DOI QR코드

DOI QR Code

Effect of 2-Bromoethanesulfonic Acid on In vitro Fermentation Characteristics and Methanogen Population

  • Lee, S.Y. (Department of Agricultural Biotechnology, Research Institute for Agriculture and Life Sciences Seoul National University) ;
  • Yang, S.H. (Dairy Science Division, National Institute of Animal Science) ;
  • Lee, W.S. (Dairy Science Division, National Institute of Animal Science) ;
  • Kim, H.S. (Dairy Science Division, National Institute of Animal Science) ;
  • Shin, D.E. (Nong Hyup Feed Inc.) ;
  • Ha, Jong K. (Department of Agricultural Biotechnology, Research Institute for Agriculture and Life Sciences Seoul National University)
  • Received : 2008.10.15
  • Accepted : 2008.11.12
  • Published : 2009.01.01

Abstract

An in vitro incubation study was conducted to investigate effects of 2-bromoethanesulfonic acid (BES) on ruminal fermentation characteristics and methanogen population. BES at the final concentration of 0, 1 and 5 mM with two different substrates having a different ratio of timothy and concentrate (100% timothy vs. 40% timothy-60% concentrate) was incubated for 0, 24, 48 and 72 h in a $39^{\circ}C$ incubator. Total DNA extracted from culture fluid was used as a template for real-time PCR to measure the population of methanogens. Four different primer sets were used for amplification of total bacteria, total methanogens, the order Methanobacteriales and the order Methanomicrobiales. BES reduced (p<0.01) total gas and methane production in a dose-dependent manner. BES at 5 mM inhibited methane production by more than 95% compared to the control. An interaction between substrate and level of BES in total gas and methane was detected (p<0.01). The decrease of methane production with increasing BES level was more pronounced on mixed substrate than on timothy alone. However, hydrogen production was increased by BES treatment (p<0.01). Total VFA concentration was not affected, but molar percentage of propionate and butyrate was increased and acetate to propionate ratio was reduced by BES treatment (p<0.01). BES did not affect the population density of total bacteria but reduced (p<0.01) the population of total methanogens, the order Methanobacteriales and the order Methanomicrobiales in a dose-dependent manner. The type of substrate did not influence the trend, although the magnitude of response was different between all-roughage and 40% roughage substrate.

Keywords

References

  1. Agarwal, N., D. N. Kamra, P. N. Chatterjee, R. Kumar and L. C. Chaudhary. 2008. In vitro methanogenesis, microbial profile and fermentation of green forages with buffalo rumen liquor as influenced by 2-bromoethanesulphonic acid. Asian-Aust. J. Anim. Sci. 21(6):818-823
  2. Bhatta, R., O. Enishi and M. Kurihara. 2007. Measurement of methane production from ruminants. Asian-Aust. J. Anim Sci. 20(8):1305-1318
  3. Balch, W. E. and R. S. Wolfe. 1979. Transport of coenzyme M (2-mercaptoethanesulfonic acid) in Methanobacterium ruminantium. J. Bacteriol. 137:264-273
  4. Behlke, E. J. 2007. Attenuation of ruminal methanogenesis. dissertations in animal science. University of Nebraska-Lincoln, USA
  5. Bonhomme, A. 1990. Rumen ciliates: their metabolism and relationships with bacteria and their hosts. Anim. Feed Sci. Technol. 30:203-266 https://doi.org/10.1016/0377-8401(90)90016-2
  6. Busquet, M., S. Calsamiglia, A. Ferret and C. Kamel. 2005. Screening for effects of plant extracts and active compounds of plants on dairy cattle rumen microbial fermentation in a continuous culture system. Anim. Feed Sci. Technol. 123-124: 597-613 https://doi.org/10.1016/j.anifeedsci.2005.03.008
  7. Choi, N. J., S. Y. Lee, H. G. Sung, S. C. Lee and Jong K. Ha. 2004. Effects of halogenated compounds, organic acids and unsaturated fatty acids on in vitro methane production and fermentation characteristics. Asian-Aust. J. Anim. Sci. 17(9):1255-1259
  8. Crutzen, P. J., I. Aselmann and W. Seiler. 1986. Methane production by domestic animals, wild ruminants, other herbivorous fauna and humans. Tellus. 388:271-284
  9. Czerkawski, J. W., K. L. Blaxter and F. W. Wainman. 1966. The metabolism of oleic, linoleic, and linolenic acids by sheep with reference to their effects on methane production. Br. J. Nutr. 20 :349-362 https://doi.org/10.1079/BJN19660035
  10. Demeyer, D. I. and C. J. Van Nevel. 1975. Methanogenesis: an integrated part of carbohydrate fermentation, and its control. pp. 366-382. In: Digestion and metabolism in the ruminant (Ed. I. W. McDonald and I. J. C. Warner). The University of New England Publishing Unit, Armidale, Australia
  11. Denman, S. E. and C. S. McSweeney. 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 https://doi.org/10.1111/j.1574-6941.2006.00190.x
  12. Denman, S. E., N. W. Tomkins and C. S. McSweeney. 2007. Quantitation and diversity analysis of ruminal methanogenic populations in response to the antimethanogenic compound bromochloromethane. FEMS Microbiol. Ecol. 62(3):313-322 https://doi.org/10.1111/j.1574-6941.2007.00394.x
  13. Dohme, F., A. Machmuller, A. Wasserfallen and M. Kreuzer. 2001. Ruminal methanogenesis as influenced by individual fatty acids supplemented to complete ruminant diets. Lett Appl Microbiol. 32(1):47-51 https://doi.org/10.1046/j.1472-765x.2001.00863.x
  14. Dong, Y., H. D. Bae, T. A. McAllister, G. W. Mathison and K.-J. Cheng. 1999. Effects of exogenous fibrolytic enzymes, alphabromoethanesulfonate and monensin on fermentation in a rumen simulation (RUSITEC) system. Can. J. Anim Sci. 79:491-498 https://doi.org/10.4141/A99-024
  15. Erwin, E. S., G. J. Marco and E. M. Emery. 1961. Volatile fatty acid analysis of blood and rumen fluid by gas chromatography. J. Dairy Sci. 41:1768-1770
  16. Hungate, R. E., W. Smith, T. Bauchop, I. Yu and J. C. Rabinowitz. 1970. Formate as an intermediate in the bovine rumenfermentation. J. Bacteriol. 102:389-397
  17. Immig, I., D. Demeyer, D. Fiedler, C. Van Nevel and L. Mbanzamihigo. 1996. Attempts to induce reductive acetogenesis into a sheep rumen. Arch. Tierernahr. 49(4):363-370 https://doi.org/10.1080/17450399609381898
  18. Joblin, K. N. 2005. Methanogenic archaea. In: Methods in gut microbial ecology for ruminants (Ed. H. P. S. Makkar and C. S. McSweeney). pp. 47-53. Springer, Dordrecht, The Netherlands
  19. Krumholz, L. R., C. W. Forsberg and D. M. Veira. 1983. Association of methanogenic bacteria with rumen protozoa. Can. J. Microbiol. 29:676-680 https://doi.org/10.1139/m83-110
  20. Lee, C. H., H. G. Sung, M. Eslami, S. Y. Lee, J. Y. Song, S. S. Lee and J. K. Ha. 2007. Effects of Tween 80 pretreatment on dry matter disappearance of rice straw and cellulolytic bacterial adhesion. Asian-Aust. J. Anim Sci. 20(9):1397-1401
  21. Lee, H. J., S. C. Lee, J. D. Kim, Y. G. Oh, B. K. Kim, C. W. Kim and K. J. Kim. 2003. Methane production potential of feed ingredients as measured by in vitro gas test. Asian-Aust. J. Anim Sci. 16(8):1143-1150
  22. Lin, C., L. Raskin and D. A. Stahl. 1997. Microbial community structure in gastrointestinal tracts of domestic animals: comparative analyses using rRNA targeted oligonucleotide probes. FEMS Micriobiology Ecology 22:281-294 https://doi.org/10.1111/j.1574-6941.1997.tb00380.x
  23. Martin, S. A. 1998. Manipulation of ruminal fermentation with organic acids: a review. J. Anim. Sci. 76(12):3123-3132
  24. Martin, S. A. and J. M. Macy. 1985. Effects of monensin, pyromellitic diimide and 2-bromoethanesulfonic acid on rumen fermentation in vitro. J. Anim. Sci. 60:544-550 https://doi.org/10.1016/S0960-8524(03)00086-5
  25. McAllister, T. A., E. K., Okine, G. W. Mathison and K. -J. Cheng. 1996. Dietary, environmental and microbiological aspects of methane production in ruminants. Can. J. Anim. Sci. 76:231-243 https://doi.org/10.1016/S1465-9972(01)00021-6
  26. McSweeney, C. S., S. E. Denman, A.-D. G. Wright and Z. Yu. 2007. Application of recent DNA/RNA-based techniques in rumen ecology. Asian-Aust. J. Anim. Sci. 20(2):283-294
  27. Menke, K. H. and H. Steingass. 1988. Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid. Anim. Res. Develop. 28:7-15
  28. Mitsumori, M. and W. Sun. 2008. Control of rumen microbial fermentation for mitigating methane emissions from the rumen. Asian-Aust. J. Anim Sci. 21(1):144-154
  29. Moe, P. W. and H. F. Tyrrell. 1979. Methane production in dairy cows. J. Dairy Sci. 62:1583-1586 https://doi.org/10.3168/jds.S0022-0302(79)83465-7
  30. Moss, A. R. 1993. Methane: global warming and production by animals. Chalcombe Publications, Kingston, UK
  31. Nicholson, M. J., P. N. Evans and K. N. Joblin. 2007. Analysis of methanogen diversity in the rumen using temporal temperature gradient gel electrophoresis: identification of uncultured methanogens. Microb. Ecol. 54:141-150 https://doi.org/10.1007/s00248-006-9182-1
  32. Nollet, L., D. Demeyer and W. Verstraete. 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
  33. SAS. 2002. SAS user's guide: Statistics (Version 9.01 Ed.). SAS Inst. Inc., Cary, N.C. USA
  34. Sauer, F. D. and R. M. Teather. 1987. Changes in oxidation reduction potentials and volatile fatty acid production by rumen bacteria when methane synthesis is inhibited. J. Dairy Sci. 70(9):1835-1840 https://doi.org/10.3168/jds.S0022-0302(87)80222-9
  35. Skillman, L. C., P. N. Evans, C. Strompl and K. N. Joblin. 2006. 16S rDNA directed PCR primers and detection of methanogens in the bovine rumen. Lett. Appl. Microbiol. 42:222-228 https://doi.org/10.1111/j.1472-765X.2005.01833.x
  36. Snedecor, G. W. and W. G. Cochran. 1967. Statistical methods (6th Ed.). Iowa State Univ. Press, Ames
  37. Sparling, R. and L. Daniels. 1987. The specificity of growth inhibition of methanogenic bacteria by bromoethanesulfonate. Can. J. Microbiol. 33:1132-1136 https://doi.org/10.1139/m87-199
  38. Tajima, K., T. Nagamine, H. Matsui, M. Nakamura and R. I. Aminov. 2001. Phylogenetic analysis of archaeal 16S rRNA libraries from the rumen suggests the existence of a novel group of archaea not associated with known methanogens. FEMS Microbiol. Lett. 200:67-72 https://doi.org/10.1111/j.1574-6968.2001.tb10694.x
  39. Theodorou, M. K., B. A. Williams, M. S. Dhanoa, A. B. McAllan and J. France. 1994. A simple gas production method using a pressure transducer to determine the fermentation kinetics of ruminant feedstuffs. Anim. Feed Sci. Technol. 48:185-197 https://doi.org/10.1016/0377-8401(94)90171-6
  40. Trei, J. E., R. C. Parish and Y. K. Singh. 1971. Effect of methane inhibitors on rumen metabolism and feedlot performance of sheep. J. Dairy Sci. 54(4):536-540 https://doi.org/10.3168/jds.S0022-0302(71)85882-4
  41. Ungerfeld, E. M., S. R. Rust, D. R. Boone and Y. Liu. 2004. Effects of several inhibitors on pure cultures of ruminal methanogens. J. Appl. Microbiol. 97(3):520-526 https://doi.org/10.1111/j.1365-2672.2004.02330.x
  42. Van Kessel, J. S. and J. B. Russell. 1996. The effect of pH on ruminal methanogenesis. FEMS Microbiol. Ecol. 20:205-210 https://doi.org/10.1016/0168-6496(96)00030-X
  43. Van Nevel, C. J. and D. I. Demeyer. 1988. Manipulation of rumen fermentation. In: The rumen microbial ecosystem (Ed. P. N. Hobson) pp. 387-443. Elsevier Science Publishers, New York, USA
  44. Van Nevel, C. J. and D. I. Demeyer. 1995. Feed additives and other interventions for decreasing methane emissions. In:Biotechnology in animal feeds and animal feeding (Ed. R. J. Wallace and A. Chesson) pp. 329-349. VCH, Weinheim, Germany
  45. Wolin, M. J. 1960. A theoretical rumen fermentation balance. J. Dairy Sci. 43:1452-1459 https://doi.org/10.3168/jds.S0022-0302(60)90348-9
  46. Wright, A. D., C. H. Auckland and D. H. Lynn. 2007. Molecular diversity of methanogens in feedlot cattle from Ontario and Prince Edward Island, Canada. Appl. Environ. Microbiol. 73:4206-4210 https://doi.org/10.1128/AEM.00103-07
  47. Yu, Y., C. Lee, J. Kim and S. Hwang. 2005. Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol. Bioeng. 89:670-679 https://doi.org/10.1002/bit.20347
  48. Zicarelli, F., Serena Calabro, Vincenzo Piccolo, Simona D'Urso, Raffaella Tudisco, Fulvia Bovera, Monica I. Cutrignelli and Federico Infascelli. 2008. Diets with different forage/concentrate ratios for the mediterranean Italian buffalo: In vivoand In vitro digestibility. Asian-Aust. J. Anim. Sci. 21(1):75-82

Cited by

  1. Using Agro-Biomass as Substrate in Solid State Fermentation vol.2012, pp.1110-7251, 2012, https://doi.org/10.1155/2012/196264
  2. Reducing in vitro rumen methanogenesis for two contrasting diets using a series of inclusion rates of different additives vol.54, pp.2, 2014, https://doi.org/10.1071/AN12204
  3. Shifts in metabolic hydrogen sinks in the methanogenesis-inhibited ruminal fermentation: a meta-analysis vol.6, pp.1664-302X, 2015, https://doi.org/10.3389/fmicb.2015.00037
  4. Dose-response effects of Asparagopsis taxiformis and Oedogonium sp. on in vitro fermentation and methane production vol.28, pp.2, 2016, https://doi.org/10.1007/s10811-015-0639-9
  5. Control of Methane Emission in Ruminants and Industrial Application of Biogas from Livestock Manure in Korea vol.24, pp.1, 2011, https://doi.org/10.5713/ajas.2011.r.02
  6. In vitro ruminal methanogenesis of a hay-rich substrate in response to different combination supplements of nitrocompounds; pyromellitic diimide and 2-bromoethanesulphonate vol.163, pp.1, 2009, https://doi.org/10.1016/j.anifeedsci.2010.09.019
  7. Lovastatin-Enriched Rice Straw Enhances Biomass Quality and Suppresses Ruminal Methanogenesis vol.2013, pp.None, 2009, https://doi.org/10.1155/2013/397934
  8. 2011년도 축산부문 온실가스 인벤토리 산정 연구 vol.20, pp.4, 2009, https://doi.org/10.11109/jaes.2014.20.4.139
  9. Naturally Produced Lovastatin Modifies the Histology and Proteome Profile of Goat Skeletal Muscle vol.10, pp.1, 2020, https://doi.org/10.3390/ani10010072