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Hydrogen production and hydrogen utilization in the rumen: key to mitigating enteric methane production

Mackie Roderick I.|Kim Hyewon|Kim Na Kyung|Cann Isaac
아세아·태평양축산학회 (Asian-Australasian Association Of Animal Production Societies)|2024.02|Animal Bioscience|제37권 제2호|pp. 323-336|DOI 10.5713/ab.23.0294

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MethaneHydrogenRumenEnteric Methane MitigationFormateInterspecies Hydrogen Transfer

초록

Molecular hydrogen (H<sub>2</sub>) and formate (HCOO<sup>-</sup>) are metabolic end products of many primary fermenters in the rumen ecosystem. Both play a vital role in fermentation where they are electron sinks for individual microbes in an anaerobic environment that lacks external electron acceptors. If H<sub>2</sub> and/or formate accumulate within the rumen, the ability of primary fermenters to regenerate electron carriers may be inhibited and microbial metabolism and growth disrupted. Consequently, H<sub>2</sub>- and/or formate-consuming microbes such as methanogens and possibly homoacetogens play a key role in maintaining the metabolic efficiency of primary fermenters. There is increasing interest in identifying approaches to manipulate the rumen ecosystem for the benefit of the host and the environment. As H<sub>2</sub> and formate are important mediators of interspecies interactions, an understanding of their production and utilization could be a significant starting point for the development of successful interventions aimed at redirecting electron flow and reducing methane emissions. We conclude by discussing in brief ruminant methane mitigation approaches as a model to help understand the fate of H<sub>2</sub> and formate in the rumen ecosystem.

Abstract

Molecular hydrogen (H2) and formate (HCOO– ) are metabolic end products of many primary fermenters in the rumen ecosystem. Both play a vital role in fermentation where they are electron sinks for individual microbes in an anaerobic environment that lacks external electron acceptors. If H2 and/or formate accumulate within the rumen, the ability of primary fermenters to regenerate electron carriers may be inhibited and microbial metabolism and growth disrupted. Consequently, H2- and/or formate-consuming microbes such as methanogens and possibly homoacetogens play a key role in maintaining the metabolic efficiency of primary fermenters. There is increasing interest in identifying approaches to manipulate the rumen ecosystem for the benefit of the host and the environment. As H2 and formate are important mediators of interspecies interactions, an understanding of their production and utilization could be a significant starting point for the development of successful interventions aimed at redirecting electron flow and reducing methane emissions. We conclude by discussing in brief ruminant methane mitigation approaches as a model to help understand the fate of H2 and formate in the rumen ecosystem.

참고문헌 (74)

  1. Terry SA, "Improving rumen function", pp.505~546 (2020), Burleigh Dodds Science Publishing
  2. McAllister TA, "Ruminant nutrition symposium : use of genomics and transcriptomics to identify strategies to lower ruminal methanogenesis", J Anim Sci, 93, pp.1431~1449 (2015)[DOI]
  3. Arndt C, "Full adoption of the most effective strategies to mitigate methane emissions by ruminants can help meet the 1. 5°C target by 2030 but not 2050", Proc Natl Acad Sci, 119, pp.e2111294119~ (2022)[DOI]
  4. Tackling climate change through livestock: a global assessment of emissions and mitigation opportunities, "Gerber PJ", Food and Agriculture Organization of the United Nations (FAO), ~ (2013)
  5. Bryant MP, "Microbial methane production—theoretical aspects", J Anim Sci, 48, pp.193~201 (1979)[DOI]
  6. Mackie RI, "Methanogenesis, biochemistry", Encycl Microbiol, 3, pp.97~109 (1992)
  7. Wolin MJ, "The rumen microbial ecosystem", pp.467~491 (1997), Springer
  8. Ungerfeld EM, "Metabolic hydrogen flows in rumen fermentation : principles and possibilities of interventions", Front Microbiol, 11, pp.589~ (2020)[DOI]
  9. Hungate RE, "Formate as an intermediate in the bovine rumen fermentation", J Bacteriol, 102, pp.389~397 (1970)[DOI]
  10. Leahy SC, "Electron flow : key to mitigating ruminant methanogenesis", Trends Microbiol, 30, pp.209~212 (2022)[DOI]
  11. Wolin MJ, "Fermentation in the rumen and human large intestine", Science, 213, pp.1463~1468 (1981)[DOI]
  12. Söllinger A, "Methylotrophic methanogens everywhere — physiology and ecology of novel players in global methane cycling", Biochem Soc Trans, 47, pp.1895~1907 (2019)[DOI]
  13. Duin EC, "Mode of action uncovered for the specific reduction of methane emissions from ruminants by the small molecule 3-nitrooxypropanol", Proc Natl Acad Sci, 113, pp.6172~6177 (2016)[DOI]
  14. Martinez-Fernandez G, "3-NOP vs. halogenated compound : methane production, ruminal fermentation and microbial community response in forage fed cattle", Front Microbiol, 9, pp.1582~ (2018)[DOI]
  15. Vijn S, "Key considerations for the use of seaweed to reduce enteric methane emissions from cattle", Front Vet Sci, 7, pp.597430~ (2020)[DOI]
  16. Poulsen M, "Methylotrophic methanogenic Thermoplasmata implicated in reduced methane emissions from bovine rumen", Nat Commun, 4, pp.1428~ (2013)[DOI]
  17. Söllinger A, "Holistic assessment of rumen microbiome dynamics through quantitative metatranscriptomics reveals multifunctional redundancy during key steps of anaerobic feed degradation", mSystems, 3 (2018)[DOI]
  18. Shi W, "Methane yield phenotypes linked to differential gene expression in the sheep rumen microbiome", Genome Res, 24, pp.1517~1525 (2014)[DOI]
  19. Li F, "Metatranscriptomic profiling reveals linkages between the active rumen microbiome and feed efficiency in beef cattle", Appl Environ Microbiol, 83, pp.e00061-17~ (2017)[DOI]
  20. Hungate R, "Hydrogen as an intermediate in the rumen fermentation", Arch Mikrobiol, 59, pp.158~164 (1967)[DOI]
  21. Zinder SH, "Methanogenesis: ecology, physiology, biochemistry and genetics", pp.128~206 (1993), Springer
  22. Iannotti EL, "Glucose fermentation products of Ruminococcus albus grown in continuous culture with Vibrio succinogenes : changes caused by interspecies transfer of H2", J Bacteriol, 114, pp.1231~1240 (1973)[DOI]
  23. Greening C, "Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival", ISME J, 10, pp.761~777 (2016)[DOI]
  24. -hydrogenases into three structural and functional groups, "Biochim Biophys Acta Gen Subj", 2016, 1910~1921 (1860), 10.1016[DOI]
  25. Vignais PM, "Occurrence, classification, and biological function of hydrogenases : an overview", Chem Rev, 107, pp.4206~4272 (2007)[DOI]
  26. Buckel W, "Energy conservation via electron bifurcating ferredoxin reduction and proton", Na+ translocating ferredoxin oxidation, 2013, pp.1827, 94~113
  27. -hydrogenase, "J Bacteriol", 2014, 3840~3852, 10.1128[DOI]
  28. Greening C, "Diverse hydrogen production and consumption pathways influence methane production in ruminants", ISME J, 13, pp.2617~2632 (2019)[DOI]
  29. Seshadri R, "Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection", Nat Biotechnol, 36, pp.359~367 (2018)[DOI]
  30. Kelly WJ, "Hydrogen and formate production and utilisation in the rumen and the human colon", Anim Microbiome, 4, pp.22~ (2022)[DOI]
  31. Belzer C, "Nutritional strategies for mucosal health : the interplay between microbes and mucin glycans", Trends Microbiol, 30, pp.13~21 (2022)[DOI]
  32. Bergman EN, "Energy contributions of volatile fatty acids from the gastrointestinal tract in various species", Physiol Rev, 70, pp.567~590 (1990)[DOI]
  33. Modesto A, "Meta-analysis of the composition of human intestinal gases", Dig Dis Sci, 67, pp.3842~3859 (2022)[DOI]
  34. Sahakian AB, "Methane and the gastrointestinal tract", Dig Dis Sci, 55, pp.2135~2143 (2010)[DOI]
  35. Polag D, "Global methane emissions from the human body : Past, present and future", Atmos Environ, 214, pp.116823~ (2019)[DOI]
  36. Kumpitsch C, "Reduced B12 uptake and increased gastrointestinal formate are associated with archaeome-mediated breath methane emission in humans", Microbiome, 9, pp.193~ (2021)[DOI]
  37. Janssen PH, "Influence of hydrogen on rumen methane formation and fermentation balances through microbial growth kinetics and fermentation thermodynamics", Anim Feed Sci Technol, 160, pp.1~22 (2010)[DOI]
  38. Xie F, "An integrated gene catalog and over 10, 000 metagenome-assembled genomes from the gastro-intestinal microbiome of ruminants", Microbiome, 9, pp.137~ (2021)[DOI]
  39. Newbold CJ, "The role of ciliate protozoa in the rumen", Front Microbiol, 6, pp.1313~ (2015)[DOI]
  40. Hess M, "Anaerobic fungi : past, present, and future", Front Microbiol, 11, pp.584893~ (2020)[DOI]
  41. Henderson G, "Presence of novel, potentially homoacetogenic bacteria in the rumen as determined by analysis of formyltetrahydrofolate synthetase sequences from ruminants", Appl Environ Microbiol, 76, pp.2058~2066 (2010)[DOI]
  42. Gagen EJ, "Functional gene analysis suggests different acetogen populations in the bovine rumen and tammar wallaby forestomach", Appl Environ Microbiol, 76, pp.7785~7795 (2010)[DOI]
  43. Mackie RI, "Acetogenesis", pp.331~364 (1994), Springer
  44. Van Zijderveld SM, "Nitrate and sulfate : Effective alternative hydrogen sinks for mitigation of ruminal methane production in sheep", J Dairy Sci, 93, pp.5856~5866 (2010)[DOI]
  45. Leng RA, "Interactions between microbial consortia in biofilms : a paradigm shift in rumen microbial ecology and enteric methane mitigation", Anim Prod Sci, 54, pp.519~543 (2014)[DOI]
  46. Wolin MJ, "A theoretical rumen fermentation balance", J Dairy Sci, 43, pp.1452~1459 (1960)[DOI]
  47. Nakamura N, "Mechanisms of microbial hydrogen disposal in the human colon and implications for health and disease", Annu Rev Food Sci Technol, 1, pp.363~395 (2010)[DOI]
  48. Hylemon PB, "Metabolism of hydrogen gases and bile acids in the gut microbiome", FEBS Lett, 592, pp.2070~2082 (2018)[DOI]
  49. Czerkawski JW, "Methane production in ruminants and its significance", World Rev Nutr Diet, 11, pp.240~282 (1969)[DOI]
  50. Reisinger A, "How necessary and feasible are reductions of methane emissions from livestock to support stringent temperature goals?", Philos Trans R Soc A Math Phys Eng Sci, 379, pp.20200452~ (2021)[DOI]
  51. Xu X, "Global greenhouse gas emissions from animal-based foods are twice those of plant-based foods", Nat Food, 2, pp.724~732 (2021)[DOI]
  52. IPCC CC, "The physical science basis. Contribution of working group I to the fourth assessment report of the Intergovernmental Panel on Climate Change", pp.113~119 (2007), Cambridge University Press
  53. Beauchemin KA, "Fifty years of research on rumen methanogenesis : Lessons learned and future challenges for mitigation", Animal, 14(S1), pp.s2~s16 (2020)[DOI]
  54. Almeida AK, "Meta-analysis quantifying the potential of dietary additives and rumen modifiers for methane mitigation in ruminant production systems", Anim Nutr, 7, pp.1219~1230 (2021)[DOI]
  55. Mizrahi I, "The rumen microbiome : balancing food security and environmental impacts", Nat Rev Microbiol, 19, pp.553~566 (2021)[DOI]
  56. Johnson KA, "Methane emissions from cattle", J Anim Sci, 73, pp.2483~2492 (1995)[DOI]
  57. Pinares-Patiño CS, "Heritability estimates of methane emissions from sheep", Animal, 7, pp.316~321 (2013)[DOI]
  58. Rowe S, "Selection for divergent methane yield in New Zealand sheep–a ten-year perspective", Proc Assoc Advmt Anim Breed Genet, 23, pp.306~309 (2019)
  59. Pinares-Patiño C, "Is rumen retention time implicated in sheep differences in methane emission", Proceedings of the New Zealand Society of Animal Production (2011), New Zealand Society of Animal Production
  60. Goopy JP, "Low-methane yield sheep have smaller rumens and shorter rumen retention time", Br J Nutr, 111, pp.578~585 (2014)[DOI]
  61. Kittelmann S, "Two different bacterial community types are linked with the low-methane emission trait in sheep", PLoS One, 9, pp.e103171~ (2014)[DOI]
  62. Kamke J, "Rumen metagenome and metatranscriptome analyses of low methane yield sheep reveals a Sharpea-enriched microbiome characterised by lactic acid formation and utilisation", Microbiome, 4, pp.56~ (2016)[DOI]
  63. Joblin KN, "Ruminal acetogens and their potential to lower ruminant methane emissions", Aust J Agric Res, 50, pp.1307~1314 (1999)[DOI]
  64. Jeyanathan J, "The use of direct-fed microbials for mitigation of ruminant methane emissions : a review", Animal, 8, pp.250~261 (2014)[DOI]
  65. Leng RA, "Unravelling methanogenesis in ruminants, horses and kangaroos : the links between gut anatomy, microbial biofilms and host immunity", Anim Prod Sci, 58, pp.1175~1191 (2018)[DOI]
  66. Baca-González V, "Are vaccines the solution for methane emissions from ruminants? A systematic review", Vaccines, 8, pp.460~ (2020)[DOI]
  67. Kelly WJ, "Occurrence and expression of genes encoding methyl-compound production in rumen bacteria", Anim Microbiome, 1, pp.15~ (2019)[DOI]
  68. Muetzel S, "Methane emissions from sheep fed fresh pasture", NZ J Agric Res, 58, pp.472~489 (2015)[DOI]
  69. Alam KY, "Anaerobic fermentation balance of Escherichia coli as observed by in vivo nuclear magnetic resonance spectroscopy", J Bacteriol, 171, pp.6213~6217 (1989)[DOI]
  70. Tiffany CR, "The metabolic footprint of Clostridia and Erysipelotrichia reveals their role in depleting sugar alcohols in the cecum", Microbiome, 9, pp.174~ (2021)[DOI]
  71. Sun X, "Lambs fed fresh winter forage rape(Brassica napus L. )emit less methane than those fed perennial ryegrass(Lolium perenne L. ), and possible mechanisms behind the difference", PLoS One, 10, pp.e0119697~ (2015)[DOI]
  72. Sun XZ, "Invited review : Glucosinolates might result in low methane emissions from ruminants fed Brassica forages", Front Vet Sci, 7, pp.588051~ (2020)[DOI]
  73. Mackie RI, "Encyclopedia of Life Sciences" (2013), John Wiley & Sons, Ltd
  74. Beauchemin KA, "Invited review : Current enteric methane mitigation options", J Dairy Sci, 105, pp.9297~9326 (2022)[DOI]

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