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Linolenic Acid in Association with Malate or Fumarate Increased CLA Production and Reduced Methane Generation by Rumen Microbes

  • Li, X.Z. (College of Grassland Science, Gansu Agricultural University) ;
  • Choi, S.H. (Department of Animal Science, Chungbuk National University) ;
  • Jin, G.L. (Department of Animal Science, Chungbuk National University) ;
  • Yan, C.G. (Department of Animal Science, Yanbian University) ;
  • Long, R.J. (International Centre for Tibetan Plateau Ecosystem Management, Lanzhou University) ;
  • Liang, C.Y. (Department of Animal Science, Yanbian University) ;
  • Song, Man K. (Department of Animal Science, Chungbuk National University)
  • Received : 2008.12.09
  • Accepted : 2009.02.23
  • Published : 2009.06.01

Abstract

An in vitro study was conducted to investigate the effect of malate or fumarate on fermentation characteristics, and production of conjugated linoleic acid (CLA) and methane ($CH_4$) by rumen microbes when incubated with linolenic acid (${\alpha}-C_{18:3}$). Sixty milligrams of ${\alpha}-C_{18:3}$ alone (LNA), or ${\alpha}-C_{18:3}$ with 24 mM malic acid (M-LNA) or ${\alpha}-C_{18:3}$ with 24 mM fumaric acid (F-LNA) were added to the 150 ml culture solution consisting of 75 ml strained rumen fluid and 75ml McDougall's artificial saliva. Culture solution for incubation was also made without malate, fumarate and ${\alpha}-C_{18:3}$ (Control). Two grams of feed consisting of 70% concentrate and 30% ground alfalfa (DM basis) were also added to the culture solution of each treatment. In vitro incubation was made anaerobically in a shaking incubator up to 12 h at $39^{\circ}C$. Supplementation of malate (M-LNA) or fumarate (F-LNA) increased pH at 6 h (p<0.01) and 12 h (p<0.001) incubation times compared to control and linolenic acid (LNA) treatments. Both malate and fumarate did not influence the ammonia-N concentration. Concentration of total VFA in culture solution was higher for M-LNA and F-LNA supplementation than for control and LNA treatments from 6 h (p<0.040) to 12 h (p<0.027) incubation times, but was not different between malate and fumarate for all incubation times. Molar proportion of $C_3$ was increased by F-LNA and M-LNA supplementation from 6 h (p<0.0001) to 12 h (p<0.004) incubation times compared to control and LNA treatments. No differences in $C_{3}$ proportion, however, were observed between M-LNA and F-LNA treatments. Accumulated total gas production for 12h incubation was increased (p<0.0002) by M-LNA or F-LNA compared to control or LNA treatment. Accumulated $CH_4$ production for 12 h incubation, however, was greatly reduced (p<0.0002) by supplementing malate or fumarate compared to the control, and its production from M-LNA or F-LNA treatment was smaller than that from LNA treatment. Methane production from LNA, M-LNA or F-LNA treatment was steadily lower (p<0.01 - p<0.001) from 3 h incubation time than that from the control, and was also lower for M-LNA or F-LNA treatment at incubation times of 6 h (p<0.01) and 9 h (p<0.001) than for LNA treatment. Methane production from LNA, however, was reduced (p<0.01 - p<0.001) from 3 h to 9 h incubation times compared to the control. Both malate and fumarate increased concentration of trans11-$C_{18:1}$ from 3 h to 12 h incubation (p<0.01), cis9,trans11-CLA up to 6 h incubation (p<0.01 - p<0.01), trans10,cis12-CLA at 3 h (p<0.05) and 12 h (p<0.01), and total CLA for all incubation times (p<0.05) compared to corresponding values for the ${\alpha}-C_{18:3}$ supplemented treatment (LNA). In conclusion, malate and fumarate rechanneled the metabolic $H_2 pathway to production of propionate and CLA, and depressed the process of biohydrogenation and methane generation. Linolenic acid alone would also be one of the optimistic alternatives to suppress the $CH_4$ generation.

Keywords

References

  1. Asanuma, N., M. Iwamoto and T. Hino. 1999. Effect of the addition of fumarate on methane production by ruminal microorganisms in vitro. J. Dairy Sci. 82:780-787 https://doi.org/10.3168/jds.S0022-0302(99)75296-3
  2. Bauman, D. E., L. H. Baumgard, B. A. Corl and J. M. Griinari. 1999. Biosynthesis of conjugated linoleic acid in ruminants. In: Proceedings of American Society of Animal Science. 1-15
  3. Bergen, W. G. and D. B. Bates. 1984. Ionophores: their effect on production efficiency and mode of action. J. Anim. Sci. 58: 1465-1483
  4. Bessa, R. J., J. Santos-Silva, J. M. Riberio and A. V. Portugal. 2000. Reticulo-rumen biohydrogenation and the enrichment of ruminal edible products with linoleic acid conjugated isomers. Appl. Enriron. Microbiol. 63:201-211
  5. Broudiscou, L., C. J. Van Nevel and D. I. Demeyer. 1990. Incorporation of soya oil hydrolysate in the diet of defaunated or refaunated sheep: effect on rumen fermentation in vitro. Arch. Anim. Nutr. 40:329-337 https://doi.org/10.1080/17450399009430929
  6. Bryant, M. P. 1979. Microbial methane production-theoretical aspects. J. Anim. Sci. 48:193-201
  7. Callaway, T. R. and S. A. Martin. 1996. Effects of organic acid and monensin treatment on in vitro mixed ruminal microorganism fermentation of cracked corn. J. Anim. Sci. 74:1982-1989
  8. Carro, M. D. and M. J. Ranilla. 2003. Effect of the addition of malate on in vitro rumen fermentation of cereal grains. Br. J. Nutr. 89:181-188 https://doi.org/10.1079/BJN2002759
  9. Castillo, C., J. L. Benedito, J. Mendez, V. Pereira, M. Lopez-Alonso, M. Miranda and J. Hernandez. 2004. Organic acids as a substitute for monensin in diets for beef cattle. Anim. Feed Sci. Tec. 115:101-116 https://doi.org/10.1016/j.anifeedsci.2004.02.001
  10. Chantaprasarn, N. and M. Wanapat. 2008. Effects of sunflower oil supplementation in Cassava hay bases-diets for lactating dairy cows. Asian-Aust. J. Anim. Sci. 21:42-50
  11. Choi, S. H. and M. K. Song. 2005. Effect of C18-polyunsaturated fatty acids on their direct incorporation into the rumen bacterial lipids and CLA production in vitro. Asian-Aust. J. Anim. Sci. 18:512-515
  12. Czerlawski, J. W. 1972. Fate of metabolic hydrogen in the rumen. Proc .Nutr. Soc. 141-146 https://doi.org/10.1079/PNS19720028
  13. Demeye, D. I. and H. K. Henderickx. 1967. Competitive inhibition of in vitro methane production by mixed rumen bacteria. Arch. Intl. Physiol. Biochim. 75:157-159
  14. Dhiman, T. R., L. D. Satter, M. W. Pariza, M. P. Galli, K. Albright and M. X. Tolosa. 2000. Conjugated linoleic acid (CLA) content of milk from cows offered diets rich in linoleic and linolenic acid. J. Dairy Sci. 83:1016-1027 https://doi.org/10.3168/jds.S0022-0302(00)74966-6
  15. Fawcett, J. K. and J. E. Scott. 1960. A rapid and precise method for the determination of urea. J. Clin. Pathol. 13:156-163 https://doi.org/10.1136/jcp.13.2.156
  16. Folch, J., M. Lee and G. H. Sloan-Stanley. 1957. A sample method for the isolation and purification of total lipids from animal tissue. J. Biol. Chem. 226:497-509 https://doi.org/10.1016/S0308-8146(03)00152-3
  17. Garcia-Lopez, P. M., L. Kung and J. M. Odom. 1996. In vitro inhibition of microbial methane production by 9,10-anthraquinone. J. Anim. Sci. 74:2276-2284
  18. Hafoot, C. G. and G. P. Hazlewood. 1998. Lipid metabolism in the rumen. In the rumen microbial ecosystem (Ed. P. N. Hobson). Elsevier Appl. Sci., London and New York. pp. 382-426
  19. Jin, G. L., S. H. Choi, H. G. Lee, Y. J. Kim and M. K. Song. 2008. Effects of monensin and fish oil on conjugated linoleic acid production by rumen microbes in Holstein cows fed diets supplemented with soybean oil and sodium bicarbonate. Asian-Aust. J. Anim. Sci. 21:1728-1735
  20. Kelly, M. L., J. R. Berry, D. A. Dwyer, J. M. Griinari, P. Y. Choinard, M. E. Vanamburgh and D. E. Bauman. 1998. Dietary fatty acid sources affect conjugated linoleic acid concentrations in milk from lactating dairy cows. J. Nutr. 128: 881-885
  21. Lepage, G. and C. C. Roy. 1986. Direct transesterification of all classes of lipid in a one-step reaction. J. Lipid Res. 27:114-221
  22. Li, X. Z., C. G. Yan, S. H. Choi, R. J. Long, G. L. Jin and M. K. Song. 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
  23. L'opez, C., C. Vald'es, C. J. Newbold and R. J. Wallace. 1999. Influence of sodium fumarate addition on rumen fermentation in vitro. Br. J. Nutr. 81:59-64
  24. Makkar, H. P. S. and P. E. Vercoe. 2007. Measuring methane production from ruminants (Ed. P. Harinder, S. Makkar and E. Philip). Vercoe. Springer publishing Company
  25. Mao, S. Y., G. Zhang and W. Y. Zhu. 2007. Effect of disodium fumarate on in vitro rumen fermentation of different substrates and rumen bacterial communities as revealed by denaturing gradient gel electrophoresis analysis of 16S ribosomal DNA. Asian-Aust. J. Anim. Sci. 20:543-49
  26. Martin, S. A. and M. N. Streeter. 1995. Effect of malate on in vitro mixed ruminal microorganism fermentation. J. Anim. Sci. 73: 2141-2145
  27. McDougall, E. I. 1948. Studies on ruminant saliva. I. The composition and output of sheep's saliva. Biochem. J. 43:99-109
  28. Nisbet, D. J. and S. A. Martin. 1990. Effect of dicarboxylic acids and Aspergillus oryzae fermentation extract on lactate uptake by the ruminal bacterium Selenomonas ruminantium. Appl. Environ. Microbiol. 56:3515-3518
  29. Nisbet, D. J. and S. A. Martin. 1991. Effect of a Saccharomyces cerevisiae culture on lactate utilization by the ruminal bacterium Selenomonas ruminantium. J. Anim. Sci. 69:4628-4633
  30. Nisbet, D. J. and S. A. Martin. 1993. Effects of fumarate, L-malate, and an Aspergillus oryzae fermentation extract on D-lactate utilization by the ruminal bacterium Selenomonas ruminantium. Curr. Microbiol. 26:133-136 https://doi.org/10.1007/BF01577366
  31. Prins, R. A., C. J. Van Nevel and D. I. Demeyer, 1972. Pure culture studies of inhibitors for methanogenic bacteria. Antonie Van Leeuwenhoek. 38:281-287 https://doi.org/10.1016/0378-1097(85)90001-1
  32. Russell, J. B. and H. J. Strobel. 1989. Effect of ionophores on ruminal fermentation. Appl. Environ. Microbiol. 55:1-6
  33. Lopez, S. and C. J. Newbold. 2007. Analysis of methane in 'Measuring methane production from ruminants' (Ed. P. S. Makkar and P. E. Vercoe). Springer
  34. SAS Inc. 1985. SAS user's guide: Statistical Analysis System Institute, SAS Inc., Cary, NC, USA
  35. Steel, R. G. D. and J. H. Torrie. 1980. Principles and procedures of statistics. Mcgraw Hill Book Co., NY
  36. Ungerfeld, E. M., S. R. Rust and R. Burnett. 2003. Use of some novel alternative electron sinks to inhibit ruminal methanogenesis. Reprod. Nutr. Dev. 43:189-202 https://doi.org/10.1051/rnd:2003016
  37. Van Nevel, C. and D. I. Demeyer. 1996. Control of rumen methanogenesis. Environ. Monit. Assess. 42:73-97 https://doi.org/10.1007/BF00394043
  38. Wang, J. H., M. K. Song, Y. S. Son and M. B.Chang. 2002a. Effect of concentrate level on the formation of conjugated linoleic acid and trans-octadecenoic acid by ruminal bacteria when incubated with oilseeds in vitro. Asian-Aust. J. Anim. Sci. 15:687-694
  39. Wang, J. H., M. K. Song, Y. S. Son and M. B. Chang. 2002b. Addition effect of seed associated or free linseed oil on the formation of cis-9,trans-11 conjugated linoleic acid and octadecenoic acid by ruminal bacteria in vitro. Asian-Aust. J. Anim. Sci. 15:1115-11120
  40. Wang, J. H., S. H. Choi and M. K. Song. 2003. Effects of concentrate to roughage ratio on the formation of cis-9, trans-11 CLA and trans11-octadecenoic acid in rumen fluid and plasma of sheep when fed high oleic or high linoleic acid oils. Asian-Aust. J. Anim. Sci. 16:1604-1609
  41. Wang, J. H., S. H. Choi, C. G. Yan and M. K. Song. 2005. Effect of monensin and fish oil supplementation on biohydrogenation and CLA production by rumen bacteria in vitro when incubated with safflower oil. Asian-Aust. J. Anim. Sci. 18:221-225

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