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Temporal fermentation and microbial community dynamics in rumens of sheep grazing a ryegrass-based pasture offered either in the morning or in the afternoon

Published online by Cambridge University Press:  21 February 2019

R. E. Vibart Open the ORCID record for R. E. Vibart [Opens in a new window] ,
S. Ganesh Open the ORCID record for S. Ganesh [Opens in a new window] ,
M. R. Kirk Open the ORCID record for M. R. Kirk [Opens in a new window] ,
S. Kittelmann ,
S. C. Leahy ,
P. H. Janssen  and
D. Pacheco
R. E. Vibart*
Affiliation:
AgResearch, Grasslands Research Centre, Tennent Drive, Private Bag 11008, Palmerston North 4442, New Zealand
S. Ganesh
Affiliation:
AgResearch, Grasslands Research Centre, Tennent Drive, Private Bag 11008, Palmerston North 4442, New Zealand
M. R. Kirk
Affiliation:
AgResearch, Grasslands Research Centre, Tennent Drive, Private Bag 11008, Palmerston North 4442, New Zealand
S. Kittelmann
Affiliation:
AgResearch, Grasslands Research Centre, Tennent Drive, Private Bag 11008, Palmerston North 4442, New Zealand
S. C. Leahy
Affiliation:
AgResearch, Grasslands Research Centre, Tennent Drive, Private Bag 11008, Palmerston North 4442, New Zealand
P. H. Janssen
Affiliation:
AgResearch, Grasslands Research Centre, Tennent Drive, Private Bag 11008, Palmerston North 4442, New Zealand
D. Pacheco
Affiliation:
AgResearch, Grasslands Research Centre, Tennent Drive, Private Bag 11008, Palmerston North 4442, New Zealand
*
†E-mail: [email protected]
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Abstract

Eight ruminally-fistulated wethers were used to examine the temporal effects of afternoon (PM; 1600h) v. morning (AM; 0800 h) allocation of fresh spring herbage from a perennial ryegrass (Lolium perenne L.)-based pasture on fermentation and microbial community dynamics. Herbage chemical composition was minimally affected by time of allocation, but daily mean ammonia concentrations were greater for the PM group. The 24-h pattern of ruminal fermentation (i.e. time of sampling relative to time of allocation), however, varied considerably for all fermentation variables (P⩽0.001). Most notably amongst ruminal fermentation characteristics, ammonia concentrations showed a substantial temporal variation; concentrations of ammonia were 1.7-, 2.0- and 2.2-fold greater in rumens of PM wethers at 4, 6 and 8h after allocation, respectively, compared with AM wethers. The relative abundances of archaeal and ciliate protozoal taxa were similar across allocation groups. In contrast, the relative abundances of members of the rumen bacterial community, like Prevotella 1 (P=0.04), Bacteroidales RF16 group (P=0.005) and Fibrobacter spp. (P=0.008) were greater for the AM group, whereas the relative abundance of Kandleria spp. was greater (P=0.04) for the PM group. Of these taxa, only Prevotella 1 (P=0.04) and Kandleria (P<0.001) showed a significant interaction between time of allocation and time of sampling relative to feed allocation. Relative abundances of Prevotella 1 were greater at 2h (P=0.05), 4h (P=0.003) and 6h (P=0.01) after AM allocation of new herbage, whereas relative abundances of Kandleria were greater at 2h (P=0.003) and 4h (P<0.001) after PM allocation. The early post-allocation rise in ammonia concentrations in PM rumens occurred simultaneously with sharp increases in the relative abundance of Kandleria spp. and with a decline in the relative abundance of Prevotella. All measures of fermentation and most microbial community composition data showed highly dynamic changes in concentrations and genus abundances, respectively, with substantial temporal changes occurring within the first 8h of allocating a new strip of herbage. The dynamic changes in the relative abundances of certain bacterial groups, in synchrony with a substantial diurnal variation in ammonia concentrations, has potential effects on the efficiency by which N is utilised by the grazing ruminant.

Keywords

rumenammoniabacteriaarchaeaciliate protozoa
Type
Research Article
Information
animal , Volume 13 , Issue 10 , October 2019 , pp. 2242 - 2251
Copyright
© The Animal Consortium 2019 

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References

Attwood, GT, Klieve, AV, Ouwerkerk, D and Patel, BKC 1998. Ammonia-hyperproducing bacteria from New Zealand ruminants. Applied and Environmental Microbiology 64, 1796–1804.Google ScholarPubMed
Belanche, A, Newbold, CJ, Lin, W, Stevens, PR and Kingston-Smith, AH 2017. A systems biology approach reveals differences in the dynamics of colonization and degradation of grass vs. hay by rumen microbes with minor effects of vitamin E supplementation. Frontiers in Microbiology 8, 1456.CrossRefGoogle ScholarPubMed
Béra-Maillet, C, Ribot, Y and Forano, E 2004. Fiber-degrading systems of different strains of the genus Fibrobacter . Applied and Environmental Microbiology 70, 2172–2179.CrossRefGoogle ScholarPubMed
Brito, AF, Tremblay, GF, Lapierre, H, Bertrand, A, Castonguay, Y, Belanger, G, Michaud, R, Benchaar, C, Ouellet, DR and Berthiaume, R 2009. Alfalfa cut at sundown and harvested as baleage increases bacterial protein synthesis in late-lactation dairy cows. Journal of Dairy Science 92, 1092–1107.CrossRefGoogle ScholarPubMed
Caporaso, JG, Kuczynski, J, Stombaugh, J, Bittinger, K, Bushman, FD, Costello, EK, Fierer, N, Peña, AG, Goodrich, JK, Gordon, JI, Huttley, GA, Kelley, ST, Knights, D, Koenig, JE, Ley, RE, Lozupone, CA, McDonald, D, Muegge, BD, Pirrung, M, Reeder, J, Sevinsky, JR, Turnbaugh, PJ, Walters, WA, Widmann, J, Yatsunenko, T, Zaneveld, J and Knight, R 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335–336.CrossRefGoogle ScholarPubMed
de Menezes, AB, Lewis, E, O’Donovan, M, O’Neill, BF, Clipson, N and Doyle, EM 2011. Microbiome analysis of dairy cows fed pasture or total mixed ration diets. FEMS Microbiology Ecology 78, 256–265.CrossRefGoogle ScholarPubMed
De Visser, H, Valk, H, Klop, A, Van Der Meulen, J, Bakker, JGM and Huntington, GB 1997. Nutrient fluxes in splanchnic tissue of dairy cows: influence of grass quality. Journal of Dairy Science 80, 1666–1673.CrossRefGoogle ScholarPubMed
Delagarde, R, Peyraud, JL, Delaby, L and Faverdin, P 2000. Vertical distribution of biomass, chemical composition and pepsin-cellulase digestibility in a perennial ryegrass sward: interaction with month of year, regrowth age and time of day. Animal Feed Science and Technology 84, 49–68.CrossRefGoogle Scholar
Edgar, RC 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.CrossRefGoogle ScholarPubMed
Felsenstein, J 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.CrossRefGoogle ScholarPubMed
González, I, Cao, K-AL, Davis, MJ and Déjean, S 2012. Visualising associations between paired ‘omics’ data sets. BioData Mining 5, 19.CrossRefGoogle Scholar
Gregorini, P, Gunter, SA and Beck, PA 2008. Matching plant and animal processes to alter nutrient supply in strip-grazed cattle: timing of herbage and fasting allocation. Journal of Animal Science 86, 1006–1020.CrossRefGoogle ScholarPubMed
Henderson, G, Yilmaz, P, Kumar, S, Forster, RJ, Kelly, WJ, Leahy, SC, Guan, LL and Janssen, PH accepted. Improved taxonomic assignment of rumen bacterial 16S rRNA sequences using a revised SILVA taxonomic framework. PeerJ.Google Scholar
Howlett, MR, Mountfort, DO, Turner, KW and Roberton, AM 1976. Metabolism and growth yields in Bacteroides ruminicola strain b14. Applied and Environmental Microbiology 32, 274–b283.Google ScholarPubMed
Huntington, GB and Archibeque, SL 2000. Practical aspects of urea and ammonia metabolism in ruminants. Journal of Animal Science 77, 1–11.CrossRefGoogle Scholar
Jouany, JP, Demeyer, DI and Grain, J 1988. Effect of defaunating the rumen. Animal Feed Science and Technology 21, 229–265.CrossRefGoogle Scholar
Jukes, TH and Cantor, CR 1969. Evolution of protein molecules. In Mammalian protein metabolism ((ed.. HN Munro), pp. 21–132. Academic Press, New York, NY, USA.CrossRefGoogle Scholar
Kamke, J, Kittelmann, S, Soni, P, Li, Y, Tavendale, M, Ganesh, S, Janssen, PH, Shi, W, Froula, J, Rubin, EM and Attwood, GT 2016. Rumen metagenome and metatranscriptome analyses of low methane yield sheep reveals a Sharpea-enriched microbiome characterised by lactic acid formation and utilisation. Microbiome 4, 56.CrossRefGoogle ScholarPubMed
Kingston-Smith, AH and Theodorou, MK 2000. Post-ingestion metabolism of fresh forage. New Phytologist 148, 37–55.CrossRefGoogle Scholar
Kittelmann, S, Devente, SR, Kirk, MR, Seedorf, H, Dehority, BA and Janssen, PH 2015. Phylogeny of intestinal ciliates, including Charonina ventriculi, and comparison of microscopy and 18S rRNA gene pyrosequencing for rumen ciliate community structure analysis. Applied and Environmental Microbiology 81, 2433–2444.CrossRefGoogle ScholarPubMed
Kittelmann, S and Janssen, PH 2011. Characterisation of rumen ciliate community composition in domestic sheep, deer, and cattle, feeding on varying diets, by means of PCR-DGGE and clone libraries. FEMS Microbiology Ecology 75, 468–481.CrossRefGoogle Scholar
Kittelmann, S, Seedorf, H, Walters, WA, Clemente, JC, Knight, R, Gordon, JI and Janssen, PH 2013. Simultaneous amplicon sequencing to explore co-occurrence patterns of bacterial, archaeal and eukaryotic microorganisms in rumen microbial communities. PLoS One 8, e47879.CrossRefGoogle ScholarPubMed
Kumar, S, Treloar, BP, Teh, KH, Henderson, G, Attwood, GT, Waters, SM, Patchett, ML and Janssen, PH 2018. Sharpea and Kandleria are lactic acid producing rumen bacteria that do not change their fermentation products when co-cultured with a methanogen. Anaerobe 54, 31–38.CrossRefGoogle Scholar
Liu, J, Zhang, M, Xue, C, Zhu, W and Mao, S 2016. Characterization and comparison of the temporal dynamics of ruminal bacterial microbiota colonizing rice straw and alfalfa hay within ruminants. Journal of Dairy Science 99, 9668–9681.CrossRefGoogle ScholarPubMed
Mayorga, OL, Kingston-Smith, AH, Kim, EJ, Allison, GG, Wilkinson, TJ, Hegarty, MJ, Theodorou, MK, Newbold, CJ and Huws, SA 2016. Temporal metagenomic and metabolomic characterization of fresh perennial ryegrass degradation by rumen bacteria. Frontiers in Microbiology 7, 1854.CrossRefGoogle ScholarPubMed
Mehrez, A, Ørskov, E and McDonald, I 1977. Rates of rumen fermentation in relation to ammonia concentration. British Journal of Nutrition 38, 437–443.CrossRefGoogle ScholarPubMed
Nolan, JV and Dobos, RC 2005. Nitrogen transactions in ruminants. In Quantitative aspects of ruminant digestion and metabolism (ed. J Dijkstra, JM Forbes and J France), pp. 177–206. CAB International, Oxfordshire, UK.CrossRefGoogle Scholar
Orr, RJ, Penning, PD, Harvey, A and Champion, RA 1997. Diurnal patterns of intake rate by sheep grazing monocultures of ryegrass or white clover. Applied Animal Behaviour Science 52, 65–77.CrossRefGoogle Scholar
Pittman, KA and Bryant, MP 1964. Peptides and other nitrogen sources for growth of Bacteroides ruminicola . Journal of Bacteriology 88, 401–410.Google ScholarPubMed
Quast, C, Pruesse, E, Yilmaz, P, Gerken, J, Schweer, T, Yarza, P, Peplies, J and Glöckner, FO 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41, D590–D596.CrossRefGoogle ScholarPubMed
Saitou, N and Nei, M 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.Google ScholarPubMed
Salvetti, E, Felis, GE, Dellaglio, F, Castioni, A, Torriani, S and Lawson, PA 2011. Reclassification of Lactobacillus catenaformis (Eggerth 1935) Moore and Holdeman 1970 and Lactobacillus vitulinus Sharpe et al. 1973 as Eggerthia catenaformis gen. nov., comb. nov. and Kandleria vitulina gen. nov., comb. nov., respectively. International Journal of Systematic and Evolutionary Microbiology 61, 2520–2524.CrossRefGoogle ScholarPubMed
Seedorf, H, Kittelmann, S and Janssen, PH 2015. Few highly abundant operational taxonomic units dominate within rumen methanogenic archaeal species in New Zealand sheep and cattle. Applied and Environmental Microbiology 81, 986–995.CrossRefGoogle ScholarPubMed
Seedorf, H, Kittelmann, S, Henderson, G and Janssen, PH 2014. RIM-DB: a taxonomic framework for community structure analysis of methanogenic archaea from the rumen and other intestinal environments. PeerJ 2, e494.CrossRefGoogle ScholarPubMed
Stevenson, DM and Weimer, PJ 2007. Dominance of Prevotella and low abundance of classical ruminal bacterial species in the bovine rumen revealed by relative quantification real-time PCR. Applied Microbiology and Biotechnology 75, 165–174.CrossRefGoogle ScholarPubMed
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.CrossRefGoogle ScholarPubMed
Thompson, JD, Higgins, DG and Gibson, TJ 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle ScholarPubMed
Vibart, RE, Burke, JL and Pacheco, D 2011. Ruminal fermentation characteristics from sheep offered a fresh grazing allocation of a ryegrass-based pasture either in the morning or in the afternoon. Proceedings of the New Zealand Society of Animal Production 71, 234–239.Google Scholar
Vibart, RE, Tavendale, MH, Burke, JL and Pacheco, D 2012. In vitro fermentation of [15N-] ryegrass and ruminal digesta of sheep grazing a ryegrass-based pasture in the morning or in the afternoon. Proceedings of the New Zealand Society of Animal Production 72, 100–105.Google Scholar
Weatherburn, MW 1967. Phenol-hypochlorite reaction for determination of ammonia. Analytical Chemistry 39, 971–974.CrossRefGoogle Scholar
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