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Dietary Transformation of Lipid in the Rumen Microbial Ecosystem

  • Kim, Eun Joong (Institute of Biological, Environmental and Rural Sciences, Aberystwyth University) ;
  • Huws, Sharon A. (Institute of Biological, Environmental and Rural Sciences, Aberystwyth University) ;
  • Lee, Michael R.F. (Institute of Biological, Environmental and Rural Sciences, Aberystwyth University) ;
  • Scollan, Nigel D. (Institute of Biological, Environmental and Rural Sciences, Aberystwyth University)
  • Published : 2009.09.01

Abstract

Dietary lipids are rapidly hydrolysed and biohydrogenated in the rumen resulting in meat and milk characterised by a high content of saturated fatty acids and low polyunsaturated fatty acids (PUFA), which contributes to increases in the risk of diseases including cardiovascular disease and cancer. There has been considerable interest in altering the fatty acid composition of ruminant products with the overall aim of improving the long-term health of consumers. Metabolism of dietary lipids in the rumen (lipolysis and biohydrogenation) is a major critical control point in determining the fatty acid composition of ruminant lipids. Our understanding of the pathways involved and metabolically important intermediates has advanced considerably in recent years. Advances in molecular microbial technology based on 16S rRNA genes have helped to further advance our knowledge of the key organisms responsible for ruminal lipid transformation. Attention has focused on ruminal biohydrogenation of lipids in forages, plant oils and oilseeds, fish oil, marine algae and fat supplements as important dietary strategies which impact on fatty acid composition of ruminant lipids. Forages, such as grass and legumes, are rich in omega-3 PUFA and are a useful natural strategy in improving nutritional value of ruminant products. Specifically this review targets two key areas in relation to forages: i) what is the fate of the lipid-rich plant chloroplast in the rumen and ii) the role of the enzyme polyphenol oxidase in red clover as a natural plant-based protection mechanism of dietary lipids in the rumen. The review also addresses major pathways and micro-organisms involved in lipolysis and biohydrogenation.

Keywords

References

  1. Abde, M., T. Iriki, N. Tobe and H. Shibui. 1981. Sequestration of holotrich protozoa in the reticulo-rumen of cattle. Appl. Environ. Microbiol. 41:758-765
  2. Al-Mabruk, R. M., N. F. G. Beck and R. J. Dewhurst. 2004. Effects of silage species and supplemental vitamin E on the oxidative stability of milk. J. Dairy Sci. 87:406-412 https://doi.org/10.3168/jds.S0022-0302(04)73180-X
  3. Ashes, J. R., B. D. Siebert, S. K. Gulati, A. Z. Cuthbertson and T. W. Scott. 1992. Incorporation of n-3 fatty acids of fish oil into tissue and serum lipids of ruminants. Lipids 27:629-631 https://doi.org/10.1007/BF02536122
  4. Atkinson, R. L., E. J. Scholljegerdes, S. L. Lake, V. Nayigihugu, B. W. Hess and D. C. Rule. 2006. Site and extent of digestion, duodenal flow, and intestinal disappearance of total and esterified fatty acids in sheep fed a high-concentrate diet supplemented with high-linoleate safflower oil. J. Anim. Sci. 84:387-396
  5. Bauman, D. E. and A. L. Lock. 2006. Concepts in lipid digestion and metabolism in dairy cows. In: Proceedings of the 2006 Tri-State Dairy Nutrition Conference, Ohio USA. pp. 1-14
  6. Carriquiry, M., W. J. Weber, L. H. Baumgard and B. A. Crooker. 2008. In vitro biohydrogenation of four dietary fats. Anim. Feed Sci. Technol. 141:339-355 https://doi.org/10.1016/j.anifeedsci.2007.06.028
  7. Collomb, M., U. Butikofer, R. Sieber, B. Jeangros and J. O. Bosset. 2002. Composition of fatty acids in cow's milk fat produced in the lowlands, mountains and highlands of Switzerland using high-resolution gas chromatography. Intl. Dairy J. 12:649-659 https://doi.org/10.1016/S0958-6946(02)00061-4
  8. Counotte, G. H. M., R. A. Prins, R. H. A. M. Janssen and M. J. A. deBie. 1981. The role of Megasphaera elsdenii in the fermentation of D,L-(2-$^{13}C$)-lactate in the rumen of dairy cattle. Appl. Environ. Microbiol. 42:649-655
  9. Dawson, R. M. C. and P. Kemp. 1969. The effect of defaunation on the phospholipids and on the hydrogenation of unsaturated fatty acids in the rumen. Biochem. J. 115:351-352
  10. Devillard, E., F. M. McIntosh, C. J. Newbold and R. J. Wallace. 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
  11. Dewhurst, R. J., K. J. Shingfield, M. R. F. Lee and N. D. Scollan. 2006. Increasing the concentrations of beneficial polyunsaturated fatty acids in milk produced by dairy cows in high-forage systems. Anim. Feed Sci. Technol. 131:168-206 https://doi.org/10.1016/j.anifeedsci.2006.04.016
  12. Dohme, F., V. Fievez, K. Raes and D. I. Demeyer. 2003. Increasing levels of two different fish oils lower ruminal biohydrogenation of eicosapentaenoic and docosahexaenoic acid in vitro. Anim. Res. 52:309-320 https://doi.org/10.1051/animres:2003028
  13. Doreau, M. and Y. Chilliard. 1997. Effects of ruminal or postruminal fish oil supplementation on intake and digestion in dairy cows. Reprod. Nutr. Dev. 37:113-124 https://doi.org/10.1051/rnd:19970112
  14. Doreau, M. and A. Ferlay. 1994. Digestion and utilisation of fatty acids by ruminants. Anim. Feed Sci. Technol. 45:379-396 https://doi.org/10.1016/0377-8401(94)90039-6
  15. Engle, T. E., V. Fellner and J. W. Spears. 2001. Copper status, serum cholesterol, and milk fatty acid profile in Holstein cows fed varying concentrations of copper. J. Dairy Sci. 84:2308-2313 https://doi.org/10.3168/jds.S0022-0302(01)74678-4
  16. Fievez, V., B. Vlaeminck, T. Jenkins, F. Enjalbert and M. Doreau. 2007. Assessing rumen biohydrogenation and its manipulation in vivo, in vitro and in situ. Eur. J. Lipid Sci. Technol. 109:740-756 https://doi.org/10.1002/ejlt.200700033
  17. Fotouhi, N. and T. C. Jenkins. 1992. Resistance of fatty acyl amides to degradation and hydrogenation by ruminal microorganisms. J. Dairy Sci. 75:1527-1532 https://doi.org/10.3168/jds.S0022-0302(92)77909-0
  18. Gerson, T., A. John and A. S. D. King. 1985. The effects of dietary starch and fibre on the in vitro rates of lipolysis and hydrogenation by sheep rumen digesta. J. Agric. Sci. (Camb.). 105:27-30 https://doi.org/10.1017/S0021859600055659
  19. Gerson, T., A. John and A. S. D. King. 1986. Effects of feeding ryegrass of varying maturity on the metabolism and composition of lipids in the rumen of sheep. J. Agric. Sci. (Camb.). 106:445-448 https://doi.org/10.1017/S0021859600063310
  20. Gerson, T., A. John and B. R. Sinclair. 1983. The effect of dietary N on in vitro lipolysis and fatty acid hydrogenation in rumen digesta from sheep fed diets high in starch. J. Agric. Sci. (Camb.). 101:97-101 https://doi.org/10.1017/S0021859600036406
  21. Gerson, T., A. S. D. King, K. E. Kelly and W. J. Kelly. 1988. Influence of particle size and surface area on in vitro rates of gas production, lipolysis of triacylglycerol and hydrogenation of linoleic acid by sheep rumen digesta or Ruminococcus flavefaciens. J. Agric. Sci. (Camb.). 110:31-37 https://doi.org/10.1017/S002185960007965X
  22. Girard, V. and J. C. Hawke. 1978. The role of holotrichs in the metabolism of dietary linoleic acid in the rumen. Biochim. Biophys. Acta. 528:17-27 https://doi.org/10.1016/0005-2760(78)90048-6
  23. Givens, D. I. 2005. The role of animal nutrition in improving the nutritive value of animal-derived foods in relation to chronic disease. Proc. Nutr. Soc. 64:395-402 https://doi.org/10.1079/PNS200544
  24. Glasser, F., R. Schmidely, D. Sauvant and M. Doreau. 2008. Digestion of fatty acids in ruminants: a meta-analysis of flows and variation factors: 2. C18 fatty acids. Anim. 2:691-704
  25. Goldfine, H. 1982. Lipids of prokaryotes: structure and distribution. In: Current topics in membranes and transport (Ed. F. Bronner and A. Kleinzeller). Academic Press. New York and London. pp. 1-43
  26. Grabber, J. H. 2008. Mechanical maceration divergently shifts protein degradability in condensed-tannin vs. o-quinone containing conserved forages. Crop Sci. 48:804-813 https://doi.org/10.2135/cropsci2007.08.0461
  27. Harfoot, C. G. 1978. Lipid metabolism in the rumen. Prog. Lipid Res. 17:21-54
  28. Harfoot, C. G. and G. P. Hazlewood. 1997. Lipid metabolism in the rumen. In: The Rumen Microbial Ecosystem (Ed. P. N. Hobson and C. S. Stewart). Chapman & Hall. London. pp.382-426
  29. Harfoot, C. G., R. C. Noble and J. H. Moore. 1973. Food particles as a site for biohydrogenation of unsaturated fatty acids in the rumen. Biochem. J. 132:829-832
  30. Hawke, J. C. 1971. The incorporation of long-chain fatty acids into lipids by rumen bacteria and the effect on biohydrogenation. Biochim. Biophys. Acta. 248:167-170 https://doi.org/10.1016/0005-2760(71)90003-8
  31. Hawke, J. C. 1973. Lipids. In: Chemistry and Biochemistry of Herbage (Ed. U. W. Butler and R. W. Bailey). Academic Press.London. pp. 213-263
  32. Hawke, J. C. and W. R. Silcock. 1970. The in vitro rates of lipolysis and biohydrogenation in rumen contents. Biochim. Biophys. Acta. 218:201-212 https://doi.org/10.1016/0005-2760(70)90138-4
  33. Hazlewood, G. P. and R. M. C. Dawson. 1975. Isolation and properties of a phospholipids-hydrolyzing bacterium from ovine rumen fluid. J. Gen. Microbiol. 89:163-174 https://doi.org/10.1099/00221287-89-1-163
  34. Henderson, C. 1973. The effects of fatty acids on pure cultures of rumen bacteria. J. Agric. Sci. (Camb.). 81:107-112 https://doi.org/10.1017/S0021859600058378
  35. Hobson, P. N. and C. S. Stewart. 1997. Lipid metabolism in the rumen. In: The Rumen Microbial Ecosystem (Ed. P. N. Hobson and C. S. Stewart). Blackie Academic and Professional Press. London. pp. 382-419
  36. Hudson, J. A., Y. Cai, R. J. Corner, B. Morvan and K. N. Joblin. 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 https://doi.org/10.1046/j.1365-2672.2000.00968.x
  37. Hudson, J. A., B. Morvan and K. N. Joblin. 1998. Hydration of linoleic acid by bacteria isolated from ruminants. FEMS Microbiol. Lett. 169:277-282 https://doi.org/10.1111/j.1574-6968.1998.tb13329.x
  38. Hungate, R. E. 1966. The Rumen and its Microbes. Academic press, London and New York
  39. Hungate, R. E., J. Reichl and R. Prins. 1971. Parameters of fermentation in a continuously fed sheep: evidence of a microbial rumination pool. Appl. Microbiol. 22:1104-1113
  40. Huws, S. A., E. J. Kim, A. H. Kingston-Smith, M. R. F. Lee, S. M. Muetzel, C. J. Newbold, R. J. Wallace and N. D. Scollan. 2009. Rumen protozoa are rich in polyunsaturated fatty acids due to the ingestion of chloroplast. FEMS Microbiol. Ecol. In press https://doi.org/10.1111/j.1574-6941.2009.00717.x
  41. Huws, S. A., M. R. F. Lee, S. Muetzel, R. J. Wallace and N. D. Scollan. 2006. Effect of forage type and level of fish oil inclusion on bacterial diversity in the rumen. Reprod. Nutr. Dev. 46(Suppl. 1):S99
  42. Igarashi, K. and T. Yasui. 1985. Oxidation of free methionine and methionine residues in protein involved in the browning reaction of phenolic compounds. Agric. Biol. Chem. 49:2309-2315 https://doi.org/10.1271/bbb1961.49.2309
  43. Jenkins, T. C., R. J. Wallace, P. J. Moate and E. E. Mosley. 2008. Board-invited review: Recent advances in biohydrogenation of unsaturated fatty acids within the rumen microbial ecosystem. J. Anim. Sci. 86:397-412 https://doi.org/10.2527/jas.2007-0588
  44. Kemp, P. and D. J. Lander. 1984. Hydrogenation in vitro of alphalinolenic acid to stearic acid by mixed cultures of pure strains of rumen bacteria. J. Gen. Microbiol. 130:527-533
  45. Kemp, P., R. W. White and D. J. Lander. 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 https://doi.org/10.1099/00221287-90-1-100
  46. Kim, E. J., S. A. Huws, M. R. F. Lee, J. D. Wood, S. M. Muetzel, R. J. Wallace and N. D. Scollan. 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
  47. Kim, Y. J., R. H. Liu, J. L. Rychlik and J. B. Russell. 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 https://doi.org/10.1046/j.1365-2672.2002.01610.x
  48. Kopecny, J., M. Zorec, J. Mrazek, Y. Kobayashi and R. Marinsek-Logar. 2003. Butyrivibrio hungatei sp nov and Pseudobutyrivibrio xylanivorans sp. nov., butyrate-producing bacteria from the rumen. Int. J. Syst. Evol. Microbiol. 53:201-209 https://doi.org/10.1099/ijs.0.02345-0
  49. Lafontan, M., M. Berlan, V. Stich, F. Crampes, D. Riviere, I. de Glisezinski, C. Sengenes and J. Galitzky. 2002. Recent data on the regulation of lipolysis by catecholamines and natriuretic peptides. Ann. Endocrinol. 63:86-90
  50. Latham, M. J., J. E. Storry and M. E. Sharpe. 1972. Effect of lowroughage diets on the microflora and lipid metabolism in the rumen. Appl. Microbiol. 24:871-877
  51. Lee, M. R. F., J. D. O. Colmenero, A. L. Winters, N. D. Scollan and F. R. Minchin. 2006. Polyphenol oxidase activity in grass and its effect on plant-mediated lipolysis and proteolysis of Dactylis glomerata (cocksfoot) in a simulated rumen environment. J. Sci. Food Agric. 86:1503-1511 https://doi.org/10.1002/jsfa.2533
  52. Lee, M. R. F., P. R. Evans, G. R. Nute, R. I. Richardson and N. D. Scollan. 2009. A comparison between red clover silage and grass silage feeding on fatty acid composition, meat stability and sensory quality of the M. Longissimus muscle of dairy cull cows. Meat Sci. 81:738-744 https://doi.org/10.1016/j.meatsci.2008.11.016
  53. Lee, M. R. F., L. J. Harris, R. J. Dewhurst, R. J. Merry and N. D. Scollan. 2003. The effect of clover silages on long chain fatty acid rumen transformations and digestion in beef steers. Anim. Sci. 76:491-501
  54. Lee, M. R. F., L. J. Parfitt, N. D. Scollan and F. R. Minchin. 2007. Lipolysis in red clover with different polyphenol oxidase activities in the presence and absence of rumen fluid. J. Sci. Food Agric. 87:1308-1314 https://doi.org/10.1002/jsfa.2849
  55. Lee, M. R. F., V. J. Theobald, J. K. S. Tweed, A. L. Winters and N. D. Scollan. 2008a. Effect of feeding fresh or conditioned red clover on milk fatty acids and nitrogen utilization in lactating dairy cows. J. Dairy Sci. doi:10.3168/jds.2008-1692
  56. Lee, M. R. F., J. K. S. Tweed, F. R. Minchin and A. L. Winters. 2008b. Red clover polyphenol oxidase: activation, activity and efficacy under grazing. Anim. Feed Sci. Technol. doi:10.1016/j.anifeedsci.2008.06.013
  57. Lee, M. R. F., J. K. S. Tweed, N. D. Scollan and M. L. Sullivan. 2008c. Mechanism of polyphenol oxidase action in reducing lipolysis and proteolysis in red clover during batch culture incubation. Proc. Br. Soc. Anim. Sci. p. 31
  58. Lee, M. R. F., J. K. S. Tweed, N. D. Scollan and M. L. Sullivan. 2008d. Ruminal micro-organisms do not adapt to increase utilization of poly-phenol oxidase protected red clover protein and glycerol-based lipid. J. Sci. Food Agric. 88:2479-2485 https://doi.org/10.1002/jsfa.3366
  59. Lee, M. R. F., A. L. Winters, N. D. Scollan, R. J. Dewhurst, M. K. Theodorou and F. R. Minchin. 2004. Plant-mediated lipolysis and proteolysis in red clover with different polyphenol oxidase activities. J. Sci. Food Agric. 84:1639-1645 https://doi.org/10.1002/jsfa.1854
  60. Li, L. and J. C. Steffens. 2002. Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. Planta. 215:239-247 https://doi.org/10.1007/s00425-002-0750-4
  61. Lough, A. K. 1970. Aspects of lipid digestion in the ruminant. In: Physiology of Digestion and Metabolism in the Ruminant (Ed. A. T. Phillipson). Oriel Press. Newcastle upon Tyne, UK. pp. 519-528
  62. Lourenco, M., G. Van Ranst and V. Fievez. 2005. Differences in extent of lipolysis in red or white clover and ryegrass silages in relation to polyphenol oxidase activity. Comm. Agr. Appl. Biol. Sci. 70:169-172
  63. Maia, M. R. G., L. C. Chaudhary, L. Figueres and R. J. Wallace. 2007. Metabolism of polyunsaturated fatty acids and their toxicity to the microflora of the rumen. Antonie Van Leeuwenhoek. 91:303-314 https://doi.org/10.1007/s10482-006-9118-2
  64. Mayer, A. M. 2006. Polyphenol oxidases in plants and fungi: Going places? A review. Phytochem. 67:2318-2331 https://doi.org/10.1016/j.phytochem.2006.08.006
  65. Min, B. R., T. N. Barry, G. T. Attwood and W. C. McNabb. 2003. The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: a review. Anim. Feed Sci. Technol. 106:3-19 https://doi.org/10.1016/S0377-8401(03)00041-5
  66. Moore, B. M. and W. H. Flurkey. 1990. Sodium dodecyl sulphate activation of a plant polyphenoloxidase - effect of sodium dodecyl sulphate on enzymatic and physical characteristics of broad bean polyphenoloxydase. J. Biol. Chem. 265:4982-4988
  67. Moreno, D. A., N. Ilic, A. Poulev, D. L. Brasaemle, S. K. Fried and I. Raskin. 2003. Inhibitory effects of grape seed extract on lipases. Nutr. 19:876-879 https://doi.org/10.1016/S0899-9007(03)00167-9
  68. Murphy, D. J. 1999. Plant lipids - their metabolism, function and utilization. In: Plant Biochemistry and Molecular Biology (Ed. P. J. Lea and R. C. Leegood). John Wiley & Sons. New York. pp. 119-135
  69. Nam, I. S. and P. C. Garnsworthy. 2007. Biohydrogenation of linoleic acid by rumen fungi compared with rumen bacteria. J. Appl. Microbiol. 103:551-556 https://doi.org/10.1111/j.1365-2672.2007.03317.x
  70. Nozue, M., D. Arakawa, Y. Iwata, H. Shioiri and M. Kojima. 1999. Activation by proteolysis in vivo of 60-kd latent polyphenol oxidases in sweet potato cells in suspension culture. J. Plant Physiol. 155:297-301 https://doi.org/10.1016/S0176-1617(99)80108-4
  71. Or-Rashid, M. M., N. E. Odongo and B. W. McBride. 2007. Fatty acid composition of ruminal bacteria and protozoa, with emphasis on conjugated linoleic acid, vaccenic acid, and odd chain and branched-chain fatty acids. J. Anim. Sci. 85:1228-1234 https://doi.org/10.2527/jas.2006-385
  72. Paillard, D., N. McKain, L. C. Chaudhary, N. D. Walker, F. Pizette, I. Koppova, N. R. McEwan, J. Kopecny, P. E. Vercoe, P. Louis and R. J. Wallace. 2007. Relation between phylogenetic position, lipid metabolism and butyrate production by different Butyrivibrio-like bacteria from the rumen. Antonie Van Leeuwenhoek. 91:417-422 https://doi.org/10.1007/s10482-006-9121-7
  73. Palmquist, D. L., A. L. Lock, K. J. Shingfield and D. E. Bauman. 2005. Biosynthesis of conjugated linoleic acid in ruminants and humans. In: Advances in Food and Nutrition Research (Ed. S. L. Taylor) No. 50. Elsevier Academic Press. San Diego, CA. pp. 179-217
  74. Park, Y., J. Storkson, K. Albright, W. Liu and M. Pariza. 1999. Evidence that the trans-10,cis-12 isomer of conjugated linoleic acid induces body composition changes in mice. Lipids 34:235-241 https://doi.org/10.1007/s11745-999-0358-8
  75. Richardson, R. I., P. Costa, G. R. Nute and N. D. Scollan. 2005. The effect of feeding clover silage on polyunsaturated fatty acid and vitamin E content, sensory, colour and lipid oxidative shelf life of beef loin steaks. In: Proceedings of the 51st international congress of meat science and technology, Exploring the wide world of meat, Baltimore, USA. pp. 1654-1661
  76. Schauff, D. J. and J. H. Clark. 1989. Effects of prilled fatty acids and calcium salts of fatty acids in rumen fermentation, nutrient digestibilities, milk production and milk composition. J. Dairy Sci. 72:917-927 https://doi.org/10.3168/jds.S0022-0302(89)79185-2
  77. Scollan, N., J.-F. Hocquette, K. Nuernberg, D. Dannenberger, I. Richardson and A. Moloney. 2006. Innovations in beef production systems that enhance the nutritional and health value of beef lipids and their relationship with meat quality. Meat Sci. 74:17-33 https://doi.org/10.1016/j.meatsci.2006.05.002
  78. Scollan, N. D., M. S. Dhanoa, N. J. Choi, W. J. Maeng, M. Enser and J. D. Wood. 2001. Biohydrogenation and digestion of long chain fatty acids in steers fed on different sources of lipid. J. Agric. Sci. 136:345-355
  79. Scollan, N. D., M. Enser, S. K. Gulati, I. Richardson and J. D. Wood. 2003. Effects of including a ruminally protected lipid supplement in the diet on the fatty acid composition of beef muscle. Br. J. Nutr. 90:709-716 https://doi.org/10.1079/BJN2003933
  80. Shi, J., K. Arunasalam, D. Yeung, Y. Kakuda, G. Mittal and Y. M. Jiang. 2004. Saponins from edible legumes: Chemistry, processing, and health benefits. J. Med. Food 7:67-78 https://doi.org/10.1089/109662004322984734
  81. Shingfield, K. J. and J. M. Griinari. 2007. Role of biohydrogenation intermediates in milk fat depression. Eur. J. Lipid Sci. Technol. 109:799-816 https://doi.org/10.1002/ejlt.200700026
  82. Sinclair, L. A. 2007. Nutritional manipulation of sheep of the fatty acid composition neat: a review. J. Agric. Sci. 145:419-434 https://doi.org/10.1017/S0021859607007186
  83. Sinclair, L. A., S. L. Cooper, J. A. Huntington, R. G. Wilkinson, K. G. Hallett, M. Enser and J. D. Wood. 2005. In vitro biohydrogenation of n-3 polyunsaturated fatty acids protected against ruminal microbial metabolism. Anim. Feed Sci. Technol. 124:579-596
  84. Stewart, R. J., B. J. B. Sawyer, C. S. Bucheli and S. P. Robinson. 2001. Polyphenol oxidase is induced by chilling and wounding in pineapple. Aust. J. Plant Physiol. 28:181-191
  85. Sullivan, M. L., R. D. Hatfield, S. L. Thoma and D. A. Samac. 2004. Cloning and characterization of red clover polyphenol oxidase cDNAs and expression of active protein in Escherichia coli and transgenic alfalfa. Plant Physiol. 136:3234-3244 https://doi.org/10.1104/pp.104.047449
  86. Thipyapong, P., J. Melkonian, D. W. Wolfe and J. C. Steffens. 2004. Suppression of polyphenol oxidases increases stress tolerance in tomato. Plant Sci. 167:693-703 https://doi.org/10.1016/j.plantsci.2004.04.008
  87. van de Vossenberg, J. and K. N. Joblin. 2003. Biohydrogenation of C18 unsaturated fatty acids to stearic acid by a strain of Butyrivibrio hungatei from the bovine rumen. Lett. Appl. Microbiol. 37:424-428 https://doi.org/10.1046/j.1472-765X.2003.01421.x
  88. Van Dorland, H. A., M. Kreuzer, H. Leuenberger and H. R. Wettstein. 2008. Comparative potential of white and red clover to modify the milk fatty acid profile of cows fed ryegrassbased diets from zero-grazing and silage systems. J. Sci. Food Agric. 88:77-85 https://doi.org/10.1002/jsfa.3024
  89. Wachira, A. M., L. A. Sinclair, R. G. Wilkinson, K. Hallett, M. Enser and J. D. Wood. 2000. Rumen biohydrogenation of n-3 polyunsaturated fatty acids and their effects on microbial efficiency and nutrient digestibility in sheep. J. Agric. Sci. 135:419-428 https://doi.org/10.1017/S0021859699008370
  90. Wallace, R. J. 2004. Antimicrobial properties of plant secondary metabolites. Proc. Nutr. Soc. 63:621-629 https://doi.org/10.1079/PNS2004393
  91. Wallace, R. J., L. C. Chaudhary, N. McKain, N. R. McEwan, A. J. Richardson, P. E. Vercoe, N. D. Walker and D. Paillard. 2006. Clostridium proteoclasticum: a ruminal bacterium that forms stearic acid from linoleic acid. FEMS Microbiol. Lett. 265:195-201 https://doi.org/10.1111/j.1574-6968.2006.00487.x
  92. Wallace, R. J., N. McKain, K. J. Shingfield and E. Devillard. 2007. Isomers of conjugated linoleic acids are synthesized via different mechanisms in ruminal digesta and bacteria. J. Lipid Res. 48:2247-2254 https://doi.org/10.1194/jlr.M700271-JLR200
  93. Wang, J. H. and C. P. Constabel. 2004. Polyphenol oxidase overexpression in transgenic Populus enhances resistance to herbivory by forest tent caterpillar (Malacosoma disstria). Planta. 220:87-96 https://doi.org/10.1007/s00425-004-1327-1
  94. Williams, A. G. and C. S. Coleman. 1992. The rumen protozoa. Springer-Verlag, New York
  95. Williams, C. M. 2000. Dietary fatty acids and human health. Ann. Zootech. (Paris). 49:165-180 https://doi.org/10.1051/animres:2000116
  96. Williams, P. P., J. Gutierrez and R. E. Davis. 1963. Lipid metabolism of rumen ciliates and bacteria. II. Uptake of fatty acids and lipid analysis of Isotrichia intestinalis and rumen bacteria with further information on Entodinium simplex. Appl. Microbiol. 11:260-264
  97. Winters, A. L. and F. R. Minchin. 2001. Red clover and the future for pasture legumes as an alternative protein source for ruminants. In: IGER Innovation No. 5. pp. 30-33
  98. Winters, A. L., F. R. Minchin, T. P. T. Michaelson-Yeates, M. R. F. Lee and P. Morris. 2008. Latent and active polyphenol oxidase (PPO) in red clover (Trifolium pratense) and use of a low PPO mutant to study the role of PPO in proteolysis reduction. J. Agric. Food Chem. 56:2817-2824 https://doi.org/10.1021/jf0726177
  99. Wright, D. E. 1959. Hydrogenation of lipids by rumen protozoa. Nature 184:875-876 https://doi.org/10.1038/184875a0
  100. Wright, D. E. 1960. Hydrogenation of chloroplast lipids by rumen bacteria. Nature 185:546-547 https://doi.org/10.1038/185546a0

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