Abstract
The occurrence oftrans unsaturated fatty acids as by-products of fatty acid transformations carried out by the obligate anaerobic ruminal microflora has been well known for a long time. In recent years, fatty acids withtrans configurations also have been detected in the membrane lipids of various aerobic bacteria. Besides several psychrophilic organisms, bacteria-degrading pollutants, such asPseudomonas putida, are able to synthesize these compoundsde novo. In contrast to thetrans fatty acids formed by rumen bacteria, the membrane constituents of aerobic bacteria are synthesized by a direct isomerization of the complementarycis configuration of the double bond without a shift of the position. This system of isomerization is located in the cytoplasmic membrane. The conversion ofcis unsaturated fatty acids totrans changes the membrane fluidity in response to environmental stimuli, particularly where growth is inhibited due to the presence of high concentrations of toxic substances. Under these conditions, lipid synthesis also stops so that the cells are not able to modify their membrane fluidity by any other mechanism.
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Bligh, E.G., and Dyer, W.J. (1959) A Rapid Method of Total Lipid Extraction and Purification,Can. J. Biochem. Physiol. 37, 911–917.
Morrison, W.R., and Smith, L.M. (1964) Preparation of Fatty Acid Methyl Esters and Dimethylacetals from Lipids with Boron Fluoride-Methanol,J. Lipid Res. 5, 600–608.
Bowman, J.P., Skerratt, J.H., Nichols, P.D., and Sly, S.I. (1991) Phospholipid Fatty Acid and Lipopolysaccharide Fatty Acid Signature Lipids in Methane-Utilizing Bacteria,FEMS Microbiol. Ecology 85, 15–22.
Guckert, J.B., Ringelberg, D.B., White, D.C., Hanson, R.S., and Bratina, B.J. (1991) Membrane Fatty Acids as Phenotypic Markers in the Polyphasic Taxonomy of Methylotrophs within Proteobacteria,J. Gen. Microbiol. 137, 2631–2641.
Caudales, R., and Wells, J.M. (1991) Differentiation of Free-LivingAnabaena andNostoc Cyanobacteria on the Basis of Fatty Acid Composition,Int. J. Syst. Bacteriol. 42, 246–251.
Ringelberg, D.B., Townsend, G.T., de Weerd, K.A., Suflita, J.M., and White, D.C. (1994) Detection of the Anaerobic Dechlorinating MicroorganismDesulfomonile tiedjei in Environmental Matrices by Its Signature Lipopolysaccharide Branched-Long-Chain Hydroxy Fatty Acids,FEMS Microbiol. Ecology 14, 9–18.
Zelles, L., and Bai, Q.V. (1994) Fatty Acid Pattern of Phospholipids and Lipopolysaccharides in Environmental Samples,Chemosphere 28, 391–411.
Gambacorta, A., Trincone, A., Nicolaus, B., Lama, L., and de Rosa, M. (1994) Unique Features of Lipids of Archaea,System Appl. Microbiol. 16, 518–527.
Hamamoto, T., Takata, N., Kudo, T., and Horikoshi, K. (1994) Effect of Temperature and Growth Phase on Fatty Acid Composition of the PsychrophilicVibrio sp. Strain no. 5710,FEMS Microbiol. Lett. 119, 77–81.
Henderson, R.J., Millar, R.M., Sargent, J.R., and Jostensen, J.P. (1993)Trans-Monoenoic and Polyunsaturated Fatty Acids in Phospholipids of aVibrio Species of Bacterium in Relation to Growth Conditions,Lipids 28, 389–396.
Nichols, D.S., McMeekin, T.A., and Nichols, P.D. (1994) Manipulation of Polyunsaturated, Branched-Chain andTrans-Fatty Acid Production inShewanella putrefaciens Strain ACAM 342,Microbiology 140, 577–584.
Ratledge, S., and Wilkinson, S.G. (1988)Microbial Lipids, Vols. 1 and 2. Academic Press, New York.
Makula, R.A. (1978) Phospholipid Composition of Methane-Utilizing Bacteria,J. Bacteriol. 134, 771–777.
Nichols, P.D., Smith, G.A., Antworth, C.P., Hanson, R.S., and White, D.C. (1985) Phospholipid and Lipopolysaccharide Normal and Hydroxy Fatty Acids as Potential Signatures for Methane-Oxidizing Bacteria,FEMS Microbiol. Ecology 31, 327–335.
Mackie, R.I., White, B.A., and Bryant, M.P. (1991) Lipid Metabolism in Anaerobic Ecosystems,CRC Crit. Rev. Microbiol. 17, 449–479.
Eyssen, H., and Verhulst, A. (1984) Biotransformation of Linoleic Acid and Bile Acids byEubacterium lentum, Appl. Environ. Microbiol. 47, 39–43.
Verhulst, A., Parmentier, G., Janssen, G., Asselberghs, S., and Eyssen, H. (1986) Biotransformation of Unsaturated Long-Chain Fatty Acids byEubacterium lentum, Appl. Environ. Microbiol. 51, 532–538.
Emken, E.A. (1984) Nutrition and Biochemistry ofTrans and Positional Fatty Acid Isomers in Hydrogenated Oils,Ann. Rev. Nutr. 4, 339.
Pettersen, J., and Opstvedt, J. (1992)Trans Fatty Acids. 5. Fatty Acid Composition of Lipids of the Brain and Other Organs in Suckling Piglets,Lipids 27, 761.
Jones, D. (1993)Trans-Fatty Acids and Dieting,Lancet 341, 1093.
Chen, Z.-Y., Pelletier, G., Hollywood, R., and Ratnayke, W.M.N. (1995)Trans Fatty Acid Isomers in Canadian Human Milk,Lipids 30, 15–21.
Willett, W.C., Stampfer, M.J., Manson, J.E., Colditz, G.A., Speizer, F.E., Rosner, B.A., Sampson, L.A., and Hennekens, C.H. (1993) Intake ofTrans-Fatty Acids and Risk of Coronary Heart Disease Among Women,Lancet 341, 581–585.
Katan, M.B., and Mensink, R.P. (1992) Isomeric Fatty Acids and Serum Lipoprotein,Nutrition Reviews, 50, 46–48.
Mensink, R.P., and Katan, M.B. (1990) Effect of DietaryTrans Fatty Acids on High-Density and Low-Density Lipoprotein Cholesterol Levels in Health Subjects,New England Journal of Medicine 323, 439–445.
Seltzer, S. (1972)Cis-Trans Isomerization, inThe Enzymes (Boyer, P.D., ed.) Vol. 6, pp. 381–406, Academic Press, New York.
Gillam, F.T., Johns, R.B., Verheyen, T.V., Volkman, J.K., and Bavor, H.J. (1981)Trans-Monounsaturated Acids in Marine Bacterial Isolate,Appl. Environ. Microbiology 41, 849–856.
Guckert, J.B., Ringelberg, D.B., and White, D.C. (1987) Biosynthesis ofTrans Fatty Acids from Acetate in the BacteriumPseudomonas atlantica, Can. J. Microbiology 33, 748–754.
Diefenbach, R., Heipieper, H.J., and Keweloh, H. (1992) The Conversion ofCis- intoTrans-Unsaturated Fatty Acids inPseudomonas putida P8: Evidence for a Role in the Regulation of Membrane Fluidity,Appl. Microbiol. Biotechnol. 38, 382–387.
Heipieper, H.J., Diefenbach, R., and Keweloh, H. (1992) A Possible Mechanism of the Protection of the Phenol Degrading StrainPseudomonas putida P8 from the Toxicity of the Substrate: The Conversion ofCis- intoTrans-Unsaturated Fatty Acids,Appl. Environ. Microbiol. 58, 1847–1852.
Heipieper, H.J., and de Bont, J.A.M. (1994) Adaptation ofPseudomonas putida S12 to Ethanol and Toluene at the Level of Fatty Acid Composition of Membranes,Appl. Environ. Microbiol. 60, 4440–4444.
Weber, F.J., Isken, S., and de Bont, J.A.M. (1994)Cis/Trans Isomerization of Fatty Acids as a Defense Mechanism ofPseudomonas putida Strains to Toxic Concentrations of Toluene,Microbiology 140, 2013–2017.
Pinkart, H.C., White, D.C., Wolfram, J., and Rodgers, R. (1994) Xylene-Induced Changes in Membrane Structure of Solvent ResistantPseudomonas putida Idaho, in94th General Meeting of The American Society for Microbiology, Abstract book, K-85, p. 290.
Conrad, R.S., Wulf, R.G., and Ankrom, K.A. (1981) Fatty Acids ofPseudomonas aeruginosa Grown on Media Affecting Polymyxin Susceptibility,Curr. Microbiology 5, 231–234.
Kieft, T.L., Ringelberg, D.B., and White, D.C. (1994) Changes in Ester-Linked Phospholipid Fatty Acid Profiles of Subsurface Bacteria During Starvation and Desiccation in a Porous Medium,Appl. Environ. Microbiol. 60, 3292–3299.
Diefenbach, R. (1993) Mechanismen einer vermehrten Phenoltoleranz bei Bakerien, Ph.D. Thesis, University of Muenster, Muenster, Germany.
Guckert, J.B., Hood, M.A., and White, D.C. (1986) Phospholipid Ester-Linked Fatty Acid Profile Changes During Nutrient Deprivation ofVibrio cholerae: Increases in theTrans/Cis Ratio and Proportions of Cyclopropyl Fatty Acids,Appl. Environ. Microbiol. 52, 794–801.
Hood, M.A., Guckert, J.B., White, D.C., and Deck, F. (1986) Effect of Nutrient Deprivation on Lipid, Carbohydrate, DNA, RNA, and Protein Levels inVibrio cholerae, Appl. Environ. Microbiol. 52, 788–793.
Okuyama, H., Sasaki, S., Higashi, S., and Murata, N. (1990) TheTrans-Unsaturated Fatty Acid in a Psychrophilic Bacterium,Vibrio sp. strain ABE-1,J. Bacteriol. 172, 3515–3518.
Okuyama, H., Okajima, N., Sasaki, S., Higashi, S., and Murata, N. (1991) TheCis/Trans Isomerization of the Double Bond of a Fatty Acid as a Strategy for Adaptation to Changes in Ambient Temperature in the Psychrophilic BacteriumVibrio sp. Strain ABE-1,Biochem. Biophys. Acta 1084, 13–20.
Morita, N., Gotoh, M., Okajima, N., Okuyama, H., Hayashi, H., Higashi, S., and Murata, N. (1992) Both the Anaerobic Pathway and the Aerobic Desaturation Are Involved in the Synthesis of Unsaturated Fatty Acids inVibrio sp. Strain ABE-1,FEBS Lett. 297, 9–12.
Morita, N., Shibahara, A., Yamamoto, K., Shinkai, K., Kajimoto, G., and Okuyama, H. (1993) Evidence forCis-Trans Isomerization of a Double Bond in the Fatty Acids of the Psychrophilic BacteriumVibrio sp. strain ABE-1,J. Bacteriol. 175, 916–918.
Moss, C.W., and Daneshvar, M.I. (1992) Identification of Some Uncommon Monounsaturated Fatty Acids of Bacteria,J. Clin. Microbiology 30, 2511–2512.
Lamberto, M., and Ackman, R.G. (1994) Confirmation by Gas Chromatography/Mass Spectrometry ot Two UnusualTrans-3-Monoethylenic Fatty Acids from the Nova Scotian SeaweedsPalmaria palmata andChororidrus crispus, Lipids 29, 441–444.
Ohnishi, M., and Thompson, G.A. (1991) Biosynthesis of the UniqueTrans-Delta3-Hexadecenoic Acid Component of Chloroplast Phosphatidylglycerol: Evidence Concerning its Site and Mechanisms of Formation,Arch. Biochem. Biophys. 288, 591–599.
Silbert, D.F., Ladenson, R.C., and Honegger, J.L. (1973) The Unsaturated Fatty Acid Requirement inEscherichia coli. Temperature Dependence and Total Replacement by Branched-Chain Fatty Acids,Biochem. Biophys. Acta 311, 349–361.
Silbert, D.F., Ruch, F., and Vagelos, P.R. (1988) Fatty Acid Replacements in a Fatty Acid Auxotroph ofEscherichia coli, J. Bacteriol. 95, 1658–1665.
Cronan, J.E., and Gelman, E.P. (1975) Physical Properties of Membrane Lipids: Biological Relevance and Regulation,Bacteriol. Reviews 39, 232–256.
Ingram, L.O. (1990) Ethanol Tolerance in Bacteria,Crit. Rev. Biotechnol. 9, 305–320.
de Veaux, L.C., Cronan, J.E., and Smith, T.L. (1989) Genetic and Biochemical Characterization of a Mutation (fatA) That AllowsTrans Unsaturated Fatty Acids to Replace the EssentialCis Unsaturated Fatty Acids ofEscherichia coli, J. Bacteriol. 171, 1562–1568.
Magnuson, K., Jackowski, S., Rock, C.O., and Cronan, Jr., J.E. (1993) Regulation of Fatty Acid Biosynthesis inEscherichia coli, Microbiol. Reviews 57, 522–542.
Russell, N.J. (1984) Mechanisms of Thermal Adaptation in Bacteria: Blueprints for Survival,Trends Biochem. Sci. 9, 108–112.
Grau, R., and de Mendoza, D. (1993) Regulation of the Synthesis of Unsaturated Fatty Acids by Growth Temperature inBacillus subtilis, Mol. Microbiol. 8, 535–542.
Foot, M., Jeffcoat, R., and Russell, N.J. (1993) Some Properties, Including the Substrate,In Vivo, of the Delta9-Desaturase inMicrococcus cryophilus, Biochem. J. 209, 345–353.
Cronan, J.E., and Rock, C.O. (1987) Biosynthesis of Membrane Lipids, in Escherichia coliand Salmonella typhimurium cellular and Molecular Biology (Neidhardt F.C., ed.) Vol. 1, pp. 474–497, American Society for Microbiology, Washington, D.C.
Diefenbach, R., and Keweloh, H. (1994) Synthesis ofTrans Unsaturated Fatty Acids inPseudomonas putida P8 by Direct Isomerization of the Double Bond of Lipids,Arch. Microbiol. 162, 120–125.
Henderson, R.J., Millar, R.M., and Sargent, J.R. (1995) Effect of Growth Temperature on the Positional Distribution of Eicosapentaenoic Acid andTrans Hexadecenoic Acid in the Phospholipids of aVibrio species of Bacterium,Lipids 30, 181–185.
Heipieper, H.J., Weber, F.J., Sikkema, J., Keweloh, H., and de Bont, J.A.M. (1994) Mechanisms Behind Resistance of Whole Cells to Toxic Organic Solvents,Trends Biotechnol. 12, 409–415.
Sikkema, J., de Bont, J.A.M., and Poolman, B. (1995) Membrane Toxicity of Cyclic Hydrocarbons,Microbiol. Rev. 59, 201–222.
Sikkema, J., Weber, F.J., Heipieper, H.J., and de Bont, J.A.M. (1994) Cellular Toxicity of Lipophilic Compounds: Mechanisms, Implications, and Adaptations,Biocatalysis 10, 113–122.
Heipieper, H.J., Keweloh, H., and Rehm, H.J. (1991) Influence of Phenols on Growth and Membrane Permeability of Free and ImmobilizedEscherichia coli, Appl. Environ. Microbiol. 57, 1213–1217.
Kitagawa, S., Orinaka, M., and Hiratan, H. (1993) Depth-Dependent Change in Membrane Fluidity by Phenolic Compounds in Bovine Platelets and Its Relationship with Their Effects on Aggregation and Adenylate Cyclase Activity,Biochim. Biophys. Acta 1179, 277–282.
Melchior, D.L. (1982) Lipid Phase Transitions and Regulation of Membrane Fluidity in Prokaryotes, inCurrent Topics in Membrane and Transport (Razin, S., and Rottem, S., eds.) Vol. 17, pp. 263–316, Academic Press, New York.
Carruthers, A., and Melchior, D.L. (1983) Studies on the Relationship Between Bilayer and Water Permeability and Bilayer Physical State,Biochemistry 22, 5797–5807.
Melchior, D.L., and Carruthers, A. (1983) Studies on the Relationship Between Bilayer and Water Permeability and Bilayer Physical State,Biochemistry 22, 5808–5814.
Inoue, A., and Horikoshi, K. (1989) APseudomonas Thrives in High Concentrations of Toluene,Nature 338 264–266.
Cruden, D.L., Wolfram, J.H., Rogers, R.D. and Gibson, D.T. (1992) Physiological Properties of aPseudomonas Strain Which Grows with p-Xylene in a Two-Phase (Organic-Aqueous) Medium,Appl. Environ. Microbiol. 58, 2723–2729.
Weber, F.J., Ooijkaas, L.P., Schemen, R.M.W., Hartmans, S., and de Bont, J.A.M. (1993) Adaptation ofPseudomonas putida to High Concentrations of Styrene and Other Organic Compounds,Appl. Environ. Microbiol. 59, 3502–3504.
Cevc, G. (1991) How Membrane Chain-Melting Phase-Transition Temperature Is Affected by the Lipid Chain Assymmetry and Degree of Saturation—An Effective Chain-Length Model,Biochemistry 30, 7186–7193.
Suutari, M., and Laakso, S. (1994) Microbial Fatty Acids and Thermal Adaptation,Critical Reviews in Microbiology 20, 285–328.
Shinitzky, M. (1984) Membrane Fluidity and Cellular Functions, inPhysiology of Membrane Fluidity (Shinitzky, M., ed.) Vol. II, pp. 1–52, CRC Press, Boca Raton.
Sinensky, M. (1974) Homeoviscous Adaptation—A Homeostatic Process That Regulates the Viscosity of Membrane Lipids inEscherichia coli, Proc. Natl. Acad. Sci. USA 71, 522–525.
Ingram, L.O. (1986) Microbial Tolerance to Alcohols: Role of the Cell Membrane,Trends Biotechnol. February 1986, 40–44.
Keweloh, H., Diefenbach, R., and Rehm, H.J. (1991) Increase of Phenol Tolerance ofEscherichia coli by Alterations of the Fatty Acid Composition of the Membrane Lipids,Archives. Microbiol. 157, 49–53.
MacDonald, P.M., Sykes, B.D., and McElhaney, R.N. (1985) Flourine-19 Nuclear Magnetic Resonance Studies of Lipid Fatty Acyl Chain Order and Dynamics inAcholeplasma laidlawii B Membranes. A Direct Comparsion of the Effects ofCis andTrans Cyclopropane Ring and Double-Bond Substituents on Orientational Order,Biochemistry 24, 4651–4659.
Golden, N.G., and Powell, G.L. (1972) Stringent and Relaxed Control of Phospholipid Metabolism inEscherichia coli, J. Biol. Chem. 247, 6651–6658.
Jiang, P., and Cronan, J.E. (1994) Inhibition of Fatty Acid Synthesis inEscherichia coli in the Absence of Phospholipid Synthesis and Release by Thioesterase Action,J. Bacteriol. 176, 2814–2821.
Heipieper, H.J., Loffeld, B., Keweloh, H., and de Bont, J.A.M. (1995) TheCis/Trans Isomerisation of Unsaturated Fatty Acids inPseudomonas putida S12: An Indicator for Environmental Stress Due to Organic Compounds,Chemosphere 30, 1041–1051.
Keweloh, H., Weyrauch, G., and Rehm, H.J. (1990) Phenol Induced Membrane Changes in Free and ImmobilizedEscherichia coli, Appl. Microbiol. Biotechnol. 33, 66–71.
de Andres, C., Espuny, M.J., Robert, M., Mercade, M.E., Manresa, A., and Guinea, J. (1991) Cellular Lipid Accumulation byPseudomonas aeruginos 44TI,Appl. Microbiol. Biotechnol. 35, 813–816.
Vestal, J.R., and White, D.C. (1989) Lipid Analysis in Microbial Ecology,BioScience 39, 535–541.
White, D.C. (1993)In Situ Measurement of Microbial Biomass, Community Structure and Nutritional Status,Phil. Trans. R. Soc. Lond. A. 344, 59–67.
Ringelberg, D.B., and White, D.C. (1992) Fatty Acid Profiles, inBioremediation of Petroleum-Contaminated Soil on Kwajalein Island: Microbial Characterization and Biotreatability Studies (Jolley, H.I., and Donaldson, T.L., eds) pp. 31–36, Oak Ridge National Laboratory, Oak Ridge.
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Keweloh, H., Heipieper, H.J. Trans unsaturated fatty acids in bacteria. Lipids 31, 129–137 (1996). https://doi.org/10.1007/BF02522611
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DOI: https://doi.org/10.1007/BF02522611