Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Enzyme- and gene-based approaches for developing methanogen-specific compounds to control ruminant methane emissions: a review

Gemma Henderson A , Gregory M. Cook B C and Ron S. Ronimus A C
+ Author Affiliations
- Author Affiliations

A Rumen Microbiology, AgResearch Ltd, Grasslands Research Centre, Palmerston North 4442, New Zealand.

B Department of Microbiology and Immunology, University of Otago, Dunedin 9054, New Zealand.

C Corresponding author. Email: gregory.cook@otago.ac.nz; ron.ronimus@agresearch.co.nz

Animal Production Science - https://doi.org/10.1071/AN15757
Submitted: 29 October 2015  Accepted: 7 January 2016   Published online: 5 April 2016

Abstract

Methane emissions from ruminants are of worldwide concern due to their potential to adversely affect climate patterns. Methane emissions can be mitigated in several ways, including dietary manipulation, the use of alternative hydrogen sinks, and by the direct inhibition of methanogens. In the present review, we summarise and emphasise studies where defined chemically synthesised compounds have been used to mitigate ruminant methane emissions by direct targeting of methanogens and discuss the future potential of such inhibitors. We also discuss experiments, where methanogen-specific enzymes and pure cultures of methanobacterial species have been used to aid development of inhibitors. Application of certain compounds can result in dramatic reductions of methane emissions from ruminant livestock, demonstrating ‘proof of principle’ of chemical inhibitors of methanogenesis. More recently, genome sequencing of rumen methanogens has enabled an in-depth analysis of the enzymatic pathways required for methane formation. Chemogenomic methods, similar to those used in the fight against cancer and infectious diseases, can now be used to specifically target a pathway or enzyme in rumen methanogens. However, few rumen methanogen enzymes have been structurally or biochemically characterised. Any compound, whether natural or man-made, that is used as a mitigation strategy will need to be non-toxic to the host animal (and humans), cost-effective, environmentally friendly, and not accumulate in host tissues or milk products. Chemically synthesised inhibitors offer potentially significant advantages, including high levels of sustained inhibition, the ability to be easily and rapidly produced for global markets, and have the potential to be incorporated into slow-release vehicles for grazing animals.

Additional keywords: chemical, greenhouse gas, high-throughput screening, inhibition, methanogenesis.


References

Abecia L, Toral PG, Martín-García AI, Martinez G, Tomkins NW, Molina-Alcaide E, Newbold CJ, Yáñez-Ruiz DR (2012) Effect of bromochloromethane on methane emission, rumen fermentation pattern, milk yield, and fatty acid profile in lactating dairy goats. Journal of Dairy Science 95, 2027–2036.
Effect of bromochloromethane on methane emission, rumen fermentation pattern, milk yield, and fatty acid profile in lactating dairy goats.CrossRef | 1:CAS:528:DC%2BC38Xksleitrw%3D&md5=766d1043207ecfa67a2187113a1ecd62CAS | 22459848PubMed |

Abecia L, Martín-García AI, Martinez G, Newbold CJ, Yáñez-Ruiz DR (2013) Nutritional intervention in early life to manipulate rumen microbial colonization and methane output by kid goats postweaning. Journal of Animal Science 91, 4832–4840.
Nutritional intervention in early life to manipulate rumen microbial colonization and methane output by kid goats postweaning.CrossRef | 1:CAS:528:DC%2BC3sXhs1SqtLvE&md5=3b46dfa5417608a17588ef119f7517f4CAS | 23965388PubMed |

Abecia L, Waddams KE, Martínez-Fernández G, Martín-García AI, Ramos-Morales E, Newbold CJ, Yáñez-Ruiz DR (2014) An antimethanogenic nutritional intervention in early life of ruminants modifies ruminal colonization by Archaea. Archaea (Vancouver, B.C.) 2014, 841463
An antimethanogenic nutritional intervention in early life of ruminants modifies ruminal colonization by Archaea.CrossRef |

Aung HL, Dey D, Janssen PH, Ronimus RS, Cook GM (2015) A high-throughput screening assay for identification of inhibitors of the A1A0–ATP synthase of the rumen methanogen Methanobrevibacter ruminantium M1. Journal of Microbiological Methods 110, 15–17.
A high-throughput screening assay for identification of inhibitors of the A1A0–ATP synthase of the rumen methanogen Methanobrevibacter ruminantium M1.CrossRef | 1:CAS:528:DC%2BC2MXhtVKqur4%3D&md5=8003d38eeede7256cb9716171670e5b8CAS | 25575416PubMed |

Baker SK (1999) Rumen methanogens, and inhibition of methanogenesis. Australian Journal of Agricultural Research 50, 1293–1298.
Rumen methanogens, and inhibition of methanogenesis.CrossRef | 1:CAS:528:DyaK1MXotVOlu7k%3D&md5=9da9530f94cbd8c6051a88437783dcdcCAS |

Balch WE, Wolfe RS (1979) Transport of coenzyme M (2-mercaptoethanesulfonic acid) in Methanobacterium ruminantium. Journal of Bacteriology 137, 264–273.

Bang C, Schilhabel A, Weidenbach K, Kopp A, Goldmann T, Gutsmann T, Schmitz RA (2012) Effects of antimicrobial peptides on methanogenic archaea. Antimicrobial Agents and Chemotherapy 56, 4123–4130.
Effects of antimicrobial peptides on methanogenic archaea.CrossRef | 1:CAS:528:DC%2BC38XhtFajs7%2FE&md5=b039ffd707a5637192d1cd068f104763CAS | 22585226PubMed |

Bauchop T (1967) Inhibition of rumen methanogenesis by methane analogues. Journal of Bacteriology 94, 171–175.

Behlke EJ (2007) Attenuation of ruminal methanogenesis. MSc Thesis, University of Nebraska, Lincoln, NE, USA.

Bell MJ, Wall E, Russell G, Morgan C, Simm G (2010) Effect of breeding for milk yield, diet and management on enteric methane emissions from dairy cows. Animal Production Science 50, 817–826.
Effect of breeding for milk yield, diet and management on enteric methane emissions from dairy cows.CrossRef |

Böck A, Kandler O (1985) Antibiotic sensitivity of archaebacteria. In ‘The bacteria: a treatise on structure and function. Vol. VIII: Archaebacteria’. (Eds CR Woese, RS Wolfe) pp. 525–544. (Academic Press: Orlando, San Diego, New Tork, London, Toronto, Montreal, Sydney, Tokyo)

Buddle BM, Denis M, Attwood GT, Altermann E, Janssen PH, Ronimus RS, Pinares-Patiño CS, Muetzel S, Wedlock ND (2011) Strategies to reduce methane emissions from farmed ruminants grazing on pasture. Veterinary Journal (London, England) 188, 11–17.
Strategies to reduce methane emissions from farmed ruminants grazing on pasture.CrossRef | 1:CAS:528:DC%2BC3MXjs1Sgt7k%3D&md5=442f7d210a5d792ca27315cd1168f6c3CAS |

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 88, 4393–4404.
Effect of garlic oil and four of its compounds on rumen microbial fermentation.CrossRef | 1:CAS:528:DC%2BD2MXhtlSqtr3O&md5=7188f6f80c47f0e2a5c25fd19b84ab0cCAS | 16291631PubMed |

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.
Invited review: essential oils as modifiers of rumen microbial fermentation.CrossRef | 1:CAS:528:DC%2BD2sXlvFOisLg%3D&md5=8e9c9eeca371a64480bed9aece6c101dCAS | 17517698PubMed |

Carbone V, Schofield LR, Beattie AK, Sutherland-Smith AJ, Ronimus RS (2013) The crystal structure of methenyltetrahydromethanopterin cyclohydrolase from Methanobrevibacter ruminantium. Proteins 81, 2064–2070.
The crystal structure of methenyltetrahydromethanopterin cyclohydrolase from Methanobrevibacter ruminantium.CrossRef | 1:CAS:528:DC%2BC3sXhtlWjt7%2FL&md5=1b071976bedd52843f2864e64197b3efCAS | 23873651PubMed |

Cedervall PE, Dey M, Pearson AR, Ragsdale SW, Wilmot CM (2010) Structural insight into methyl-coenzyme M reductase chemistry using coenzyme B analogues. Biochemistry 49, 7683–7693.
Structural insight into methyl-coenzyme M reductase chemistry using coenzyme B analogues.CrossRef | 1:CAS:528:DC%2BC3cXhtVSmsLrK&md5=f6e6d4633e950804730af3f45cb59155CAS | 20707311PubMed |

Chalupa W (1980) Chemical control of rumen microbial metabolism. Digestive physiology and metabolism in ruminants. In ‘Proceedings of the 5th international symposium on ruminant physiology’. pp. 325–347. (MTP Press International Medical Publishers: Lancaster, UK)

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.

Conrad R, Klose M (2000) Selective inhibition of reactions involved in methanogenesis and fatty acid production on rice roots. FEMS Microbiology Ecology 34, 27–34.
Selective inhibition of reactions involved in methanogenesis and fatty acid production on rice roots.CrossRef | 1:CAS:528:DC%2BD3cXosVyrt7c%3D&md5=aa1878ce82fda844ce4d76e6c170e016CAS | 11053733PubMed |

Cottle DJ, Nolan JV, Wiedemann SG (2011) Ruminant enteric methane mitigation: a review. Animal Production Science 51, 491–514.
Ruminant enteric methane mitigation: a review.CrossRef | 1:CAS:528:DC%2BC3MXntVGisLY%3D&md5=ca8409519db155f19af58311f9f4e1d4CAS |

Davies A, Nwaonu HN, Stanier G, Boyle FT (1982) Properties of a novel series of inhibitors of rumen methanogenesis; in vitro and in vivo experiments including growth trials on 2,4-bis(trichloromethyl)-benzo [1,3]dioxin-6-carboxylic acid. British Journal of Nutrition 47, 565–576.
Properties of a novel series of inhibitors of rumen methanogenesis; in vitro and in vivo experiments including growth trials on 2,4-bis(trichloromethyl)-benzo [1,3]dioxin-6-carboxylic acid.CrossRef | 1:CAS:528:DyaL38XksFCmtLc%3D&md5=fc445cf20eaefd518b32ac04d74a809dCAS | 7082625PubMed |

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.
Quantitation and diversity analysis of ruminal methanogenic populations in response to the antimethanogenic compound bromochloromethane.CrossRef | 1:CAS:528:DC%2BD2sXhsValtr7E&md5=3b4d5b31de81b675f96bb2da5d913747CAS | 17949432PubMed |

Duffield TF, Rabiee A, Lean IJ (2012) Overview of meta-analysis of monensin in dairy cattle. The Veterinary Clinics of North America. Food Animal Practice 28, 107–119.
Overview of meta-analysis of monensin in dairy cattle.CrossRef | 22374121PubMed |

Dumitru R, Palencia H, Schroeder SD, DeMontigny BA, Takacs JM, Rasche ME, Miner JL, Ragsdale SW (2003) Targeting methanopterin biosynthesis to inhibit methanogenesis. Applied and Environmental Microbiology 69, 7236–7241.
Targeting methanopterin biosynthesis to inhibit methanogenesis.CrossRef | 1:CAS:528:DC%2BD3sXpvFCls78%3D&md5=50686863d3a63ef6b90f6c73868ca041CAS | 14660371PubMed |

Duval S, Kindermann M (2012) ‘Use of nitrooxy organic molecules in feed for reducing enteric methane emissions in ruminants, and/or to improve ruminant performance.’ International Patent Application WO 2012/084629 A1. (World Intellectual Property Organization: Geneva, Switzerland)

Eckard RJ, Grainger C, de Klein CAM (2010) Options for the abatement of methane and nitrous oxide from ruminant production: a review. Livestock Science 130, 47–56.
Options for the abatement of methane and nitrous oxide from ruminant production: a review.CrossRef |

Eijssen AFMM, Barry TN, Brookes IM (1990) The effect of pyromelittic diimide upon the rumen fermentation of sheep fed a forage diet. Animal Feed Science and Technology 28, 145–153.
The effect of pyromelittic diimide upon the rumen fermentation of sheep fed a forage diet.CrossRef | 1:CAS:528:DyaK3cXltlWjtbc%3D&md5=ed7977c70f5d59b6c14f2812fa7f2a16CAS |

Ermler U, Grabarse W, Shima S, Goubeaud M, Thauer RK (1997) Crystal structure of methyl-coenzyme M reductase: the key enzyme of biological methane formation. Science 278, 1457–1462.
Crystal structure of methyl-coenzyme M reductase: the key enzyme of biological methane formation.CrossRef | 1:CAS:528:DyaK2sXnsVGlu7g%3D&md5=fc37a3b3e60c19878e6569dc1e411110CAS | 9367957PubMed |

Garcia-Lopez PM, Kung L, Odom JM (1996) In vitro inhibition of microbial methane production by 9,10-anthraquinone. Journal of Animal Science 74, 2276–2284.

Goel G, Makkar HP (2012) Methane mitigation from ruminants using tannins and saponins. Tropical Animal Health and Production 44, 729–739.
Methane mitigation from ruminants using tannins and saponins.CrossRef | 21894531PubMed |

Goopy JP, Donaldson A, Hegarty R, Vercoe PE, Haynes F, Barnett M, Oddy VH (2014) Low-methane yield sheep have smaller rumens and shorter rumen retention time. British Journal of Nutrition 111, 578–585.
Low-methane yield sheep have smaller rumens and shorter rumen retention time.CrossRef | 1:CAS:528:DC%2BC2cXisVCgtL8%3D&md5=cac2f7f0ba77edadd550219925926c12CAS | 24103253PubMed |

Graham DE, White RH (2002) Elucidation of methanogenic coenzyme biosynthesis: from spectroscopy to genomics. Natural Product Reports 19, 133–147.
Elucidation of methanogenic coenzyme biosynthesis: from spectroscopy to genomics.CrossRef | 1:CAS:528:DC%2BD38XktFShsrk%3D&md5=6e0ab9ee663eb00556260b734add6d1bCAS | 12013276PubMed |

Gräwert T, Hohmann HP, Kindermann M, Duval S, Bacher A, Fischer M (2014) Inhibition of methyl-CoM reductase from Methanobrevibacter ruminantium by 2-bromoethanesulfonate. Journal of Agricultural and Food Chemistry 62, 12487–12490.
Inhibition of methyl-CoM reductase from Methanobrevibacter ruminantium by 2-bromoethanesulfonate.CrossRef | 25483006PubMed |

Haisan J, Sun Y, Beauchemin KA, Guan LL, Duval S, Barreda DR, Oba M (2014) The effects of feeding 3-nitrooxypropanol on methane emissions and productivity of Holstein cows in mid lactation. Journal of Dairy Science 97, 3110–3119.
The effects of feeding 3-nitrooxypropanol on methane emissions and productivity of Holstein cows in mid lactation.CrossRef | 1:CAS:528:DC%2BC2cXktlWlsLk%3D&md5=41d346be1ff7e47558ed894005e5ff36CAS | 24630651PubMed |

Hammes WP, Winter J, Kandler O (1979) The sensitivity of the pseudomurein-containing genus Methanobacterium to inhibitors of murein synthesis. Archives of Microbiology 123, 275–279.
The sensitivity of the pseudomurein-containing genus Methanobacterium to inhibitors of murein synthesis.CrossRef | 1:CAS:528:DyaL3cXovVGjsA%3D%3D&md5=b9bbc72fc2ee9d7196114008deffef5fCAS |

Hegarty RS (1999) Reducing rumen methane emissions through elimination of rumen protozoa. Australian Journal of Agricultural Research 50, 1321–1327.
Reducing rumen methane emissions through elimination of rumen protozoa.CrossRef |

Hilpert R, Winter J, Hammnes W, Kandler O (1981) The sensitivity of archaebacteria to antibiotics. Zentralblatt für Bakteriologie Mikrobiologie und Hygiene: I. Abt. Originale C: Allgemeine, angewandte und ökologische Mikrobiologie 2, 11–20.

Hook SE, Wright AD, McBride BW (2010) Methanogens: methane producers of the rumen and mitigation strategies. Archaea (Vancouver, B.C.)
Methanogens: methane producers of the rumen and mitigation strategies.CrossRef |

Hristov AN, Oh J, Firkins JL, Dijkstra J, Kebreab E, Waghorn G, Makkar HP, Adesogan AT, Yang W, Lee C, Gerber PJ, Henderson B, Tricarico JM (2013) Special topics: mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options. Journal of Animal Science 91, 5045–5069.
Special topics: mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options.CrossRef | 1:CAS:528:DC%2BC3sXhslKktrrL&md5=0cfa1e01345e20be5c9e6a663f7d8040CAS | 24045497PubMed |

Hristov AN, Oh J, Giallongo F, Frederick TW, Harper MT, Weeks HL, Branco AF, Moate PJ, Deighton MH, Williams SR, Kindermann M, Duval S (2015) An inhibitor persistently decreased enteric methane emission from dairy cows with no negative effect on milk production. Proceedings of the National Academy of Sciences of the United States of America 112, 10663–10668.
An inhibitor persistently decreased enteric methane emission from dairy cows with no negative effect on milk production.CrossRef | 1:CAS:528:DC%2BC2MXht1GrsL3P&md5=1c3d9175995aea8695a264f3f1772926CAS | 26229078PubMed |

Hubbard R, Murray JB (2011) Experiences in fragment-based lead discovery. Methods in Enzymology 493, 509–531.
Experiences in fragment-based lead discovery.CrossRef | 1:CAS:528:DC%2BC3MXoslers70%3D&md5=1d723a20b333d1016b6e999dec3c4b3bCAS | 21371604PubMed |

Immig I, Demeyer D, Fiedler D, Van Nevel C, Mbanzamihigo L (1996) Attempts to induce reductive acetogenesis into a sheep rumen. Archiv fur Tierernahrung 49, 363–370.
Attempts to induce reductive acetogenesis into a sheep rumen.CrossRef | 1:CAS:528:DyaK2sXntF2jsg%3D%3D&md5=ee825d55e3ab4d442beb2c8522c24029CAS | 8988318PubMed |

Janssen PH (2010) Influence of hydrogen on rumen methane formation and fermentation balances through microbial growth kinetics and fermentation thermodynamics. Animal Feed Science and Technology 160, 1–22.
Influence of hydrogen on rumen methane formation and fermentation balances through microbial growth kinetics and fermentation thermodynamics.CrossRef | 1:CAS:528:DC%2BC3cXhtV2itLvF&md5=8b633b0832b1c0985b793ee6af3ece67CAS |

Janssen PH, Kirs M (2008) Structure of the archaeal community of the rumen. Applied and Environmental Microbiology 74, 3619–3625.
Structure of the archaeal community of the rumen.CrossRef | 1:CAS:528:DC%2BD1cXnvFWlsrk%3D&md5=35649b167d6ae2e2ef007770213fb840CAS | 18424540PubMed |

Jarrell KF, Sprott GD (1982) Nickel transport in Methanobacterium bryantii. Journal of Bacteriology 151, 1195–1203.

Jarrell KF, Sprott GD (1983) The effects of ionophores and metabolic inhibitors on methanogenesis and energy-related properties of Methanobacterium bryantii. Archives of Biochemistry and Biophysics 225, 33–41.
The effects of ionophores and metabolic inhibitors on methanogenesis and energy-related properties of Methanobacterium bryantii.CrossRef | 1:CAS:528:DyaL3sXltF2jsLg%3D&md5=42b8ab41693ca5b00d4e0737310912f3CAS | 6311108PubMed |

Jeyanathan J, Martin C, Morgavi DP (2014) The use of direct-fed microbials for mitigation of ruminant methane emissions: a review. Animal 8, 250–261.
The use of direct-fed microbials for mitigation of ruminant methane emissions: a review.CrossRef | 1:CAS:528:DC%2BC2cXptlSisA%3D%3D&md5=08cfcf4da9fd55ccbd6fd5d974fdf5e5CAS | 24274095PubMed |

Johnson KA, Johnson DE (1995) Methane emissions from cattle. Journal of Animal Science 73, 2483–2492.

Jouany JP (1994) Manipulation of microbial activity in the rumen. Archiv fur Tierernahrung 46, 133–153.
Manipulation of microbial activity in the rumen.CrossRef | 1:CAS:528:DyaK2sXhsFSnu74%3D&md5=01d7e315e43e072b256895010017b3d4CAS | 7717843PubMed |

Kandler O, König H (1993) Cell envelopes of Archaea: structure and chemistry. In ‘The biochemistry of Archaea (Archaebacteria)’. (Eds M Kates, DJ Kushner, AT Matheson) pp. 223–259 (Elsevier: Amsterdam)

Kaster AK, Goenrich M, Seedorf H, Liesegang H, Wollherr A, Gottschalk G, Thauer RK (2011) More than 200 genes required for methane formation from H2 and CO2 and energy conservation are present in Methanothermobacter marburgensis and Methanothermobacter thermautotrophicus. Archaea (Vancouver, B.C.)
More than 200 genes required for methane formation from H2 and CO2 and energy conservation are present in Methanothermobacter marburgensis and Methanothermobacter thermautotrophicus.CrossRef |

Kenealy W, Zeikus JG (1981) Influence of corrinoid antagonists on methanogen metabolism. Journal of Bacteriology 146, 133–140.

Klevenhusen F, Duval S, Zeitz JO, Kreuzer M, Soliva CR (2011) Diallyl disulphide and lovastatin: effects on energy and protein utilisation in, as well as methane emission from, sheep. Archives of Animal Nutrition 65, 255–266.
Diallyl disulphide and lovastatin: effects on energy and protein utilisation in, as well as methane emission from, sheep.CrossRef | 1:CAS:528:DC%2BC3MXptFKnu74%3D&md5=d7517fc07b103a7118cc4c4286373e10CAS |

Knight T, Ronimus RS, Dey D, Tootill C, Naylor GE, Evans P, Molano G, Smith A, Tavendale M, Pinares-Patiño CS, Clark H (2011) Chloroform decreases rumen methanogenesis and methanogen populations without altering rumen function in cattle. Animal Feed Science and Technology 166–167, 101–112.
Chloroform decreases rumen methanogenesis and methanogen populations without altering rumen function in cattle.CrossRef |

Kung L, Smith KA, Smagala AM, Endres KM, Bessett CA, Ranjit NK, Yaissle J (2003) Effects of 9,10 anthraquinone on ruminal fermentation, total-tract digestion, and blood metabolite concentrations in sheep. Journal of Animal Science 81, 323–328.

Leahy SC, Kelly WJ, Altermann E, Ronimus RS, Yeoman CJ, Pacheco DM, Li D, Kong Z, McTavish S, Sang C, Lambie SC, Janssen PH, Dey D, Attwood GT (2010) The genome sequence of the rumen methanogen Methanobrevibacter ruminantium reveals new possibilities for controlling ruminant methane emissions. PLoS One 5, e8926
The genome sequence of the rumen methanogen Methanobrevibacter ruminantium reveals new possibilities for controlling ruminant methane emissions.CrossRef | 20126622PubMed |

Leahy SC, Kelly WJ, Ronimus RS, Wedlock N, Altermann E, Attwood GT (2013) Genome sequencing of rumen bacteria and archaea and its application to methane mitigation strategies. Animal 7, 235–243.
Genome sequencing of rumen bacteria and archaea and its application to methane mitigation strategies.CrossRef | 23739466PubMed |

Liesack W, Schnell S, Revsbech NP (2000) Microbiology of flooded rice paddies. FEMS Microbiology Reviews 24, 625–645.
Microbiology of flooded rice paddies.CrossRef | 1:CAS:528:DC%2BD3cXotVCksLY%3D&md5=fb0cea9587511d6e9e89f729144940deCAS | 11077155PubMed |

Lou XF, Nair J (2009) The impact of landfilling and composting on greenhouse gas emissions – a review. Bioresource Technology 100, 3792–3798.

Martínez-Fernández G, Abecia L, Arco A, Cantalapiedra-Hijar G, Martín-García AI, Molina-Alcaide E, Kindermann M, Duval S, Yáñez-Ruiz DR (2014) Effects of ethyl-3-nitrooxy propionate and 3-nitrooxypropanol on ruminal fermentation, microbial abundance, and methane emissions in sheep. Journal of Dairy Science 97, 3790–3799.

May HD, Wu Q, Blake CK (2000) Effects of the Fusarium spp. mycotoxins fusaric acid and deoxynivalenol on the growth of Ruminococcus albus and Methanobrevibacter ruminantium. Canadian Journal of Microbiology 46, 692–699.
Effects of the Fusarium spp. mycotoxins fusaric acid and deoxynivalenol on the growth of Ruminococcus albus and Methanobrevibacter ruminantium.CrossRef | 1:CAS:528:DC%2BD3cXlsFOks7s%3D&md5=7dbe02b375345afc35d665900affeb18CAS | 10941514PubMed |

McAllister TA, Newbold CJ (2008) Redirecting rumen fermentation to reduce methanogenesis. Australian Journal of Experimental Agriculture 48, 7–13.
Redirecting rumen fermentation to reduce methanogenesis.CrossRef | 1:CAS:528:DC%2BD1cXovVKh&md5=d7a78771cda0b15fd05ada6c366c00c1CAS |

McMillan DG, Ferguson SA, Dey D, Schroder K, Aung HL, Carbone V, Attwood GT, Ronimus RS, Meier T, Janssen PH, Cook GM (2011) A1A0–ATP synthase of Methanobrevibacter ruminantium couples sodium ions for ATP synthesis under physiological conditions. The Journal of Biological Chemistry 286, 39882–39892.
A1A0–ATP synthase of Methanobrevibacter ruminantium couples sodium ions for ATP synthesis under physiological conditions.CrossRef | 1:CAS:528:DC%2BC3MXhsVKjsrrE&md5=f77fe24dc52408e52256884d70d2ebdfCAS | 21953465PubMed |

Miller TL, Wolin MJ (2001) Inhibition of growth of methane-producing bacteria of the ruminant forestomach by hydroxymethylglutaryl–SCoA reductase inhibitors. Journal of Dairy Science 84, 1445–1448.
Inhibition of growth of methane-producing bacteria of the ruminant forestomach by hydroxymethylglutaryl–SCoA reductase inhibitors.CrossRef | 1:CAS:528:DC%2BD3MXktlKgs7k%3D&md5=1c09f8192db3be40213fb4bd31e92411CAS | 11417704PubMed |

Miner JL, Ragsdale SW, Takacs JM (2003) ‘Method for the inhibition of methanogenesis.’ Patent WO2003038109 A3. (University of Nebraska: Lincoln, NE)

Mitsumori M, Shinkai T, Takenaka A, Enishi O, Higuchi K, Kobayashi Y, Nonaka I, Asanuma N, Denman SE, McSweeney CS (2012) Responses in digestion, rumen fermentation and microbial populations to inhibition of methane formation by a halogenated methane analogue. British Journal of Nutrition 108, 482–491.
Responses in digestion, rumen fermentation and microbial populations to inhibition of methane formation by a halogenated methane analogue.CrossRef | 1:CAS:528:DC%2BC38XhtFClu7fK&md5=83b9473bdb1c81c275a8f41dc27dae8eCAS | 22059589PubMed |

Mohammed N, Lila ZA, Ajisaka N, Hara K, Mikuni K, Kanda S, Itabashi H (2004) Inhibition of ruminal microbial methane production by beta-cyclodextrin iodopropane, malate and their combination in vitro. Journal of Animal Physiology and Animal Nutrition 88, 188–195.
Inhibition of ruminal microbial methane production by beta-cyclodextrin iodopropane, malate and their combination in vitro.CrossRef | 1:CAS:528:DC%2BD2cXmt1OrtbY%3D&md5=f8403008f9cbe4a7a25d5d15e88ac7efCAS | 15189423PubMed |

Morgavi DP, Martin C, Boudra H (2013) Fungal secondary metabolites from Monascus spp. reduce rumen methane production in vitro and in vivo. Journal of Animal Science 91, 848–860.
Fungal secondary metabolites from Monascus spp. reduce rumen methane production in vitro and in vivo.CrossRef | 1:CAS:528:DC%2BC3sXlvVKmsrY%3D&md5=ca51ee646a0869d2abac8a901f6dae82CAS | 23307850PubMed |

New Zealand Government (2014) ‘New Zealand’s greenhouse gas inventory 1990–2012.’ Available at http://www.mfe.govt.nz/publications/climate-change/new-zealands-greenhouse-gas-inventory-1990%E2%80%932012. [Verified September 2015]

Oremland RS, Capone DG (1988) Use of ‘specific’ inhibitors in biogeochemistry and microbial ecology. Advances in Microbial Ecology 10, 285–383.
Use of ‘specific’ inhibitors in biogeochemistry and microbial ecology.CrossRef | 1:CAS:528:DyaL1MXhs12rt7s%3D&md5=98339bacdf7c919288175dd0fc86e164CAS |

Ozone Secretariat, United Nations Environment Programme (2000) ‘Action on ozone.’ 2000 edn. (The Secretariat for The Vienna Convention for the Protection of the Ozone Layer & The Montreal Protocol on Substances that Deplete the Ozone Layer: Nairobi, Kenya)

Patra AK, Saxena J (2010) A new perspective on the use of plant secondary metabolites to inhibit methanogenesis in the rumen. Phytochemistry 71, 1198–1222.
A new perspective on the use of plant secondary metabolites to inhibit methanogenesis in the rumen.CrossRef | 1:CAS:528:DC%2BC3cXosV2htbk%3D&md5=7ee8f0e4c070ec5a741b7d00dcca9d59CAS | 20570294PubMed |

Prins RA (1978) Nutritional impact of intestinal drug-microbe interactions. In ‘Nutrition and drug interrelationships’. (Ed. J Hathcock) pp. 189–252. (Academic Press: New York)

Ramírez-Restrepo CA, O’Neill CJ, López-Villabos N, Padmanabha J, McSweeney CS (2014) Tropical cattle methane emissions: the role of natural statins supplementation. Animal Production Science 54, 1294–1299.
Tropical cattle methane emissions: the role of natural statins supplementation.CrossRef |

Reynolds CK, Humphries DJ, Kirton DJ, Kindermann M, Duval S, Steinberg W (2014) Effect of 3-nitrooxypropanl on methane emission, digestion, and energy and nitrogen balance of lactating dairy cows. Journal of Dairy Science 97, 3777–3789.
Effect of 3-nitrooxypropanl on methane emission, digestion, and energy and nitrogen balance of lactating dairy cows.CrossRef | 1:CAS:528:DC%2BC2cXls1WktLw%3D&md5=9fcf737d37bdc891c4ed958bad343826CAS | 24704240PubMed |

Ripple WJ, Smith P, Haberl H, Montzka SA, McAlpine C, Boucher DH (2014) Ruminants, climate change and climate policy. Nature Climate Change 4, 2–5.
Ruminants, climate change and climate policy.CrossRef | 1:CAS:528:DC%2BC3sXhvFOjtb%2FO&md5=785bf5c0ffa01eb50b196523e7596afeCAS |

Romero-Perez A, Okine EK, McGinn SM, Guan LL, Oba M, Duval SM, Kindermann M, Beauchemin KA (2014) The potential of 3-nitrooxypropanol to lower enteric methane emissions from beef cattle. Journal of Animal Science 92, 4682–4693.
The potential of 3-nitrooxypropanol to lower enteric methane emissions from beef cattle.CrossRef | 1:CAS:528:DC%2BC2cXhvFKrtr3K&md5=9afaaa67105cbff6ec976fee4600a42fCAS | 25184838PubMed |

Romero-Perez A, Okine EK, McGinn SM, Guan LL, Oba M, Duval SM, Kindermann M, Beauchemin KA (2015) Sustained reduction in methane production from long-term addition of 3-nitrooxypropanol to a beef cattle diet. Journal of Animal Science 93, 1780–1791.
Sustained reduction in methane production from long-term addition of 3-nitrooxypropanol to a beef cattle diet.CrossRef | 1:CAS:528:DC%2BC2MXoslWrtLg%3D&md5=83b3fb719978d5aae1c16a5ae5565ab2CAS | 26020199PubMed |

Ronimus RS, Muetzel S, Tavendale MH, Lunn K, Zhang Y, Sang C, Dey D, Atua R, Weimar M, Cheung J, Sutherland-Smith AJ, Edwards PJW, Whitman WB, Denny WA, Cook GM, Carbone V, Schofield LR (2015) Targeting rumen methanogens to aid the development of methane mitigation agents. In ‘Proceedings of the 23rd IUBMB congress & 44th annual SBBq meeting’. (Ed. C Bando) pp. 1–743. (Sociedade Brasileira de Bioquímica e Biologia Molecular (SBBq): Foz do Iguacu, Brazil)

Russell JB, Strobel HJ (1989) Effect of ionophores on ruminal fermentation. Applied and Environmental Microbiology 55, 1–6.

Russell JB, Mantovani HC (2002) The bacteriocins of ruminal bacteria and their potential as an alternative to antibiotics. Journal of MolecularMicrobiology and Biotechnology 4, 347–355.

Santoro N, Konisky J (1987) Characterization of bromoethanesulfonate-resistant mutants of Methanococcus voltae: evidence of a coenzyme M transport system. Journal of Bacteriology 169, 660–665.

Sarmiento F, Mrázek J, Whitman WB (2013) Genome-scale analysis of gene function in the hydrogenotrophic methanogenic archaeon Methanococcus maripaludis. Proceedings of the National Academy of Sciences of the United States of America 110, 4726–4731.
Genome-scale analysis of gene function in the hydrogenotrophic methanogenic archaeon Methanococcus maripaludis.CrossRef | 1:CAS:528:DC%2BC3sXmslans7w%3D&md5=692ba0089d2b441d635af78061c343d1CAS | 23487778PubMed |

Seedorf H, Kittelmann S, 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.
Few highly abundant operational taxonomic units dominate within rumen methanogenic archaeal species in New Zealand sheep and cattle.CrossRef | 1:CAS:528:DC%2BC2MXhvVGqur0%3D&md5=494489ea42c0110aaf36366f50e0fafcCAS | 25416771PubMed |

Selje N, Hoffmann EM, Muetzel S, Ningrat R, Wallace RJ, Becker K (2007) Results of a screening programme to identify plants or plant extracts that inhibit ruminal protein degradation. British Journal of Nutrition 98, 45–53.
Results of a screening programme to identify plants or plant extracts that inhibit ruminal protein degradation.CrossRef | 1:CAS:528:DC%2BD2sXosVOjs7k%3D&md5=48d58ec4530c93ef341d1bc4f297eb93CAS | 17445338PubMed |

Shi W, Moon CD, Leahy SC, Kang D, Froula J, Kittelmann S, Fan C, Deutsch S, Gagic D, Seedorf H, Kelly WJ, Atua R, Sang C, Soni P, Li D, Pinares-Patiño CS, McEwan JC, Janssen PH, Chen F, Visel A, Wang Z, Attwood GT, Rubin EM (2014) Methane yield phenotypes linked to differential gene expression in the sheep rumen microbiome. Genome Research 24, 1517–1525.
Methane yield phenotypes linked to differential gene expression in the sheep rumen microbiome.CrossRef | 1:CAS:528:DC%2BC2cXhsFaksLnJ&md5=4a799e0c9c12ca2b77064b7ec58af1feCAS | 24907284PubMed |

Shinkai T, Enishi O, Mitsumori M, Higuchi K, Kobayashi Y, Takenaka A, Nagashima K, Mochizuki M, Kobayashi Y (2012) Mitigation of methane production from cattle by feeding cashew nut shell liquid. Journal of Dairy Science 95, 5308–5316.
Mitigation of methane production from cattle by feeding cashew nut shell liquid.CrossRef | 1:CAS:528:DC%2BC38Xht1emur7J&md5=f1f21dea82c4b0b4c54dd89761961d63CAS | 22916936PubMed |

Surín S, Cubonova L, Majernik AI, McDermott P, Chong JP, Smigan P (2007) Isolation and characterization of an amiloride-resistant mutant of Methanothermobacter thermautotrophicus possessing a defective Na+/H+ antiport. FEMS Microbiology Letters 269, 301–308.
Isolation and characterization of an amiloride-resistant mutant of Methanothermobacter thermautotrophicus possessing a defective Na+/H+ antiport.CrossRef | 17286571PubMed |

Tomkins NW, Colegate SM, Hunter RA (2009) A bromochloromethane formulation reduces enteric methanogenesis in cattle fed grain-based diets. Animal Production Science 49, 1053–1058.
A bromochloromethane formulation reduces enteric methanogenesis in cattle fed grain-based diets.CrossRef | 1:CAS:528:DC%2BD1MXhsVWqtLnE&md5=a58afb32860a8af661d3dcc368b5abc9CAS |

Trei JE, Scott GC, Parish RC (1972) Influence of methane inhibition on energetic efficiency of lambs. Journal of Animal Science 34, 510–515.

Tritscher A, Miyagishima K, Nishida C, Branca F (2013) Ensuring food safety and nutrition security to protect consumer health: 50 years of the Codex Alimentarius Commission. Bulletin of the World Health Organization 91, 468-8A
Ensuring food safety and nutrition security to protect consumer health: 50 years of the Codex Alimentarius Commission.CrossRef | 23825870PubMed |

Ungerfeld EM, Rust SR, Burnett R (2006) Effects of butyrate precursors on electron relocation when methanogenesis is inhibited in ruminal mixed cultures. Letters in Applied Microbiology 42, 567–572.

Van Nevel CJ, Demeyer DI (1996) Control of rumen methanogenesis. Environmental Monitoring and Assessment 42, 73–97.
Control of rumen methanogenesis.CrossRef | 1:CAS:528:DyaK28Xltlars7w%3D&md5=4785e0a51b315f4c5fd8bf5a1ef0afcfCAS | 24193494PubMed |

Van Nevel C, Demeyer D (2007) Feed additives and other interventions for decreasing methane emissions. In ‘Biotechnology in animal feeds and animal feeding’. (Eds RJ Wallace, A Chesson) pp. 329–349. (Wiley–VCH Verlag GmbH: Weinheim, Germany)

van Zijderveld SM, Gerrits WJ, Apajalahti JA, Newbold JR, Dijkstra J, Leng RA, Perdok HB (2010) Nitrate and sulfate: effective alternative hydrogen sinks for mitigation of ruminal methane production in sheep. Journal of Dairy Science 93, 5856–5866.
Nitrate and sulfate: effective alternative hydrogen sinks for mitigation of ruminal methane production in sheep.CrossRef | 1:CAS:528:DC%2BC3MXjs1Kis7Y%3D&md5=c84de18e60e1d808cc7a5d43ed5f5cd6CAS | 21094759PubMed |

van Zijderveld SM, Dijkstra J, Perdok HB, Newbold JR, Gerrits WJ (2011) Dietary inclusion of diallyl disulfide, yucca powder, calcium fumarate, an extruded linseed product, or medium-chain fatty acids does not affect methane production in lactating dairy cows. Journal of Dairy Science 94, 3094–3104.
Dietary inclusion of diallyl disulfide, yucca powder, calcium fumarate, an extruded linseed product, or medium-chain fatty acids does not affect methane production in lactating dairy cows.CrossRef | 1:CAS:528:DC%2BC3MXnvFCnsr8%3D&md5=1f702ccfc95537d0013c698136aeed9aCAS | 21605778PubMed |

Wackett LP, Honek JF, Begley TP, Shames SL, Niederhoffer EC, Hausinger RP, Orme-Johnson WH, Walsh CT (1988) Methyl-S-coenzyme-M reductase: a nickel-dependent enzyme catalysing the terminal redox step in methane biogenesis. In ‘The bioinorganic chemistry of nickel’. (Ed. JR Lancaster) pp. 249–274. (VCH, John Wiley and Sons: New York)

Wallace RJ, McEwan NR, McIntosh FM, Teferedegne B, Newbold CJ (2002) Natural products as manipulators of rumen fermentation. Asian-Australasian Journal of Animal Sciences 15, 1458–1468.
Natural products as manipulators of rumen fermentation.CrossRef | 1:CAS:528:DC%2BD38Xns1ansrg%3D&md5=e8c3a19bbd50dc62043eea38f2e9b022CAS |

Wedlock DN, Pedersen G, Denis M, Dey D, Janssen PH, Buddle BM (2010) Development of a vaccine to mitigate greenhouse gas emissions in agriculture: vaccination of sheep with methanogen fractions induces antibodies that block methane production in vitro. New Zealand Veterinary Journal 58, 29–36.
Development of a vaccine to mitigate greenhouse gas emissions in agriculture: vaccination of sheep with methanogen fractions induces antibodies that block methane production in vitro.CrossRef | 1:CAS:528:DC%2BC3cXpt1Okurw%3D&md5=e34424cb8ec5bc1535a3e4db7d875593CAS | 20200573PubMed |

Weimer PJ (1998) Manipulating ruminal fermentation: a microbial ecological perspective. Journal of Animal Science 76, 3114–3122.

Williams YJ, Popovski S, Rea SM, Skillman LC, Toovey AF, Northwood KS, Wright AD (2009) A vaccine against rumen methanogens can alter the composition of archaeal populations. Applied and Environmental Microbiology 75, 1860–1866.
A vaccine against rumen methanogens can alter the composition of archaeal populations.CrossRef | 1:CAS:528:DC%2BD1MXksFWlsb0%3D&md5=c9bbbba891176c412cb56884f62c575fCAS | 19201957PubMed |

Woese CR, Magrum LJ, Fox GE (1978) Archaebacteria. Journal of Molecular Evolution 11, 245–252.
Archaebacteria.CrossRef | 1:CAS:528:DyaE1cXlsF2rsr8%3D&md5=1c1919ba0f5b4581d226d6cb5fb00431CAS | 691075PubMed |

Wolin MJ, Miller TL (2006) Control of rumen methanogenesis by inhibiting the growth and activity of methanogens with hydroxymethylglutaryl–SCoA inhibitors. International Congress Series 1293, 131–137.
Control of rumen methanogenesis by inhibiting the growth and activity of methanogens with hydroxymethylglutaryl–SCoA inhibitors.CrossRef | 1:CAS:528:DC%2BD1cXhs1amsbc%3D&md5=b380cc2e44787f131285839fc4a0f31eCAS |

Wood JM, Kennedy FS, Wolfe RS (1968) The reaction of multihalogenated hydrocarbons with free and bound reduced vitamin B12. Biochemistry 7, 1707–1713.
The reaction of multihalogenated hydrocarbons with free and bound reduced vitamin B12.CrossRef | 1:CAS:528:DyaF1cXktFKhtbw%3D&md5=7d46bedbed666068348577a5fa592475CAS | 4870333PubMed |

Wright AD, Kennedy P, O’Neill CJ, Toovey AF, Popovski S, Rea SM, Pimm CL, Klein L (2004) Reducing methane emissions in sheep by immunization against rumen methanogens. Vaccine 22, 3976–3985.
Reducing methane emissions in sheep by immunization against rumen methanogens.CrossRef | 1:CAS:528:DC%2BD2cXnsFGns7s%3D&md5=a7596c6e6f0a073321133a21d6ee9d23CAS | 15364447PubMed |



Export Citation Cited By (1)