Skip to main content
NCBI home page
Applied and Environmental Microbiology logoLink to Applied and Environmental Microbiology
. 1996 Aug;62(8):2773–2777. doi: 10.1128/aem.62.8.2773-2777.1996

Effect of Environmental Factors on the trans/cis Ratio of Unsaturated Fatty Acids in Pseudomonas putida S12

H J Heipieper, G Meulenbeld, Q van Oirschot, J de Bont
PMCID: PMC1388911  PMID: 16535373

Abstract

The membrane reactions of Pseudomonas putida S12 to environmental stress were investigated. Cells reacted to the addition of six different heavy metals with an increase in the ratio of trans to cis unsaturated fatty acids. A correlation among the increase in the trans/cis ratio, the toxic effects of the heavy metals, and nonspecific permeabilization of the cytoplasmic membrane, as indicated by an efflux of potassium ions, was measured. Cells previously adapted to toxic concentrations of toluene exhibited increased tolerance to all applied concentrations of zinc compared with nonadapted cells. Cells exposed to different temperatures grew optimally at 30(deg)C. The degree of saturation of the membrane fatty acids of these cells decreased with decreasing temperature. An increase in the trans/cis ratio of unsaturated fatty acids took place only at higher temperatures. Osmotic stress, expressed as reduced water activity, was obtained by using different types of solutes. Only in the presence of toxic concentrations of sodium chloride or sucrose did the trans/cis ratio increase. At no applied water activity a significant effect of glycerol on the trans/cis ratio was measured. When cells were exposed to different pHs, a distinct optimum cis/trans isomerase activity was measured at pHs between 4.0 and 5.0, whereas at higher or lower pHs no reaction occurred. This optimum coincided with a loss of viability between pH 4 and 5.

Full Text

The Full Text of this article is available as a PDF (219.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alemohammad M. M., Knowles C. J. Osmotically induced volume and turbidity changes of Escherichia coli due to salts, sucrose and glycerol, with particular reference to the rapid permeation of glycerol into the cell. J Gen Microbiol. 1974 May;82(1):125–142. doi: 10.1099/00221287-82-1-125. [DOI] [PubMed] [Google Scholar]
  2. Asha H., Gowrishankar J. Regulation of kdp operon expression in Escherichia coli: evidence against turgor as signal for transcriptional control. J Bacteriol. 1993 Jul;175(14):4528–4537. doi: 10.1128/jb.175.14.4528-4537.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BLIGH E. G., DYER W. J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959 Aug;37(8):911–917. doi: 10.1139/o59-099. [DOI] [PubMed] [Google Scholar]
  4. Bakker E. P., Mangerich W. E. The effects of weak acids on potassium uptake by Escherichia coli K-12 inhibition by low cytoplasmic pH. Biochim Biophys Acta. 1983 May 5;730(2):379–386. doi: 10.1016/0005-2736(83)90355-3. [DOI] [PubMed] [Google Scholar]
  5. Blom A., Harder W., Matin A. Unique and overlapping pollutant stress proteins of Escherichia coli. Appl Environ Microbiol. 1992 Jan;58(1):331–334. doi: 10.1128/aem.58.1.331-334.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Booth I. R. Regulation of cytoplasmic pH in bacteria. Microbiol Rev. 1985 Dec;49(4):359–378. doi: 10.1128/mr.49.4.359-378.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cevc G. How membrane chain melting properties are regulated by the polar surface of the lipid bilayer. Biochemistry. 1987 Oct 6;26(20):6305–6310. doi: 10.1021/bi00394a002. [DOI] [PubMed] [Google Scholar]
  8. Chapman D., Peel W. E., Kingston B., Lilley T. H. Lipid phase transitions in model biomembranes. The effect of ions on phosphatidylcholine bilayers. Biochim Biophys Acta. 1977 Jan 21;464(2):260–275. doi: 10.1016/0005-2736(77)90002-5. [DOI] [PubMed] [Google Scholar]
  9. Chen Q., Janssen D. B., Witholt B. Growth on octane alters the membrane lipid fatty acids of Pseudomonas oleovorans due to the induction of alkB and synthesis of octanol. J Bacteriol. 1995 Dec;177(23):6894–6901. doi: 10.1128/jb.177.23.6894-6901.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Diefenbach R., Keweloh H. Synthesis of trans unsaturated fatty acids in Pseudomonas putida P8 by direct isomerization of the double bond of lipids. Arch Microbiol. 1994;162(1-2):120–125. doi: 10.1007/s002030050112. [DOI] [PubMed] [Google Scholar]
  11. Frostegård A., Tunlid A., Båth E. Phospholipid Fatty Acid composition, biomass, and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Appl Environ Microbiol. 1993 Nov;59(11):3605–3617. doi: 10.1128/aem.59.11.3605-3617.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gage D. J., Neidhardt F. C. Adaptation of Escherichia coli to the uncoupler of oxidative phosphorylation 2,4-dinitrophenol. J Bacteriol. 1993 Nov;175(21):7105–7108. doi: 10.1128/jb.175.21.7105-7108.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gill C. O., Suisted J. R. The effects of temperature and growth rate on the proportion of unsaturated fatty acids in bacterial lipids. J Gen Microbiol. 1978 Jan;104(1):31–36. doi: 10.1099/00221287-104-1-31. [DOI] [PubMed] [Google Scholar]
  14. Guckert J. B., Hood M. A., White D. C. Phospholipid ester-linked fatty acid profile changes during nutrient deprivation of Vibrio cholerae: increases in the trans/cis ratio and proportions of cyclopropyl fatty acids. Appl Environ Microbiol. 1986 Oct;52(4):794–801. doi: 10.1128/aem.52.4.794-801.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hartmans S., Smits J. P., van der Werf M. J., Volkering F., de Bont J. A. Metabolism of Styrene Oxide and 2-Phenylethanol in the Styrene-Degrading Xanthobacter Strain 124X. Appl Environ Microbiol. 1989 Nov;55(11):2850–2855. doi: 10.1128/aem.55.11.2850-2855.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hartmans S., van der Werf M. J., de Bont J. A. Bacterial degradation of styrene involving a novel flavin adenine dinucleotide-dependent styrene monooxygenase. Appl Environ Microbiol. 1990 May;56(5):1347–1351. doi: 10.1128/aem.56.5.1347-1351.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hauser H. Effect of inorganic cations on phase transitions. Chem Phys Lipids. 1991 Mar;57(2-3):309–325. doi: 10.1016/0009-3084(91)90083-n. [DOI] [PubMed] [Google Scholar]
  18. Heipieper H. J., Diefenbach R., Keweloh H. Conversion of cis unsaturated fatty acids to trans, a possible mechanism for the protection of phenol-degrading Pseudomonas putida P8 from substrate toxicity. Appl Environ Microbiol. 1992 Jun;58(6):1847–1852. doi: 10.1128/aem.58.6.1847-1852.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Heipieper H. J., Keweloh H., Rehm H. J. Influence of phenols on growth and membrane permeability of free and immobilized Escherichia coli. Appl Environ Microbiol. 1991 Apr;57(4):1213–1217. doi: 10.1128/aem.57.4.1213-1217.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Heipieper H. J., de Bont J. A. Adaptation of Pseudomonas putida S12 to ethanol and toluene at the level of fatty acid composition of membranes. Appl Environ Microbiol. 1994 Dec;60(12):4440–4444. doi: 10.1128/aem.60.12.4440-4444.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Keweloh H., Heipieper H. J. Trans unsaturated fatty acids in bacteria. Lipids. 1996 Feb;31(2):129–137. doi: 10.1007/BF02522611. [DOI] [PubMed] [Google Scholar]
  22. Kroll R. G., Booth I. R. The relationship between intracellular pH, the pH gradient and potassium transport in Escherichia coli. Biochem J. 1983 Dec 15;216(3):709–716. doi: 10.1042/bj2160709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kroll R. G., Booth I. R. The role of potassium transport in the generation of a pH gradient in Escherichia coli. Biochem J. 1981 Sep 15;198(3):691–698. doi: 10.1042/bj1980691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kropinski A. M., Lewis V., Berry D. Effect of growth temperature on the lipids, outer membrane proteins, and lipopolysaccharides of Pseudomonas aeruginosa PAO. J Bacteriol. 1987 May;169(5):1960–1966. doi: 10.1128/jb.169.5.1960-1966.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lambert P. A., Hammond S. M. Potassium fluxes, first indications of membrane damage in micro-organisms. Biochem Biophys Res Commun. 1973 Sep 18;54(2):796–799. doi: 10.1016/0006-291x(73)91494-0. [DOI] [PubMed] [Google Scholar]
  26. MORRISON W. R., SMITH L. M. PREPARATION OF FATTY ACID METHYL ESTERS AND DIMETHYLACETALS FROM LIPIDS WITH BORON FLUORIDE--METHANOL. J Lipid Res. 1964 Oct;5:600–608. [PubMed] [Google Scholar]
  27. Marr A. G., Ingraham J. L. EFFECT OF TEMPERATURE ON THE COMPOSITION OF FATTY ACIDS IN ESCHERICHIA COLI. J Bacteriol. 1962 Dec;84(6):1260–1267. doi: 10.1128/jb.84.6.1260-1267.1962. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Meyer U., Schweim P., Fracella F., Rensing L. Close Correlation between Heat Shock Response and Cytotoxicity in Neurospora crassa Treated with Aliphatic Alcohols and Phenols. Appl Environ Microbiol. 1995 Mar;61(3):979–984. doi: 10.1128/aem.61.3.979-984.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ohno Y., Yano I., Masui M. Effect of NaCl concentration and temperature on the phospholipid and fatty acid compositions of a moderately halophilic bacterium, Pseudomonas halosaccharolytica. J Biochem. 1979 Feb;85(2):413–421. doi: 10.1093/oxfordjournals.jbchem.a132348. [DOI] [PubMed] [Google Scholar]
  30. Pinkart H. C., Wolfram J. W., Rogers R., White D. C. Cell Envelope Changes in Solvent-Tolerant and Solvent-Sensitive Pseudomonas putida Strains following Exposure to o-Xylene. Appl Environ Microbiol. 1996 Mar;62(3):1129–1132. doi: 10.1128/aem.62.3.1129-1132.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sikkema J., de Bont J. A., Poolman B. Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev. 1995 Jun;59(2):201–222. doi: 10.1128/mr.59.2.201-222.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Springael D., Diels L., Hooyberghs L., Kreps S., Mergeay M. Construction and characterization of heavy metal-resistant haloaromatic-degrading Alcaligenes eutrophus strains. Appl Environ Microbiol. 1993 Jan;59(1):334–339. doi: 10.1128/aem.59.1.334-339.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Weber F. J., Isken S., de Bont J. A. Cis/trans isomerization of fatty acids as a defence mechanism of Pseudomonas putida strains to toxic concentrations of toluene. Microbiology. 1994 Aug;140(Pt 8):2013–2017. doi: 10.1099/13500872-140-8-2013. [DOI] [PubMed] [Google Scholar]
  34. Weber F. J., Ooijkaas L. P., Schemen R. M., Hartmans S., de Bont J. A. Adaptation of Pseudomonas putida S12 to high concentrations of styrene and other organic solvents. Appl Environ Microbiol. 1993 Oct;59(10):3502–3504. doi: 10.1128/aem.59.10.3502-3504.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. van Dijck P. W., de Kruijff B., Verkleij A. J., van Deenen L. L., de Gier J. Comparative studies on the effects of pH and Ca2+ on bilayers of various negatively charged phospholipids and their mixtures with phosphatidylcholine. Biochim Biophys Acta. 1978 Sep 11;512(1):84–96. doi: 10.1016/0005-2736(78)90219-5. [DOI] [PubMed] [Google Scholar]
  36. van der Meer J. R., de Vos W. M., Harayama S., Zehnder A. J. Molecular mechanisms of genetic adaptation to xenobiotic compounds. Microbiol Rev. 1992 Dec;56(4):677–694. doi: 10.1128/mr.56.4.677-694.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Applied and Environmental Microbiology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES

OSZAR »