Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-28T03:56:10.500Z Has data issue: false hasContentIssue false
  • English
  • Français

Microbial ecosystem and methanogenesis in ruminants

Published online by Cambridge University Press:  13 April 2010

D. P. Morgavi ,
E. Forano ,
C. Martin  and
C. J. Newbold
D. P. Morgavi*
Affiliation:
INRA UR1213 Herbivores, Site de Theix, F-63122 Saint-Genès-Champanelle, France
E. Forano
Affiliation:
INRA UR454 Microbiologie, Site de Theix, F-63122 Saint-Genès-Champanelle, France
C. Martin
Affiliation:
INRA UR1213 Herbivores, Site de Theix, F-63122 Saint-Genès-Champanelle, France
C. J. Newbold
Affiliation:
Institute of Biological Environmental and Rural Sciences, Aberystwyth University SY23 3AL, Ceredigion, UK
*
†E-mail: morgavi@clermont.inra.fr
Get access

Abstract

Ruminant production is under increased public scrutiny in terms of the importance of cattle and other ruminants as major producers of the greenhouse gas methane. Methanogenesis is performed by methanogenic archaea, a specialised group of microbes present in several anaerobic environments including the rumen. In the rumen, methanogens utilise predominantly H2 and CO2 as substrates to produce methane, filling an important functional niche in the ecosystem. However, in addition to methanogens, other microbes also have an influence on methane production either because they are involved in hydrogen (H2) metabolism or because they affect the numbers of methanogens or other members of the microbiota. This study explores the relationship between some of these microbes and methanogenesis and highlights some functional groups that could play a role in decreasing methane emissions. Dihydrogen (‘H2’ from this point on) is the key element that drives methane production in the rumen. Among H2 producers, protozoa have a prominent position, which is strengthened by their close physical association with methanogens, which favours H2 transfer from one to the other. A strong positive interaction was found between protozoal numbers and methane emissions, and because this group is possibly not essential for rumen function, protozoa might be a target for methane mitigation. An important function that is associated with production of H2 is the degradation of fibrous plant material. However, not all members of the rumen fibrolytic community produce H2. Increasing the proportion of non-H2 producing fibrolytic microorganisms might decrease methane production without affecting forage degradability. Alternative pathways that use electron acceptors other than CO2 to oxidise H2 also exist in the rumen. Bacteria with this type of metabolism normally occupy a distinct ecological niche and are not dominant members of the microbiota; however, their numbers can increase if the right potential electron acceptor is present in the diet. Nitrate is an alternative electron sinks that can promote the growth of particular bacteria able to compete with methanogens. Because of the toxicity of the intermediate product, nitrite, the use of nitrate has not been fully explored, but in adapted animals, nitrite does not accumulate and nitrate supplementation may be an alternative under some dietary conditions that deserves to be further studied. In conclusion, methanogens in the rumen co-exist with other microbes, which have contrasting activities. A better understanding of these populations and the pathways that compete with methanogenesis may provide novel targets for emissions abatement in ruminant production.

Keywords

rumen fermentationH2 sinkshydrogen producersmethanogensmethane
Type
Full Paper
Information
animal , Volume 4 , Issue 7: XIth International Symposium on Ruminant Physiology (ISRP), 6–9 September, 2009 Clermont-Ferrand (France) , July 2010 , pp. 1024 - 1036
Copyright
Copyright © The Animal Consortium 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, RC, Rasmussen, MA 1998. Use of a novel nitrotoxin-metabolising bacterium to reduce ruminal methane production. Bioresource Technology 64, 89–95.CrossRefGoogle Scholar
Anderson, RC, Rasmussen, MA, Jensen, NS, Allison, MJ 2000. Denitrobacterium detoxificans gen. nov., sp. nov., a ruminal bacterium that respires on nitrocompounds. International Journal of Systematic and Evolutionary Microbiology 50, 633–638.CrossRefGoogle Scholar
Anderson, RC, Carstens, GE, Miller, RK, Callaway, TR, Schultz, CL, Edrington, TS, Harvey, RB, Nisbet, DJ 2006. Effect of oral nitroethane and 2-nitropropanol administration on methane-producing activity and volatile fatty acid production in the ovine rumen. Bioresource Technology 97, 2421–2426.CrossRefGoogle ScholarPubMed
Anderson, RC, Krueger, NA, Stanton, TB, Callaway, TR, Edrington, TS, Harvey, RB, Jung, YS, Nisbet, DJ 2008. Effects of select nitrocompounds on in vitro ruminal fermentation during conditions of limiting or excess added reductant. Bioresource Technology 99, 8655–8661.CrossRefGoogle ScholarPubMed
Animut, G, Puchala, R, Goetsch, AL, Patra, AK, Sahlu, T, Varel, VH, Wells, J 2008. Methane emission by goats consuming diets with different levels of condensed tannins from lespedeza. Animal Feed Science and Technology 144, 212–227.CrossRefGoogle Scholar
Attwood, GT, Kelly, WJ, Altermann, EH, Leahy, SC 2008. Analysis of the Methanobrevibacter ruminantium draft genome: understanding methanogen biology to inhibit their action in the rumen. Australian Journal of Experimental Agriculture 48, 83–88.CrossRefGoogle Scholar
Beauchemin, KA, McGinn, SM, Benchaar, C, Holtshausen, L 2009. Crushed sunflower, flax, or canola seeds in lactating dairy cow diets: effects on methane production, rumen fermentation, and milk production. Journal of Dairy Science 92, 2118–2127.CrossRefGoogle ScholarPubMed
Bird, SH, Hegarty, RS, Woodgate, R 2008. Persistence of defaunation effects on digestion and methane production in ewes. Australian Journal of Experimental Agriculture 48, 152–155.Google Scholar
Chandramoni, Tiwari, CM, Haque, N, Murari, L, Jadhao, SB, Khan, MY 2002. Energy balance in faunated and defaunated sheep on a ration high in concentrate to roughage (good quality) ratio. Pakistan Journal of Nutrition 1, 31–33.Google Scholar
Chaucheyras-Durand, F, Masseglia, S, Fonty, G, Forano, E 2008. Development of hydrogenotrophic microorganisms and H2 utilisation in the rumen of gnotobiotically-reared lambs. Influence of the composition of the cellulolytic microbial community and effect of the feed additive Saccharomyces cerevisiae I-1077. In Proceedings of the 6th INRA-RRI symposium. Gut microbiome: functionality, interaction with the host and impact on the environment, Clermont-Ferrand, France, pp. 48–49.Google Scholar
Chen, M, Wolin, MJ 1979. Effect of monensin and lasalocid-sodium on the growth of methanogenic and rumen saccharolytic bacteria. Applied and Environmental Microbiology 38, 72–77.CrossRefGoogle ScholarPubMed
Dehority, BA 1971. Carbon dioxide requirement of various species of rumen bacteria. The Journal of Bacteriology 105, 70–76.CrossRefGoogle ScholarPubMed
Delgado, C, Rosegrant, M, Steinfeld, H, Ehui, S, Courbois, C 2001. Livestock to 2020: the next food revolution. Outlook on Agriculture 30, 27–29.CrossRefGoogle Scholar
Demeyer, DI 1991. Quantitative aspects of microbial metabolism in the rumen and hindgut. In Rumen microbial metabolism and ruminant digestion (ed. JP Jouany), pp. 217–237. INRA Editions, Versailles, France.Google Scholar
Demeyer, DI, Fiedler, D, DeGraeve, KG 1996. Attempted induction of reductive acetogenesis into the rumen fermentation in vitro. Reproduction, Nutrition, Development 36, 233–240.CrossRefGoogle ScholarPubMed
Denman, SE, Tomkins, NW, McSweeney, CS 2007. Quantitation and diversity analysis of ruminal methanogenic populations in response to the antimethanogenic compound bromochloromethane. FEMS Microbiology Ecology 62, 313–322.CrossRefGoogle Scholar
Edwards, JE, McEwan, NR, Travis, AJ, Wallace, RJ 2004. 16S rDNA library-based analysis of ruminal bacterial diversity. Antonie van Leeuwenhoek 86, 263–281.CrossRefGoogle Scholar
Eugène, M, Archimède, H, Sauvant, D 2004. Quantitative meta-analysis on the effects of defaunation of the rumen on growth, intake and digestion in ruminants. Livestock Production Science 85, 81–97.CrossRefGoogle Scholar
FAO 2006. World agriculture: towards 2030/2050. Interim Report, Rome.Google Scholar
FAO 2009. Newsroom. Retrieved July 22, 2009, from www.fao.org/news/newsroom-home/Google Scholar
Finlay, BJ, Esteban, G, Clarke, KJ, Williams, AG, Embley, TM, Hirt, RP 1994. Some rumen ciliates have endosymbiotic methanogens. FEMS Microbiology Letters 117, 157–162.CrossRefGoogle ScholarPubMed
Fonty, G, Williams, AG, Bonnemoy, F, Morvan, B, Withers, SE, Gouet, P 1997. Effect of Methanobrevibacter sp. MF1 inoculation on glycoside hydrolase and polysaccharide depolymerase activities, wheat straw degradation and volatile fatty acid concentrations in the rumen of gnotobiotically-reared lambs. Anaerobe 3, 383–389.CrossRefGoogle ScholarPubMed
Fonty, G, Joblin, K, Chavarot, M, Roux, R, Naylor, G, Michallon, F 2007. Establishment and development of ruminal hydrogenotrophs in methanogen-free lambs. Applied and Environmental Microbiology 73, 6391–6403.CrossRefGoogle ScholarPubMed
Gill, M, Smith, P, Wilkinson, JM 2010. Mitigating climate change: the role of domestic livestock. Animal 4, 323–333.CrossRefGoogle ScholarPubMed
Goel, G, Makkar, HPS, Becker, K 2008. Changes in microbial community structure, methanogenesis and rumen fermentation in response to saponin-rich fractions from different plant materials. Journal of Applied Microbiology 105, 770–777.CrossRefGoogle ScholarPubMed
Goel, G, Makkar, HP, Becker, K 2009. Inhibition of methanogens by bromochloromethane: effects on microbial communities and rumen fermentation using batch and continuous fermentations. The British Journal of Nutrition 101, 1484–1492.CrossRefGoogle ScholarPubMed
Gould, DH, Cummings, BA, Hamar, DW 1997. In vivo indicators of pathologic ruminal sulphide production in steers with diet-induced polioencephalomalacia. Journal of Veterinary Diagnostic Investigation 9, 72–76.CrossRefGoogle ScholarPubMed
Grigg, D 1999. The changing geography of world food consumption in the second half of the twentieth century. The Geographical Journal 165, 1–11.Google Scholar
Gruby, D, Delafond, HMO 1843. Recherches sur des animalcules se développant en grand nombre dans l’estomac et dans les intestins, pendant la digestion des animaux herbivores et carnivores. Comptes Rendus de l’Académie des Sciences 17, 1304–1308.Google Scholar
Guan, H, Wittenberg, KM, Ominski, KH, Krause, DO 2006. Efficacy of ionophores in cattle diets for mitigation of enteric methane. Journal of Animal Science 84, 1896–1906.CrossRefGoogle ScholarPubMed
Guo, Y, Liu, J, Zhu, W, McSweeney, C 2007. Shifts of rumen microbial population detected by real-time PCR when methanogenesis is inhibited. Journal of Animal and Feed Science 16, 107–112.CrossRefGoogle Scholar
Guo, YQ, Liu, JX, Lu, Y, Zhu, WY, Denman, SE, McSweeney, CS 2008. Effect of tea saponin on methanogenesis, microbial community structure and expression of mcrA gene, in cultures of rumen micro-organisms. Letters in Applied Microbilology 47, 421–426.CrossRefGoogle ScholarPubMed
Gutierrez-Banuelos, H, Anderson, RC, Carstens, GE, Slay, LJ, Ramlachan, N, Horrocks, SM, Callaway, TR, Edrington, TS, Nisbet, DJ 2007. Zoonotic bacterial populations, gut fermentation characteristics and methane production in feedlot steers during oral nitroethane treatment and after the feeding of an experimental chlorate product. Anaerobe 13, 21–31.CrossRefGoogle ScholarPubMed
Hegarty, RS 1999. Reducing rumen methane emissions through elimination of rumen protozoa. Australian Journal of Agricultural Research 50, 1321–1327.CrossRefGoogle Scholar
Hegarty, RS, Bird, SH, Vanselow, BA, Woodgate, R 2008. Effects of the absence of protozoa from birth or from weaning on the growth and methane production of lambs. The British Journal of Nutrition 100, 1220–1227.CrossRefGoogle ScholarPubMed
Hess, HD, Beuret, RA, Lotscher, M, Hindrichsen, IK, Machmüller, A, Carulla, JE, Lascano, CE, Kreuzer, M 2004. Ruminal fermentation, methanogenesis and nitrogen utilisation of sheep receiving tropical grass hay-concentrate diets offered with sapindus saponaria fruits and cratylia argentea foliage. Animal Science 79, 177–189.CrossRefGoogle Scholar
Hillman, K, Lloyd, D, Williams, AG 1988. Interactions between the methanogen Methanosarcina barkeri and rumen holotrich ciliate protozoa. Letters in Applied Microbiology 7, 49–53.CrossRefGoogle Scholar
Hillman, K, Williams, AG, Lloyd, D 1995. Postprandial variations in endogenous metabolic activities of ovine rumen ciliate protozoa. Animal Feed Science and Technology 52, 237–247.CrossRefGoogle Scholar
Hoehler, TM, Alperin, MJ, Albert, DB, Martens, CS 1998. Thermodynamic control on hydrogen concentrations in anoxic sediments. Geochimica et Cosmochimica Acta 62, 1745–1756.CrossRefGoogle Scholar
Holtshausen, L, Chaves, AV, Beauchemin, KA, McGinn, SM, McAllister, TA, Odongo, NE, Cheeke, PR, Benchaar, C 2009. Feeding saponin-containing Yucca schidigera and Quillaja saponaria to decrease enteric methane production in dairy cows. Journal of Dairy Science 92, 2809–2821.CrossRefGoogle ScholarPubMed
Hong, SH, Kim, JS, Lee, SY, In, YH, Choi, SS, Rih, J-K, Kim, CH, Jeong, H, Hur, CG, Kim, JJ 2004. The genome sequence of the capnophilic rumen bacterium Mannheimia succiniciproducens. Nature Biotechnology 22, 1275–1281.CrossRefGoogle ScholarPubMed
Hungate, RE 1967. Hydrogen as an intermediate in the rumen fermentation. Archives of Microbiology 59, 158–164.Google ScholarPubMed
Hungate, RE, Smith, W, Bauchop, T, Yu, I, Rabinowitz, JC 1970. Formate as an intermediate in the bovine rumen fermentation. Journal of Bacteriology 102, 389–397.CrossRefGoogle ScholarPubMed
Immig, I, Demeyer, D, Fiedler, D, Van Nevel, C, Mbanzamihigo, L 1996. Attempts to induce reductive acetogenesis into a sheep rumen. Archiv für Tiernahrung 49, 363–370.CrossRefGoogle ScholarPubMed
IPPC 2007. Climate change 2007: the physical science basis: summary for policymakers. Intergovernmental panel on climate change, Paris.Google Scholar
Itabashi, H, Kobayashi, T, Matsumoto, M 1984. The effects of rumen ciliate protozoa on energy metabolism and some constituents in rumen fluid and blood plasma of goats. Japanese Journal of Zoological Science 55, 248–256.Google Scholar
Iwamoto, M, Asanuma, N, Hino, T 1999. Effects of nitrate combined with fumarate on methanogenesis, fermentation, and cellulose digestion by mixed ruminal microbes in vitro. Animal Science Journal 70, 471–478.Google Scholar
Iwamoto, M, Asanuma, N, Hino, T 2002. Ability of Selenomonas ruminantium, Veillonella parvula, and Wolinella succinogenes to reduce nitrate and nitrite with special reference to the suppression of ruminal methanogenesis. Anaerobe 8, 209–215.CrossRefGoogle Scholar
Janssen, PH, Kirs, M 2008. Structure of the archaeal community of the rumen. Applied and Environmental Microbiology 74, 3619–3625.CrossRefGoogle ScholarPubMed
Joblin, KN, Naylor, GE, Williams, AG 1990. Effect of Methanobrevibacter smithii xylanolytic activity of anaerobic ruminal fungi. Applied and Environmental Microbiology 56, 2287–2295.CrossRefGoogle ScholarPubMed
Johnson, K, Huyler, M, Westberg, H, Lamb, B, Zimmerman, P 1994. Measurement of methane emissions from ruminant livestock using a SF6 tracer technique. Environmental Science & Technoogy 28, 359–362.CrossRefGoogle Scholar
Jordan, E, Lovett, DK, Hawkins, M, Callan, JJ, O’Mara, FP 2006a. The effect of varying levels of coconut oil on intake, digestibility and methane output from continental cross beef heifers. Animal Science 82, 859–865.CrossRefGoogle Scholar
Jordan, E, Kenny, D, Hawkins, M, Malone, R, Lovett, DK, O’Mara, FP 2006b. Effect of refined soy oil or whole soybeans on intake, methane output, and performance of young bulls. Journal of Animal Science 84, 2418–2425.CrossRefGoogle ScholarPubMed
Kajikawa, H, Valdes, C, Hillman, K, Wallace, RJ, Newbold, CJ 2003. Methane oxidation and its coupled electron-sink reactions in ruminal fluid. Letters in Applied Microbiology 36, 354–357.CrossRefGoogle ScholarPubMed
Klieve, AV, Ouwerkerk, D 2007. Comparative greenhouse gas emissions from herbivores. In Proceedings of the 7th International Symposium on the Nutrition of Herbivores, Beijing, China, pp. 487–500.Google Scholar
Kreuzer, M, Kirchgessner, M, Muller, HL 1986. Effect of defaunation on the loss of energy in wethers fed different quantities of cellulose and normal or steamflaked maize starch. Animal Feed Science and Technology 16, 233–241.CrossRefGoogle Scholar
Larue, R, Yu, Z, Parisi, VA, Egan, AR, Morrison, M 2005. Novel microbial diversity adherent to plant biomass in the herbivore gastrointestinal tract, as revealed by ribosomal intergenic spacer analysis and rrs gene sequencing. Environmental Microbiology 7, 530–543.CrossRefGoogle ScholarPubMed
Latham, MJ, Wolin, MJ 1977. Fermentation of cellulose by Ruminococcus flavefaciens in the presence and absence of Methanobacterium ruminantium. Applied Environmental Microbiology 34, 297–301.Google Scholar
Le Van, TD, Robinson, JA, Ralph, J, Greening, RC, Smolenski, WJ, Leedle, JAZ, Schaefer, DM 1998. Assessment of reductive acetogenesis with indigenous ruminal bacterium populations and Acetitomaculum ruminis. Applied and Environmental Microbiology 64, 3429–3436.CrossRefGoogle ScholarPubMed
Leadbetter, JR, Breznak, JA 1996. Physiological ecology of Methanobrevibacter cuticularis sp. nov. and Methanobrevibacter curvatus sp. nov., isolated from the hindgut of the termite Reticulitermes flavipes. Applied and Environmental Microbiology 62, 3620–3631.CrossRefGoogle ScholarPubMed
Lila, ZA, Mohammed, N, Kanda, S, Kurihara, M, Itabashi, H 2005. Sarsaponin effects on ruminal fermentation and microbes, methane production, digestibility and blood metabolites in steers.. Asian–Australasian Journal of Animal Science 18, 1746–1751.CrossRefGoogle Scholar
Liu, Y, Whitman, WB 2008. Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Annals of the New York Academy of Sciences 1125, 171–189.CrossRefGoogle ScholarPubMed
Lopez, S, McIntosh, FM, Wallace, RJ, Newbold, CJ 1999. Effect of adding acetogenic bacteria on methane production by mixed rumen microorganisms. Animal Feed Science and Technology 78, 1–9.CrossRefGoogle Scholar
Lovett, D, Lovell, S, Stack, L, Callan, J, Finlay, M, Conolly, J, O’Mara, FP 2003. Effect of forage/concentrate ratio and dietary coconut oil level on methane output and performance of finishing beef heifers. Livestock Production Science 84, 135–146.CrossRefGoogle Scholar
Machmüller, A, Kreuzer, M 1999. Methane suppression by coconut oil and associated effects on nutrient and energy balance in sheep. Canadian Journal of Animal Science 79, 65–72.CrossRefGoogle Scholar
Machmüller, A, Ossowski, DA, Kreuzer, M 2000. Comparative evaluation of the effects of coconut oil, oilseeds and crystalline fat on methane release, digestion and energy balance in lambs. Animal Feed Science and Technology 85, 41–60.CrossRefGoogle Scholar
Machmüller, A, Soliva, CR, Kreuzer, M 2003a. Methane-suppressing effect of myristic acid in sheep as affected by dietary calcium and forage proportion. The British Journal of Nutrition 90, 529–540.CrossRefGoogle ScholarPubMed
Machmüller, A, Soliva, CR, Kreuzer, M 2003b. Effect of coconut oil and defaunation treatment on methanogenesis in sheep. Reproduction, Nutrition, Development 43, 41–55.CrossRefGoogle ScholarPubMed
Martin, C, Ferlay, A, Chilliard, Y, Doreau, M 2007a. Rumen methanogenesis of dairy cows in response to increasing levels of dietary extruded linseeds. In Energy and protein metabolism and nutrition, EAAP publication (ed. I Ortigues-Marty, N Miraux and W Brand-Williams), pp. 609–610. Wageningen Academic Publishers, Wageningen, The Netherlands.Google Scholar
Martin, C, Dubroeucq, H, Micol, D, Agabriel, J, Doreau, M 2007b. Methane output from beef cattle fed different high-concentrate diets. In Proceedings of the British Society of Animal Science, Southport, UK, p. 46.Google Scholar
Mitsumori, M, Ajisaka, N, Tajima, K, Kajikawa, H, Kurihara, M 2002. Detection of Proteobacteria from the rumen by PCR using methanotroph-specific primers. Letters in Applied Microbiology 35, 251–255.CrossRefGoogle ScholarPubMed
Morgavi, DP, Jouany, JP, Martin, C 2008. Changes in methane emission and rumen fermentation parameters induced by refaunation in sheep. Australian Journal of Experimental Agriculture 48, 69–72.CrossRefGoogle Scholar
Morvan, B, Dore, J, Rieu-Lesme, F, Foucat, L, Fonty, G, Gouet, P 1994. Establishment of hydrogen-utilizing bacteria in the rumen of the newborn lamb. FEMS Microbiology Letters 117, 249–256.Google Scholar
Morvan, B, Bonnemoy, F, Fonty, G, Gouet, P 1996. Quantitative determination of H2-utilizing acetogenic and sulfate-reducing bacteria and methanogenic archaea from digestive tract of different mammals. Current Microbiology 32, 129–133.Google Scholar
Mosoni, P, Chaucheyras-Durand, F, Bera-Maillet, C, Forano, E 2007. Quantification by real-time PCR of cellulolytic bacteria in the rumen of sheep after supplementation of a forage diet with readily fermentable carbohydrates: effect of a yeast additive. Journal of Applied Microbiology 103, 2676–2685.Google Scholar
Mosoni, P, Gagen, E, Denman, R, McSweeney, C, Forano, E 2008. Quantification of rumen cellulolytic bacteria and analysis of bacterial diversity before and after establishment of Methanobrevibacter wolinii in methanogen-free lambs. In Proceedings of the 6th INRA-RRI symposium. Gut microbiome: functionality, interaction with the host and impact on the environment, Clermont-Ferrand, France, pp. 50–51.Google Scholar
Newbold, CJ, Lassalas, B, Jouany, JP 1995. The importance of methanogens associated with ciliate protozoa in ruminal methane production in vitro. Letters in Applied Microbiology 21, 230–234.CrossRefGoogle ScholarPubMed
Nollet, L, Demeyer, D, Verstraete, W 1997. Effect of 2-bromoethanesulfonic acid and peptostreptococcus productus ATCC 35244 addition on stimulation of reductive acetogenesis in the ruminal ecosystem by selective inhibition of methanogenesis. Applied and Environmental Microbiology 63, 194–200.CrossRefGoogle ScholarPubMed
Nollet, L, Mbanzamihigo, L, Demeyer, D, Verstraete, W 1998. Effect of the addition of Peptostreptococcus productus ATCC 35244 on reductive acetogenesis in the ruminal ecosystem after inhibition of methanogenesis by cell-free supernatant of Lactobacillus plantarum 80. Animal Feed Science and Technology 71, 49–66.CrossRefGoogle Scholar
Ohene-Adjei, S, Teather, RM, Ivan, M, Forster, RJ 2007. Postinoculation protozoan establishment and association patterns of methanogenic archaea in the ovine rumen. Applied and Environmental Microbiology 73, 4609–4618.Google Scholar
Oppermann, RA, Nelson, WO, Brown, RE 1961. In vivo studies of methanogenesis in the bovine rumen: dissimilation of acetate. Journal of General Microbiology 25, 103–111.CrossRefGoogle ScholarPubMed
Pavlostathis, SG, Miller, TL, Wolin, MJ 1990. Cellulose fermentation by continuous cultures of Ruminococcus albus and Methanobrevibacter smithii. Applied Microbiology and Biotechnology 33, 109–116.CrossRefGoogle Scholar
Pei, C-X, Mao, S-Y, Cheng, Y-F, Zhu, W-Y 2010. Diversity, abundance and novel 16S rRNA gene sequences of methanogens in rumen liquid, solid and epithelium fractions of Jinnan cattle. Animal 4, 20–29.Google Scholar
Pen, B, Takaura, K, Yamaguchi, S, Asa, R, Takahashi, J 2007. Effects of Yucca schidigera and Quillaja saponaria with or without β 1-4 galacto-oligosaccharides on ruminal fermentation, methane production and nitrogen utilisation in sheep. Animal Feed Science and Technology 138, 75–88.CrossRefGoogle Scholar
Ranilla, MJ, Jouany, JP, Morgavi, DP 2007. Methane production and substrate degradation by rumen microbial communities containing single protozoal species in vitro. Letters in Applied Microbiology 45, 675–680.CrossRefGoogle ScholarPubMed
Sar, C, Mwenya, B, Santoso, B, Takaura, K, Morikawa, R, Isogai, N, Asakura, Y, Toride, Y, Takahashi, J 2005a. Effect of Escherichia coli W3110 on ruminal methanogenesis and nitrate/nitrite reduction in vitro. Animal Feed Science and Technology 118, 295–306.Google Scholar
Sar, C, Mwenya, B, Santoso, B, Takaura, K, Morikawa, R, Isogai, N, Asakura, Y, Toride, Y, Takahashi, J 2005b. Effect of Escherichia coli wild type or its derivative with high nitrite reductase activity on in vitro ruminal methanogenesis and nitrate/nitrite reduction. Journal of Animal Science 83, 644–652.CrossRefGoogle ScholarPubMed
Sauvant, D, Schmidely, P, Daudin, JJ, St-Pierre, NR 2008. Meta-analyses of experimental data in animal nutrition. Animal 2, 1203–1214.Google Scholar
Sharp, R, Ziemer, CJ, Stern, MD, Stahl, DA 1998. Taxon-specific associations between protozoal and methanogen populations in the rumen and a model rumen system. FEMS Microbiology Ecology 26, 71–78.CrossRefGoogle Scholar
Shin, EC, Choi, BR, Lim, WJ, Hong, SY, An, CL, Cho, KM, Kim, YK, An, JM, Kang, JM, Lee, SS 2004. Phylogenetic analysis of archaea in three fractions of cow rumen based on the 16S rDNA sequence. Anaerobe 10, 313–319.CrossRefGoogle ScholarPubMed
Simon, J 2002. Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiology Reviews 26, 285–309.Google Scholar
Skillman, LC, Evans, PN, Naylor, GE, Morvan, B, Jarvis, GN, Joblin, KN 2004. 16S ribosomal DNA-directed PCR primers for ruminal methanogens and identification of methanogens colonising young lambs. Anaerobe 10, 277–285.CrossRefGoogle ScholarPubMed
Sliwinski, BJ, Kreuzer, M, Wettstein, HR, Machmüller, A 2002. Rumen fermentation and nitrogen balance of lambs fed diets containing plant extracts rich in tannins and saponins, and associated emissions of nitrogen and methane. Archiv für Tierernahnung 56, 379–392.CrossRefGoogle Scholar
Steinfeld, H, Gerber, P, Wassenaar, T, Castel, V, Rosales, M, de Haan, C 2006. Livestock’s long shadow environmental issues and options. FAO, p. 390.Google Scholar
Stewart, CS, Flint, HJ, Bryant, MP 1997. The rumen bacteria. In The rumen microbial ecosystem (ed. PN Hobson and CS Stewart), pp. 10–72. Chapman & Hall, London.Google Scholar
Stumm, CK, Gijzen, HJ, Vogels, GD 1982. Association of methanogenic bacteria with ovine rumen ciliates. The British Journal of Nutrition 47, 95–99.Google Scholar
Thauer, RK, Kaster, AK, Seedorf, H, Buckel, W, Hedderich, R 2008. Methanogenic archaea: ecologically relevant differences in energy conservation. Nature Reviews Microbiology 6, 579–591.CrossRefGoogle ScholarPubMed
Tholen, A, Pester, M, Brune, A 2007. Simultaneous methanogenesis and oxygen reduction by Methanobrevibacter cuticularis at low oxygen fluxes. FEMS Microbiology Ecology 62, 303–312.Google Scholar
Thornton, P, Herrero, M, Freeman, A, Mwai, O, Rege, E, Jones, P, McDermott, J 2007. Vulnerability, climate change and livestock – research opportunities and challenges for poverty alleviation. SAT Journal 4, 23.Google Scholar
Tokura, M, Ushida, K, Miyazaki, K, Kojima, Y 1997. Methanogens associated with rumen ciliates. FEMS Microbiology Ecology 22, 137–143.CrossRefGoogle Scholar
Tóthová, T, Piknová, M, Kišidayová, S, Javorský, P, Pristaš, P 2008. Distinctive archaebacterial species associated with anaerobic rumen protozoan Entodinium caudatum. Folia Microbiologica 53, 259–262.Google Scholar
Ushida, K, Jouany, JP 1996. Methane production associated with rumen-ciliated protozoa and its effect on protozoan activity. Letters in Applied Microbiology 23, 129–132.CrossRefGoogle ScholarPubMed
Ushida, K, Newbold, CJ, Jouany, JP 1997. Interspecies hydrogen transfer between the rumen ciliate Polyplastron multivesiculatum and Methanosarcina barkeri. The Journal of General and Applied Microbiology 43, 129–131.CrossRefGoogle ScholarPubMed
van Hoek, AH, van Alen, TA, Sprakel, VS, Leunissen, JA, Brigge, T, Vogels, GD, Hackstein, JH 2000. Multiple acquisition of methanogenic archaeal symbionts by anaerobic ciliates. Molecular Biology and Evolution 17, 251–258.CrossRefGoogle ScholarPubMed
Vogels, GD, Hoppe, WF, Stumm, CK 1980. Association of methanogenic bacteria with rumen ciliates. Applied Environmental Microbiology 40, 608–612.CrossRefGoogle ScholarPubMed
Weimer, PJ 1998. Manipulating ruminal fermentation: a microbial ecological perspective. Journal of Animal Science 76, 3114–3122.CrossRefGoogle ScholarPubMed
Whitelaw, FG, Eadie, JM, Bruce, LA, Shand, WJ 1984. Methane formation in faunated and ciliate-free cattle and its relationship with rumen volatile fatty acid proportions. The British Journal of Nutrition 52, 261–275.CrossRefGoogle ScholarPubMed
Williams, AG, Coleman, GS 1992. The rumen protozoa. Springer-Verlag New York Inc., New York.Google Scholar
Williams, AG, Withers, SE 1993. Changes in the rumen microbial population and its activities during the refaunation period after the reintroduction of ciliate protozoa into the rumen of defaunated sheep. Canadian Journal of Microbiology 39, 61–69.Google Scholar
Williams, AG, Withers, SE, Joblin, KN 1994. The effect of cocultivation with hydrogen-consuming bacteria on xylanolysis by Ruminococcus flavefaciens. Current Microbiology 29, 133–138.Google Scholar
Wina, E, Muetzel, S, Hoffmann, E, Makkar, HPS, Becker, K 2005. Saponins containing methanol extract of sapindus rarak affect microbial fermentation, microbial activity and microbial community structure in vitro. Animal Feed Science and Technology 121, 159–174.CrossRefGoogle Scholar
Wolin, M, Miller, T, Stewart, C 1997. Microbe-microbe interactions. In The rumen microbial ecosystem (ed. P Hobson and C Stewart), pp. 467–491. Chapman & Hall, London.Google Scholar
World_Bank 2008. Rising food and fuel prices: addressing the risks to future generations. Retrieved September 2009, from http://siteresources.worldbank.org/DEVCOMMEXT/Resources/Food-Fuel.pdf2009Google Scholar
Yanez-Ruiz, DR, Hart, KJ, Belanche, A, Martin-Garcia, AI, Newbold, CJ 2007. The effect of protozoa on methane emissions by lambs. In Proceedings of the British Society of Animal Science, p. 47.CrossRefGoogle Scholar
Yanez-Ruiz, DR, Hart, KJ, Martin-Garcia, AI, Ramos, S, Newbold, CJ 2008. Diet composition at weaning affects the rumen microbial population and methane emissions by lambs. Australian Journal of Experimental Agriculture 48, 186–188.CrossRefGoogle Scholar
Yu, Z, Yu, M, Morrison, M 2006. Improved serial analysis of V1 ribosomal sequence tags (SARST-V1) provides a rapid, comprehensive, sequence-based characterisation of bacterial diversity and community composition. Environmental Microbiology 8, 603–611.Google Scholar