Repeated inoculation with fresh rumen fluid before or during weaning modulates the microbiota composition and co-occurrence of the rumen and colon of lambs
Tóm tắt
Many recent studies have gravitated towards manipulating the gastrointestinal (GI) microbiome of livestock to improve host nutrition and health using dietary interventions. Few studies, however, have evaluated if inoculation with rumen fluid could effectively reprogram the development of GI microbiota. We hypothesized that inoculation with rumen fluid at an early age could modulate the development of GI microbiota because of its low colonization resistance. In this study, we tested the above hypothesis using young lambs as a model. Young lambs were orally inoculated repeatedly (four times before or twice during gradual weaning) with the rumen fluid collected from adult sheep. The oral inoculation did not significantly affect starter intake, growth performance, or ruminal fermentation. Based on sequencing analysis of 16S rRNA gene amplicons, however, the inoculation (both before and during weaning) affected the assemblage of the rumen microbiota, increasing or enabling some bacterial taxa to colonize the rumen. These included operational taxonomic units (OTUs) belonging to Moryella, Acetitomaculum, Tyzzerella 4, Succiniclasticum, Prevotella 1, Lachnospiraceae, Christensenellaceae R-7 group, Family XIII AD3011, and Bacteroidales S24–7 corresponding to inoculation before weaning; and OTUs belonging to Succiniclasticum, Prevotellaceae UCG-003, Erysipelotrichaceae UCG-004, Prevotella 1, Bacteroidales S24–7 gut group uncultured bacterium, and candidate Family XIII AD3011 corresponding to inoculation during weaning. Compared to the inoculation during weaning, the inoculation before weaning resulted in more co-occurrences of OTUs that were exclusively predominant in the inoculum. However, inoculation during weaning appeared to have more impacts on the colonic microbiota than the inoculation before weaning. Considerable successions in the microbial colonization of the GI tracts accompanied the transition from liquid feed to solid feed during weaning. Repeated rumen fluid inoculation during early life can modulate the establishment of the microbiota in both the rumen and the colon and co-occurrence of some bacteria. Oral inoculation with rumen microbiota may be a useful approach to redirect the development of the microbiota in both the rumen and colon.
Tài liệu tham khảo
Kim M, Morrison M, Yu Z. Status of the phylogenetic diversity census of ruminal microbiomes. FEMS Microbiol Ecol. 2011;76:49–63.
Creevey CJ, Kelly WJ, Henderson G, Leahy SC. Determining the culturability of the rumen bacterial microbiome. Microb Biotechnol. 2014;7:467–79.
Koike S, Kobayashi Y. Fibrolytic rumen bacteria: their ecology and functions. Asian-Aust J Anim Sci. 2009;22:131–8.
McCann JC, Wickersham TA, Loor JJ. High-throughput methods redefine the rumen microbiome and its relationship with nutrition and metabolism. Bioinform Biol Insights. 2014;8:109–25.
Perea K, Perz K, Olivo SK, Williams A, Lachman M, Ishaq SL, Thomson J, Yeoman CJ. Feed efficiency phenotypes in lambs involve changes in ruminal, colonic, and small-intestine-located microbiota. J Anim Sci. 2017;95:2585.
Zhou M, Peng YJ, Chen Y, Klinger CM, Oba M, Liu JX, Guan LL. Assessment of microbiome changes after rumen transfaunation: implications on improving feed efficiency in beef cattle. Microbiome. 2018;6:62.
Duffield TF, Rabiee A, Lean IJ. Overview of meta-analysis of monensin in dairy cattle. Vet Clin North Am Food Anim Pract. 2012;28:107–19.
Hart KJ, Yáñez-Ruiz DR, Duval SM, McEwan NR, Newbold CJ. Plant extracts to manipulate rumen fermentation. Anim Feed Sci Technol. 2008;147:8–35.
Weimer PJ. Redundancy, resilience, and host specificity of the ruminal microbiota: implications for engineering improved ruminal fermentations. Front Microbiol. 2015;6:296.
Krause DO, Smith WJM, Ryan FME, Mackie RI, McSweeney CS. Use of 16S-rRNA based techniques to investigate the ecological succession of microbial populations in the immature lamb rumen: tracking of a specific strain of inoculated Ruminococcus and interactions with other microbial populations in vivo. Microb Ecol. 1999;38:365–76.
Zebeli Q, Terrill SJ, Mazzolari A, Dunn SM, Yang WZ, Ametaj BN. Intraruminal administration of Megasphaera elsdenii modulated rumen fermentation profile in mid-lactation dairy cows. J Dairy Res. 2012;79:16–25.
Arik HD, Gulsen N, Hayirli A, Alatas MS. Efficacy of Megasphaera elsdenii inoculation in subacute ruminal acidosis in cattle. J Anim Physiol Anim Nutr. 2019;103:411–26.
Klieve AV, Hennessy D, Ouwerkerk D, Forster RJ, Mackie RI, Attwood GT. Establishing populations of Megasphaera elsdenii YE 34 and Butyrivibrio fibrisolvens YE 44 in the rumen of cattle fed high grain diets. J Appl Microbiol. 2003;95:621–30.
Rico DE, Ying Y, Clarke AR, Harvatine KJ. The effect of rumen digesta inoculation on the time course of recovery from classical diet-induced milk fat depression in dairy cows. J Dairy Sci. 2014;97:3752–60.
Weimer PJ, Cox MS, Vieira de Paula T, Lin M, Hall MB, Suen G. Transient changes in milk production efficiency and bacterial community composition resulting from near-total exchange of ruminal contents between high- and low-efficiency Holstein cows. J Dairy Sci. 2017;100:7165–82.
Ribeiro GO, Oss DB, He Z, Gruninger RJ, Elekwachi C, Forster RJ, Yang W, Beauchemin KA, McAllister TA. Repeated inoculation of cattle rumen with bison rumen contents alters the rumen microbiome and improves nitrogen digestibility in cattle. Sci Rep. 2017;7:1276.
Weimer PJ, Stevenson DM, Mantovani HC, Man SL. Host specificity of the ruminal bacterial community in the dairy cow following near-total exchange of ruminal contents. J Dairy Sci. 2010;93:5902–12.
Soberon F, Van Amburgh ME. Lactation biology symposium: the effect of nutrient intake from milk or milk replacer of preweaned dairy calves on lactation milk yield as adults: a meta-analysis of current data. J Anim Sci. 2013;91:706–12.
Yanez-Ruiz DR, Abecia L, Newbold CJ. Manipulating rumen microbiome and fermentation through interventions during early life: a review. Front Microbiol. 2015;6:1133.
Distel RA, Villalba JJ, Laborde HE. Effects of early experience on voluntary intake of low-quality roughage by sheep. J Anim Sci. 1994;72:1191–5.
Distel RA, Villalba JJ, Laborde HE, Burgos MA. Persistence of the effects of early experience on consumption of low-quality roughage by sheep. J Anim Sci. 1996;74:965–8.
Provenza FD, Balph DF. Applicability of five diet-selection models to various foraging challenges ruminants encounter. In: Hughes RN, editor. Behavioural mechanisms of food selection. Berlin: Springer-Verlag; 1990. p. 423–59.
Soares JH, Leffel EC, Larsen RK. Neonatal lambs in a gnotobiotic environment. J Anim Sci. 1970;31:733–40.
Alexander TJL, Lysons RJ. Observations on rearing gnotobiotic lambs. Br Vet J. 1971;127:349–57.
Fonty G, Gouet P, Jouany JP, Senaud J. Establishment of the microflora and anaerobic fungi in the rumen of lambs. Microbiology. 1987;133:1835–43.
Rey M, Enjalbert F, Combes S, Cauquil L, Bouchez O, Monteils V. Establishment of ruminal bacterial community in dairy calves from birth to weaning is sequential. J Appl Microbiol. 2014;116:245–57.
Jami E, Israel A, Kotser A, Mizrahi I. Exploring the bovine rumen bacterial community from birth to adulthood. ISME J. 2013;7:1069–79.
Wang L, Xu Q, Kong F, Yang Y, Wu D, Mishra S, Li Y. Exploring the goat rumen microbiome from seven days to two years. PLoS One. 2016;11:e0154354.
De Mulder T, Goossens K, Peiren N, Vandaele L, Haegeman A, De Tender C, Ruttink T, de Wiele TV, De Campeneere S. Exploring the methanogen and bacterial communities of rumen environments: solid adherent, fluid and epimural. FEMS Microbiol Ecol. 2016;93:fiw251.
Meale SJ, Li S, Azevedo P, Derakhshani H, Plaizier JC, Khafipour E, Steele MA. Development of ruminal and fecal microbiomes are affected by weaning but not weaning strategy in dairy calves. Front Microbiol. 2016;7:582.
Budzynska M, Weary DM. Weaning distress in dairy calves: effects of alternative weaning procedures. Appl Anim Behav Sci. 2008;112:33–9.
de Passille AM, Borderas TF, Rushen J. Weaning age of calves fed a high milk allowance by automated feeders: effects on feed, water, and energy intake, behavioral signs of hunger, and weight gains. J Dairy Sci. 2011;94:1401–8.
Dill-McFarland KA, Weimer PJ, Breaker JD, Suen G. Diet influences early microbiota development in dairy calves without long-term impacts on milk production. Appl Environ Microbiol. 2018;85:e02141–18.
Saro C, Hohenester UM, Bernard M, Lagrée M, Martin C, Doreau M, Boudra H, Popova M, Morgavi DP. Effectiveness of interventions to modulate the rumen microbiota composition and function in pre-ruminant and ruminant lambs. Front Microbiol. 2018;9:1273.
De Barbieri I, Hegarty RS, Silveira C, Gulino LM, Oddy VH, Gilbert RA, Klieve AV, Ouwerkerk D. Programming rumen bacterial communities in newborn merino lambs. Small Ruminant Res. 2015;129:48–59.
Zhong RZ, Sun HX, Li GD, Liu HW, Zhou DW. Effects of inoculation with rumen fluid on nutrient digestibility, growth performance and rumen fermentation of early weaned lambs. Livest Sci. 2014;162:154–8.
De Barbieri I, Hegarty RS, Silveira C, Oddy VH. Positive consequences of maternal diet and post-natal rumen inoculation on rumen function and animal performance of merino lambs. Small Ruminant Res. 2015;129:37–47.
Abecia L, Ramos-Morales E, Martínez-Fernandez G, Arco A, Martín-García AI, Newbold CJ, Yáñez-Ruiz DR. Feeding management in early life influences microbial colonisation and fermentation in the rumen of newborn goat kids. Anim Prod Sci. 2014;54:1449–54.
Ishaq SL, Kim CJ, Reis D, Wright AD. Fibrolytic bacteria isolated from the rumen of north american moose (Alces alces) and their use as a probiotic in neonatal lambs. PLoS One. 2015;10:e0144804.
Abecia L, Jimenez E, Martinez-Fernandez G, Martin-Garcia AI, Ramos-Morales E, Pinloche E, Denman SE, Newbold CJ, Yanez-Ruiz DR. 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:e0182235.
Dias J, Marcondes MI, Noronha MF, Resende RT, Machado FS, Mantovani HC, Dill-McFarland KA, Suen G. Effect of pre-weaning diet on the ruminal archaeal, bacterial, and fungal communities of dairy calves. Front Microbiol. 2017;8:1553.
van Gylswyk NO. Succiniclasticum ruminis gen. nov., sp. nov., a ruminal bacterium converting succinate to propionate as the sole energy-yielding mechanism. Int J Syst Bacteriol. 1995;45:297–300.
Hook SE, Steele MA, Northwood KS, Dijkstra J, France J, Wright AD, McBride BW. Impact of subacute ruminal acidosis (SARA) adaptation and recovery on the density and diversity of bacteria in the rumen of dairy cows. FEMS Microbiol Ecol. 2011;78:275–84.
Shabat SK, Sasson G, Doron-Faigenboim A, Durman T, Yaacoby S, Berg Miller ME, White BA, Shterzer N, Mizrahi I. Specific microbiome-dependent mechanisms underlie the energy harvest efficiency of ruminants. ISME J. 2016;10:2958–72.
Hernandez-Sanabria E, Goonewardene LA, Wang Z, Durunna ON, Moore SS, Guan LL. Impact of feed efficiency and diet on adaptive variations in the bacterial community in the rumen fluid of cattle. Appl Environ Microbiol. 2012;78:1203–14.
Ormerod KL, Wood DLA, Lachner N, Gellatly SL, Daly JN, Parsons JD, Dal’Molin CGO, Palfreyman RW, Nielsen LK, Cooper MA, et al. Genomic characterization of the uncultured Bacteroidales family S24-7 inhabiting the guts of homeothermic animals. Microbiome. 2016;4:36.
Anderson CL, Schneider CJ, Erickson GE, MacDonald JC, Fernando SC. Rumen bacterial communities can be acclimated faster to high concentrate diets than currently implemented feedlot programs. J Appl Microbiol. 2016;120:588–99.
Plaizier JC, Li S, Danscher AM, Derakshani H, Andersen PH, Khafipour E. Changes in microbiota in rumen digesta and feces due to a grain-based subacute ruminal acidosis (SARA) challenge. Microb Ecol. 2017;74:485–95.
Dai X, Paula EM, Lelis ALJ, Silva LG, Brandao VLN, Monteiro HF, Fan P, Poulson SR, Jeong KC, Faciola AP. Effects of lipopolysaccharide dosing on bacterial community composition and fermentation in a dual-flow continuous culture system. J Dairy Sci. 2019;102:334–50.
Muscato TV, Tedeschi LO, Russell JB. The effect of ruminal fluid preparations on the growth and health of newborn, milk-fed dairy calves. J Dairy Sci. 2002;85:648–56.
De Mulder T, Peiren N, Vandaele L, Ruttink T, De Campeneere S, Van de Wiele T, Goossens K. Impact of breed on the rumen microbial community composition and methane emission of Holstein Friesian and Belgian blue heifers. Livest Sci. 2018;207:38–44.
Carlier JP, K'Ouas G, Han XY. Moryella indoligenes gen. nov., sp. nov., an anaerobic bacterium isolated from clinical specimens. Int J Syst Evol Microbiol. 2007;57:725–9.
Ellison MJ, Conant GC, Lamberson WR, Cockrum RR, Austin KJ, Rule DC, Cammack KM. Diet and feed efficiency status affect rumen microbial profiles of sheep. Small Ruminant Res. 2017;156:12–9.
Faust K, Sathirapongsasuti JF, Izard J, Segata N, Gevers D, Raes J, Huttenhower C. Microbial co-occurrence relationships in the human microbiome. PLoS Comput Biol. 2012;8:e1002606.
Saavedra S, Stouffer DB, Uzzi B, Bascompte J. Strong contributors to network persistence are the most vulnerable to extinction. Nature. 2011;478:233–5.
Fuentes S, van Nood E, Tims S, Heikamp-de Jong I, ter Braak CJ, Keller JJ, Zoetendal EG, de Vos WM. Reset of a critically disturbed microbial ecosystem: faecal transplant in recurrent Clostridium difficile infection. ISME J. 2014;8:1621–33.
Maldonado-Gomez MX, Martinez I, Bottacini F, O'Callaghan A, Ventura M, van Sinderen D, Hillmann B, Vangay P, Knights D, Hutkins RW, Walter J. Stable engraftment of Bifidobacterium longum AH1206 in the human gut depends on individualized features of the resident microbiome. Cell Host Microbe. 2016;20:515–26.
Oikonomou G, Teixeira AGV, Foditsch C, Bicalho ML, Machado VS, Bicalho RC. Fecal microbial diversity in pre-weaned dairy calves as described by pyrosequencing of metagenomic 16S rDNA. associations of Faecalibacterium species with health and growth. PLoS One. 2013;8:e63157.
Samuel BS, Shaito A, Motoike T, Rey FE, Backhed F, Manchester JK, Hammer RE, Williams SC, Crowley J, Yanagisawa M, Gordon JI. Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41. Proc Natl Acad Sci U S A. 2008;105:16767–72.
Vlková E, Rada V, Trojanová I, Killer J, Šmehilová M, Molatová Z. Occurrence of bifidobacteria in faeces of calves fed milk or a combined diet. Arch Anim Nutr. 2008;62:359–65.
Dias J, Marcondes MI, Motta de Souza S, Cardoso da Mata e Silva B, Fontes Noronha M, Tassinari Resende R, Machado FS, Cuquetto Mantovani H, KA D-MF, Suen G. Bacterial community dynamics across the gastrointestinal tracts of dairy calves during preweaning development. Appl Environ Microbiol. 2018;84:e02675–17.
Louis P, Hold GL, Flint HJ. The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol. 2014;12:661–72.
Mayer M, Abenthum A, Matthes JM, Kleeberger D, Ege MJ, Hölzel C, Bauer J, Schwaiger K. Development and genetic influence of the rectal bacterial flora of newborn calves. Vet Microbiol. 2012;161:179–85.
Ferretti P, Pasolli E, Tett A, Asnicar F, Gorfer V, Fedi S, Armanini F, Truong DT, Manara S, Zolfo M, et al. Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome. Cell Host Microbe. 2018;24:133–45.
Lagendijk EL, Validov S, Lamers GEM, De Weert S, Bloemberg GV. Genetic tools for tagging gram-negative bacteria with mCherry for visualization in vitro and in natural habitats, biofilm and pathogenicity studies. FEMS Microbiol Lett. 2010;305:81–90.
Lodge-Ivey SL, Browne-Silva J, Horvath MB. Technical note: bacterial diversity and fermentation end products in rumen fluid samples collected via oral lavage or rumen cannula. J Anim Sci. 2009;87:2333–7.
Lesmeister KE, Heinrichs AJ. Effects of corn processing on growth characteristics, rumen development, and rumen parameters in neonatal dairy calves. J Dairy Sci. 2004;87:3439–50.
Mi L, Yang B, Hu X, Luo Y, Liu J, Yu Z, Wang J. Comparative analysis of the microbiota between sheep rumen and rabbit cecum provides new insight into their differential methane production. Front Microbiol. 2018;9:575.
Fawcett JKS, J. E. A rapid and precise method for the determination of urea. J Clin Pathol. 1960;13:156–9.
Baldwin RL. Sheep gastrointestinal development in response to different dietary treatments. Small Ruminant Res. 1999;35:39–47.
Gagen EJ, Denman SE, Padmanabha J, Zadbuke S, Al Jassim R, Morrison M, McSweeney CS. Functional gene analysis suggests different acetogen populations in the bovine rumen and tammar wallaby forestomach. Appl Environ Microbiol. 2010;76:7785–95.
Li M, Penner GB, Hernandez-Sanabria E, Oba M, Guan LL. Effects of sampling location and time, and host animal on assessment of bacterial diversity and fermentation parameters in the bovine rumen. J Appl Microbiol. 2009;107:1924–34.
Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glockner FO. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 2013;41:e1.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27:2194–200.
Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–1.
Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics. 2010;26:266–7.
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–6.
Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73:5261–7.
McArdle Brian H, Anderson MJ. Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology. 2001;82:290–7.
McMurdie PJ, Holmes S. phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PloS One. 2013;8:e61217.
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60.
Bastian M, Heymann S, Jacomy M. Gephi: an open source software for exploring and manipulating networks. ICWSM. 2009;8:361–2.