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Rumen ciliate protozoa contain high concentrations of conjugated linoleic acids and vaccenic acid, yet do not hydrogenate linoleic acid or desaturate stearic acid

Published online by Cambridge University Press:  08 March 2007

Estelle Devillard ,
Freda M. McIntosh ,
C. James Newbold  and
R. John Wallace
Estelle Devillard*
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK
Freda M. McIntosh
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK
C. James Newbold
Affiliation:
Institute of Rural Sciences, University of Wales, Aberystwyth, SY23 3AL, UK
R. John Wallace
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK
*
*Corresponding author: Dr Estelle Devillard, fax +44 (0)1224 716687, email [email protected]
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Abstract

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Conjugated linoleic acids (CLA) have been shown to improve human health. They are derived from the microbial conversion of dietary linoleic acid (cis-9,cis-12-18 : 2 (LA)) in the rumen. An investigation was undertaken to determine the role of ruminal ciliate protozoa v. bacteria in the formation of CLA and its precursor in animal tissues, vaccenic acid (trans-11-18 : 1 (VA)). Mixed protozoa from the sheep rumen contained at least two to three times more unsaturated fatty acids, including CLA and VA, than bacteria. Different species had different composition, with larger fibrolytic species such as Epidinium ecaudatum caudatum containing more than ten times more CLA and VA than some small species, including Entodinium nanellum. In incubations with ruminal microbial fractions (bacterial fraction (BAC), protozoal fraction (PRO)), LA metabolism was very similar in strained ruminal fluid (SRF) and in the BAC, while the PRO had LA-metabolising activity an order of magnitude lower. Using PCR-based methods, no genes homologous to fatty acid desaturase genes were found in cDNA libraries from ruminal protozoa. The absence of an alternative route of VA/CLA formation via desaturation of stearate was confirmed by incubations of SRF, BAC or PRO with [14C]stearate. Thus, although protozoa are rich in CLA and VA, they appear to lack the ability to form these two fatty acids from LA or stearate. The most likely explanation is that protozoa preferentially incorporate CLA and VA formed by bacteria. The implication of the present findings is that the flow of unsaturated fatty acids, including CLA and VA, from the rumen could depend on the flow of protozoa rather than bacteria.

Keywords

BiohydrogenationRumen protozoaConjugated linoleic acidsTrans fatty acids
Type
Research Article
Information
British Journal of Nutrition , Volume 96 , Issue 4 , October 2006 , pp. 697 - 704
Copyright
Copyright © The Nutrition Society 2006

References

Abaza, MA, Abou, Akkada, AR, El & Shazly, K (1975) Effect of rumen protozoa on dietary lipid in sheep. J Agric Sci 85, 135–143.CrossRefGoogle Scholar
Abe, M, Iriki, T, Tobe, N & Shibui, H (1981) Sequestration of holotrich protozoa in the reticulo-rumen of cattle. Appl Environ Microbiol 41, 758–765.CrossRefGoogle ScholarPubMed
Ankrah, P, Loerch, SC & Dehority, BA (1990) Sequestration, migration and lysis of protozoa in the rumen. J Gen Microbiol 136, 1869–1875.CrossRefGoogle Scholar
Belury, MA (2002) Dietary conjugated linoleic acid in health: physiological effects and mechanisms of action. Annu Rev Nutr 22, 505–531.CrossRefGoogle ScholarPubMed
Chalupa, W & Kutches, AJ (1968) Biohydrogenation of linoleic-1- 14 C-acid by rumen protozoa. J Anim Sci 27, 1502–1508.CrossRefGoogle Scholar
Coleman, GS (1992) The rate of uptake and metabolism of starch grains and cellulose particles by Entodinium species, Eudiplodinium maggii, some other entodiniomorphid protozoa and natural protozoal populations taken from the ovine rumen. J Appl Bacteriol 73, 507–513.CrossRefGoogle ScholarPubMed
Dawson, RM & Kemp, P (1969) The effect of defaunation on the phospholipids and on the hydrogenation of unsaturated fatty acids in the rumen. Biochem J 115, 351–352.CrossRefGoogle ScholarPubMed
Emmanuel, B (1974) On the origin of rumen protozoan fatty acids. Biochim Biophys Acta 337, 404–413.CrossRefGoogle ScholarPubMed
Folch, J, Lees, M, Sloane-Stanley, GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226, 497–509.CrossRefGoogle ScholarPubMed
Girard, V & Hawke, JC (1978) The role of holotrichs in the metabolism of dietary linoleic acid in the rumen. Biochim Biophys Acta 528, 17–27.CrossRefGoogle Scholar
Griinari, JM, Corl, BA, Lacy, SH, Chouinard, PY, Nurmela, KV & Bauman, DE (2000) Conjugated linoleic acid is synthesized endogenously in lactating dairy cows by delta(9)-desaturase. J Nutr 130, 2285–2291.CrossRefGoogle ScholarPubMed
Harfoot, CG (1978) Lipid metabolism in the rumen. Progr Lipid Res 17, 21–54.CrossRefGoogle ScholarPubMed
Harfoot, CG & Hazlewood, GP (1997) Lipid metabolism in the rumen. In The Rumen Microbial Ecosystem, 2nd ed., pp. 382–426 [Hobson, PN and Stewart, CS, editors]. London: Chapman & Hall.CrossRefGoogle Scholar
Herbert, D, Phipps, PJ & Strange, RE (1971) Chemical analysis of microbial cells. In Methods in Microbiology, pp. 209–344 [Norris, JR and Ribbons, DW, editors]. London: Academic Press.Google Scholar
Hungate, RE, Reichl, J & Prins, R (1971) Parameters of fermentation in a continuously fed sheep: evidence of a microbial rumination pool. Appl Microbiol 22, 1104–1113.CrossRefGoogle Scholar
Jouany, JP & Lassalas, B (2003) Effects of rumen protozoa on biohydrogenation of polyunsaturated fatty acids and synthesis of conjugated linoleic acids Proceedings of the International Conference on the Molecular Biology and Biotechnology of Ciliates and Anaerobic Protozoa The Netherlands: German Society for Protozoology NijmegenGoogle Scholar
Jouany, JP & Senaud, J (1979) Défaunation du rumen de mouton. Ann Biol Anim Biochem Biophys 19, 619–624.CrossRefGoogle Scholar
Kaluzny, MA, Duncan, LA, Merritt, MV & Epps, DE (1985) Rapid separation of lipid classes in high yield and purity using bonded phase column. J Lipid Res 26, 135–140.CrossRefGoogle Scholar
Katz, I & Keeney, M (1966) Characterization of the octadecenoic acids in rumen digesta and rumen bacteria. J Dairy Sci 49, 962–966.CrossRefGoogle ScholarPubMed
Keeney, M (1970) Lipid metabolism in the rumen. In Physiology and Metabolism in the Ruminant, pp. 489–503 [Phillipson, AT, editors]. Newcastle-upon-Tyne: Oriel Press.Google Scholar
Klopfenstein, TJ, Purser, DB & Tyznik, WJ (1966) Effect of defaunation on feed digestibility, rumen metabolism and blood metabolites. J Anim Sci 25, 765–773.CrossRefGoogle ScholarPubMed
Los, DA & Murata, N (1998) Structure and expression of fatty acid desaturases. Biochim Biophys Acta 1394, 3–15.CrossRefGoogle ScholarPubMed
Martin, C, Devillard, E, Michalet-Doreau, B (1999) Influence of sampling site on concentrations and carbohydrate-degrading enzyme activities of protozoa and bacteria in the rumen. J Anim Sci 77, 979–987.CrossRefGoogle ScholarPubMed
Noble, RC (1981) Digestion, absorption and transport of lipids in ruminant animals. In Lipid Metabolism in Ruminant Animals, pp. 57–93 [Christie, WW, editors]. Oxford: Pergamon Press.CrossRefGoogle Scholar
Pariza, MW (2004) Perspective on the safety and effectiveness of conjugated linoleic acid. Am J Clin Nutr 79 1132S – 1136SCrossRefGoogle ScholarPubMed
Pereira, SL, Leonard, AE & Mukerji, P (2003) Recent advances in the study of fatty acid desaturases from animals and lower eukaryotes. Prostaglandins Leukot Essent Fatty Acids 68, 97–106.CrossRefGoogle Scholar
Polan, CE, McNeill, JJ & Tove, SB (1964) Biohydrogenation of unsaturated fatty acids. J Bact 88, 1056–1064.CrossRefGoogle ScholarPubMed
Ricard, G, McEwan, NR & Dutilh, BE (2006) Horizontal gene transfer from bacteria to rumen ciliates indicates adaptation to their anaerobic carbohydrates rich environment. BMC Genomics 7, 22CrossRefGoogle ScholarPubMed
Ritzenthaler, KL, McGuire, MK, Falen, R, Shultz, TD, Dasgupta, N & McGuire, MA (2001) Estimation of conjugated linoleic acid intake by written dietary assessment methodologies underestimates actual intake evaluated by food duplicate methodology. J Nutr 131, 1548–1554.CrossRefGoogle ScholarPubMed
Singh, S & Hawke, JC (1979) The in vitro lipolysis and biohydrogenation of monogalactosyldiglyceride by whole rumen contents and its fractions. J Sci Food Agric 30, 603–612.CrossRefGoogle ScholarPubMed
Tonon, T, Harvey, D, Qing, R, Li, Y, Larson, TR & Graha, IA (2004) Identification of a fatty acid Delta11-desaturase from the microalga Thalassiosira pseudonana. FEBS Lett 563, 28–34.CrossRefGoogle ScholarPubMed
van de Vossenberg, JL & Joblin, KN (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.CrossRefGoogle ScholarPubMed
van Hoek, AH, van Alen, TA, Sprakel, VS, Hackstein, JH & Vogels, GD (1998) Evolution of anaerobic ciliates from the gastrointestinal tract: phylogenetic analysis of the ribosomal repeat from Nyctotherus ovalis and its relatives. Mol Biol Evol 15, 1195–1206.CrossRefGoogle ScholarPubMed
Viviani, R (1970) Metablism of long-chain fatty acids in the rumen. Adv Lipid Res 8, 267–346.CrossRefGoogle Scholar
Wasowska, I, Maia, MRG, Niedzwiedzka, KM, Czauderna, M, Ramalho, Ribeiro JMCDevillard, E, Shingfield, KJ & Wallace, RJ (2006) Influence of fish oil on ruminal biohydrogenation of C18 unsaturated fatty acids. Br J Nutr 95, 1199–1211.CrossRefGoogle ScholarPubMed
Weller, RA & Pilgrim, AF (1974) Passage of protozoa and volatile fatty acids from the rumen of the sheep and from a continuous in vitro fermentation system. Br J Nutr 32, 341–351.CrossRefGoogle ScholarPubMed
Williams, AG & Coleman, GS (1992) The Rumen Protozoa, New York: Springer-Verlag.CrossRefGoogle Scholar
Wongwathanarat, P, Michaelson, LV, Carter, AT, Lazarus, CM, Griffiths, G, Stobart, AK, Archer, DB & MacKenzie, DA (1999) Two fatty acid delta9-desaturase genes, ole1 and ole2, from Mortierella alpina complement the yeast ole1 mutation. Microbiology 145, 2939–2946.CrossRefGoogle ScholarPubMed
Wright, DE (1959) Hydrogenation of lipids by rumen protozoa. Nature 184, 875–876.CrossRefGoogle ScholarPubMed
Wright, DE (1960) Hydrogenation of chloroplast lipids by rumen bacteria. Nature 185, 546–547.Google ScholarPubMed