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Effects of copper and cadmium ions on the physicochemical properties of lipids of the marine bacterium Pseudomonas putida IB28 at different growth temperatures

  • Biochemistry of Microorganisms
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Abstract

The phospholipid and fatty acid composition and thermotropic behavior of total lipids were studied in the metal-accumulating marine strain Pseudomonas putida IB28 grown in the presence of Cu2+ and Cd2+ at 4 and 24°C. Despite the changes in acidic lipid content, unsaturated/saturated fatty acid ratio, and cyclopropane fatty acid level, the temperature range of calorimetric phase transitions of bacterial total lipids was slightly altered under these factors. The suppressive action of heavy metals on bacterial growth is attributable to the phase separation of lipids and, as a consequence, to a sharp increase in the ion permeability of the lipid bilayer. The increase in acidic phospholipid level under the influence of Cu2+ and Cd2+, especially at 24°C, is likely to be indicative of their complexation with heavy metal ions.

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References

  1. Bezverbnaya, I.P., Dimitrieva, G.Yu., Tazaki, K., and Watanabe, H., An Experience of Evaluation of Near-Shore Seawaters in Primorye Based on Microbial Indication, Vodnye Resursy, 2003, no. 2, pp. 222–231.

  2. Ivkov, V.G. and Berestovsky, G.N., Dinamicheskaya struktura lipidnogo bisloya (Dynamic Structure of Lipid Bilayer), Moscow: Nauka, 1981.

    Google Scholar 

  3. Nikolaev, Yu.A., Prosser, J.I., and Panikov, N.S., Extracellular Factors of Adaptation to Unfavorable Conditions in a Periodic Culture of Pseudomonas fluorescens, Mikrobiologiya, 2000, vol. 69, no. 5, pp. 629–635.

    Google Scholar 

  4. Abbas, C.A. and Card, G.L., The Relationships between Growth Temperature, Fatty Acid Composition and the Physical State and Fluidity of Membrane Lipids in Yersinia enterocolitica, Biochim. Biophys. Acta, 1980, vol. 602, no. 3. pp. 469–476.

    Article  PubMed  CAS  Google Scholar 

  5. Bakholdina, S.I., Sanina, N.M., Krasikova, I.N., et al., The Impact of Abiotic Factors (Temperature and Glucose) on Physicochemical Properties of Lipids from Yersinia pseudotuberculosis, Biochimie, 2004, vol. 86, pp. 875–881.

    Article  PubMed  CAS  Google Scholar 

  6. Barton, P.G., The Influence of Surface Charge Density of Phosphatides on the Binding of Some Cations, J. Biol. Chem., 1968, vol. 243, pp. 3884–3890.

    PubMed  CAS  Google Scholar 

  7. Beney, L. and Gervais, P., Influence of the Fluidity of the Membrane on the Response of Microorganisms to Environmental Stresses, Appl. Microbiol. Biotechnol., 2001, vol. 57, no. 1–2, pp. 34–42.

    PubMed  CAS  Google Scholar 

  8. Beney, L., Mille, Y., and Gervais, P., Death of Escherichia coli during Rapid and Severe Dehydration is Related to Lipid Phase Transition, Appl. Microbiol. Biotechnol., 2004, vol. 65, pp. 457–464.

    Article  PubMed  CAS  Google Scholar 

  9. Cervantes, C. and Gutierez-Corona, F., Copper Resistance Mechanisms in Bacteria and Fungi, FEMS Microbiol. Rev., 1994, vol. 14, no. 2, pp. 23–30.

    Article  Google Scholar 

  10. Domènech, O., Morros, A., Cabañas, M.E., et al., Supported Planar Bilayers from Hexagonal Phases, Biochim. Biophys. Acta, 2007, vol. 1768, pp. 100–106.

    Article  PubMed  CAS  Google Scholar 

  11. Härtig, C., Loffhagen, N., and Harms, H., Formation of Trans Fatty Acids Is Not Involved in Growth-Linked Membrane Adaptation of Pseudomonas putida, Appl. Environ. Microbiol., 2005, vol. 71, pp. 1915–1922.

    Article  PubMed  CAS  Google Scholar 

  12. Hazel, J.R. and Williams, E.E., The Role of Alterations in Membrane Lipid Composition in Enabling Physiological Adaptation of Organisms to Their Physical Environment, Prog. Lipid Res., 1990, vol. 29, pp. 167–227.

    Article  PubMed  CAS  Google Scholar 

  13. Jøstensen, J.-P. and Landfald, B., Influence of Growth Conditions on Fatty Acid Composition of a Polyunsaturated Fatty-Acid-producing Vibrio Species, Arch. Microbiol., 1996, vol. 165, pp. 306–310.

    Article  PubMed  Google Scholar 

  14. Julshamn, K. and Andersen, K.J., A Study on the Digestion of Human Muscle Biopsies for Trace Metal Analysis Using an Organic Tissue Solubilizer, Anal. Biochem., 1979, vol. 98, pp. 315–318.

    Article  PubMed  CAS  Google Scholar 

  15. Kozloff, L.M., Turner, M.A., Arellano, F., and Lute, M., Phosphatidylinositol, a Phospholipid of Ice-nucleating Bacteria, J. Bacteriol., 1991, vol. 173, pp. 2053–2060.

    PubMed  CAS  Google Scholar 

  16. Kramer, J.K.G., Fouchard, R.C., and Jenkins, K.J., Differences in Chromatographic Properties of Fused Silica Capillary Columns, Coated, Crosslinked, Bonded, or Crosslinked and Bonded with Polyethylene Glycols (Carbowax 20M) Using Complex Fatty Acid Methyl Ester Mixtures, J. Chromatogr. Sci., 1985, vol. 23, no. 2. pp. 54–56.

    CAS  Google Scholar 

  17. Laddaga, R.A. and Silver, S., Cadmium Uptake in Escherichia coli K-12, J. Bacteriol., 1985, vol. 162, pp. 1100–1105.

    PubMed  CAS  Google Scholar 

  18. Lewis, R. and McElhaney, R.N., Thermotropic Phase Behavior of Models Membranes Composed of Phosphatidylcholines Containing iso-Branched Fatty Acids. 1. Differential Scanning Calorimetric Study, Biophys. J., 2000, vol. 79, pp. 1455–1464.

    Article  PubMed  CAS  Google Scholar 

  19. McGarrity, J.T. and Armstrong, J.B., Phase Transition Behaviour of Artificial Liposomes Composed of Phosphatidylcholines Acylated with Cyclopropane Fatty Acids, Biochim. Biophys. Acta., 1981, vol. 640, pp. 544–548.

    Article  PubMed  CAS  Google Scholar 

  20. Medeot, D.B., Bueno, M.A., Dardanelli, M.S., and García de Lema, M., Adaptational Changes in Lipids of Bradyrhizobium SEMIA 6144 Nodulating Peanut as a Response to Growth Temperature and Salinity, Curr. Microbiol., 2007, vol. 54, pp. 31–35.

    Article  PubMed  CAS  Google Scholar 

  21. Meyer, J.-M., Pyoverdines: Pigments, Siderophores and Potential Taxonomic Markers of Fluorescent Pseudomonas Species, Arch. Microbiol., 2000, vol. 174, no. 3, pp. 135–152.

    Article  PubMed  CAS  Google Scholar 

  22. Morein, S., Andersson, A., Rilfors, L., and Lindblom, G., Wild-Type Escherichia coli Cells Regulate the Membrane Lipid Composition in a “Window” between Gel and non-Lamellar Structures, J. Biol. Chem., 1996, vol. 22, pp. 6801–6809.

    Google Scholar 

  23. Mouritsen, O.G. and Kinnunen, P.K.J., Role of Lipid Organisation and Dynamics for Membrane Fluidity, Biological Membranes, Boston: Birkhäuser, 1996, pp. 463–502.

    Google Scholar 

  24. Mueller, P., Rudin, D.O., Tien, H., and Wescott, W., Reconstitution of Cell Membrane Structure in vitro and Its Transformation into an Excitable System Nature, 1962, vol. 194, pp. 979–981.

    CAS  Google Scholar 

  25. Nagamachi, E., Shibuya, S., Hirai, Y., et al. Adaptational Changes of Fatty Acid Composition and Physical State of Membrane Lipids Following the Change of Growth Temperature in Yersinia enterocolitica, Microbiol. Immunol., 1991, vol. 35, no. 12, pp. 1085–1093.

    PubMed  CAS  Google Scholar 

  26. Nies, D.H., Microbial Heavy-Metal Resistance, Appl. Microbiol. Biotechnol., 1999, vol. 51, pp. 730–750.

    Article  PubMed  CAS  Google Scholar 

  27. Park, J.B., Kim, H.J., Ryu, P.D., and Moczydlowski, E. Effect of Phosphatidylserine on Unitary Conductance and Ba2+ Block of the BK Ca2+-Activated K+ Channel: Reexamination of the Surface Charge Hypothesis, J. Gen. Physiol., 2003, vol. 121, P. 375–397.

    Article  PubMed  CAS  Google Scholar 

  28. Pinkart, H.C. and White, D.C., Phospholipid Biosynthesis and Solvent Tolerance in Pseudomonas putida Strains, J. Bacteriol., 1997, vol. 179, pp. 4219–4226.

    PubMed  CAS  Google Scholar 

  29. Sanina, N.M. and Kostetsky, E.Y., Seasonal Changes in Thermotropic Behavior of Phosphatidylcholine and Phosphatidylethanolamine in Different Organs of the Ascidian Halocynthia aurantium, Comp. Biochem. Physiol., Ser. B., 2001, vol. 128, pp. 295–305.

    Article  CAS  Google Scholar 

  30. Shiba, Y., Yokoyama, Y., Aono, Y., et al., Activation of the Rcs Signal Transduction System Is Responsible for the Thermosensitive Growth Defect of an Escherichia coli Mutant Lacking Phosphatidylglycerol and Cardiolipin, J. Bacteriol., 2004, vol. 186, no. 19, pp. 6526–6535.

    Article  PubMed  CAS  Google Scholar 

  31. Tang, Y. and Hollingsworth, R., Regulation of Lipid Synthesis in Bradyrhizobium japonicum: Low Oxygen Concentrations Trigger Phosphatidylinositol Biosynthesis, Appl. Environ. Microbiol., 1998, vol. 64, pp. 1963–1966.

    PubMed  CAS  Google Scholar 

  32. Theuvenet, A.P.R., Kesseles, B.G.F., Blankensteijn, W.M., and Borst-Pawels, G.W.H.F., A Comparative Study of K+-Loss from a Cadmium-sensitive and a Cadmium-resistant Strain of Saccharomyces cerevisiae, FEMS Microbiol. Lett., 1987, vol. 43, pp. 147–153.

    Article  CAS  Google Scholar 

  33. Vanounou, S., Parola, A.H., and Fishov, I., Phosphatidylethanolamine and Phosphatidylglycerol Are Segregated into Different Domains in Bacterial Membrane. A Study with Pyrene-Labelled Phospholipids, Mol. Microbiol., 2003, vol. 49, pp. 1067–1079.

    Article  PubMed  CAS  Google Scholar 

  34. Vaskovsky, V. and Khotimchenko, S., HPTLC of Polar Lipids of Algae and Other Plants, J. High Resol. Chromatogr., 1982, vol. 5, pp. 635–636.

    Article  CAS  Google Scholar 

  35. Vaskovsky, V.E., Kostetsky, E.Y., and Vasendin, I.M., A Universal Reagent for Phospholipid Analysis, J. Chromatogr., 1975, vol. 114, pp. 129–141.

    Article  PubMed  CAS  Google Scholar 

  36. Vaskovsky, V.E. and Terekhova, T.A., HPTLC of Phospholipid Mixtures Containing Phosphatidylglycerol, J. High. Resol. Chromatogr., 1979, vol. 2, pp. 671–672.

    Article  Google Scholar 

  37. Wang, L., Li, F., and Zhou, Q., Contribution of Cell-Surface Components to Cu2+ Adsorption by Pseudomonas putida 5-x, Appl. Biochem. Biotechnol., 2006, vol. 128, no. 1, pp. 33–46.

    Article  PubMed  CAS  Google Scholar 

  38. Williams, W.P., Cold Induced Lipid Phase Transitions, Phil. Trans. Roy. Soc. London, Ser. B: Biol. Sci., 1990, vol. 326, pp. 555–570.

  39. Wolf, C., Koumanov, K., Tenchov, B., and Quinn, P.J., Cholesterol Favors Phase Separation of Sphingomyelin, Biophys. Chem., 2001, vol. 89, pp. 163–172.

    Article  PubMed  CAS  Google Scholar 

  40. Youchimizu, M. and Kimura, T., Study of Intestinal Microflora of Salmonids, Fish Pathol., 1976, vol. 10, pp. 243–259.

    Google Scholar 

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Correspondence to O. B. Popova.

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Original Russian Text © O.B. Popova, N.M. Sanina, G.N. Likhatskaya, I.P. Bezverbnaya, 2008, published in Biologiya Morya.

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Popova, O.B., Sanina, N.M., Likhatskaya, G.N. et al. Effects of copper and cadmium ions on the physicochemical properties of lipids of the marine bacterium Pseudomonas putida IB28 at different growth temperatures. Russ J Mar Biol 34, 179–185 (2008). https://doi.org/10.1134/S1063074008030073

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