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The inhibitory action mode of nitrocompounds on in vitro rumen methanogenesis: a comparison of nitroethane, 2-nitroethanol and 2-nitro-1-propanol

Published online by Cambridge University Press:  09 December 2019

Z. W. Zhang
Affiliation:
State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing100193, PR China
Y. L. Wang
Affiliation:
State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing100193, PR China
W. K. Wang
Affiliation:
State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing100193, PR China
Y. H Li
Affiliation:
Department of Quality and Safety Testing for Animal Products, China Animal Disease Control Centre, Beijing100125, PR China
Z. J. Cao
Affiliation:
State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing100193, PR China
S. L. Li
Affiliation:
State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing100193, PR China
H. J. Yang*
Affiliation:
State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing100193, PR China
*
Author for correspondence: H. J. Yang, E-mail: [email protected]

Abstract

Nitroethane (NE), 2-nitroethanol (NEOH) and 2-nitro-1-propanol (NPOH) were investigated in order to determine their inhibitory effects on in vitro ruminal fermentation and methane (CH4) production of a hay-rich substrate (alfalfa hay: maize meal = 4:1, w/w). The rumen liquor collected from cannulated Holstein dairy cows was incubated at 39 °C for 72 h. The addition of NE, NEOH and NPOH slowed down the fermentation process and notably decreased molar CH4 proportion by 96.8, 96.4 and 35.0%, respectively. The abundance of total methanogen and methanogens from the order Methanobacteriales were all decreased with NE, NEOH and NPOH supplementation. Meanwhile, the nitrocompound addition reduced mcrA gene expression, coenzyme F420 and F430 contents. The correlation analysis showed that CH4 production was correlated positively with the population abundance of total methanogens, Methanobacteriales, mcrA gene expression, coenzyme contents of F420 and F430. The nitrocompound addition decreased acetate concentration and increased propionate and butyrate concentrations in the culture fluid. In summary, both NE and NEOH addition presented nearly the same inhibitory effectiveness on in vitro CH4 production; they were more effective than NPOH. The results of the current study provide evidence that NE, NEOH and NPOH can dramatically decrease methanogen population, mcrA gene expression and the coenzyme content of F420 and F430 in ruminal methanogenesis.

Type
Climate Change and Agriculture Research Paper
Copyright
Copyright © Cambridge University Press 2019

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References

Anderson, RC, Callaway, TR, Van Kessel, JAS, Jung, YS, Edrington, TS and Nisbet, DJ (2003) Effect of select nitrocompounds on ruminal fermentation; an initial look at their potential to reduce economic and environmental costs associated with ruminal methanogenesis. Bioresource Technology 90, 5963.CrossRefGoogle Scholar
Anderson, RC, Carstens, GE, Miller, RK, Callaway, TR, Schultz, CL, Edrington, TS, Harvey, RB and Nisbet, DJ (2006) Effect of oral nitroethane and 2-nitropropanol administration on methane-producing activity and volatile fatty acid production in the ovine rumen. Bioresource Technology 97, 24212426.CrossRefGoogle ScholarPubMed
Anderson, RC, Krueger, NA, Stanton, TB, Callaway, TR, Edrington, TS, Harvey, RB, Jung, YS and Nisbet, DJ (2008) Effects of select nitrocompounds on in vitro ruminal fermentation during conditions of limiting or excess added reductant. Bioresource Technology 99, 86558661.CrossRefGoogle ScholarPubMed
Ankel-Fuchs, D, Jaenchen, R, Gebhardt, NA and Thauer, RK (1984) Functional relationship between protein-bound and free factor F430 in Methanobacterium. Archives of Microbiology 139, 332337.CrossRefGoogle Scholar
Božic, AK, Anderson, RC, Carstens, GE, Ricke, SC, Callaway, TR, Yokoyama, MT, Wang, JK and Nisbet, DJ (2009) Effects of the methane-inhibitors nitrate, nitroethane, lauric acid, Lauricidin and the Hawaiian marine algae Chaetoceros on ruminal fermentation in vitro. Bioresource Technology 100, 40174025.CrossRefGoogle ScholarPubMed
Cieslak, A, Szumacher-Strabel, M, Stochmal, A and Oleszek, W (2013) Plant components with specific activities against rumen methanogens. Animal 7(suppl. 2), 253265.CrossRefGoogle ScholarPubMed
Correa, AC, Trachsel, J, Allen, HK, Corral-Luna, A, Gutierrez-Bañuelos, H, Ochoa-Garcia, PA, Ruiz-Barrera, O, Hume, ME, Callaway, TR, Harvey, RB, Beier, RC, Anderson, RC and Nisbet, DJ (2017) Effect of sole or combined administration of nitrate and 3-nitro-1-propionic acid on fermentation and Salmonella survivability in alfalfa-fed rumen cultures in vitro. Bioresource Technology 229, 6977.CrossRefGoogle ScholarPubMed
Demeyer, D and Graeve, KD (1991) Differences in stoichiometry between rumen and hindgut fermentation. Advances in Animal Physiology and Animal Nutrition 22, 5061.Google Scholar
Denman, SE and McSweeney, CS (2006) Development of a real-time PCR assay for monitoring anaerobic fungal and cellulolytic bacterial populations within the rumen. FEMS Microbiology Ecology 58, 572582.CrossRefGoogle ScholarPubMed
Denman, SE, Tomkins, NW and McSweeney, CS (2007) Quantitation and diversity analysis of ruminal methanogenic populations in response to the antimethanogenic compound bromochloromethane. FEMS Microbiology Ecology 62, 313322.CrossRefGoogle ScholarPubMed
Dolfing, J and Willem, JW (1985) Comparison of methane production rate and coenzyme F420 content of methanogenic consortia in anaerobic granular sludge. Applied and Environmental Microbiology 49, 11421145.CrossRefGoogle Scholar
Ellefson, WL, Whitman, WB and Wolfe, RS (1982) Nickel-containing factor F430: chromophore of the methylreductase of Methanobacterium. Proceedings of the National Academy of Sciences of the USA 79, 37073710.CrossRefGoogle ScholarPubMed
France, J, Dijkstra, J, Dhanoa, MS, Lopez, S and Bannink, A (2000) Estimating the extent of degradation of ruminant feeds from a description of their gas production profiles observed in vitro: derivation of models and other mathematical considerations. British Journal of Nutrition 83, 143150.CrossRefGoogle ScholarPubMed
García-Martínez, R, Ranilla, MJ, Tejido, ML and Carro, MD (2005) Effects of disodium fumarate on in vitro rumen microbial growth, methane production and fermentation of diets differing in their forage:concentrate ratio. British Journal of Nutrition 94, 7177.CrossRefGoogle ScholarPubMed
Guo, YQ, Liu, JX, Lu, Y, Zhu, WY, Denman, SE and McSweeney, CS (2008) Effect of tea saponin on methanogenesis, microbial community structure and expression of mcrA gene, in cultures of rumen micro-organisms. Letters in Applied Microbiology 47, 421426.CrossRefGoogle ScholarPubMed
Gutierrez-Bañuelos, H, Anderson, RC, Carstens, GE, Slay, LJ, Ramlachan, N, Horrocks, SM, Callaway, TR, Edrington, TS and Nisbet, DJ (2007) Zoonotic bacterial populations, gut fermentation characteristics and methane production in feedlot steers during oral nitroethane treatment and after the feeding of an experimental chlorate product. Anaerobe 13, 2131.CrossRefGoogle ScholarPubMed
Hendrickson, EL and Leigh, JA (2008) Roles of coenzyme F420-reducing hydrogenases and hydrogen- and f420-dependent methylenetetrahydromethanopterin dehydrogenases in reduction of F420 and production of hydrogen during methanogenesis. Journal of Bacteriology 190, 48184821.CrossRefGoogle ScholarPubMed
Johnson, KA and Johnson, DE (1995) Methane emissions from cattle. Journal of Animal Science 73, 24832492.CrossRefGoogle ScholarPubMed
Latham, EA, Anderson, RC, Pinchak, WE and Nisbet, DJ (2016) Insights on alterations to the rumen ecosystem by nitrate and nitrocompounds. Frontiers in Microbiology 7, 115. doi: 10.3389/fmicb.2016.00228.CrossRefGoogle ScholarPubMed
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25, 402408.CrossRefGoogle Scholar
Menke, KH and Steingass, H (1988) Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid. Animal Research and Development 28, 755.Google Scholar
Ochoa-García, PA, Arevalos-Sánchez, MM, Ruiz-Barrera, O, Anderson, RC, Maynez-Pérez, AO, Rodríguez-Almeida, FA, Chávez-Martínez, A, Gutiérrez-Bañuelos, H and Corral-Luna, A (2019) In vitro reduction of methane production by 3-nitro-1-propionic acid is dose-dependent. Journal of Animal Science 97, 13171324.CrossRefGoogle Scholar
Patra, AK (2012) Enteric methane mitigation technologies for ruminant livestock: a synthesis of current research and future directions. Environmental Monitoring and Assessment 184, 19291952.CrossRefGoogle ScholarPubMed
Reuter, BW, Egeler, T, Schneckenburger, H and Schoberth, SM (1986) In vivo measurement of F420 fluorescence in cultures of Methanobacterium thermoautotrophicum. Journal of Biotechnology 4, 325332.CrossRefGoogle Scholar
Russell, JB (1998) Strategies that ruminal bacteria use to handle excess carbohydrate. Journal of Animal Science 76, 19551963.CrossRefGoogle ScholarPubMed
Saminathan, M, Sieo, CC, Gan, HM, Abdullah, N, Wong, CMVL and Ho, YW (2016) Effects of condensed tannin fractions of different molecular weights on population and diversity of bovine rumen methanogenic archaea in vitro, as determined by high-throughput sequencing. Animal Feed Science and Technology 216, 146160.CrossRefGoogle Scholar
Schulze, D, Menkhaus, M, Fiebig, R and Dellweg, H (1988) Anaerobic treatment of protein-containing waste waters: correlation between coenzyme F420 and methane production. Applied Microbiology and Biotechnology 29, 506510.CrossRefGoogle Scholar
Smith, DJ and Anderson, RC (2013) Toxicity and metabolism of nitroalkanes and substituted nitroalkanes. Journal of Agricultural and Food Chemistry 61, 763779.CrossRefGoogle ScholarPubMed
Thauer, RK (1998) Biochemistry of methanogenesis: a tribute to Marjory Stephenson. 1998 Marjory Stephenson Prize Lecture. Microbiology (Reading, England) 144, 23772406.CrossRefGoogle ScholarPubMed
Thauer, RK, Jungermann, K and Decker, K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriological Reviews 41, 100180.CrossRefGoogle ScholarPubMed
Thauer, RK, Kaster, AK, Goenrich, M, Schick, M, Hiromoto, T and Shima, S (2010) Hydrogenases from methanogenic archaea, nickel, a novel cofactor, and H2 storage. Annual Review of Biochemistry 79, 507536.CrossRefGoogle ScholarPubMed
Van Nevel, CJ and Demeyer, DI (1996) Control of rumen methanogenesis. Environmental Monitoring and Assessment 42, 7397.CrossRefGoogle ScholarPubMed
Vyas, D, Alemu, AW, McGinn, SM, Duval, SM, Kindermann, M and Beauchemin, KA (2018) The combined effects of supplementing monensin and 3-nitrooxypropanol on methane emissions, growth rate, and feed conversion efficiency in beef cattle fed high forage and high grain diets. Journal of Animal Science 96, 29232938.CrossRefGoogle ScholarPubMed
Wachenheim, DE and Patterson, JA (1992) Anaerobic production of extracellular polysaccharide by Butyrivibrio fibrisolvens nyx. Applied and Environmental Microbiology 58, 385391.CrossRefGoogle ScholarPubMed
Yu, Y, Lee, C, Kim, J and Hwang, S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnology and Bioengineering 89, 670679.CrossRefGoogle ScholarPubMed
Zhang, DF and Yang, HJ (2011) In vitro ruminal methanogenesis of a hay-rich substrate in response to different combination supplements of nitrocompounds; pyromellitic diimide and 2-bromoethanesulphonate. Animal Feed Science and Technology 163, 2032.CrossRefGoogle Scholar
Zhang, DF and Yang, HJ (2012) Combination effects of nitrocompounds, pyromellitic diimide, and 2-bromoethanesulfonate on in vitro ruminal methane production and fermentation of a grain-rich feed. Journal of Agricultural and Food Chemistry 60, 364371.CrossRefGoogle ScholarPubMed
Zhang, ZW, Cao, ZJ, Wang, YL, Wang, YJ, Yang, HJ and Li, SL (2018) Nitrocompounds as potential methanogenic inhibitors in ruminant animals: a review. Animal Feed Science and Technology 236, 107114.CrossRefGoogle Scholar
Zhou, M, Hernandez-Sanabria, E and Guan, LL (2009) Assessment of the microbial ecology of ruminal methanogens in cattle with different feed efficiencies. Applied and Environmental Microbiology 75, 65246533.CrossRefGoogle ScholarPubMed
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