2014(3):48-50.(in Chinese)
[56] EZEMA C, EZE D C.Determination of the effect of probiotic (Saccharomyces cerevisiae) on growth performance and hematological parameters of rabbits[J].Comparative Clinical Pathology, 2012, 21(1):73-76.  
[57] ABD EL-AZIZ A H, EL-KASRAWY N I, ABD EL-HACK M E, et al.Growth, immunity, relative gene expression, carcass traits and economic efficiency of two rabbit breeds fed prebiotic supplemented diets[J].Animal Biotechnology, 2020:1-12.
[58] XIAO J, METZLER-ZEBELI B U, ZEBELI Q.Gut function-enhancing properties and metabolic effects of dietary indigestible sugars in rodents and rabbits[J].Nutrients, 2015, 7(10):8348-8365.  
[59] OSO A O, IDOWU O M O, HAASTRUP A S, et al.Growth performance, apparent nutrient digestibility, caecal fermentation, ileal morphology and caecal microflora of growing rabbits fed diets containing probiotics and prebiotic[J].Livestock Science, 2013, 157(1):184-190.  
[60] 吴峰洋, 杨新宇, 崔嘉, 等.魔芋甘露寡糖对生长獭兔肠道菌群、挥发性脂肪酸含量及结构形态的影响[J].中国兽医学报, 2019, 39(6):1227-1232. WU F Y, YANG X Y, CUI J, et al.Effects of konjac mannan oligosaccharide on intestinal flora, content of volatile fatty acids and morphology and structure of growing Rex rabbits[J].Chinese Journal of Veterinary Science, 2019, 39(6):1227-1232.(in Chinese)
[61] EL-ASHRAM S A, ABOELHADID S M, ABDEL-KAFY E S M, et al.Prophylactic and therapeutic efficacy of prebiotic supplementation against intestinal coccidiosis in rabbits[J].Animals, 2019, 9(11):965.
[62] FALCÃO-E-CUNHA L, CASTRO-SOLLA L, MAERTENS L, et al.Alternatives to antibiotic growth promoters in rabbit feeding:a review[J].World Rabbit Science, 2007, 15(3):127-140.
[63] MAERTENS L, FALCAO-E-CUNHA L, MAROUNEK M.Feed additives to reduce the use of antibiotics[J].Recent Advances in Rabbit Sciences, 2006, 259-265.
[64] 侯爱香, 成焕, 李宗军, 等.OPO乳脂粉对肠道微生物体外发酵的影响[J].食品科学, 2019, 40(12):115-122. HOU A X, CHENG H, LI Z J, et al.In vitro fermentation characteristics of OPO-enriched formula powder by gut microbiota[J].Food Science, 2019, 40(12):115-122.(in Chinese)
[65] CARDINALI R, REBOLLAR P G, DAL BOSCO A, et al.et al.Effect of dietary supplementation of organic acids and essential oils on immune function and intestinal characteristics of experimentally infected rabbits[C]//9th World Rabbit Congress, Verona:World Rabbit Science Association, 2008:573-578.
[66] PAPATSIROS V G, CHRISTODOULOPOULOS G.The use of organic acids in rabbit farming[J].Online Journal of Animal and Feed Research, 2011, 1(6):434-438.
[67] PAPATSIROS V G, CHRISTODOULOPOULOS G, FILIPPOPOULOS L C.The use of organic acids in monogastric animals (swine and rabbits)[J].Journal of Cell and Animal Biology, 2012, 6(10):154-159.
[68] BARUG D, DE JONG J, KIES A K, et al.Antimicrobial growth promoters:where do we go from here[M].Wageningen:Wageningen Academic Publishers, 2006:311-327.
[69] SKRIVANOVÁ E, WORGAN H J, PINLOCHE E, et al.Changes in the bacterial population of the caecum and stomach of the rabbit in response to addition of dietary caprylic acid[J].Veterinary Microbiology, 2010, 144(3/4):334-339.
[70] SCAPINELLO C, DE FARIA H G, FURLAN A C, et al.Efeito da utilização de oligossacarídeo manose e acidificantes sobre o desempenho de coelhos em crescimento[J].Revista Brasileira de Zootecnia, 2001, 30(4):1272-1277.  
[71] ABECIA L, FONDEVILA M, BALCELLS J, et al. Effect of fumaric acid on diet digestibility and the caecal environment of growing rabbits[J].Animal Research, 2005, 54(6):493-498.  
[72] ZHU K H, XU X R, SUN D F, et al.Effects of drinking water acidification by organic acidifier on growth performance, digestive enzyme activity and caecal bacteria in growing rabbits[J].Animal Feed Science and Technology, 2014, 190:87-94.
[73] PLACHA I, CHRASTINOVA L, LAUKOVA A, et al.Effect of thyme oil on small intestine integrity and antioxidant status, phagocytic activity and gastrointestinal microbiota in rabbits[J].Acta Veterinaria Hungarica, 2013, 61(2):197-208.  
[74] DABBOU S, FERROCINO I, GASCO L, et al.Antimicrobial effects of black soldier fly and yellow mealworm fats and their impact on gut microbiota of growing rabbits[J].Animals, 2020, 10(8):1292.
[75] RODRÍGUEZ M, CARRO M D, VALIENTE V, et al.Supplementation with fish oil improves meat fatty acid profile although impairs growth performance of early weaned rabbits[J].Animals, 2019, 9(7):437.
[76] ISMAIL I E, ABDELNOUR S A, SHEHATA S A, et al.Effect of dietary Boswellia serrata resin on growth performance, blood biochemistry, and cecal microbiota of growing rabbits[J].Frontiers in Veterinary Science, 2019, 6:471.
[77] ALAGAWANY M, ABD EL-HACK M E, AL-SAGHEER A A, et al.Dietary cold pressed watercress and coconut oil mixture enhances growth performance, intestinal microbiota, antioxidant status, and immunity of growing rabbits[J].Animals, 2018, 8(11):212.
[78] JURGOŃSKI A, JUŚKIEWICZ J, ZDUŃCZYK Z, et al.Polyphenol-rich extract from blackcurrant pomace attenuates the intestinal tract and serum lipid changes induced by a high-fat diet in rabbits[J].European Journal of Nutrition, 2014, 53(8):1603-1613.  
[79] XING Y W, LEI G T, WU Q H, et al.Procyanidin B2 protects against diet-induced obesity and non-alcoholic fatty liver disease via the modulation of the gut microbiota in rabbits[J].World Journal of Gastroenterology, 2019, 25(8):955-966.  
[80] HASHEM N M, SOLTAN Y A, EL-DESOKY N I, et al.Effects of Moringa oleifera extracts and monensin on performance of growing rabbits[J].Livestock Science, 2019, 228:136-143.
[81] POGÁNY SIMONOVÁ M, CHRASTINOVÁ L', KANDRIČÁKOVÁ A, et al.Can enterocin M in combination with sage extract have beneficial effect on microbiota, blood biochemistry, phagocytic activity and jejunal morphometry in broiler rabbits?[J].Animals, 2020, 10(1):115.
[82] RODRÍGUEZ M, CARRO M D, VALIENTE V, et al.Effects of dietary fish oil supplementation on performance, meat quality, and cecal fermentation of growing rabbits[J].Journal of Animal Science, 2017, 95(8):3620-3630.
[83] FANG S M, CHEN X, YE X X, et al.Effects of gut microbiome and short-chain fatty acids (SCFAs) on finishing weight of meat rabbits[J].Frontiers in Microbiology, 2020, 11:1835.
[84] SWANSON K S, GIBSON G R, HUTKINS R, et al.The international scientific association for probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of synbiotics[J].Nature Reviews Gastroenterology & Hepatology, 2020, 17(11):687-701.  
[85] HASSANIN A, TONY M, SAWIRESS F A R, et al.Influence of dietary supplementation of coated sodium butyrate and/or synbiotic on growth performances, caecal fermentation, intestinal morphometry and metabolic profile of growing rabbits[J].Journal of Agricultural Science, 2015, 7(2):180.
[86] GALLOIS M, GIDENNE T, FORTUN-LAMOTHE L, et al.An early stimulation of solid feed intake slightly influences the morphological gut maturation in the rabbit[J].Reproduction, Nutrition, Development, 2005, 45(1):109-122.  
[87] PAËS C, GIDENNE T, BÉBIN K, et al.Early introduction of solid feeds:ingestion level matters more than prebiotic supplementation for shaping gut microbiota[J].Frontiers in Veterinary Science, 2020, 7:261.
[88] MASSIP K, COMBES S, CAUQUIL L, et al.High throughput 16S-DNA sequencing for phylogenetic affiliation of the caecal bacterial community in the rabbit:impact o.f the hygiene of housing and of the intake level[C]//Clermont-Ferrand, France:8th INRA-Rowett Symposium on Gut Microbiology.[s.n.]:[s.l.], 2012:57.
[89] WANG Q J, FU W, GUO Y, et al.Drinking warm water improves growth performance and optimizes the gut microbiota in early postweaning rabbits during winter[J].Animals, 2019, 9(6):346.
Outlines

/