Redirecting rumen fermentation to reduce methanogenesis
T. A. McAllister A C and C. J. Newbold BA Agriculture and Agri-Food Canada Research Centre, PO Box 3000, Lethbridge, Alberta, T1J 4B1, Canada.
B University of Wales, Llanbadarn Campus, Aberystwyth, SY23 3AL, Wales.
C Corresponding author. Email: mcallistert@agr.gc.ca
Australian Journal of Experimental Agriculture 48(2) 7-13 https://doi.org/10.1071/EA07218
Submitted: 26 July 2007 Accepted: 25 August 2007 Published: 2 January 2008
Abstract
Methane production in ruminants has received global attention in relation to its contribution to the greenhouse gas effect and global warming. In the last two decades, research programs in Europe, Oceania and North America have explored a variety of approaches to redirecting reducing equivalents towards other reductive substrates as a means of decreasing methane production in ruminants. Some approaches such as vaccination, biocontrols (bacteriophage, bacteriocins) and chemical inhibitors directly target methanogens. Other approaches, such as defaunation, diet manipulations including various plant extracts or organic acids, and promotion of acetogenic populations, seek to lower the supply of metabolic hydrogen to methanogens. The microbial ecology of the rumen ecosystem is exceedingly complex and the ability of this system to efficiently convert complex carbohydrates to fermentable sugars is in part due to the effective disposal of H2 through reduction of CO2 to methane by methanogens. Although methane production can be inhibited for short periods, the ecology of the system is such that it frequently reverts back to initial levels of methane production though a variety of adaptive mechanisms. Hydrogen flow in the rumen can be modelled stoichiometrically, but accounting for H2 by direct measurement of reduced substrates often does not concur with the predictions of stoichiometric models. Clearly, substantial gaps remain in our knowledge of the intricacies of hydrogen flow within the ruminal ecosystem. Further characterisation of the fundamental microbial biochemistry of hydrogen generation and methane production in the rumen may provide insight for development of effective strategies for reducing methane emissions from ruminants.
Ambrozic J,
Ferme D,
Grabnar M,
Ravnikar M, Avgustin G
(2001) The bacteriophages of ruminal prevotellas. Folia Microbiologica 46, 37–39.
|
CAS |
PubMed |
Bach SJ,
McAllister TA,
Veira DM,
Gannon VPJ, Holley RA
(2003) Effect of bacteriophage DC22 on Escherichia coli O157:H7 in an artificial rumen system (Rusitec) and inoculated sheep. Animal Research 52, 89–101.
| Crossref | GoogleScholarGoogle Scholar |
Beauchemin KA, McGinn SM
(2006) Methane emissions from beef cattle: effects of fumaric acid, essential oil and canola oil. Journal of Animal Science 84, 1489–1496.
|
CAS |
PubMed |
Busquet M,
Calsamiglia S,
Ferret A,
Carro MD, Kamel C
(2005) Effect of garlic oil and four of its compounds on rumen microbial fermentation. Journal of Dairy Science 8, 4393–4404.
Calsamiglia S,
Busquet M,
Cardozo PW,
Castillejos L, Ferret A
(2007) Invited review: essential oils as modifiers of rumen microbial fermentation. Journal of Dairy Science 90, 2580–2595.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Choi NJ,
Lee SY,
Sung HC,
Lee SC, Ha JK
(2004) Effects of halogenated compounds, organic acids and unsaturated fatty acids on in vitro methane production and fermentation characteristics. Asian-Australasian Journal of Animal Sciences 17, 1255–1259.
|
CAS |
Coleman GS
(1986) The distribution of carboxymethylcellulase between fractions taken from the rumen of sheep containing no protozoa or one of five different protozoal populations. The Journal of Agricultural Science 106, 121–127.
|
CAS |
Cook SR,
Maiti PK,
Chaves AV,
Benchaar C,
Beauchemin KA, McAllister TA
(2008) Avian (IgY) anti-methanogen antibodies for reducing ruminal methane production: in vitro assessment of their effects. Australian Journal of Experimental Agriculture 48, 260–264.
|
CAS |
Cookson SL,
Noel SJ,
Kelly WJ, Attwood GT
(2004) The use of PCR for the identification and characterisation of bacteriocin genes from bacterial strains isolated from the rumen or caecal contents of cattle and sheep. FEMS Microbiology Ecology 48, 199–207.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
De Graeve KG,
Grivet JP,
Durand M,
Beaumatein P,
Cordelet C,
Hannequart G, Demeyer D
(1994) Competition between reductive acetogenesis and methanogenesis in the pig large-intestinal flora. The Journal of Applied Bacteriology 76, 55–61.
|
CAS |
PubMed |
Dong Y,
Bae HD,
McAllister TA,
Mathison GW, Cheng KJ
(1999) Effects of exogenous fibrolytic enzymes, 2-bromoethanesulfonate and monensin on fermentation in a rumen simulation (RUSITEC) system. Canadian Journal of Animal Science 79, 491–498.
|
CAS |
Doré J,
Morvan B,
Rieu-Lesme F,
Goderel I,
Gouet P, Pochart P
(1995) Most probable number enumeration of H2-utilizing acetogenic bacteria from the digestive tract of animals and man. FEMS Microbiology Letters 130, 7–12.
| PubMed |
European Union
(2003) Regulation EC No 1831/2003 of the European Parliament and Council of 22 September 2003 on additives for use in animal nutrition. Official Journal of the European Union L268, 29–43.
Finlay BJ,
Esteban G,
Clarke KJ,
Williams AG,
Embley TM, Hirt RR
(1994) Some rumen ciliates have endosymbiotic methanogens. FEMS Microbiology Letters 117, 157–162.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
García-González R,
López S,
Fernández M, González JS
(2006) Effects of the addition of some medicinal plants on methane production in a rumen simulating fermenter (RUSITEC). International Congress Series 1293, 172–175.
| Crossref | GoogleScholarGoogle 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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hegarty RS
(2004) Genotype differences and their impact on digestive tract function of ruminants: a review. Australian Journal of Experimental Agriculture 44, 459–467.
| Crossref | GoogleScholarGoogle Scholar |
Hu WL,
Liu JX,
Ye JA,
Wu YM, Guo YQ
(2005) Effect of tea saponin on rumen fermentation in vitro. Animal Feed Science and Technology 120, 333–339.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Joblin KN
(1999) Ruminal acetogens and their potential to lower ruminant methane emissions. Australian Journal of Agricultural Research 50, 1307–1313.
| Crossref | GoogleScholarGoogle Scholar |
Johnson KA, Johnson DE
(1995) Methane emissions from cattle. Journal of Animal Science 73, 2483–2492.
|
CAS |
PubMed |
Kalmokoff ML,
Bartlett F, Teather RM
(1996) Are ruminal bacteria armed with bacteriocins? Journal of Dairy Science 79, 2297–2306.
|
CAS |
PubMed |
Klieve AV, Hegarty RS
(1999) Opportunities for biological control of ruminal methanogenesis. Australian Journal of Agricultural Research 50, 1315–1319.
| Crossref | GoogleScholarGoogle Scholar |
Klieve AV,
Heck GL,
Prance MA, Shu Q
(1999) Genetic homogeneity and phage susceptibility of ruminal strains of Streptococcus bovis isolated in Australia. Letters in Applied Microbiology 29, 108–112.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Kolver ES,
Aspin PW,
Jarvis GN,
Elborough KM, Roche JR
(2004) Fumarate reduces methane production from pasture fermented in continuous culture. Proceedings of the New Zealand Society of Animal Production 64, 155–159.
Lee SS,
Hsu JT,
Mantovani HC, Russell JB
(2002) The effect of bovicin HC5, a bacteriocin from Streptococcus bovis HC5, on ruminal methane production in vitro. FEMS Microbiology Letters 217, 51–55.
|
CAS |
PubMed |
LeVan 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.
|
CAS |
PubMed |
Lopez SM,
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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
McAllister TA,
Okine EK,
Mathison GW, Cheng K-J
(1996) Dietary, environmental and microbiological aspects of methane production in ruminants. Canadian Journal of Animal Science 76, 231–243.
|
CAS |
McGinn SM,
Beauchemin KA,
Coates T, Colombatto D
(2004) Methane emissions from beef cattle: effects of monensin, sunflower oil, enzymes, yeast and fumaric acid. Journal of Animal Science 82, 3346–3356.
|
CAS |
PubMed |
Morvan B,
Doré 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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Newbold CJ,
Lassalas B, Jouany JP
(1995) The importance of methanogenesis associated with ciliate protozoa in ruminal methane production in vitro. Letters in Applied Microbiology 21, 230–234.
|
CAS |
PubMed |
Newbold CJ,
El Hassan SM,
Wang J,
Ortega ME, Wallace RJ
(1997) Influence of foliage from African multipurpose trees on activity of rumen protozoa and bacteria. The British Journal of Nutrition 78, 237–249.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Newbold CJ,
López S,
Nelson N,
Ouda JO,
Wallace RJ, Moss AR
(2005) Propionate precursors and other metabolic intermediates as possible alternative electron acceptors to methanogenesis in ruminal fermentation in vitro. The British Journal of Nutrition 94, 27–35.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Park MO,
Ikenaga H, Watanabe K
(2007) Phage diversity in a methanogenic digester. Microbial Ecology 53, 98–103.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Pinares-Patiño CS,
Baumont R, Matin C
(2003) Methane emissions by Charolais cows grazing a monospecific pasture of timothy at four stages of maturity. Canadian Journal of Animal Science 83, 769–777.
Ranilla MJ,
Morgavi DP, Jouany JP
(2003) Effect of time after defaunation on methane production in vitro. Reproduction, Nutrition, Development Suppl 1 44, 60.
Robert C,
Del’Homme C, Bernalier-Donadille A
(2001) Interspecies H2 transfer in ceullulose degradation between fibrolytic bacteria and H2 utilizing microorgansims from the human colon. FEMS Microbiology Letters 205, 209–214.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Sar C,
Santoso B,
Mwenya B,
Gamo Y,
Kobayashi T,
Morikawa R,
Kimura K,
Mizukoshi H, Takahashi J
(2004) Manipulation of rumen methanogenesis by the combination of nitrate and β-1-4 galacto-oligosaccharides of nisin in sheep. Animal Feed Science and Technology 115, 129–142.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Sar C,
Mwenya B,
Pen B,
Morikawa R,
Takaura K,
Kobayashi T, Takahashi J
(2005a) Effect of nisin on ruminal methane production and nitrate/nitrite reduction in vitro. Australian Journal of Agricultural Research 56, 803–810.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
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.
|
CAS |
PubMed |
Sheng HQ,
Knecht HJ,
Kudva IT, Hovde CJ
(2006) Application of bacteriophage to control intestinal Escherichia coli O157:H7 levels in ruminants. Applied and Environmental Microbiology 72, 5359–5366.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ungerfeld EM,
Rust SR,
Boone DR, Liu Y
(2004) Effects of several inhibitors on pure cultures of ruminal methanogens. Journal of Applied Microbiology 97, 520–526.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Vogels GD,
Hoppe WF, Stumm CK
(1980) Association of methanogenic bacteria with rumen ciliates. Applied and Environmental Microbiology 40, 608–612.
|
CAS |
PubMed |
Waghorn GC,
Tavendale MH, Woodfield DR
(2002) Methanogenesis from forages fed to sheep. Proceedings of the New Zealand Grasslands Association 64, 167–171.
Wallace RJ,
Wood TA,
Rowe A,
Price J,
Yanez DR,
Williams SP, Newbold CJ
(2006) Encapsulated fumaric acid as a means of decreasing ruminal methane emissions. International Congress Series 1293, 148–151.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Williams YJ,
Rea SM,
Popovski S,
Pimm CL,
Williams AJ,
Toovey AF,
Skillman LC, Wright AD
(2007) Responses of sheep to a vaccination of entodinal or mixed rumen protozoal antigens to reduce rumen protozoal numbers. The British Journal of Nutrition n press ,
| PubMed |
Wright ADG,
Kennedy P,
O’Neill CJ,
Toovey AF,
Popovski S,
Rea SM,
Pimm CL, Klein L
(2004) Reducing methane emission in sheep by immunization against rumen methanogens. Vaccine 22, 3976–3985.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Wright ADG,
Toovey AF, Pimm CL
(2006) Molecular identification of methanogenic archaea from sheep in Queensland, Australia reveal more uncultured novel archaea. Anaerobe 12, 134–139.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Wright ADG,
Auckland CH, Lynn DH
(2007) Molecular diversity of methanogens in feedlot cattle from Ontario and Prince Edward Island, Canada. Applied and Environmental Microbiology 73, 4206–4210.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
