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Cited by 472Ruminant Nutrition and Digestive PhysiologyAnaerobic Digestion and Biogas ProductionAnimal Nutrition and Physiology

Metabolic Hydrogen Flows in Rumen Fermentation: Principles and Possibilities of Interventions

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Ungerfeld, Emilio M.·2020·Frontiers in Microbiology
DOI 10.3389/fmicb.2020.00589PMC PMC7174568
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Abstract

Rumen fermentation affects ruminants productivity and the environmental impact of ruminant production. The release to the atmosphere of methane produced in the rumen is a loss of energy and a cause of climate change, and the profile of volatile fatty acids produced in the rumen affects the post-absorptive metabolism of the host animal. Rumen fermentation is shaped by intracellular and intercellular flows of metabolic hydrogen centered on the production, interspecies transfer, and incorporation of dihydrogen into competing pathways. Factors that affect the growth of methanogens and the rate of feed fermentation impact dihydrogen concentration in the rumen, which in turn controls the balance between pathways that produce and incorporate metabolic hydrogen, determining methane production and the profile of volatile fatty acids. A basic kinetic model of competition for dihydrogen is presented, and possibilities for intervention to redirect metabolic hydrogen from methanogenesis toward alternative useful electron sinks are discussed. The flows of metabolic hydrogen toward nutritionally beneficial sinks could be enhanced by adding to the rumen fermentation electron acceptors or direct fed microbials. It is proposed to screen hydrogenotrophs for dihydrogen thresholds and affinities, as well as identifying and studying microorganisms that produce and utilize intercellular electron carriers other than dihydrogen. These approaches can allow identifying potential microbial additives to compete with methanogens for metabolic hydrogen. The combination of adequate microbial additives or electron acceptors with inhibitors of methanogenesis can be effective approaches to decrease methane production and simultaneously redirect metabolic hydrogen toward end products of fermentation with a nutritional value for the host animal. The design of strategies to redirect metabolic hydrogen from methane to other sinks should be based on knowledge of the physicochemical control of rumen fermentation pathways. The application of new -omics techniques together with classical biochemistry methods and mechanistic modeling can lead to exciting developments in the understanding and manipulation of the flows of metabolic hydrogen in rumen fermentation.

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  • Acetate production during fermentative carbohydrate fermentation is accompanied by H2 release.

    “Acetate production during fermentative carbohydrate fermentation is accompanied by H2 release, whereas acetate production through reductive acetogenesis is an H2 sink [51].”

    From Reductive acetogenesis is a dominant process in the ruminant hindgut (2025) · cites this paper as [51]

    The Background section on volatile fatty acid balances says acetate production from glucose releases metabolic hydrogen ([H]), but it does not establish that H2 is always released: it also identifies an acetate-producing pathway with no net [H] production. The Background section on other hydrogen-incorporating pathways explicitly describes reductive acetogenesis as using H2 to produce acetate, supporting the sentence’s second clause. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Acetate production through reductive acetogenesis is an H2 sink.

    “Acetate production during fermentative carbohydrate fermentation is accompanied by H2 release, whereas acetate production through reductive acetogenesis is an H2 sink [51].”

    From Reductive acetogenesis is a dominant process in the ruminant hindgut (2025) · cites this paper as [51]

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Research works printed but not linked: 158

  1. Alazzeh A. Y. Sultana H. Beauchemin K. A. Wang Y. Holo H. Harstad O. M. (2012). Using strains of Propionibacteria to mitigate methane emissions in vitro. Acta Agric. Scand. A 62 263– 272. 10.1080/09064702.2013.773056 · DOI
  2. Allen M. S. Bradford B. J. Oba M. (2009). Board-invited review: the hepatic oxidation theory of the control of feed intake and its application to ruminants. J. Anim. Sci. 87 3317– 3334. 10.2527/jas.2009-1779 19648500 · DOI
  3. Amgarten M. Schatzmann H. J. Wüthrich A. (1981). ‘Lactate type’ response of ruminal fermentation to chloral hydrate, chloroform and trichloroethanol. J. Vet. Pharmacol. Ther. 4 241– 248. 10.1111/j.1365-2885.1981.tb00736.x 7349340 · DOI
  4. Armstrong D. G. Blaxter K. L. (1957). The utilization of acetic, propionic and butyric acids by fattening sheep. Br. J. Nutr. 11 413– 425. 10.1079/BJN19570063 13489151 · DOI
  5. Asanuma N. Iwamoto M. Hino T. (1998). Formate metabolism by ruminal microorganisms in relation to methanogenesis. Anim. Sci. Technol. 69 576– 584. 10.2508/chikusan.69.576 · DOI
  6. Asanuma N. Iwamoto M. Hino T. (1999). Effect of the addition of fumarate on methane production by ruminal microorganisms in vitro. J. Dairy Sci. 82 780– 787. 10.3168/jds.s0022-0302(99)75296-3 10212465 · DOI
  7. Aschenbach J. R. Kristensen N. B. Donkin S. S. Hammon H. M. Penner G. B. (2010). Gluconeogenesis in dairy cows: the secret of making sweet milk from sour dough. IUBMB Life 62 869– 877. 10.1002/iub.400 21171012 · DOI
  8. Bauchop T. Mountfort D. O. (1981). Cellulose fermentation by a rumen anaerobic fungus in both the absence and the presence of rumen methanogens. Appl. Environ. Microbiol. 42 1103– 1110. 10.1128/aem.42.6.1103-1110.1981 16345902 PMC244160 · DOI
  9. Beauchemin K. A. McGinn S. M. (2006). Methane emissions from beef cattle: effects of fumaric acid, essential oil, and canola oil1. J. Anim. Sci. 84 1489– 1496. 10.2527/2006.8461489x 16699105 · DOI
  10. Blackburn T. H. Hungate R. E. (1963). Succinic acid turnover and propionate production in the bovine rumen. Appl. Microbiol. 11 132– 135. 10.1128/aem.11.2.132-135.1963 13971386 PMC1057956 · DOI
  11. Božic A. K. Anderson R. C. Carstens G. E. Ricke S. C. Callaway T. R. Yokoyama M. T. (2009). Effects of the methane-inhibitors nitrate, nitroethane, lauric acid, Lauricidin§and the Hawaiian marine algae Chaetoceros on ruminal fermentation in vitro. Bioresour. Technol. 100 4017– 4025. 10.1016/j.biortech.2008.12.061 19362827 · DOI
  12. Breznak J. A. Switzer J. M. Seitz H. J. (1988). Sporomusa termitida sp. nov., an H2/CO2-utilizing acetogen isolated from termites. Arch. Microbiol. 150 282– 288. 10.1007/BF00407793 · DOI
  13. Broudiscou L. P. Offner A. Sauvant D. (2014). Effects of inoculum source, pH, redox potential and headspace di-hydrogen on rumen in vitro fermentation yields. Animal 8 931– 937. 10.1017/s1751731114000640 24679594 · DOI
  14. Buckel W. Thauer R. K. (2018a). Flavin-based electron bifurcation, a new mechanism of biological energy coupling. Chem. Rev. 118 3862– 3886. 10.1021/acs.chemrev.7b00707 29561602 · DOI · Paper page
  15. Buckel W. Thauer R. K. (2018b). Flavin-based electron bifurcation, ferredoxin, flavodoxin, and anaerobic respiration with protons (Ech) or NAD+ (Rnf) as electron acceptors: a historical review. Front. Microbiol. 9: 401. 10.3389/fmicb.2018.00401 29593673 PMC5861303 · DOI
  16. Cabezas-Garcia E. H. Krizsan S. J. Shingfield K. J. Huhtanen P. (2017). Between-cow variation in digestion and rumen fermentation variables associated with methane production. J. Dairy Sci. 100 4409– 4424. 10.3168/jds.2016-12206 28390728 · DOI
  17. Callaway T. R. Martin S. A. (1996). Effects of organic acid and monensin treatment on in vitro mixed ruminal microorganism fermentation of cracked corn. J. Anim. Sci. 74 1982– 1989. 10.2527/1996.7481982x 8856454 · DOI
  18. Carro M. D. Ranilla M. J. (2003). Influence of different concentrations of disodium fumarate on methane production and fermentation of concentrate feeds by rumen micro-organisms in vitro. Br. J. Nutr. 90 617– 623. 10.1079/bjn2003935 13129468 · DOI
  19. Carro M. D. Ungerfeld E. M. (2015). “ Utilization of organic acids to manipulate ruminal fermentation and improve ruminant productivity,” in Rumen Microbiology: From Evolution to Revolution, eds Puniya A. K. Singh R. Kamra D. N., (New Dehli: Springer), 177– 197. 10.1007/978-81-322-2401-3_13 · DOI
  20. Chalupa W. (1977). Manipulating rumen fermentation. J. Anim. Sci. 46 585– 599. 10.2527/jas1977.453585x · DOI
  21. Chalupa W. Evans J. L. Stillions M. C. (1964). Influence of ethanol on rumen fermentation and nitrogen metabolism. J. Anim. Sci. 23 802– 807. 10.2527/jas1964.233802x · DOI
  22. Chaucheyras F. Fonty G. Bertin G. Gouet P. (1995). In vitro H2 utilization by a ruminal acetogenic bacterium cultivated alone or in association with an archaea methanogen is stimulated by a probiotic strain of Saccharomyces cerevisiae. Appl. Environ. Microbiol. 61 3466– 3467. 10.1128/aem.61.9.3466-3467.1995 7574654 PMC167624 · DOI
  23. Chen L. Shen Y. Wang C. Ding L. Zhao F. Wang M. (2019). Megasphaera elsdenii lactate degradation pattern shifts in rumen acidosis models. Front. Microbiol. 10: 162. 10.3389/fmicb.2019.00162 30792704 PMC6374331 · DOI
  24. Chen M. Wolin M. J. (1977). Influence of CH4 production by Methanobacterium ruminantium on the fermentation of glucose and lactate by Selenomonas ruminantium. Appl. Environ. Microbiol. 34 756– 759. 10.1128/aem.34.6.756-759.1977 596874 PMC242743 · DOI
  25. Choi S. Song H. Lim S. W. Kim T. Y. Ahn J. H. Lee J. W. (2016). Highly selective production of succinic acid by metabolically engineered Mannheimia succiniciproducens and its efficient purification. Biotechnol. Bioeng. 113 2168– 2177. 10.1002/bit.25988 27070659 · DOI
  26. Chung K. T. (1976). Inhibitory effects of H2 on growth of Clostridium cellobioparum. Appl. Environ. Microbiol. 31 342– 348. 10.1128/aem.31.3.342-348.1976 779644 PMC169777 · DOI
  27. Cord-Ruwisch R. Seitz H. J. Conrad R. (1988). The capacity of hydrogenotrophic anaerobic bacteria to compete for traces of hydrogen depends on the redox potential of the terminal electron acceptor. Arch. Microbiol. 149 350– 357. 10.1007/bf00411655 · DOI · Paper page
  28. Czerkawski J. W. (1986). An Introduction to Rumen Studies. Exeter: Pergamon Press.
  29. Czerkawski J. W. Breckenridge G. (1975a). New inhibitors of methane production by rumen micro- organisms. Experiments with animals and other practical possibilities. Br. J. Nutr. 34 447– 457. 10.1017/s0007114575000505 1201268 · DOI
  30. Czerkawski J. W. Breckenridge G. (1975b). New inhibitors of methane production by rumen micro-organisms. Development and testing of inhibitors in vitro. Br. J. Nutr. 34 429– 446. 10.1017/S0007114575000499 1201267 · DOI
  31. Davies A. Nwaonu H. N. Stanier G. Boyle F. T. (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. Br. J. Nutr. 47 565– 576. 10.1079/bjn19820068 7082625 · DOI
  32. de Graef M. R. Alexeeva S. Snoep J. L. Teixeira de Mattos M. J. (1999). The steady-state internal redox state (NADH/NAD) reflects the external redox state and is correlated with catabolic adaptation in Escherichia coli. J. Bacteriol. 181 2351– 2357. 10.1128/jb.181.8.2351-2357.1999 10197995 PMC93657 · DOI
  33. De Vries W. van Wyck-Kapteyn W. M. Stouthamer A. H. (1973). Generation of ATP during cytochrome-linked anaerobic electron transport in propionic acid bacteria. J. Gen. Microbiol. 76 31– 41. 10.1099/00221287-76-1-31 4353042 · DOI
  34. Denman S. E. Martínez-Fernández G. Shinkai T. Mitsumori M. McSweeney C. S. (2015). Metagenomic analysis of the rumen microbial community following inhibition of methane formation by a halogenated methane analogue. Front. Microbiol. 6: 1087 10.3389/fmicb.2015.01087 PMC4602129 26528253 · DOI
  35. Dijkstra J. Boer H. Van Bruchem J. Bruining M. Tamminga S. (1993). Absorption of volatile fatty acids from the rumen of lactating dairy cows as influenced by volatile fatty acid concentration, pH and rumen liquid volume. Br. J. Nutr. 69 385– 396. 10.1079/bjn19930041 8489996 · DOI
  36. Ebrahimi S. H. Mohinia M. Singhala K. K. Miria V. H. Tyagi A. K. (2011). Evaluation of complementary effects of 9,10-anthraquinone and fumaric acid on methanogenesis and ruminal fermentation in vitro. Arch. Anim. Nutr. 65 267– 277. 10.1080/1745039X.2011.594345 21888033 · DOI
  37. Eckard R. J. Grainger C. De Klein C. A. M. (2010). Options for the abatement of methane and nitrous oxide from ruminant production: a review. Livestock Sci. 130 47– 56. 10.1016/j.livsci.2010.02.010 · DOI
  38. Emery R. S. Lewis T. R. Everett J. P. Lassiter C. A. (1959). Effect of ethanol on rumen fermentation. J. Dairy Sci. 42 1182– 1186. 10.3168/jds.S0022-0302(59)90710-6 · DOI
  39. Frei M. (2013). Lignin: characterization of a multifaceted crop component. Sci. World J. 2013: 436517. 10.1155/2013/436517 24348159 PMC3848262 · DOI
  40. Frey M. (2002). Hydrogenases: hydrogen-activating enzymes. Chembiochem 3 153– 160. 10.1002/1439-7633(20020301)3:2/3<153::aid-cbic153>3.0.co;2-b 11921392 · DOI
  41. Gagen E. J. Mosoni P. Denman S. E. Al Jassim R. McSweeney C. S. Forano E. (2012). Methanogen colonisation does not significantly alter acetogen diversity in lambs isolated 17 h after birth and raised aseptically. Microb. Ecol. 64 628– 640. 10.1007/s00248-012-0024-z 22383121 · DOI
  42. Genthner B. R. Davis C. L. Bryant M. P. (1981). Features of rumen and sewage sludge strains of Eubacterium limosum, a methanol- and H2-CO2-utilizing species. Appl. Environ. Microbiol. 42 12– 19. 10.1128/aem.42.1.12-19.1981 6791591 PMC243953 · DOI
  43. Gerber P. J. Hristov A. N. Henderson B. Makkar H. Oh J. Lee C. (2013). Technical options for the mitigation of direct methane and nitrous oxide emissions from livestock: a review. Animal 7 220– 234. 10.1017/S1751731113000876 23739465 · DOI
  44. Gottschalk G. (1986). Bacterial Metabolism. New York, NY: Springer.
  45. Greening C. Geier R. Wang C. Woods L. C. Morales S. E. McDonald M. J. (2019). Diverse hydrogen production and consumption pathways influence methane production in ruminants. ISME J. 13 2617– 2632. 10.1038/s41396-019-0464-2 31243332 PMC6776011 · DOI
  46. Guyader J. Eugene M. Meunier B. Doreau M. Morgavi D. P. Silberberg M. (2015). Additive methane-mitigating effect between linseed oil and nitrate fed to cattle. J. Anim. Sci. 93 3564– 3577. 10.2527/jas.2014-8196 26440025 · DOI
  47. Hackmann T. J. Firkins J. (2015). Electron transport phosphorylation in rumen butyrivibrios: unprecedented ATP yield for glucose fermentation to butyrate. Front. Microbiol. 6: 622. 10.3389/fmicb.2015.00622 26157432 PMC4478896 · DOI
  48. Hackmann T. J. Ngugi D. K. Firkins J. L. Tao J. (2017). Genomes of rumen bacteria encode atypical pathways for fermenting hexoses to short-chain fatty acids. Environ. Microbiol. 19 4670– 4683. 10.1111/1462-2920.13929 28892251 · DOI
  49. Hall M. B. Nennich T. D. Doane P. H. Brink G. E. (2015). Total volatile fatty acid concentrations are unreliable estimators of treatment effects on ruminal fermentation in vivo. J. Dairy Sci. 98 3988– 3999. 10.3168/jds.2014-8854 25828661 · DOI
  50. Henderson C. (1980). The influence of extracellular hydrogen on the metabolism of Bacteroides rurninicola, Anaerovibrio lipolytica and Selenomonas ruminantiurn. J. Gen. Microbiol. 119 485– 491. 10.1099/00221287-119-2-485 6785381 · DOI
  51. Hino T. Russell J. B. (1985). Effect of reducing-equivalent disposal and NADH/NAD on deamination of amino acids by intact rumen microorganisms and their cell extracts. Appl. Environ. Microbiol. 50 1368– 1374. 10.1128/aem.50.6.1368-1374.1985 4091565 PMC238765 · DOI
  52. Hungate R. E. (1967). Hydrogen as an intermediate in the rumen fermentation. Arch. Mikrobiol. 59 158– 164. 10.1007/bf00406327 5628850 · DOI
  53. Hungate R. E. Smith W. Bauchop T. Yu I. Rabinowitz J. C. (1970). Formate as an intermediate in the bovine rumen fermentation. J. Bacteriol. 102 389– 397. 10.1128/jb.102.2.389-397.1970 5419259 PMC247563 · DOI
  54. Immig I. (1996). The rumen and hindgut as source of ruminant methanogenesis. Environ. Monit. Assess. 42 57– 72. 10.1007/BF00394042 24193493 · DOI
  55. Ingram L. O. (1990). Ethanol tolerance in bacteria. Crit. Rev. Biotechnol. 9 305– 319. 10.3109/07388558909036741 2178781 · DOI · Paper page
  56. Isaacson H. R. Hinds F. C. Bryant M. P. Owens F. N. (1975). Efficiency of energy utilization by mixed rumen bacteria in continuous culture. J. Dairy Sci. 58 1645– 1659. 10.3168/jds.s0022-0302(75)84763-1 1194467 · DOI
  57. Janssen P. H. (2010). Influence of hydrogen on rumen methane formation and fermentation balances through microbial growth kinetics and fermentation thermodynamics. Anim. Feed Sci. Technol. 160 1– 22. 10.1016/j.anifeedsci.2010.07.002 · DOI
  58. Joblin K. N. (1999). Ruminal acetogens and their potential to lower ruminant methane emissions. Aust. J. Agric. Res. 50 1307– 1313. 10.1071/AR99004 · DOI · Paper page
  59. Kamke J. Kittelmann S. Soni P. Li Y. Tavendale M. Ganesh S. (2016). Rumen metagenome and metatranscriptome analyses of low methane yield sheep reveals a Sharpea-enriched microbiome characterised by lactic acid formation and utilisation. Microbiome 4: 56. 10.1186/s40168-016-0201-2 27760570 PMC5069950 · DOI · Paper page
  60. Kim S. H. Mamuad L. L. Kim D. W. Kim S. K. Lee S. S. (2016). Fumarate reductase-producing enterococci reduce methane production in in vitro rumen fermentation. J. Microbiol. Biotechnol. 26 558– 566. 10.4014/jmb.1512.12008 26767574 · DOI
  61. Kittelmann S. Pinares-Patiño C. S. Seedorf H. Kirk M. R. Ganesh S. McEwan J. C. (2014). Two different bacterial community types are linked with the low-methane emission trait in sheep. PLoS One 9: e103171. 10.1371/journal.pone.0103171 25078564 PMC4117531 · DOI · Paper page
  62. Klieve A. V. Ouwerkerk D. Maguire A. J. (2012). Archaea in the foregut of macropod marsupials: PCR and amplicon sequence-based observations. J. Appl. Microbiol. 113 1065– 1075. 10.1111/j.1365-2672.2012.05428.x 22897363 · DOI
  63. Kolver E. S. Aspin P. W. (2006). “ Supplemental fumarate did not influence milksolids or methane production from dairy cows fed high quality pasture,” in Proceedings of the New Zealand Society of Animal Production (Wellington: New Zealand Society of Animal Production), 409– 415.
  64. Kristensen N. B. (2001). Rumen microbial sequestration of [2-13C]acetate in cattle. J. Anim. Sci. 79 2491– 2498. 11583438
  65. Kröger A. Biel S. Simon J. Gross R. Unden G. Lancaster C. R. D. (2002). Fumarate respiration of Wolinella succinogenes: enzymology, energetics and coupling mechanism. Biochim. Biopys. Acta 1553 23– 38. 10.1016/S0005-2728(01)00234-1 11803015 · DOI
  66. Kumar S. Treloar B. P. Teh K. H. McKenzie C. M. Henderson G. Attwood G. T. (2018). Sharpea and Kandleria are lactic acid producing rumen bacteria that do not change their fermentation products when co-cultured with a methanogen. Anaerobe 54 31– 38. 10.1016/j.anaerobe.2018.07.008 30055268 · DOI
  67. Latham M. J. Wolin M. J. (1977). Fermentation of cellulose by Ruminococcus flavefaciens in the presence and absence of Methanobacterium ruminantium. Appl. Environ. Microbiol. 34 297– 301. 10.1128/aem.34.3.297-301.1977 562131 PMC242646 · DOI
  68. Le Van T. D. Robinson J. A. Ralph J. Greening R. C. Smolenski W. J. Leedle J. A. Z. (1998). Assessment of reductive acetogenesis with indigenous ruminal bacterium populations and Acetitomaculum ruminis. Appl. Environ. Microbiol. 64 3429– 3436. 10.1128/aem.64.9.3429-3436.1998 9726893 PMC106743 · DOI
  69. Lee S. J. Song H. Lee S. Y. (2006). Genome-based metabolic engineering of Mannheimia succiniciproducens for succinic acid production. Appl. Environ. Microbiol. 72 1939– 1948. 10.1128/AEM.72.3.1939-1948.2006 16517641 PMC1393240 · DOI
  70. Leng R. A. (2014). Interactions between microbial consortia in biofilms: a paradigm shift in rumen microbial ecology and enteric methane mitigation. Anim. Prod. Sci. 54 519– 543. 10.1071/AN13381 · DOI
  71. Leng R. A. Nolan J. V. (1984). Nitrogen metabolism in the rumen. J. Dairy Sci. 67 1072– 1089. 10.3168/jds.S0022-0302(84)81409-5 6376562 · DOI
  72. Li X. Z. Yan C. Choi S. H. Long R. Jin G. Song M. (2009). Effects of addition level and chemical type of propionate precursors in dicarboxylic acid pathway on fermentation characteristics and methane production by rumen microbes in vitro. Asian Aust. J. Anim. Sci. 22 82– 89. 10.5713/ajas.2009.80413 · DOI
  73. Lopez S. McIntosh F. M. Wallace R. J. Newbold C. J. (1999). Effect of adding acetogenic bacteria on methane production by mixed rumen microorganisms. Anim. Feed Sci. Technol. 78 1– 9. 10.1016/s0377-8401(98)00273-9 · DOI
  74. Lubner C. E. Peters J. W. (2017). Electron bifurcation makes the puzzle pieces fall energetically into place in methanogenic energy conservation. Chembiochem 18 2295– 2297. 10.1002/cbic.201700533 28986941 · DOI
  75. Lynch T. A. Wang Y. van Brunt B. Pacheco D. Janssen P. H. (2019). Modelling thermodynamic feedback on the metabolism of hydrogenotrophic methanogens. J. Theor. Biol. 477 14– 23. 10.1016/j.jtbi.2019.05.018 31150665 · DOI
  76. Mamuad L. Kim S. H. Jeong C. D. Choi Y. J. Jeon C. O. Lee S.-S. (2014). Effect of fumarate reducing bacteria on in vitro rumen fermentation, methane mitigation and microbial diversity. J. Microbiol. 52 120– 128. 10.1007/s12275-014-3518-1 24500476 · DOI
  77. Martin C. Morgavi D. P. Doreau M. (2010). Methane mitigation in ruminants: from microbe to the farm scale. Animal 4 351– 365. 10.1017/S1751731109990620 22443940 · DOI
  78. Martinez-Fernandez G. Denman S. E. Cheung J. McSweeney C. S. (2017). Phloroglucinol degradation in the rumen promotes the capture of excess hydrogen generated from methanogenesis inhibition. Front. Microbiol. 8: 1871. 10.3389/fmicb.2017.01871 29051749 PMC5633678 · DOI · Paper page
  79. Martinez-Fernandez G. Denman S. E. Yang C. Cheung J. Mitsumori M. McSweeney C. S. (2016). Methane inhibition alters the microbial community, hydrogen flow, and fermentation response in the rumen of cattle. Front. Microbiol. 7: 1122. 10.3389/fmicb.2016.01122 27486452 PMC4949212 · DOI
  80. Martinez-Fernandez G. Duval S. Kindermann M. Schirra H. J. Denman S. E. McSweeney C. S. (2018). 3-NOP vs. halogenated compound: methane production, ruminal fermentation and microbial community response in forage fed cattle. Front. Microbiol. 9: 1582. 10.3389/fmicb.2018.01582 30131771 PMC6090035 · DOI
  81. Marty R. J. Demeyer D. I. (1973). The effect of inhibitors of methane production on fermentation pattern and stoichiometry in vitro using rumen contents from sheep given molasses. Br. J. Nutr. 30 369– 376. 10.1079/bjn19730041 4746693 · DOI
  82. Marvin-Sikkema F. D. Richardson A. J. Stewart C. S. Gottschal J. C. Prins R. A. (1990). Influence of hydrogen-consuming bacteria on cellulose degradation by anaerobic fungi. Appl. Environ. Microbiol. 56 3793– 3797. 10.1128/aem.56.12.3793-3797.1990 2082826 PMC185069 · DOI
  83. Maxin G. Rulquin H. Glasser F. (2011). Response of milk fat concentration and yield to nutrient supply in dairy cows. Animal 5 1299– 1310. 10.1017/s1751731111000206 22440183 · DOI
  84. McGinn S. M. Beauchemin K. A. Coates T. Colombatto D. (2004). Methane emissions from beef cattle: effects of monensin, sunflower oil, enzymes, yeast, and fumaric acid. J. Anim. Sci. 82 3346– 3356. 10.2527/2004.82113346x 15542482 · DOI
  85. McKenzie R. A. Rayner A. C. Thompson G. K. Pidgeon G. F. Burren B. R. (2004). Nitrate-nitrite toxicity in cattle and sheep grazing Dactyloctenium radulans (button grass) in stockyards. Aust. Vet. J. 82 630– 634. 10.1111/j.1751-0813.2004.tb12612.x 15887389 · DOI
  86. Melgar A. Harper M. T. Oh J. Giallongo F. Young M. E. Ott T. L. (2019). Effects of 3-nitrooxypropanol on rumen fermentation, lactational performance, and resumption of ovarian cyclicity in dairy cows. J. Dairy Sci. 103 410– 432. 10.3168/jds.2019-17085 31733848 · DOI
  87. Miller T. L. Wolin M. J. (2001). Inhibition of growth of methane-producing bacteria of the Ruminant Forestomach by Hydroxymethylglutaryl SCoA reductase inhibitors. J. Dairy Sci. 84 1445– 1448. 10.3168/jds.S0022-0302(01)70177-4 11417704 · DOI
  88. Mitchell A. D. Chappell A. Knox K. L. (1979). Metabolism of Betaine in the Ruminant. J. Anim. Sci. 49 764– 774. 10.2527/jas1979.493764x 528435 · DOI
  89. Mohammed N. Lila Z. A. Ajisaka N. Hara K. Mikuni K. Hara K. (2004). Inhibition of ruminal microbial methane production by β-cyclodextrin iodopropane, malate and their combination in vitro. J. Anim. Physiol. Anim. Nutr. 88 188– 195. 10.1111/j.1439-0396.2004.00456.x 15189423 · DOI
  90. Morgavi D. P. Forano E. Martin C. Newbold C. J. (2010). Microbial ecosystem and methanogenesis in ruminants. Animal 4 1024– 1036. 10.1017/S1751731110000546 22444607 · DOI · Paper page
  91. Muñoz-Tamayo R. Popova M. Tillier M. Morgavi D. P. Morel J. P. Fonty G. (2019). Hydrogenotrophic methanogens of the mammalian gut: functionally similar, thermodynamically different-A modelling approach. PLoS One 14: e0226243. 10.1371/journal.pone.0226243 31826000 PMC6905546 · DOI
  92. Neill A. R. Grime D. W. Dawson R. M. (1978). Conversion of choline methyl groups through trimethylamine into methane in the rumen. Biochem. J. 170 529– 535. 10.1042/bj1700529 646798 PMC1183928 · DOI
  93. Newbold C. J. Lopez S. Nelson N. Ouda J. O. Wallace R. J. Moss A. R. (2005). Propionate precursors and other metabolic intermediates as possible alternative electron acceptors to methanogenesis in ruminal fermentation in vitro. Br. J. Nutr. 94 27– 35. 10.1079/bjn20051445 16115329 · DOI
  94. Nitschke W. Russell M. J. (2012). Redox bifurcations: mechanisms and importance to life now, and at its origin: a widespread means of energy conversion in biology unfolds. Bioessays 34 106– 109. 10.1002/bies.201100134 22045626 · DOI
  95. Nollet L. Demeyer D. I. 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. Appl. Environ. Microbiol. 63 194– 200. 10.1128/aem.63.1.194-200.1997 8979351 PMC168314 · DOI
  96. Noziere P. Martin C. Remond D. Kristensen N. B. Bernard R. Doreau M. (2000). Effect of composition of ruminally-infused short-chain fatty acids on net fluxes of nutrients across portal-drained viscera in underfed ewes. Br. J. Nutr. 83 521– 531. 10.1017/s0007114500000660 10953677 · DOI
  97. Oba M. Allen M. S. (2003). Dose-response effects of intrauminal infusion of propionate on feeding behavior of lactating cows in early or midlactation. J. Dairy Sci. 86 2922– 2931. 10.3168/jds.S0022-0302(03)73889-2 14507028 · DOI
  98. Patra A. Park T. Kim M. Yu Z. (2017). Rumen methanogens and mitigation of methane emission by anti-methanogenic compounds and substances. J. Anim. Sci. Biotechnol. 8: 13. 10.1186/s40104-017-0145-9 28149512 PMC5270371 · DOI
  99. Patra A. K. Yu Z. (2013). Effects of gas composition in headspace and bicarbonate concentrations in media on gas and methane production, degradability, and rumen fermentation using in vitro gas production techniques. J. Dairy Sci. 96 4592– 4600. 10.3168/jds.2013-6606 23684023 · DOI
  100. Pavlostathis S. G. Miller T. L. Wolin M. J. (1990). Cellulose fermentation by continuous cultures of Ruminococcus albus and Methanobrevibacter smithii. Appl. Microbiol. Biotechnol. 33 109– 116. 10.1007/bf00170581 · DOI
  101. Petersen S. O. Hellwing A. L. Brask M. Hojberg O. Poulsen M. Zhu Z. (2015). Dietary nitrate for methane mitigation leads to nitrous oxide emissions from dairy cows. J. Environ. Qual. 44 1063– 1070. 10.2134/jeq2015.02.0107 26437087 · DOI
  102. Pol A. Demeyer D. I. (1988). Fermentation of methanol in the sheep rumen. Appl. Environ. Microbiol. 54 832– 834. 10.1128/aem.54.3.832-834.1988 3377496 PMC202551 · DOI
  103. Pradhan K. Hemken R. W. (1970). Utilization of ethanol and its effect on fatty acid patterns in ruminants. J. Dairy Sci. 53 1739– 1746. 10.3168/jds.S0022-0302(70)86472-4 5530981 · DOI
  104. Qiao J. Y. Tana Z. L. Guan L. L. Tang S. X. Zhou C. S. Hana X. F. (2015). Effects of hydrogen in headspace and bicarbonate in media onrumen fermentation, methane production and methanogenic population using in vitro gas production techniques. Anim. Feed Sci. Technol. 206 19– 28. 10.1016/j.anifeedsci.2015.05.004 · DOI
  105. Ragsdale S. W. Pierce E. (2008). Acetogenesis and the Wood–Ljungdahl pathway of CO2 fixation. Biochim. Biophys. Acta 1784 1873– 1898. 10.1016/j.bbapap.2008.08.012 18801467 PMC2646786 · DOI
  106. Raju P. (2016). Homoacetogenesis as an Alternative Hydrogen Sink in the Rumen. Ph.D. thesis, University of Massey, Auckland.
  107. Riede S. Boguhn J. Breves G. (2013). Studies on potential effects of fumaric acid on rumen microbial fermentation, methane production and microbial community. Arch. Anim. Nutr. 67 368– 380. 10.1080/1745039x.2013.830518 23971537 · DOI
  108. Robinson J. A. Strayer R. F. Tiedje J. M. (1981). Method for measuring dissolved hydrogen in anaerobic ecosystems: application to the rumen. Appl. Environ. Microbiol. 41 545– 548. 10.1128/aem.41.2.545-548.1981 7235697 PMC243729 · DOI
  109. Rook J. A. Balch C. C. Campling R. C. Fisher L. J. (1963). The utilization of acetic, propionic and butyric acids by growing heifers. Br. J. Nutr. 17 399– 406. 10.1079/bjn19630043 14045342 · DOI
  110. Rooke J. A. Wallace R. J. Duthie C. A. McKain N. de Souza S. M. Hyslop J. J. (2014). Hydrogen and methane emissions from beef cattle and their rumen microbial community vary with diet, time after feeding and genotype. Br. J. Nutr. 112 398– 407. 10.1017/s0007114514000932 24780126 · DOI
  111. Russell J. B. (1991). Intracellular pH of acid-tolerant ruminal bacteria. Appl. Environ. Microbiol. 57 3383– 3384. 10.1128/aem.57.11.3383-3384.1991 1781695 PMC183976 · DOI
  112. Russell J. B. (1998). The importance of pH in the regulation of ruminal acetate to propionate ratio and methane production in vitro. J. Dairy Sci. 81 3222– 3230. 10.3168/jds.s0022-0302(98)75886-2 9891267 · DOI · Paper page
  113. Russell J. B. Baldwin R. L. (1978). Substrate preferences in rumen bacteria: evidence of catabolite regulatory mechanisms. Appl. Environ. Microbiol. 36 319– 329. 10.1128/aem.36.2.319-329.1978 16345311 PMC291221 · DOI
  114. Russell J. B. Baldwin R. L. (1979). Comparison of substrate affinities among several rumen bacteria: a possible determinant of rumen bacterial competition. Appl. Environ. Microbiol. 37 531– 536. 10.1128/aem.37.3.531-536.1979 16345358 PMC243250 · DOI
  115. Russell J. B. Wallace R. J. (1997). “ Energy-yielding and energy-consuming reactions,” in The Rumen Microbial Ecosystem, eds Hobson P. N. Stewart C. S., (London: Blackie Academic & Professional), 246– 282. 10.1007/978-94-009-1453-7_6 · DOI
  116. Sauer F. D. Teather R. M. (1987). Changes in oxidation reduction potentials and volatile fatty acids production by rumen bacteria when methane synthesis is inhibited. J. Dairy Sci. 70 1835– 1840. 10.3168/jds.s0022-0302(87)80222-9 2822785 · DOI
  117. Scheller H. V. Ulvskov P. (2010). Hemicelluloses. Annu. Rev. Plant Biol. 61 263– 289. 10.1146/annurev-arplant-042809-112315 20192742 · DOI
  118. Schulman M. D. Valentino D. (1976). Factors influencing rumen fermentation: effect of hydrogen on formation of propionate. J. Dairy Sci. 59 1444– 1451. 10.3168/jds.s0022-0302(76)84383-4 956483 · DOI
  119. Seeliger S. Janssen P. H. Schink B. (2002). Energetics and kinetics of lactate fermentation to acetate and propionate via methylmalonyl-CoA or acrylyl-CoA. FEMS Microbiol. Lett. 211 65– 70. 10.1111/j.1574-6968.2002.tb11204.x 12052552 · DOI
  120. Shabat S. K. Sasson G. Doron-Faigenboim A. Durman T. Yaacoby S. Berg Miller M. E. (2016). Specific microbiome-dependent mechanisms underlie the energy harvest efficiency of ruminants. ISME J. 10 2958– 2972. 10.1038/ismej.2016.62 27152936 PMC5148187 · DOI · Paper page
  121. Sheperd A. C. Combs D. K. (1998). Long-term effects of acetate and propionate on voluntary feed intake by midlactation cows. J. Dairy Sci. 81 2240– 2250. 10.3168/jds.s0022-0302(98)75803-5 9749390 · DOI
  122. Slyter L. L. (1979). Monensin and dichloroacetamide influences on methane and volatile fatty acid production by rumen bacteria in vitro. Appl. Environ. Microbiol. 37 283– 288. 10.1128/aem.37.2.283-288.1979 16345344 PMC243201 · DOI
  123. Smolenski W. J. Robinson J. A. (1988). In situ rumen hydrogen concentrations in steers fed eight times daily, measured using a mercury reduction detector. FEMS Microbiol. Ecol. 4 95– 100. 10.1111/j.1574-6968.1988.tb02652.x · DOI
  124. Snelling T. J. Wallace R. J. (2017). The rumen microbial metaproteome as revealed by SDS-PAGE. BMC Microbiol. 17: 9. 10.1186/s12866-016-0917-y 28061817 PMC5219685 · DOI
  125. Söllinger A. Tveit A. T. Poulsen M. Noel S. J. Bengtsson M. Bernhardt J. (2018). Holistic assessment of rumen microbiome dynamics through quantitative metatranscriptomics reveals multifunctional redundancy during key steps of anaerobic feed degradation. mSystems 3: e00038-18. 10.1128/mSystems.00038-18 30116788 PMC6081794 · DOI
  126. Søndergaard D. Pedersen C. N. S. Greening C. (2016). HydDB: a web tool for hydrogenase classification and analysis. Sci. Rep. 6: 34212. 10.1038/srep34212 27670643 PMC5037454 · DOI
  127. Stanier G. Davies A. (1981). Effects of the antibiotic monensin and an inhibitor of methanogenesis on in vitro continuous rumen fermentations. Br. J. Nutr. 45 567– 578. 10.1079/bjn19810135 7236582 · DOI
  128. Storm A. C. Kristensen N. B. Hanigan M. D. (2012). A model of ruminal volatile fatty acid absorption kinetics and rumen epithelial blood flow in lactating Holstein cows. J. Dairy Sci. 95 2919– 2934. 10.3168/jds.2011-4239 22612930 · DOI
  129. St-Pierre B. Cersosimo L. M. Ishaq S. L. Wright A. D. (2015). Toward the identification of methanogenic archaeal groups as targets of methane mitigation in livestock animals. Front. Microbiol. 6: 776 10.3389/fmicb.2015.00776 PMC4519756 26284054 · DOI
  130. Tatsuoka N. Hara K. Mikuni K. Hara K. Hashimoto H. Itabashi H. (2008). Effects of the essential oil cyclodextrin complexes on ruminal methane production in vitro. Anim. Sci. J. 79 68– 75. 10.1111/j.1740-0929.2007.00499.x · DOI
  131. Thauer R. K. Kaster A. K. Seedorf H. Buckel W. Hedderich R. (2008). Methanogenic archaea: ecologically relevant differences in energy conservation. Nat. Rev. Microbiol. 6 579– 591. 10.1038/nrmicro1931 18587410 · DOI · Paper page
  132. Ungerfeld E. M. (2015a). Limits to dihydrogen incorporation into electron sinks alternative to methanogenesis in ruminal fermentation. Front. Microbiol. 6: 1272. 10.3389/fmicb.2015.01272 26635743 PMC4649033 · DOI
  133. Ungerfeld E. M. (2015b). Shifts in metabolic hydrogen sinks in the methanogenesis-inhibited ruminal fermentation: a meta-analysis. Front. Microbiol. 6: 37 10.3389/fmicb.2015.00037 PMC4316778 25699029 · DOI
  134. Ungerfeld E. M. (2018). Inhibition of rumen methanogenesis and ruminant productivity: a meta-analysis. Front. Vet. Sci. 5: 113 10.3389/fvets.2018.00113 PMC6018482 29971241 · DOI
  135. Ungerfeld E. M. Aedo M. F. Martínez E. D. Saldivia M. (2019). Inhibiting methanogenesis in Rumen batch cultures did not increase the recovery of metabolic hydrogen in microbial amino acids. Microorganisms 7: 115 10.3390/microorganisms7050115 PMC6560395 31035537 · DOI
  136. Ungerfeld E. M. Rust S. R. Burnett R. (2003). Use of some novel alternative electron sinks to inhibit ruminal methanogenesis. Reprod. Nutr. Dev. 43 189– 202. 10.1051/rnd:2003016 12956318 · DOI
  137. Ungerfeld E. M. Rust S. R. Burnett R. (2006). Effects of butyrate precursors on electron relocation when methanogenesis is inhibited in ruminal mixed cultures. Lett. Appl. Microbiol. 42 567– 572. 16706893
  138. Urrutia N. Bomberger R. Matamoros C. Harvatine K. J. (2019). Effect of dietary supplementation of sodium acetate and calcium butyrate on milk fat synthesis in lactating dairy cows. J. Dairy Sci. 102 5172– 5181. 10.3168/jds.2018-16024 30981489 PMC6564677 · DOI
  139. Van Lingen H. J. Edwards J. E. Vaidya J. D. Van Gastelen S. Saccenti E. Van den Bogert B. (2017). Diurnal dynamics of gaseous and dissolved metabolites and microbiota composition in the bovine rumen. Front. Microbiol. 8: 425. 10.3389/fmicb.2017.00425 28367142 PMC5355475 · DOI
  140. Van Lingen H. J. Fadel J. G. Moraes L. E. Bannink A. Dijkstra J. (2019). Bayesian mechanistic modeling of thermodynamically controlled volatile fatty acid, hydrogen and methane production in the bovine rumen. J. Theor. Biol. 480 150– 165. 10.1016/j.jtbi.2019.08.008 31401059 · DOI
  141. Van Lingen H. J. Plugge C. M. Fadel J. G. Kebreab E. Bannink A. Dijkstra J. (2016). Thermodynamic driving force of hydrogen on rumen microbial metabolism: a theoretical investigation. PLoS One 11: e0161362. 10.1371/journal.pone.0161362 27783615 PMC5081179 · DOI
  142. Van Zijderveld S. M. Gerrits W. J. J. Apajalahti J. A. Newbold J. R. Dijkstra J. Leng R. A. (2010). Nitrate and sulfate: effective alternative hydrogen sinks for mitigation of ruminal methane production in sheep. J. Dairy Sci. 93 5856– 5866. 10.3168/jds.2010-3281 21094759 · DOI
  143. Vanwonterghem I. Evans P. N. Parks D. H. Jensen P. D. Woodcroft B. J. Hugenholtz P. (2016). Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota. Nat. Microbiol. 1: 16170. 10.1038/nmicrobiol.2016.170 27694807 · DOI
  144. Vercoe J. E. Blaxter K. L. (1965). The metabolism of formic acid in sheep. Br. J. Nutr. 19 523– 530. 10.1079/bjn19650047 5852119 · DOI
  145. Voet D. Voet J. G. (1995). Biochemistry. New York, NY: John Wiley & Sons, Inc.
  146. Vyas D. Alazzeh A. McGinn S. M. McAllister T. A. Harstad O. M. Holo H. (2016). Enteric methane emissions in response to ruminal inoculation of Propionibacterium strains in beef cattle fed a mixed diet. Anim. Prod. Sci. 56 1035– 1040. 10.1071/AN14801 · DOI
  147. Vyas D. McGeough E. J. McGinn S. M. McAllister T. A. Beauchemin K. A. (2014a). Effect of Propionibacterium spp. on ruminal fermentation, nutrient digestibility, and methane emissions in beef heifers fed a high-forage diet. J. Anim. Sci. 92 2192– 2201. 10.2527/jas.2013-7492 24663192 · DOI
  148. Vyas D. McGeough E. J. Mohammed R. McGinn S. M. McAllister T. A. Beauchemin K. A. (2014b). Effects of Propionibacterium strains on ruminal fermentation, nutrient digestibility and methane emissions in beef cattle fed a corn grain finishing diet. Animal 8 1807– 1815. 10.1017/s1751731114001657 25322788 · DOI
  149. Waldrip H. M. Martin S. A. (1993). Effects of an Aspergillus oryzae fermentation extract and other factors on lactate utilization by the ruminal bacterium Megasphaera elsdenii. J. Anim. Sci. 71 2770– 2776. 10.2527/1993.71102770x 8226379 · DOI
  150. Wallace R. J. Onodera R. Cotta M. A. (1997). “ Metabolism of nitrogen-containing compounds,” in The Rumen Microbial Ecosystem, eds Hobson P. N. Stewart C. S., (London: Blackie Academic & Professional), 283– 328. 10.1007/978-94-009-1453-7_7 · DOI · Paper page
  151. Wang M. Ungerfeld E. M. Wang R. Zhou C. S. Basang Z. Z. Ao S. M. (2016). Supersaturation of dissolved hydrogen and methane in rumen of Tibetan sheep. Front. Microbiol. 7: 850. 10.3389/fmicb.2016.00850 27379028 PMC4906022 · DOI
  152. Wang M. Wang R. Zhang X. M. Ungerfeld E. M. Long D. Mao H. X. (2017). Molecular hydrogen generated by elemental magnesium supplementation alters rumen fermentation and microbiota in goats. Br. J. Nutr. 118 401– 410. 10.1017/S0007114517002161 28927478 · DOI
  153. Wang R. Wang M. Ungerfeld E. M. Zhang X. M. Long D. L. Mao H. X. (2018). Nitrate improves ammonia incorporation into rumen microbial protein in lactating dairy cows fed a low-protein diet. J. Dairy Sci. 101 9789– 9799. 10.3168/jds.2018-14904 30172398 · DOI
  154. Weiss W. P. (2017). A 100-year review: from ascorbic acid to zinc—Mineral and vitamin nutrition of dairy cows. J. Dairy Sci. 100 10045– 10060. 10.3168/jds.2017-12935 29153154 · DOI
  155. Wenner B. A. de Souza J. Batistel F. Hackmann T. J. Yu Z. Firkins J. L. (2017). Association of aqueous hydrogen concentration with methane production in continuous cultures modulated to vary pH and solids passage rate. J. Dairy Sci. 100 5378– 5389. 10.3168/jds.2016-12332 28456412 · DOI
  156. Wood T. A. Wallace R. J. Rowe A. Price J. Yáñez-Ruiz D. R. Murray P. (2009). Encapsulated fumaric acid as a feed ingredient to decrease ruminal methane emissions. Anim. Feed Sci. Technol. 152 62– 71. 10.1016/j.anifeedsci.2009.03.006 · DOI
  157. Yang C. J. Mao S. Y. Long L. M. Zhu W. Y. (2012). Effect of disodium fumarate on microbial abundance, ruminal fermentation and methane emission in goats under different forage: concentrate ratios. Animal 6 1788– 1794. 10.1017/s1751731112000857 22717128 · DOI
  158. Zheng Y. Kahnt J. Kwon I. H. Mackie R. I. Thauer R. K. (2014). Hydrogen formation and its regulation in Ruminococcus albus: involvement of an electron-bifurcating [FeFe]-hydrogenase, of a non-electron-bifurcating [FeFe]-hydrogenase, and of a putative hydrogen-sensing [FeFe]-hydrogenase. J. Bacteriol. 196 3840– 3852. 10.1128/jb.02070-14 25157086 PMC4248817 · DOI

Cited by

Sorted by citations

Authors
Ungerfeld, E. M.
Affiliations
Instituto de Investigaciones Agropecuarias (CL)
Corresponding author
Ungerfeld, Emilio M.
ORCID
Ungerfeld, Emilio M.
Venue
Frontiers in Microbiology
Publisher
Frontiers Media SA
Published
2020-04-15
Volume
11
Pages
589-589
ISSN
1664-302X (ISSN-L)
DOI
10.3389/fmicb.2020.00589
PMC
PMC7174568
OpenAlex
W3017330954
Cited by
472
References
9
Citations by year
2026: 129 · 2025: 110 · 2024: 81 · 2023: 66 · 2022: 55 · 2021: 27 · 2020: 4
FWCI
47.52
Type
journal article
Language
en
Open access
Licence
Locations
  • Frontiers in Microbiology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Comisión Nacional de Investigación Científica y Tecnológica
Topics
  • Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Ruminant Nutrition and Digestive Physiology
  • Physical Sciences › Engineering › Building and Construction › Anaerobic Digestion and Biogas Production
  • Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Nutrition and Physiology
Keywords
rumen fermentation, methanogenesis, methane mitigation, volatile fatty acids, methanogenic archaea, electron acceptors, direct-fed microbials, kinetic modeling, ruminant nutrition, microbial additives

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