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Effect of Nitrooxy Compounds with Different Molecular Structures on the Rumen Methanogenesis, Metabolic Profile, and Methanogenic Community

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Abstract

Rumen in vitro fermentation was used to evaluate the capacity of nitrooxy compounds to mitigate rumen methane production. The following three nitrooxy compounds, each with different molecular structures, were evaluated: 2,2-dimethyl-3-(nitrooxy) propanoic (DNP), N-[2-(Nitrooxy)ethyl]-3-pyridinecarboxamide (NPD), and nitroglycerin (NG). All three compounds substantially decreased the total gas production, methane production, and the acetate:propionate ratio, while increasing hydrogen production. The growth of methanogens was specifically inhibited by all three compounds, without affecting the abundance of bacteria, anaerobic fungi, or protozoa. However, inhibition of methanogenesis required a much higher dose of DNP when compared to NPD or NG. Further investigations were conducted on NG to determine its effects on the methanogenic community. NG reduced the relative abundance of Methanomassiliicoccales, while increasing the relative abundance of Methanobrevibacter and Methanosphaera. Overall, the results suggested that all three of these nitrooxy compounds could specifically inhibit rumen methanogenesis, but NPD and NG were much more efficient than DNP at rumen methane mitigation.

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References

  1. Abecia L, Toral P, Martín-García A, Martínez G, Tomkins N, Molina-Alcaide E, Newbold C, Yáñez-Ruiz DR (2012) Effect of bromochloromethane on methane emission, rumen fermentation pattern, milk yield, and fatty acid profile in lactating dairy goats. J Dairy Sci 95:2027–2036. doi:10.3168/jds.2011-4831

    Article  CAS  PubMed  Google Scholar 

  2. Albracht SPJ, Ankel-Fuchs D, Böcher R, Ellermann J, Moll J, Zwaan JWVD, Thauer RK (1988) Five new EPR signals assigned to nickel in methyl-coenzyme m reductase from Methanobacterium thermoautotrophicum, strain marburg. Biochem Biophys Acta 955:86–102. doi:10.1016/0167-4838(88)90182-3

    CAS  Google Scholar 

  3. Bartram AK, Lynch MDJ, Stearns JC, Moreno-Hagelsieb G, Neufeld JD (2011) Generation of multimillion-sequence 16S rRNA gene libraries from complex microbial communities by assembling paired-end illumine reads. Appl Environ Microbiol 77:3846–3852. doi:10.1128/AEM.02772-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. doi:10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Cersosimo LM, Lachance H, St-Pierre B, van Hoven W, Wright AD (2015) Examination of the rumen bacteria and methanogenic archaea of wild impalas (Aepyceros melampus melampus) from Pongola, South Africa. Microb Ecol 69:577–585. doi:10.1007/s00248-014-0521-3

    Article  PubMed  Google Scholar 

  6. Conrad R (2009) The global methane cycle: recent advances in understanding the microbial processes involved. Environ Microbiol Rep 1:285–292. doi:10.1111/j.1758-2229.2009.00038.x

    Article  CAS  PubMed  Google Scholar 

  7. Denman SE, McSweeney CS (2006) Development of a real-time PCR assay for monitoring anaerobic fungal and cellulolytic bacterial populations within the rumen. FEMS Microbiol Ecol 58:572–582. doi:10.1111/j.1574-6941.2006.00190.x

    Article  CAS  PubMed  Google Scholar 

  8. Duin EC, Wagner T, Shima S, Prakash D, Cronin B, Yáñez-Ruiz DR, Duval S, Rümbeli R, Stemmler RT, Thauer RK, Kindermann M (2016) Mode of action uncovered for the specific reduction of methane emissions from ruminants by the small molecule 3-nitrooxypropanol. Proc Natl Acad Sci U S A 113:6172–6177. doi:10.1073/pnas.1600298113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. 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. World Intellectual Property Organization. International Patent Application WO 2012/084629 A1

  10. Eckard RJ, Grainger C, de Klein CAM (2010) Options for the abatement of methane and nitrous oxide from ruminant production: a review. Livest Sci 130:47–56. doi:10.1016/j.livsci.2010.02.010

    Article  Google Scholar 

  11. 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. doi:10.1126/science.278.5342.1457

    Article  CAS  PubMed  Google Scholar 

  12. Haisan J, Sun Y, Guan LL, Beauchemin KA, Iwaasa A, Duval S, Barreda DR, Oba M (2014) The effects of feeding 3-nitrooxypropanol on methane emissions and productivity of holstein cows in mid lactation. J Dairy Sci 97:3110–3119. doi:10.3168/jds.2013-7834

    Article  CAS  PubMed  Google Scholar 

  13. Haisan J, Sun Y, Guan L, Beauchemin KA, Iwaasa A, Duval S, Kindermann M, Barreda DR, Oba M (2016) The effects of feeding 3-nitrooxypropanol at two doses on milk production, rumen fermentation, plasma metabolites, nutrient digestibility, and methane emissions in lactating Holstein cows. Anim Prod Sci. doi:10.1071/AN15219

    Google Scholar 

  14. 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) Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options. J Anim Sci 91:5045–5069. doi:10.2527/jas.2013-6583

    Article  CAS  PubMed  Google Scholar 

  15. 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. Proc Natl Acad Sci U S A 112:10663–10668. doi:10.1073/pnas.1504124112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. 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. doi:10.1017/S1751731113002085

    Article  CAS  PubMed  Google Scholar 

  17. Johnson KA, Johnson DE (1995) Methane emissions from cattle. J Anim Sci 73:2483–2492. doi:10.2527/1995.7382483x

    Article  CAS  PubMed  Google Scholar 

  18. Knapp JR, Laur GL, Vadas PA, Weiss WP, Tricarico JM (2014) Invited review: enteric methane in dairy cattle production: quantifying the opportunities and impact of reducing emissions. J Dairy Sci 97:3231–3261. doi:10.3168/jds.2013-7234

    Article  CAS  PubMed  Google Scholar 

  19. Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235. doi:10.1128/AEM.71.12.8228-8235.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. 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. J Dairy Sci 97:3790–3799. doi:10.3168/jds.2013-7398

    Article  PubMed  Google Scholar 

  21. Menke KH, Steingass H (1988) Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid. Anim Res Dev 28:7–55

    Google Scholar 

  22. Reynolds CK, Humphries DJ, Kirton P, Kindermann M, Duval S, Steinberg W (2014) Effects of 3-nitrooxypropanol on methane emission, digestion, and energy and nitrogen balance of lactating dairy cows. J Dairy Sci 97:3777–3789. doi:10.3168/jds.2013-7397

    Article  CAS  PubMed  Google Scholar 

  23. Romero- Pérez 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. J Anim Sci 93:1780–1791. doi:10.2527/jas.2014-8726

    Article  PubMed  Google Scholar 

  24. Romero- Pérez A, Okine EK, Guan LL, Duval SM, Kindermann M, Beauchemin KA (2015) Effects of 3-nitrooxypropanol on methane production using the rumen simulation technique (rusitec). Anim Feed Sci Technol 209:98–109. doi:10.1016/j.anifeedsci.2015.09.002

    Article  Google Scholar 

  25. Soliva CR, Amelchanka SL, Duval SM, Kreuzer M (2011) Ruminal methane inhibition potential of various pure compounds in comparison with garlic oil as determined with a rumen simulation technique (Rusitec). Br J Nutr 106:114–122. doi:10.1017/S0007114510005684

    Article  CAS  PubMed  Google Scholar 

  26. Theodorou MK, Williams BA, Dhanoa MS, McAllan AB, France J (1994) A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feeds. Anim Feed Sci Technol 48:185–197. doi:10.1016/0377-8401(94)90171-6

    Article  Google Scholar 

  27. Theodorou MK, Mennim G, Davies DR, Zhu WY, Trinci AP, Brookman JL (1996) Anaerobic fungi in the digestive tract of mammalian herbivores and their potential for exploitation. Proc Nutr Soc USA 55:913–926. doi:10.1079/PNS19960088

    Article  CAS  Google Scholar 

  28. Ungerfeld EM (2015) Corrigendum: shifts in metabolic hydrogen sinks in the methanogenesis-inhibited ruminal fermentation: a meta-analysis. Front Microbiol 6:538. doi:10.3389/fmicb.2015.00037

    PubMed  PubMed Central  Google Scholar 

  29. 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. J Dairy Sci 93:5856–5866. doi:10.3168/jds.2010-3281

    Article  PubMed  Google Scholar 

  30. Weatherburn M (1967) Phenol-hypochlorite reaction for determination of ammonia. Anal Chem 39:971–974

    Article  CAS  Google Scholar 

  31. Wolin MJ (1981) Fermentation in the rumen and human large intestine. Science 213:1463–1468. doi:10.1126/science.7280665

    Article  CAS  PubMed  Google Scholar 

  32. Wood TA, Wallace RJ, Rowe A, Price J, Yáñez-Ruiz DR, Murray P, Newbold CJ (2009) Encapsulated fumaric acid as a feed ingredient to decrease ruminal methane emissions. Anim Feed Sci Technol 152:62–71. doi:10.1016/j.anifeedsci.2009.03.006

    Article  Google Scholar 

  33. Wright ADG, Dehority BA, Lynn DH (1997) Phylogeny of the rumen ciliates Entodinium, Epidinium and Polyplastron (Litostomatea: Entodiniomorphida) inferred from small subunit ribosomal RNA sequences. J Euk Microbiol 44:61–67. doi:10.1111/j.1550-7408.1997.tb05693.x

    Article  CAS  PubMed  Google Scholar 

  34. Zhang T, Lang Q, Zeng L, Li T, Wei M, Liu A (2014) Substituent effect on the oxidation peak potentials of phenol derivatives at ordered mesoporous carbons modified electrode and its application in determination of acidity coefficients (p k a). Electrochim Acta 115:283–289. doi:10.1016/j.electacta.2013.10.158

    Article  CAS  Google Scholar 

  35. Zinder SH (1993) Physiological ecology of methanogens. In: Ferry JG (ed) Methanogenesis: ecology, physiology, biochemistry and genetics. Chapman and Hall, New York, pp 128–206

    Chapter  Google Scholar 

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Acknowledgements

This research was supported by the Natural Science Foundation of China (31301999), and by the Fundamental Research Funds for the Central Universities, China (KYRC201402; KYZ201412). The authors also thank Jiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control and Jiangsu province (the funds for establishing advanced disciplines—Phase two) for financial support.

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  1. Jiangsu Province Key Laboratory of Gastrointestinal Nutrition and Animal Health, Laboratory of Gastrointestinal Microbiology, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, China

    Wei Jin, Zhenxiang Meng, Jing Wang, Yanfen Cheng & Weiyun Zhu

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  1. Wei Jin
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Correspondence to Jing Wang.

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Jin, W., Meng, Z., Wang, J. et al. Effect of Nitrooxy Compounds with Different Molecular Structures on the Rumen Methanogenesis, Metabolic Profile, and Methanogenic Community. Curr Microbiol 74, 891–898 (2017). https://doi.org/10.1007/s00284-017-1261-7

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