Metanogénesis ruminal y estrategias para su mitigación

Sandra Posada Ochoa, Ricardo Noguera

Resumen


El mantenimiento de la fermentación ruminal depende de la remoción de los productos generados durante la degradación de los alimentos. Los ácidos grasos volátiles (AGV´s) son rápidamente absorbidos por el animal hospedero y utilizados como fuente de energía, mientras otros productos como el hidrógeno (H2) y el dióxido de carbono (CO2) son utilizados en el rumen por microrganismos pertenecientes al dominio Archaea para producir metano (CH4), el cual es eructado por el animal. La actividad metanogénica genera la energía necesaria para la supervivencia de los metanógenos y mantiene una presión baja de H2, creandoun ambiente favorable para la oxidación de co-factores reducidos generados durante la glucolisis. A pesar de su importancia para la degradación ruminal de los alimentos, la metanogénesis representa pérdida de la energía consumida por el rumiante y su remoción hacia la atmosfera contribuye al incremento en el total de gases de efecto invernadero (GEI). La reducción de las emisiones de CH4 desde el rumen puede alcanzarse a través del manejo de la alimentación, el mejoramiento del desempeño productivo de los animales y la utilización de aditivos. El objetivo de este trabajo es ofrecer elementos conceptuales que permitan comprender el origen y la importancia de la metanogénesis en la fermentación ruminal y como este proceso puede ser modulado sin afectar negativamente la productividad animal.

 

Ruminal methanogenesis and mitigation strategies

Maintaining rumen fermentation depends on the removal of products generated during food degradation. Volatile fatty acids (AGV's) are rapidly absorbed by the host animal and used as energy source, while other products such as hydrogen (H2) and carbon dioxide (CO2) are used in the rumen by Archaea microorganisms to produce methane (CH4), which is belched by the animal. Methanogenic activity generates the energy required for the survival of methanogens and maintains a low H2 pressure, creating a favorable environment for the oxidation of reduced cofactors produced during glycolysis. Despite its importance for ruminal degradation, methanogenesis represents loss of energy consumed by the ruminant and its escape to the atmosphere increases total greenhouse gas (GHG) emissions. Reducing rumen emissions of CH4 can be achieved through feeding strategies, improved animal performance, and the use of feed additives. The aim of this paper is to provide conceptual tools for understanding the origin and importance of methanogenesis in ruminal fermentation and how this process can be modulated without adversely affecting animal productivity.

 

Metanogênese ruminal e estratégias para a sua  mitigação

A manutenção da fermentação ruminal depende da remoção dos produtos gerados durante a degradação dos alimentos. Os ácidos graxos voláteis (AGV's) são rapidamente absorvidos pelo animal hospedeiro e utilizados como fonte de energia, enquanto que outros produtos tais como o hidrogénio (H2) e o dióxido de carbono (CO2) são utilizados no rúmen por microorganismos pertences ao domínio Archaea para produzir metano (CH4), o qual é expelido pelo animal. A atividade metanogênica gera a energia necessária para a sobrevivência da methanogens e mantém uma baixa pressão de H2, criando um ambiente favorável para a oxidação de co-fatores reduzidos gerados durante a glicólise. Apesar da sua importância para a degradação ruminal dos alimentos, a methanogenesis representa uma perda significativa da energia consumida pelos ruminantes e sua remoção para a atmosfera contribui ao aumento do total de gases de efeito estufa (GEE). Redução das emissões de CH4 do rúmen pode ser alcançada através do manejo alimentar, aumento do desempenho produtivo dos animais e utilização de aditivos. O objetivo deste trabalho é fornecer elementos conceituais para compreender a origem e a importância do methanogenesis na fermentação ruminal e como este processo pode ser modulado sem afetar negativamente a produtividade animal.



Palabras clave


Archaea, calentamiento global, efecto invernadero, fermentación en el rumen, hidrógeno, metano (Fuente: CAB).

Texto completo:

PDF

Referencias


Alaboudi AR, Jones GA. Effect of acclimation to high nitrate intakes on some rumen fermentation parameters in sheep. Can J Anim Sci 1985; 65(4): 841-849.

Asanuma N, Iwamoto M, Hino T. Effect of the addition of fumarate on methane production by ruminal microorganisms in vitro. J Dairy Sci 1999; 82(4): 780-787.

Benchaar C, Calsamiglia S, Chaves AV, Fraser GR, Colombatto D, et al. A review of plant-derived essential oils in ruminant nutrition and production. Anim Feed Sci Technol 2008; 145(1): 209-228.

Blaxter KL, Clapperton JL. Prediction of the amount of methane produced by ruminants. Brit J Nutr 1965; 19(01): 511-522.

Boone DR, Johnson RL, Liu Y. Diffusion of the interspecies electron carriers H2 and formate in methanogenic ecosystems and its implications in the measurement of Km for H2 or formate uptake. Appl Environ Microbiol 1989; 55(7): 1735-1741.

Busquet M, Calsamiglia S, Ferret A, Cardozo PW, Kamel C. Effects of cinnamaldehyde and garlic oil on rumen microbial fermentation in a dual flow continuous culture. J Dairy Sci 2005a; 88(7): 2508-2516.

Busquet M, Calsamiglia S, Ferret A, Carro MD, Kamel C. Effect of garlic oil and four of its compounds on rumen microbial fermentation. J Dairy Sci 2005b; 88(12): 4393-4404.

Busquet M, Calsamiglia S, Ferret A, Kamel C. Plant extracts affect in vitro rumen microbial fermentation. J Dairy Sci 2006; 89(2): 761-771.

Chaves AV, He ML, Yang WZ, Hristov AN, McAllister TA, et al. Effects of essential oils on proteolytic, deaminative and methanogenic activities of mixed ruminal bacteria. Can J Anim Sci 2008; 88(1): 117-122.

Chin KJ, Janssen PH. Propionate formation by Opitutus terrae in pure culture and in mixed culture with a hydrogenotrophic methanogen and implications for carbon fluxes in anoxic rice paddy soil. Appl Environ Microbiol 2002; 68(4): 2089-2092.

Czerkawski JW. Methane production in ruminants and its significance. World Rev Nutr Diet 1969; 11: 240-282.

Czerkawski JW. Fate of metabolic hydrogen in the rumen. Proc Nutr Soc 1972; 31(02): 141-146.

Dawson KA, Rasmussen MA, Allison MJ. Digestive disorders and nutritional toxicity. In: Hobson PN, Stewart CS (eds). The Rumen Microbial Ecosystem. 2nd ed. London: Chapman & Hall; 1997. p. 633-660.

De Haas Y, Windig JJ, Calus MPL, Dijkstra J, De Haan M, et al. Genetic parameters for predicted methane production and potential for reducing enteric emissions through genomic selection. J Dairy Sci 2011; 94(12): 6122-6134.

Deppenmeier U, Müller V. Life close to the thermodynamic limit: how methanogenic archaea conserve energy. Results Probl Cell Differ 2008; 45: 123-152.

Faseleh Jahromi M, Liang JB, Ho YW, Mohamad R, Goh YM, et al. Lovastatin in Aspergillus terreus: Fermented Rice Straw Extracts Interferes with Methane Production and Gene Expression in Methanobrevibacter smithii. BioMed Research International 2013; [acceso: 27 de enero de 2014]. URL: http://dx.doi.org/10.1155/2013/604721

Finlay BJ, Esteban G, Clarke KJ, Williams AG, Embley TM, et al. Some rumen ciliates have endosymbiotic methanogens. FEMS Microbiol Lett 1994; 117(2): 157-161.

Fonty G, Williams AG, Bonnemoy F, Morvan B, Withers SE, et al. 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 1997; 3(6): 383-389.

Galbraith H, Miller TB. Physicochemical effects of long chain fatty acids on bacterial cells and their protoplasts. J App Microbiol 1973; 36(4): 647-658.

Garton GA. The digestion and absorption of lipids in ruminant animals. World Rev Nutr Diet 1967; 7: 225-250.

Hales KE, Cole NA, MacDonald JC. Effects of corn processing method and dietary inclusion of wet distillers grains with solubles on energy metabolism, carbon− nitrogen balance, and methane emissions of cattle. J Anim Sci 2012; 90(9): 3174-3185.

Hammond KJ, Burke JL, Koolaard JP, Muetzel S, Pinares-Patiño CS, et al. Effects of feed intake on enteric methane emissions from sheep fed fresh white clover (Trifolium repens) and perennial ryegrass (Lolium perenne) forages. Anim Feed Sci Technol 2013; 179 (s 1-4): 121-132.

Hammond KJ, Muetzel S, Waghorn GG, Pinares-Patino, CS, Burke JL, et al. The variation in methane emissions from sheep and cattle is not explained by the chemical composition of ryegrass. Proceedings of the 69th Conference of the New Zealand Society of Animal Production; 2009 June 24-26; Canterbury, New Zealand. New Zealand Society of Animal Production; vol. 69, p. 174-178.

Hegarty RS, Gerdes R. Hydrogen production and transfer in the rumen. Rec Adv Anim Nutr 1998; 12: 37-44.

Hino T, Russell JB. Effect of reducing-equivalent disposal and NADH/NAD on deamination of amino acids by intact rumen microorganisms and their cell extracts. Appl Environ Microbiol 1985; 50(6): 1368-1374.

Holter JB, Young AJ. Methane prediction in dry and lactating Holstein cows. J Dairy Sci 1992; 75(8): 2165-2175.

Hubert C, Voordouw G. Oil field souring control by nitrate-reducing Sulfurospirillum spp. that outcompete sulfate-reducing bacteria for organic electron donors. Appl Environ Microbiol 2007; 73(8): 2644-2652.

Hungate RE. The rumen microbial ecosystem. Annu Rev Ecol Syst 1975; 6: 39-66.

Hungate RE, Smith W, Bauchop T, Yu I, Rabinowitz JC. Formate as an intermediate in the bovine rumen fermentation. J Bacteriol 1970; 102(2): 389-397.

Hybu Cig Cymru/Meat Promotion Wales. Reducing methane emissions through improved lamb production. Tŷ Rheidol, UK 2011; [acceso: 26 de febrero de 2014]. URL:http://hccmpw.org.uk/medialibrary/publications/Reducing%20Methane.pdf

Iannotti EL, Kafkewitz D, Wolin MJ, Bryant MP. Glucose fermentation products of Ruminococcus albus grown in continuous culture with Vibrio succinogenes: changes caused by interspecies transfer of H2. J Bacteriol 1973; 114(3): 1231-1240.

IPCC (2007) Changes in atmospheric constituents and in radiative forcing. In: Solomon S, Quin D, Manning M, Chen Z, Marquis M, et al. (eds) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, New York, pp 212–213.

Iwamoto M, Asanuma N, Hino T. Effect of nitrate combined with fumarate on methanogenesis, fermentation, and cellulose digestion by mixed ruminal microbes in vitro. Anim Sci J 1999; 70(6): 471–478.

Janssen PH. Influence of hydrogen on rumen methane formation and fermentation balances through microbial growth kinetics and fermentation thermodynamics. Anim Feed Sci Technol 2010; 160(1): 1-22.

Janssen PH, Kirs M. Structure of the archaeal community of the rumen. Appl Environ Microbiol 2008; 74(12): 3619-3625.

Jayanegara A, Leiber F, Kreuzer M. Meta‐analysis of the relationship between dietary tannin level and methane formation in ruminants from in vivo and in vitro experiments. J Anim Physiol Anim Nutr 2012; 96(3): 365-375.

Johnson DE, Hill TM, Ward GM, Johnson KA, Branine ME, et al. Principle factors varying methane emissions from ruminants and other animals. In: Khalil MAK (ed). Atmospheric Methane: Sources, Sinks, and Role in Global Change. NATO ADI Series Vol. 113. Berlin: Springer-Verlag; 1993. p. 199–229.

Johnson KA, Johnson DE. Methane emissions from cattle. J Anim Sci 1995; 73(8): 2483-2492.

Kamra DN, Agarwal N, Chaudhary LC. Inhibition of ruminal methanogenesis by tropical plants containing secondary compounds. In: Soliva CR, Takahashi J, Kreuzer M (eds). Greenhouse Gases and Animal Agriculture: An Update. International Congress Series No. 1293. The Netherlands: Elsevier; 2006. p. 156-163.

Kappler O, Janssen PH, Kreft, JU, Schink B. Effects of alternative methyl group acceptors on the growth energetics of the O-demethylating anaerobe Holophaga foetida. Microbiology 1997; 143(4): 1105-1114.

Kim BH, Gadd GM. Bacterial physiology and metabolism. 1a ed. Cambridge: Cambridge University Press; 2008.

Klevenhusen F, Zeitz JO, Duval S, Kreuzer M, Soliva CR. Garlic oil and its principal component diallyl disulfide fail to mitigate methane, but improve digestibility in sheep. Anim Feed Sci Technol 2011; 166: 356-363.

Lana RP, Russell JB, Van Amburgh ME. The role of pH in regulating ruminal methane and ammonia production. J Anim Sci 1998; 76(8): 2190-2196.

Latham MJ, Wolin MJ. Fermentation of cellulose by Ruminococcus flavefaciens in the presence and absence of Methanobacterium ruminantium. Appl Environ Microbiol 1977; 34(3): 297-301.

Laube VM, Martin SM. Conversion of Cellulose to Methane and Carbon Dioxide by Triculture of Acetivibrio cellulolyticus, Desulfovibrio sp., and Methanosarcina barkeri. Appl Environ Microbiol 1981; 42(3): 413-420.

Leahy SC, Kelly WJ, Altermann E, Ronimus RS, Yeoman CJ, et al. The genome sequence of the rumen methanogen Methanobrevibacter ruminantium reveals new possibilities for controlling ruminant methane emissions. Plos One 2010; 5(1): 1-17

Leng RA. The potential of feeding nitrate to reduce enteric methane production in ruminants. Report to Department of Climate Change, Commonwealth Government of Australia, Canberra 2008; [acceso: 18 de marzo de 2014]. URL:http://www.penambulbooks.com/Downloads/Leng-Final%20Modified%20%2017-9-2008.pdf

Liu H, Wang J, Wang A, Chen J. Chemical inhibitors of methanogenesis and putative applications. Appl Microbiol Biotechnol 2011; 89(5): 1333-1340.

López MC, Ibáñez C, García-Diego FJ, Javier Moya V, Estellés, F, et al. Determination of methane production from lactating goats fed diets with different starch levels. International Livestock Environment Symposium (ILES IX). International Conference of Agricultural Engineering-CIGR-AgEng 2012; [acceso: 20 de abril de 2014]. URL: http://mobile.cigr.ageng2012.org/images/fotosg/tabla_137_C0842.pdf

López S, Valdes C, Newbold CJ, Wallace RJ. Influence of sodium fumarate addition on rumen fermentation in vitro. Brit J Nutr 1999; 81: 59-64.

Machmüller A, Soliva CR, Kreuzer M. In vitro ruminal methane suppression by lauric acid as influenced by dietary calcium. Can J Anim Sci 2002; 82(2): 233-239.

Marais JP, Therion JJ, Mackie RI, Kistner A, Dennison C. Effect of nitrate and its reduction products on the growth and activity of the rumen microbial population. Brit J Nutr 1988; 59(2): 301-313.

Matsuyama H, Horiguchi K, Takahashi T, Kayaba T, Ishida M, et al. Control of methane production from expiratory gas by ruminal dosing with mechanical stimulating goods in Holstein steer. Asian-Aus J Anim Sci 2000; 13: 215-215.

Miller TL, Wolin MJ. Inhibition of growth of methane-producing bacteria of the ruminant forestomach by hydroxymethylflutaryl-SCoA reductase inhibitors. J Dairy Sci 2001; 84:1445–1448.

Mitsumori M, Sun W. Control of rumen microbial fermentation for mitigating methane emissions from the rumen. Asian-Aus J Anim Sci 2008; 21(1): 144-154.

Moe PW, Tyrrell HF. Methane production in dairy cows. J Dairy Sci 1979; 62(10): 1583-1586.

Moss AR, Jouany JP, Newbold J. Methane production by ruminants: its contribution to global warming. Ann Zootech 2000; 49(3): 231-254.

Müller M. Review Article: The hydrogenosome. J Gen Microbiol 1993; 139(12): 2879-2889.

Müller V, Lemker T, Lingl A, Weidner C, Coskun Ü, et al. Bioenergetics of archaea: ATP synthesis under harsh environmental conditions. J Mol Microbiol Biotechnol 2006, 10(2-4): 167-180.

Murphy MR, Baldwin RL, Koong LJ. Estimation of stoichiometric parameters for rumen fermentation of roughage and concentrate diets. J Anim Sci 1982; 55(2): 411-421.

Murray K, Rodwell V, Bender D, Botham KM, Weil PA, et al. Harper's Illustrated Biochemistry. 29th ed. New York: McGraw-Hill; 2011.

Nagaraja TG, Newbold CJ, Van Nevel CJ, Demeyer DI. Manipulation of ruminal fermentation. In: Hobson PN, Stewart CS (eds). The Rumen Microbial Ecosystem. 2nd ed. London: Blackie Acad and Prof; 1997. p. 523–632.

Navarro-Villa A, O’Brien M, López S, Boland TM, O’Kiely P. In vitro rumen methane output of grasses and grass silages differing in fermentation characteristics using the gas-production technique (GPT). Grass Forage Sci 2012; 68: 228–244.

Newbold CJ, Lassalas B, Jouany JP. The importance of methanogens associated with ciliate protozoa in ruminal methane production in vitro. Lett Appl Microbiol 1995; 21(4): 230-234.

Nováková Z, Blaško J, Hapala I, Šmigáň P. Effects of 3-hydroxy-3-methylglutaryl-coenzyme a reductase inhibitor pravastatin on membrane lipids and membrane associated functions of Methanothermobacter thermautotrophicus. Folia Microbiol 2010, 55(4): 359-362.

Patra AK, Saxena J. Exploitation of dietary tannins to improve rumen metabolism and ruminant nutrition. J Sci Food Agric 2011; 91(1): 24-37.

Paynter MJB, Hungate RE. Characterization of Methanobacterium mobilis, sp. n., isolated from the bovine rumen. J Bacteriol 1968; 95(5): 1943-1951.

Polan CE, McNeill JJ, Tove SB. Biohydrogenation of unsaturated fatty acids by rumen bacteria. J Bacteriol 1964; 88(4): 1056-1064.

Ragsdale SW, Pierce E. Acetogenesis and the Wood–Ljungdahl pathway of CO2 fixation. Biochim Biophys Acta 2008; 1784(12): 1873-1898.

Russell JB, Jeraci JL. Effect of carbon monoxide on fermentation of fiber, starch, and amino acids by mixed rumen microorganisms in vitro. Appl Environ Microbiol 1984; 48(1): 211-217.

Sauer FD, Teather RM. Changes in oxidation reduction potentials and volatile fatty acid production by rumen bacteria when methane synthesis is inhibited. J Dairy Sci 1987; 70(9):1835-1840.

Schäfer G, Engelhard M, Müller V. Bioenergetics of the Archaea. Microbiol Mol Biol Rev 1999; 63(3): 570-620.

Schink B. Syntrophic associations in methanogenic degradation. In: Overmann J (ed.). Molecular Basis of Symbiosis. Berlin: Springer; 2006. p.: 1-19

Schink B, Stams AJM. Syntrophism among prokaryotes. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds). The Prokaryotes: an evolving electronic resource for the microbiological community. 3rd ed. New York: Springer-Verlag; 2006. p. 309-335.

Sharp R, Ziemer CJ, Stern MD, Stahl DA. Taxon‐specific associations between protozoal and methanogen populations in the rumen and a model rumen system. FEMS Microbiol Ecol 1998; 26(1): 71-78.

Shibata M, Terada F. Factors affecting methane production and mitigation in ruminants. Anim Sci J 2010, 81(1): 2-10.

Skillman LC, Evans PN, Naylor GE, Morvan B, Jarvis GN, et al. 16S ribosomal DNA-directed PCR primers for ruminal methanogens and identification of methanogens colonising young lambs. Anaerobe 2004; 10(5): 277-285.

Soliva CR, Hindrichsen IK, Meile L, Kreuzer M, Machmüller A. Effects of mixtures of lauric and myristic acid on rumen methanogens and methanogenesis in vitro. Lett Appl Microbiol 2003; 37(1): 35-39.

Takahashi J, Johchi N, Fujita H. Inhibitory effects of sulphur compounds, copper and tungsten on nitrate reduction by mixed rumen micro-organisms. Brit J Nutr 1989; 61(03): 741-748.

Thauer RK, Kaster AK, Seedorf H, Buckel W, Hedderich R. Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol 2008; 6(8): 579-591.

Ungerfeld EM, Kohn RA. The role of thermodynamics in the control of ruminal fermentation. In: Sejrsen K, Hvelplund T, Nielsen MO (eds). Ruminant physiology: Digestion, metabolism and impact of nutrition on gene expression, immunology and stress. The Netherlands: Wageningen Academic Publishers; 2006. p. 55-85.

Ungerfeld EM, Kohn RA, Wallace RJ, Newbold CJ. A meta-analysis of fumarate effects on methane production in ruminal batch cultures. J Anim Sci 2007; 85(10): 2556-2563.

Ungerfeld EM, Rust SR, Boone DR, Liu Y. Effects of several inhibitors on pure cultures of ruminal methanogens. J Appl Microbiol 2004; 97(3): 520-526.

Ungerfeld EM, Rust SR, Burnett RJ, Yokoyama MT, Wang JK. Effects of two lipids on in vitro ruminal methane production. Anim Feed Sci Technol 2005; 119(1): 179-185.

Ushida K, Ohashi Y, Tokura M, Miyazaki K, Kojima Y. Sulphate reduction and methanogenesis in the ovine rumen and porcine caecum: a comparison of two microbial ecosystems. Dtsch Tieraerztl Wochenschr 1995; 102(4): 154-156.

Van Kessel JAS, Russell JB. The effect of pH on ruminal methanogenesis. FEMS Microbiol Ecol 1996; 20(4): 205-210.

Vogels GD, Hoppe WF, Stumm CK. Association of methanogenic bacteria with rumen ciliates. Appl Environ Microbiol 1980; 40(3): 608-612.

Whitford MF, Teather RM, Forster RJ. Phylogenetic analysis of methanogens from the bovine rumen. BMC Microbiology 2001; 1: 1-5.

Williams AG, Coleman GS. The rumen protozoa. In: Hobson PN, Stewart CS (eds). The Rumen Microbial Ecosystem. 2nd ed. New York: Springer; 1997. p. 77–139.

Wolin MJ, Miller TL. Control of rumen methanogenesis by inhibiting the growth and activity of methanogens with hydroxymethylglutaryl-SCoA inhibitors. Int Congr Ser 2006; 1293: 131-137.

Zhou MI, Hernandez-Sanabria E. Assessment of the microbial ecology of ruminal methanogens in cattle with different feed efficiencies. Appl Environ Microbiol 2009; 75(20): 6524-6533.

Zhou M, Hernandez-Sanabria E. Characterization of variation in rumen methanogenic communities under different dietary and host feed efficiency conditions, as determined by PCR-denaturing gradient gel electrophoresis analysis. Appl Environ Microbiol 2010; 76(12): 3776-3786.




Licencia de Creative Commons

Este obra está bajo una licencia de Creative Commons Reconocimiento-NoComercial-SinObraDerivada 4.0 Internacional.