Effect of early nutrition intervention on rumen microflora development in young ruminants

doi:10.11686/cyxb2020102

Abstract

Abstract:

The presence of a normal and stable rumen microflora is an important indicator of rumen health in ruminants. It also plays an important role in the development of rumen morphology， microbial colonization， regulation of immune function， and resistance to invasion by exogenous pathogenic factors. Recent studies have shown that the composition of rumen microbes in neonatal ruminants is relatively simple. However， different microbial communities begin to colonize and occupy different niches during early rumen development， so nutritional interventions at this point may result in the formation of specific microbial communities and may have lasting effects. Such interventions provide a better long-term strategy for further improving ruminant productivity and health. In this paper， the latest research findings on early nutrition intervention in the development of the rumen microecological system are reviewed in detail from the following three perspectives： Exploring the development of rumen morphology and function of young ruminants， the factors affecting the early rumen microbial community colonization and the selection of a ‘window period’ for intervention， and brief analysis of the immune interaction between host and microbial communities. This information would help in the improvement of the performance of ruminants through early nutrition intervention to meet the global challenge of animal husbandry， as well as improvements in straw fiber utilization and the control of methane emission.

Key words: rumen microflora, early nutrition intervention, microbial colonization, immune interaction

Jian-bo ZHANG, KAO Ren-qing DING, Ze-yi LIANG, Ahmad Anum-ali, Mei DU, Juan-shan ZHENG, Xue-zhi DING. Effect of early nutrition intervention on rumen microflora development in young ruminants[J]. Acta Prataculturae Sinica, 2021, 30(2): 199-211.

Figures/Tables 2

References 106

1	Alexandratos N， Bruinsma J. World agriculture towards 2030/2050： The 2012 revision.Rome： Food and Agriculture Organization of the United Nations （FAO）， 2012.
2	Eisler M C， Lee M R， Tarlton J F， et al. Agriculture： Steps to sustainable livestock. Nature， 2014， 507（7490）： 32-34.
3	Dehority B A. Rumen microbiology. Nottingham： Nottingham University Press， 2003.
4	Yeoman C J， White B A. Gastrointestinal tract microbiota and probiotics in production animals. Annual Review of Animal Biosciences， 2014， 2（1）： 469-486.
5	Hart K， Yáñez-Ruiz D R， Duval S， et al. Plant extracts to manipulate rumen fermentation. Animal Feed Science and Technology， 2008， 147（1/2/3）： 8-35.
6	Kittelmann S， Pinares-Patino C S， Seedorf H， et al. Two different bacterial community types are linked with the low-methane emission trait in sheep. PLoS One， 2014， 9（7）： e103171.
7	Griffith C， Ribeiro Jr G， Oba M， et al. Potential for improving fiber digestion in the rumen of cattle （Bos taurus） through microbial inoculation from bison （Bison bison）： In situ fiber degradation. Journal of Animal Science， 2017， 95（5）： 2156-2167.
8	Weimer P， Stevenson D， Mantovani H， et al. Host specificity of the ruminal bacterial community in the dairy cow following near-total exchange of ruminal contents. Journal of Dairy Science， 2010， 93（12）： 5902-5912.
9	Li F， Li C， Chen Y， et al. Host genetics influence the rumen microbiota and heritable rumen microbial features associate with feed efficiency in cattle. Microbiome， 2019， 7（1）： 92.
10	Distel R， Villalba J， Laborde H. Effects of early experience on voluntary intake of low-quality roughage by sheep. Journal of Animal Science， 1994， 72（5）： 1191-1195.
11	Saro C， Hohenester U M， Bernard M， et al. Effectiveness of interventions to modulate the rumen microbiota composition and function in pre-ruminant and ruminant lambs. Frontiers in Microbiology， 2018， 9： 1273.
12	Li R W， Connor E E， Li C， et al. Characterization of the rumen microbiota of pre‐ruminant calves using metagenomic tools. Environmental Microbiology， 2012， 14（1）： 129-139.
13	Abecia L， Ramos-Morales E， Martínez-Fernandez G， et al. Feeding management in early life influences microbial colonisation and fermentation in the rumen of newborn goat kids. Animal Production Science， 2014， 54（9）： 1449-1454.
14	Rey M， Enjalbert F， Combes S， et al. Establishment of ruminal bacterial community in dairy calves from birth to weaning is sequential. Journal of Applied Microbiology， 2014， 116（2）： 245-257.
15	Zhang Y， Cheng J， Zheng N， et al. Different milk replacers alter growth performance and rumen bacterial diversity of dairy bull calves. Livestock Science， 2020， 231： 103862.
16	Yáñez-Ruiz D R， Abecia L， Newbold C J. Manipulating rumen microbiome and fermentation through interventions during early life： A review. Frontiers in Microbiology， 2015， 6： 1133.
17	Jiao J， Li X， Beauchemin K A， et al. Rumen development process in goats as affected by supplemental feeding v. grazing： Age-related anatomic development， functional achievement and microbial colonisation. British Journal of Nutrition， 2015， 113（6）： 888-900.
18	Baldwin V R， McLeod K， Klotz J， et al. Rumen development， intestinal growth and hepatic metabolism in the pre-and postweaning ruminant. Journal of Dairy Science， 2004， 87： 55-65.
19	Žitnan R， Voigt J， Schönhusen U， et al. Influence of dietary concentrate to forage ratio on the development of rumen mucosa in calves. Archives of Animal Nutrition， 1998， 51（4）： 279-291.
20	Fonty G， Gouet P， Jouany J P， et al. Establishment of the microflora and anaerobic fungi in the rumen of lambs. Microbiology， 1987， 133（7）： 1835-1843.
21	Abecia L， Jiménez E， Martinez-Fernandez G， et al. Natural and artificial feeding management before weaning promote different rumen microbial colonization but not differences in gene expression levels at the rumen epithelium of newborn goats. PLoS One， 2017， 12（8）： e0182235.
22	Rey M， Enjalbert F， Monteils V. Establishment of ruminal enzyme activities and fermentation capacity in dairy calves from birth through weaning. Journal of Dairy Science， 2012， 95（3）： 1500-1512.
23	Malmuthuge N， Liang G， Guan L L. Regulation of rumen development in neonatal ruminants through microbial metagenomes and host transcriptomes. Genome Biology， 2019， 20（1）： 172.
24	Baldwin R L， McLeod K R. Effects of diet forage： Concentrate ratio and metabolizable energy intake on isolated rumen epithelial cell metabolism in vitro. Journal of Animal Science， 2000， 78（3）： 771-783.
25	Khan M， Weary D， Von Keyserlingk M. Hay intake improves performance and rumen development of calves fed higher quantities of milk. Journal of Dairy Science， 2011， 94（7）： 3547-3553.
26	Malmuthuge N， Guan L L. Understanding host-microbial interactions in rumen： Searching the best opportunity for microbiota manipulation. Journal of Animal Science and Biotechnology， 2017， 8（1）： 8.
27	Liang G， Malmuthuge N， McFadden T B， et al. Potential regulatory role of microRNAs in the development of bovine gastrointestinal tract during early life. PLoS One， 2014， 9（3）： e92592.
28	Malmuthuge N， Li M， 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. Veterinary Immunology and Immunopathology， 2012， 146（1）： 18-26.
29	Warner R， Flatt W， Loosli J. Ruminant nutrition， dietary factors influencing development of ruminant stomach. Journal of Agricultural and Food Chemistry， 1956， 4（9）： 788-792.
30	Tamate H， McGilliard A， Jacobson N， et al. Effect of various dietaries on the anatomical development of the stomach in the calf. Journal of Dairy Science， 1962， 45（3）： 408-420.
31	Lesmeister K， Heinrichs A J， Gabler M. Effects of supplemental yeast （Saccharomyces cerevisiae） culture on rumen development， growth characteristics， and blood parameters in neonatal dairy calves. Journal of Dairy Science， 2004， 87（6）： 1832-1839.
32	Harrison H， Warner R， Sander E， et al. Changes in the tissue and volume of the stomachs of calves following the removal of dry feed or consumption of inert bulk. Journal of Dairy Science， 1960， 43（9）： 1301-1312.
33	Suárez B， Van Reenen C， Stockhofe N， et al. Effect of roughage source and roughage to concentrate ratio on animal performance and rumen development in veal calves. Journal of Dairy Science， 2007， 90（5）： 2390-2403.
34	Nemati M， Amanlou H， Khorvash M， et al. Effect of different alfalfa hay levels on growth performance， rumen fermentation， and structural growth of Holstein dairy calves. Journal of Animal Science， 2016， 94（3）： 1141-1148.
35	Xie B， Zhang N F， Zhang C X， et al. Effects of forage on rumen development in young ruminants and its mechanisms. Chinese Journal of Animal Nutrition， 2018， 30（4）： 1245-1252.
	解彪，张乃锋，张春香，等. 粗饲料对幼龄反刍动物瘤胃发育的影响及其作用机制. 动物营养学报， 2018， 30（4）： 1245-1252.
36	Vieira A D P， Von Keyserlingk M， Weary D. Presence of an older weaned companion influences feeding behavior and improves performance of dairy calves before and after weaning from milk. Journal of Dairy Science， 2012， 95（6）： 3218-3224.
37	Soberon F， Raffrenato E， Everett R， et al. Preweaning milk replacer intake and effects on long-term productivity of dairy calves. Journal of Dairy Science， 2012， 95（2）： 783-793.
38	Khan M， Bach A， Weary D， et al. Invited review： Transitioning from milk to solid feed in dairy heifers. Journal of Dairy Science， 2016， 99（2）： 885-902.
39	Yang H B， Liu H， Zhan J Y， et al. Effects of diet pellets with different concentrate-roughage ratios on rumen fermenta-tion parameters and microorganism abundance in weaned bull calves. Acta Prataculturae Sinica， 2015， 24（12）： 134-141.
	杨宏波，刘红，占今舜，等. 不同精粗比颗粒饲料对断奶公犊牛瘤胃发酵参数和微生物的影响. 草业学报， 2015， 24（12）： 134-141.
40	Phillips C. The effects of forage provision and group size on the behavior of calves. Journal of Dairy Science， 2004， 87（5）： 1380-1388.
41	McCann J C， Wickersham T A， Loor J J. High-throughput methods redefine the rumen microbiome and its relationship with nutrition and metabolism. Bioinformatics and Biology Insights， 2014， 8： 109-125.
42	Fan P， Bian B， Teng L， et al. Host genetic effects upon the early gut microbiota in a bovine model with graduated spectrum of genetic variation. The International Society for Microbial Ecology Journal， 2020， 14（1）： 302-317.
43	Lesmeister K， Heinrichs A J. Effects of corn processing on growth characteristics， rumen development， and rumen parameters in neonatal dairy calves. Journal of Dairy Science， 2004， 87（10）： 3439-3450.
44	Suárez B， Van Reenen C， Gerrits W， et al. Effects of supplementing concentrates differing in carbohydrate composition in veal calf diets： II. Rumen development. Journal of Dairy Science， 2006， 89（11）： 4376-4386.
45	Khan M， Lee H， Lee W， et al. Pre-and postweaning performance of Holstein female calves fed milk through step-down and conventional methods. Journal of Dairy Science， 2007， 90（2）： 876-885.
46	Khan M， Lee H， Lee W， et al. Starch source evaluation in calf starter： II. Ruminal parameters， rumen development， nutrient digestibilities， and nitrogen utilization in Holstein calves. Journal of Dairy Science， 2008， 91（3）： 1140-1149.
47	Ziolecki A， Briggs C. The microflora of the rumen of the young calf： II. Source， nature and development. Journal of Applied Bacteriology， 1961， 24（2）： 148-163.
48	Niekerk J K V， Fischer-Tlustos A J， Deikun L L， et al. Effect of amount of milk replacer fed and the processing of corn in starter on growth performance， nutrient digestibility， and rumen and fecal fibrolytic bacteria of dairy calves. Journal of Dairy Science 2020， 103（3）： 2186-2199.
49	Stewart C， Fonty G， Gouet P. The establishment of rumen microbial communities. Animal Feed Science and Technology， 1988， 21（2/3/4）： 69-97.
50	Jami E， Israel A， Kotser A， et al. Exploring the bovine rumen bacterial community from birth to adulthood. The International Society for Microbial Ecology Journal， 2013， 7（6）： 1069-1079.
51	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. Frontiers in Microbiology， 2018， 9： 2161.
52	Becker E R， Hsiung T S. The method by which ruminants acquire their fauna of infusoria， and remarks concerning experiments on the host-specificity of these protozoa. Proceedings of the National Academy of Sciences of the United States of America， 1929， 15（8）： 684-690.
53	Williams A G， Coleman G S. The rumen protozoa. New York： Springer-Verlag， 1991.
54	Eadie J M. The development of rumen microbial populations in lambs and calves under various conditions of management. Microbiology， 1962， 29（4）： 563-578.
55	Belanche A， Gabriel D L F， Newbold C J. Effect of progressive inoculation of fauna-free sheep with holotrich protozoa and total-fauna on rumen fermentation， microbial diversity and methane emissions. Federation of European Microbiological Societies Microbiology Ecology， 2015， 91（3）： 191-197.
56	Belanche A， Gabriel D L F， Newbold C. Study of methanogen communities associated with different rumen protozoal populations. Federation of European Microbiological Societies Microbiology Ecology， 2014， 90（3）： 663-677.
57	Newbold C J， Gabriel D L F， Belanche A， et al. The role of ciliate protozoa in the rumen. Frontiers in Microbiology， 2015， 6： 1313.
58	Gagen E J， Mosoni P， Denman S E， et al. Methanogen colonisation does not significantly alter acetogen diversity in lambs isolated 17 h after birth and raised aseptically. Microbial Ecology， 2012， 64（3）： 628-640.
59	Morvan B， Dore J， Rieu-Lesme F， et al. Establishment of hydrogen-utilizing bacteria in the rumen of the newborn lamb. FEMS Microbiology Letters， 1994， 117（3）： 249-256.
60	Guzman C E， Bereza-Malcolm L T， De Groef B， et al. Presence of selected methanogens， fibrolytic bacteria， and proteobacteria in the gastrointestinal tract of neonatal dairy calves from birth to 72 hours. PLoS One， 2015， 10（7）： e0133048.
61	Mueller R E， Asplund J M， Iannotti E. Successive changes in the epimural bacterial community of young lambs as revealed by scanning electron microscopy. Applied and Environmental Microbiology， 1984， 47（4）： 715-723.
62	Mueller R， Iannotti E， Asplund J. Isolation and identification of adherent epimural bacteria during succession in young lambs. Applied and Environmental Microbiology， 1984， 47（4）： 724-730.
63	Sadet S， Martin C， Meunier B， et al. PCR-DGGE analysis reveals a distinct diversity in the bacterial population attached to the rumen epithelium. Animal， 2007， 1（7）： 939-944.
64	Malmuthuge N， Griebel P J. Taxonomic identification of commensal bacteria associated with the mucosa and digesta throughout the gastrointestinal tracts of preweaned calves. Applied and Environmental Microbiology， 2014， 80（6）： 2021-2028.
65	Hobson P N， Stewart C S. The rumen microbial ecosystem. New York： Springer Netherlands， 1997.
66	Belanche A， Abecia L， Holtrop G， et al. Study of the effect of presence or absence of protozoa on rumen fermentation and microbial protein contribution to the chyme. Journal of Animal Science， 2011， 89（12）： 4163-4174.
67	Miltko R， Bełżecki G， Kowalik B， et al. Can fungal zoospores be the source of energy for the rumen protozoa Eudiplodinium maggii？ Anaerobe， 2014， 29： 68-72.
68	Anderson K， Nagaraja T， Morrill J. Ruminal metabolic development in calves weaned conventionally or early. Journal of Dairy Science， 1987， 70（5）： 1000-1005.
69	Skillman L C， Evans P N， Naylor G E， et al. 16S ribosomal DNA-directed PCR primers for ruminal methanogens and identification of methanogens colonising young lambs. Anaerobe， 2004， 10（5）： 277-285.
70	Abecia L， Waddams K E， Martínez-Fernandez G， et al. An antimethanogenic nutritional intervention in early life of ruminants modifies ruminal colonization by Archaea. Archaea， 2014： 841463.
71	Yáñez-Ruiz D R， Macías B， Pinloche E， et al. The persistence of bacterial and methanogenic archaeal communities residing in the rumen of young lambs. Federation of European Microbiological Societies Microbiology Ecology， 2010， 72（2）： 272-278.
72	Martin S A， Nisbet D J. Effect of direct-fed microbials on rumen microbial fermentation. Journal of Dairy Science， 1992， 75（6）： 1736-1744.
73	Jeyanathan J， Martin C， Morgavi D. The use of direct-fed microbials for mitigation of ruminant methane emissions： A review. Animal， 2014， 8（2）： 250-261.
74	Ziolecki A， Osińska Z， Ziolecki A. The effect of stabilized rumen extract on growth and development of calves： 1. Liveweight gain and efficiency of feed utilization. Zeitschrift für Tierphysiologie Tierernährung und Futtermittelkunde， 1984， 51（1/2/3/4/5）： 13-20.
75	Ziolecki A， Kwiatkowska E， Laskowska H. The effect of stabilized rumen extract on growth and development of calves： 2. Digestive activity in the rumen and development of microflora in the rumen and faeces. Zeitschrift für Tierphysiologie Tierernährung und Futtermittelkunde， 1984， 51（1/2/3/4/5）： 20-31.
76	Gruninger R J， Puniya A K， Callaghan T M， et al. Anaerobic fungi （phylum Neocallimastigomycota）： Advances in understanding their taxonomy， life cycle， ecology， role and biotechnological potential. Federation of European Microbiological Societies Microbiology Ecology， 2014， 90（1）： 1-17.
77	Al Ibrahim R， Gath V， Campion D， et al. The effect of abrupt or gradual introduction to pasture after calving and supplementation with Saccharomyces cerevisiae （Strain 1026） on ruminal pH and fermentation in early lactation dairy cows. Animal Feed Science and Technology， 2012， 178（1/2）： 40-47.
78	Uyeno Y， Shigemori S， Shimosato T. Effect of probiotics/prebiotics on cattle health and productivity. Microbes and Environments， 2015， 30（2）： 126-132.
79	Zhong R， Sun H， Li G， et al. Effects of inoculation with rumen fluid on nutrient digestibility， growth performance and rumen fermentation of early weaned lambs. Livestock Science， 2014， 162： 154-158.
80	Foditsch C， Pereira R V V， Ganda E K， et al. Oral administration of Faecalibacterium prausnitzii decreased the incidence of severe diarrhea and related mortality rate and increased weight gain in preweaned dairy heifers. PLoS One， 2015， 10（12）： e0145485.
81	Fernando S C， Purvis H， Najar F， et al. Rumen microbial population dynamics during adaptation to a high-grain diet. Applied and Environmental Microbiology， 2010， 76（22）： 7482-7490.
82	Qadis A Q， Goya S， Ikuta K， et al. Effects of a bacteria-based probiotic on ruminal pH， volatile fatty acids， and bacterial flora of Holstein calves. Journal of Veterinary Medical Science， 2014， 76（6）： 877-885.
83	Fonty G， Joblin K， Chavarot M， et al. Establishment and development of ruminal hydrogenotrophs in methanogen-free lambs. Applied and Environmental Microbiology， 2007， 73（20）： 6391-6403.
84	Abecia L， Martín-García A， Martínez G， et al. Nutritional intervention in early life to manipulate rumen microbial colonization and methane output by kid goats postweaning. Journal of Animal Science， 2013， 91（10）： 4832-4840.
85	Griffith C， Ribeiro G O， Oba M， et al. Potential for improving fiber digestion in the rumen of cattle （Bos taurus） through microbial inoculation from bison （Bison bison）： In situ fiber degradation. Journal of Animal Science， 2017， 95（5）： 2156-2167.
86	Chang Z. Important aspects of Toll-like receptors， ligands and their signaling pathways. Inflammation Research， 2010， 59（10）： 791-808.
87	Meade K G， Cormican P， Narciandi F， et al. Bovine β-defensin gene family： Opportunities to improve animal health？ Physiological Genomics， 2014， 46（1）： 17-28.
88	Newbold C J， Ramos-Morales E. Ruminal microbiome and microbial metabolome： Effects of diet and ruminant host. Animal， 2020， 14（S1）： 78-86.
89	Guan Y， Ranoa D R E， Jiang S， et al. Human TLRs 10 and 1 share common mechanisms of innate immune sensing but not signaling. The Journal of Immunology， 2010， 184（9）： 5094-5103.
90	Hooper L V， Littman D R， Macpherson A. Interactions between the microbiota and the immune system. Science， 2012， 336（6086）： 1268-1273.
91	Kuhn K A， Stappenbeck T S. Peripheral education of the immune system by the colonic microbiota. Seminars in Immunology， 2013， 25（5）： 364-369.
92	Wu H J， Wu E. The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes， 2012， 3（1）： 4-14.
93	Collado M C， Cernada M， Baüerl C， et al. Microbial ecology and host-microbiota interactions during early life stages. Gut Microbes， 2012， 3（4）： 352-365.
94	Trevisi E， Amadori M， Riva F， et al. Evaluation of innate immune responses in bovine forestomachs. Research in Veterinary Science， 2014， 96（1）： 69-78.
95	Dong G Z， Liu S M， Wu Y X， et al. Diet-induced bacterial immunogens in the gastrointestinal tract of dairy cows： Impacts on immunity and metabolism. Acta Veterinaria Scandinavica， 2011， 53（1）： 48.
96	Williams Y J， Popovski S， Rea S M， et al. A vaccine against rumen methanogens can alter the composition of archaeal populations. Applied and Environmental Microbiology， 2009， 75（7）： 1860-1866.
97	Seabury C M， Seabury P M， Decker J E， et al. Diversity and evolution of 11 innate immune genes in Bos taurus taurus and Bos taurus indicus cattle. Proceedings of the National Academy of Sciences， 2010， 107（1）： 151-156.
98	Landy M， Weidanz W P. Natural antibodies against gram-negative bacteria. Bacterial Endotoxins， 1964， 13： 275-290.
99	Sharpe M E， Latham M J， Reiter B. The occurrence of natural antibodies to rumen bacteria. Journal of General Microbiology， 1969， 56（3）： 353-364.
100	Sharpe M E， Brock J H， Phillips B A. Glycerol teichoic acid as an antigenic determinant in a Gram-negative bacterium Butyrivibrio fibrisolvens. Journal of General Microbiology， 1975， 88（2）： 355-363.
101	Fischer A， Song Y， He Z， et al. Effect of delaying colostrum feeding on passive transfer and intestinal bacterial colonization in neonatal male Holstein calves. Journal of Dairy Science， 2018， 101（4）： 3099-3109.
102	Latham M， Sharpe M E， Sutton J. The microbial flora of the rumen of cows fed hay and high cereal rations and its relationship to the rumen fermentation. Journal of Applied Bacteriology， 1971， 34（2）： 425-434.
103	Subharat S， Shu D， Zheng T， et al. Vaccination of cattle with a methanogen protein produces specific antibodies in the saliva which are stable in the rumen. Veterinary Immunology and Immunopathology， 2015， 164（3/4）： 201-207.
104	Snoeck V， Peters I R， Cox E. The IgA system： A comparison of structure and function in different species. Veterinary Research， 2006， 37（3）： 455-467.
105	Petri R M， Schwaiger T， Penner G B， et al. Characterization of the core rumen microbiome in cattle during transition from forage to concentrate as well as during and after an acidotic challenge. PLoS One， 2013， 8（12）： e83424.
106	Chen Y， Oba M. Variation of bacterial communities and expression of Toll-like receptor genes in the rumen of steers differing in susceptibility to subacute ruminal acidosis. Veterinary Microbiology， 2012， 159（3/4）： 451-459.