1887

Abstract

Cultures of ruminal bacteria known to metabolize unsaturated fatty acids were grown in medium containing 50 μg ml of geometric and positional isomers of conjugated linoleic acid (CLA) or 18 : 1 fatty acids and 37.4 % deuterium oxide to investigate the mechanisms responsible for fatty acid metabolism. JW11 converted 9,11-18 : 2 and 9,11-18 : 2 to -11-18 : 1 as the main product, labelled at C-9, and metabolized 10,12-18 : 2 to 10-18 : 1, labelled at C-13, and smaller amounts of -12-18 : 1 and -12-18 : 1. P-18 did not grow in the presence of 9,11-18 : 2 or 10,12-18 : 2, but grew in medium containing 9,11-18 : 2, forming 18 : 0. , a ruminal species that isomerizes linoleic acid to 10,12-18 : 2, did not metabolize CLA isomers further. metabolized small amounts of 10-18 : 1, 11-18 : 1 and 9-18 : 1, but the products formed were not detected. , on the other hand, carried out substantial conversion of 18 : 1 substrates to 18 : 0. hydrated 9-18 : 1 and 11-18 : 1 to 10-OH-18 : 0, which was further oxidized to yield 10-O-18 : 0. The deuterium enrichment in the intermediates formed during incubations with 9,11 geometric isomers of CLA was about half that of the products from 10,12 CLA and 18 : 1 isomers, suggesting that the reduction of 9,11 geometric isomers CLA by ruminal bacteria occurs via different mechanisms compared with the metabolism of other unsaturated fatty acids.

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2010-02-01
2019-10-17
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References

  1. Bauman, D. E., Lock, A. L., Corl, B. A., Ip, C., Salter, A. M. & Parodi, P. M. ( 2005; ). Milk fatty acids and human health: potential role of conjugated linoleic acid and trans fatty acids. In Ruminant Physiology: Digestion, Metabolism and Impact of Nutrition on Gene Expression, Immunology and Stress, pp. 529–561. Edited by K. Serjrsen, T. Hvelplund & M. O. Nielsen. Wageningen, The Netherlands: Wageningen Academic Publishers.
  2. Baumgard, L. H., Corl, B. A., Dwyer, D. A., Sæbø, A. & Bauman, D. E. ( 2000; ). Identification of the conjugated linoleic acid isomer that inhibits milk fat synthesis. Am J Physiol Regul Integr Comp Physiol 278, R179–R184.
    [Google Scholar]
  3. Beam, T. M., Jenkins, T. C., Moate, P. J., Kohn, R. A. & Palmquist, D. L. ( 2000; ). Effects of amount and source of fat on the rates of lipolysis and biohydrogenation of fatty acids in ruminal contents. J Dairy Sci 83, 2564–2573.[CrossRef]
    [Google Scholar]
  4. Boeckaert, C., Vlaeminck, B., Fievez, V., Maignien, L., Dijkstra, J. & Boon, N. ( 2008; ). Accumulation of trans C-18:1 fatty acids in the rumen after dietary algal supplementation is associated with changes in the Butyrivibrio community. Appl Environ Microbiol 74, 6923–6930.[CrossRef]
    [Google Scholar]
  5. Brechany, E. Y. & Christie, W. W. ( 1992; ). Identification of the saturated oxo fatty acids in cheese. J Dairy Res 59, 57–64.[CrossRef]
    [Google Scholar]
  6. Campbell, I. M. ( 1974; ). Incorporation and dilution values – their calculation in mass spectrally stable isotope labeling experiments. Bioorg Chem 3, 386–397.[CrossRef]
    [Google Scholar]
  7. Christie, W. W., Sébédio, J. L. & Juanéda, P. ( 2001; ). A practical guide to the analysis of conjugated linoleic acid (CLA). Inform 12, 147–154.
    [Google Scholar]
  8. Dawson, R. M. & Hemington, N. ( 1974; ). Digestion of grass lipids and pigments in the sheep rumen. Br J Nutr 32, 327–340.[CrossRef]
    [Google Scholar]
  9. Devillard, E., McIntosh, F. M., Newbold, C. J. & Wallace, R. J. ( 2006; ). Rumen ciliate protozoa contain high concentrations of conjugated linoleic acids and vaccenic acid, yet do not hydrogenate linoleic acid or desaturate stearic acid. Br J Nutr 96, 697–704.
    [Google Scholar]
  10. Devillard, E., McIntosh, F. M., Duncan, S. H. & Wallace, R. J. ( 2007; ). Metabolism of linoleic acid by human gut bacteria: different routes for biosynthesis of conjugated linoleic acid. J Bacteriol 189, 2566–2570.[CrossRef]
    [Google Scholar]
  11. Fievez, V., Vlaeminck, B., Jenkins, T., Enjalbert, F. & Doreau, M. ( 2007; ). Assessing rumen biohydrogenation and its manipulation in vivo, in vitro and in situ. Eur J Lipid Sci Technol 109, 740–756.[CrossRef]
    [Google Scholar]
  12. Folch, J., Lees, M. & Sloane, G. H. ( 1957; ). A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226, 497–509.
    [Google Scholar]
  13. Harfoot, C. G. & Hazlewood, G. P. ( 1997; ). Lipid metabolism in the rumen. In The Rumen Microbial Ecosystem, pp. 382–426. Edited by P. N. Hobson & C. S. Stewart. London: Chapman & Hall.
  14. Hazlewood, G. P., Kemp, P., Lander, D. & Dawson, R. M. C. ( 1976; ). C18 unsaturated fatty acid hydrogenation patterns of some rumen bacteria and their ability to hydrolyse exogenous phospholipid. Br J Nutr 35, 293–297.[CrossRef]
    [Google Scholar]
  15. Hobson, P. N. ( 1969; ). Rumen bacteria. Methods Microbiol 3B, 133–139.
    [Google Scholar]
  16. Hou, C. T. ( 1994; ). Production of 10-ketostearic acid from oleic acid by Flavobacterium sp. strain Ds5 (Nrrl B-14859). Appl Environ Microbiol 60, 3760–3763.
    [Google Scholar]
  17. Hudson, J. A., MacKenzie, C. A. & Joblin, K. N. ( 1995; ). Conversion of oleic acid to 10-hydroxystearic acid by two species of ruminal bacteria. Appl Microbiol Biotechnol 44, 1–6.[CrossRef]
    [Google Scholar]
  18. Hudson, J. A., Cai, Y., Corner, R. J., Morvan, B. & Joblin, K. N. ( 2000; ). Identification and enumeration of oleic acid and linoleic acid hydrating bacteria in the rumen of sheep and cows. J Appl Microbiol 88, 286–292.[CrossRef]
    [Google Scholar]
  19. Hungate, R. E. ( 1969; ). A roll tube method for cultivation of strict anaerobes. Methods Microbiol 3B, 117–132.
    [Google Scholar]
  20. Huws, S. A., Kim, E. J., Kingston-Smith, A. H., Lee, M. R. F., Muetzel, S. M., Cookson, A. R., Newbold, C. J., Wallace, R. J. & Scollan, N. D. ( 2009; ). Rumen protozoa are rich in polyunsaturated fatty acids due to the ingestion of chloroplasts. FEMS Microbiol Ecol 69, 461–471.[CrossRef]
    [Google Scholar]
  21. Jenkins, T. C., AbuGhazaleh, A. A., Freeman, S. & Thies, E. J. ( 2006; ). The production of 10-hydroxystearic and 10-ketostearic acids is an alternative route of oleic acid transformation by the ruminal microbiota in cattle. J Nutr 136, 926–931.
    [Google Scholar]
  22. Jenkins, T. C., Wallace, R. J., Moate, P. J. & Mosley, E. E. ( 2008; ). Recent advances in biohydrogenation of unsaturated fatty acids within the rumen microbial ecosystem. J Anim Sci 86, 397–412.
    [Google Scholar]
  23. Kemp, P., White, R. W. & Lander, D. J. ( 1975; ). The hydrogenation of unsaturated fatty acids by five bacterial isolates from the sheep rumen, including a new species. J Gen Microbiol 90, 100–114.[CrossRef]
    [Google Scholar]
  24. Kepler, C. R., Hirons, K. P., McNeill, J. J. & Tove, S. B. ( 1966; ). Intermediates and products of the biohydrogenation of linoleic acid by Butyrivibrio fibrisolvens. J Biol Chem 241, 1350–1354.
    [Google Scholar]
  25. Kim, Y. J., Liu, R. H., Rychlik, J. L. & Russell, J. B. ( 2002; ). The enrichment of a ruminal bacterium (Megasphaera elsdenii YJ-4) that produces the trans-10,cis-12 isomer of conjugated linoleic acid. J Appl Microbiol 92, 976–982.[CrossRef]
    [Google Scholar]
  26. Kim, E. J., Huws, S. A., Lee, M. R. F., Wood, J. D., Muetzel, S. M., Wallace, R. J. & Scollan, N. D. ( 2008; ). Fish oil increases the duodenal flow of long chain polyunsaturated fatty acids and trans-11 18 : 1 and decreases 18 : 0 in steers via changes in the rumen bacterial community. J Nutr 138, 889–896.
    [Google Scholar]
  27. Lanser, A. C. ( 1993; ). Conversion of oleic acid to 10-ketostearic acid by a Staphylococcus species. J Am Oil Chem Soc 70, 543–545.[CrossRef]
    [Google Scholar]
  28. Lock, A. L., Teles, B. M., Perfield, J. W., Bauman, D. E. & Sinclair, L. A. ( 2006; ). A conjugated linoleic acid supplement containing trans-10, cis-12 reduces milk fat synthesis in lactating sheep. J Dairy Sci 89, 1525–1532.[CrossRef]
    [Google Scholar]
  29. Maia, M. R. G., Chaudhary, L. C., Figueres, L. & Wallace, R. J. ( 2007; ). Metabolism of polyunsaturated fatty acids and their toxicity to the microflora of the rumen. Antonie Van Leeuwenhoek 91, 303–314.[CrossRef]
    [Google Scholar]
  30. Mensink, R. P., Zock, P. L., Kester, A. D. & Katan, M. B. ( 2003; ). Effects of dietary fatty acids and carbohydrates on the ratio of serum total to HDL cholesterol and on serum lipids and apolipoproteins: a meta-analysis of 60 controlled trials. Am J Clin Nutr 77, 1146–1155.
    [Google Scholar]
  31. Moon, C. D., Pacheco, D. M., Kelly, W. J., Leahy, S. C., Li, D., Kopecny, J. & Attwood, G. T. ( 2008; ). Reclassification of Clostridium proteoclasticum as Butyrivibrio proteoclasticus comb. nov., a butyrate-producing ruminal bacterium. Int J Syst Evol Microbiol 58, 2041–2045.[CrossRef]
    [Google Scholar]
  32. Morris, L. J. ( 1970; ). Mechanisms and stereochemistry in fatty acid metabolism – Fifth Colworth Medal Lecture. Biochem J 118, 681–693.
    [Google Scholar]
  33. Mortimer, C. E. & Niehaus, W. G. ( 1972; ). Enzymatic isomerization of oleic acid to trans-Δ10-octadecenoic acid. Biochem Biophys Res Commun 49, 1650–1656.[CrossRef]
    [Google Scholar]
  34. Nam, I. S. & Garnsworthy, P. C. ( 2007; ). Biohydrogenation of linoleic acid by rumen fungi compared with rumen bacteria. J Appl Microbiol 103, 551–556.[CrossRef]
    [Google Scholar]
  35. Nugent, A. P. ( 2004; ). The metabolic syndrome. Nutr Bull 29, 36–43.[CrossRef]
    [Google Scholar]
  36. Paillard, D., McKain, N., Chaudhary, L. C., Walker, N. D., Pizette, F., Koppova, I., McEwan, N. R., Kopečný, J., Vercoe, P. E. & other authors ( 2007; ). Relation between phylogenetic position, lipid metabolism and butyrate production by different Butyrivibrio-like bacteria from the rumen. Antonie Van Leeuwenhoek 91, 417–422.[CrossRef]
    [Google Scholar]
  37. Pariza, M. W. ( 2004; ). Perspective on the safety and effectiveness of conjugated linoleic acid. Am J Clin Nutr 79, 1132S–1136S.
    [Google Scholar]
  38. Polan, C. E., McNeill, J. J. & Tove, S. B. ( 1964; ). Biohydrogenation of unsaturated fatty acids by rumen bacteria. J Bacteriol 88, 1056–1064.
    [Google Scholar]
  39. Rosenfeld, I. S. & Tove, S. B. ( 1971; ). Biohydrogenation of unsaturated fatty acids. VI. Source of hydrogen and stereospecificity of reduction. J Biol Chem 246, 5025–5030.
    [Google Scholar]
  40. Sæbø, A., Sæbø, P., Griinari, J. M. & Shingfield, K. J. ( 2005; ). Effect of abomasal infusion of geometric isomers of 10,12 conjugated linoleic acid on milk fat synthesis in dairy cows. Lipids 40, 823–832.[CrossRef]
    [Google Scholar]
  41. Scollan, N. D., Dhanoa, M. S., Choi, N. J., Maeng, W. J., Enser, M. & Wood, J. D. ( 2001; ). Biohydrogenation and digestion of long chain fatty acids in steers fed on different sources of lipid. J Agric Sci Camb 136, 345–355.
    [Google Scholar]
  42. Shingfield, K. J. & Griinari, J. M. ( 2007; ). Role of biohydrogenation intermediates in milk fat depression. Eur J Lipid Sci Technol 109, 799–816.[CrossRef]
    [Google Scholar]
  43. Shingfield, K. J., Chilliard, Y., Toivonen, V., Kairenius, P. & Givens, D. I. ( 2008; ). Trans fatty acids and bioactive lipids in ruminant milk. In Bioactive Components of Milk. Adv Exp Med Biol 606, 3–65.
    [Google Scholar]
  44. Shingfield, K. J., Sæbø, A., Sæbø, P.-C., Toivonen, V. & Griinari, J. M. ( 2009; ). Effect of abomasal infusions of a mixture of octadecenoic acids on milk fat synthesis in lactating cows. J Dairy Sci 92, 4317–4329.[CrossRef]
    [Google Scholar]
  45. Troegeler-Meynadier, A., Nicot, M. C., Bayourthe, C., Moncoulon, R. & Enjalbert, F. ( 2003; ). Effects of pH and concentrations of linoleic and linolenic acids on extent and intermediates of ruminal biohydrogenation in vitro. J Dairy Sci 86, 4054–4063.[CrossRef]
    [Google Scholar]
  46. Wallace, R. J. & Brammall, M. L. ( 1985; ). The role of different species of rumen bacteria in the hydrolysis of protein in the rumen. J Gen Microbiol 131, 821–832.
    [Google Scholar]
  47. Wallace, R. J., Chaudhary, L. C., McKain, N., McEwan, N. R., Richardson, A. J., Vercoe, P. E., Walker, N. D. & Paillard, D. ( 2006; ). Clostridium proteoclasticum: a ruminal bacterium that forms stearic acid from linoleic acid. FEMS Microbiol Lett 265, 195–201.[CrossRef]
    [Google Scholar]
  48. Wallace, R. J., McKain, N., Shingfield, K. J. & Devillard, E. ( 2007; ). Isomers of conjugated linoleic acids are synthesized via different mechanisms in ruminal digesta and bacteria. J Lipid Res 48, 2247–2254.[CrossRef]
    [Google Scholar]
  49. Waşowska, I., Maia, M. R. G., Niedzwiedzka, K. M., Czauderna, M., Ramalho Ribeiro, J. M. C., Devillard, E., Shingfield, K. J. & Wallace, R. J. ( 2006; ). Influence of fish oil on ruminal biohydrogenation of C18 unsaturated fatty acids. Br J Nutr 95, 1199–1211.[CrossRef]
    [Google Scholar]
  50. World Health Organization ( 2003; ). Diet, nutrition and prevention of chronic diseases. WHO Technical Report Series 916, 1–148.
    [Google Scholar]
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Mass spectrum of the methyl ester of 10-O-18:0 that represented the most abundant product formed from -9-18:1 during 96 h incubations with [ PDF] (13 kb) Mass spectra of (a) the 4,4-dimethyloxazoline derivative of -11-18:1 synthesized from -9, -11-18:2 during 24 h incubations with and (b) the 4,4-dimethyloxazoline derivative of -10-18:1 synthesized from -10, -12-18:2 during 24 h incubations with [ PDF] (17 kb)

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Mass spectrum of the methyl ester of 10-O-18:0 that represented the most abundant product formed from -9-18:1 during 96 h incubations with [ PDF] (13 kb) Mass spectra of (a) the 4,4-dimethyloxazoline derivative of -11-18:1 synthesized from -9, -11-18:2 during 24 h incubations with and (b) the 4,4-dimethyloxazoline derivative of -10-18:1 synthesized from -10, -12-18:2 during 24 h incubations with [ PDF] (17 kb)

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