Coordinated response of phospholipids and acyl components of membrane lipids in Pseudomonas putida A (ATCC 12633) under stress caused by cationic surfactants

Microbiology (United Kingdom)

Volumn 160, Issue , 2014, Pages 2618-2626

  Heredia, Romina Marisa ^a   Boeris, Paola Sabrina ^a   Biasutti, María Alicia ^a   López, Gastón Alberto ^a   Paulucci, Natalia Soledad ^a   Lucchesi, Gloria Inés ^a  

^a DEPARTAMENTO DE QUÍMICA   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOLIPIN; CETRIMIDE; MEMBRANE PHOSPHOLIPID; PHOSPHATIDYLGLYCEROL; SATURATED FATTY ACID; UNSATURATED FATTY ACID; CATION; MEMBRANE LIPID; PHOSPHOLIPID; SURFACTANT; TETRADECYLTRIMETHYLAMMONIUM; TRIMETHYLAMMONIUM SALT DERIVATIVE;

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; CELL MEMBRANE FLUIDITY; CHEMICAL STRESS; CONTROLLED STUDY; DEGRADATION; FLUORESCENCE POLARIZATION; LIPID COMPOSITION; MEMBRANE COMPONENT; NONHUMAN; PSEUDOMONAS PUTIDA; CELL MEMBRANE; CHEMISTRY; DRUG EFFECTS; MEMBRANE FLUIDITY; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

PSEUDOMONAS PUTIDA;

CATIONS; CELL MEMBRANE; MEMBRANE FLUIDITY; MEMBRANE LIPIDS; PHOSPHOLIPIDS; PSEUDOMONAS PUTIDA; STRESS, PHYSIOLOGICAL; SURFACE-ACTIVE AGENTS; TRIMETHYL AMMONIUM COMPOUNDS;

EID: 84915748020     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.081943-0     Document Type: Article

References (65)

1. Aase, B., Sundheim, G., Langsrud, S. & Rørvik, L. M. (2000). Occurrence of and a possible mechanism for resistance to a quaternary ammonium compound in Listeria monocytogenes. Int J Food Microbiol 62, 57-63.
2. Baysse, C. & O'Gara, F. (2007). Role of membrane structure during stress signaling and adaptation in Pseudomonas. In Pseudomonas, pp. 193-224. Edited by J. L. Ramos & A. Filloux. New York: Springer.
3. Bernal, P., Muñoz-Rojas, J., Hurtado, A., Ramos, J. L. & Segura, A. (2007a). A Pseudomonas putida cardiolipin synthesis mutant exhibits increased sensitivity to drugs related to transport functionality. Environ Microbiol 9, 1135-1145.
4. Bernal, P., Segura, A. & Ramos, J. L. (2007b). Compensatory role of the cis/trans-isomerase and cardiolipin synthase in the membrane fluidity of Pseudomonas putida DOT-T1E. Environ Microbiol 9, 1658-1664.
5. Bisbiroulas, P., Psylou, M., Iliopoulou, I., Diakogiannis, I., Berberi, A. & Mastronicolis, S. K. (2011). Adaptational changes in cellular phospholipids and fatty acid composition of the food pathogen Listeria monocytogenes as a stress response to disinfectant sanitizer benzalkonium chloride. Lett Appl Microbiol 52, 275-280.
6. Bligh, E. G. & Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37, 911-917.
7. Boeris, P. S., Domenech, C. E. & Lucchesi, G. I. (2007). Modification of phospholipid composition in Pseudomonas putida A ATCC 12633 induced by contact with tetradecyltrimethylammonium. J Appl Microbiol 103, 1048-1054.
8. Boeris, P. S., Liffourrena, A. S., Salvano, M. A. & Lucchesi, G. I. (2009). Physiological role of phosphatidylcholine in the Pseudomonas putida A ATCC 12633 response to tetradecyltrimethylammonium bromide and aluminum. Appl Microbiol 49, 491-496.
9. Catucci, L., Depalo, N., Lattanzio, V. M. T., Agostiano, A. & Corcelli, A. (2004). Neosynthesis of cardiolipin in Rhodobacter sphaeroides under osmotic stress. Biochemistry 43, 15066-15072.
10. Cronan, J. E., Jr (2002). Phospholipid modifications in bacteria. Curr Opin Microbiol 5, 202-205.
11. Cronan, J. E., Jr & Gelmann, E. P. (1975). Physical properties of membrane lipids: biological relevance and regulation. Bacteriol Rev 39, 232-256.
12. Dean-Raymond, D. & Alexander, M. (1977). Bacterial metabolism of quaternary ammonium compounds. Appl Environ Microbiol 33, 1037-1041.
13. Denich, T. J., Beaudette, L. A., Lee, H. & Trevors, J. T. (2003). Effect of selected environmental and physico-chemical factors on bacterial cytoplasmic membranes. J Microbiol Methods 52, 149-182.
14. Diefenbach, R., Heipieper, H. J. & Keweloh, H. (1992). The conversion of cis into trans unsaturated fatty acids in Pseudomonas putida P8: evidence for a role in the regulation of membrane fluidity. Appl Microbiol Biotechnol 38, 382-387.
15. Fiske, C. H. & Subbarow, Y. (1925). The colorimetric determination of phosphorus. J Biol Chem 66, 361-375.
16. Ghosh, A. K., Ramakrishnan, G. & Rajasekharan, R. (2008). YLR099C (ICT1) encodes a soluble Acyl-CoA-dependent lysophosphatidic acid acyltransferase responsible for enhanced phospholipid synthesis on organic solvent stress in Saccharomyces cerevisiae. J Biol Chem 283, 9768-9775.
17. Gilbert, P. & Moore, L. E. (2005). Cationic antiseptics: diversity of action under a common epithet. J Appl Microbiol 99, 703-715.
18. Gillan, F. T., Johns, R. B., Verheyen, T. V., Volkman, J. K. & Bavor, H. J. (1981). Trans-monounsaturated acids in a marine bacterial isolate. Appl Environ Microbiol 41, 849-856.
19. Guérin-Méchin, L., Dubois-Brissonnet, F., Heyd, B. & Leveau, J. Y. (1999). Specific variations of fatty acid composition of Pseudomonas aeruginosa ATCC 15442 induced by quaternary ammonium compounds and relation with resistance to bactericidal activity. J Appl Microbiol 87, 735-742.
20. Gutierrez, J. A., Nichols, P. & Couperwhite, I. (1999). Changes in whole cell-derived fatty acids induced by benzene and occurrence of the unusual 16 : 1 v6c in Rhodoccocus sp. 33. FEMS Microbiol Lett 176, 213-218.
21. Härtig, C., Loffhagen, N. & Babel, W. (1999). Glucose stimulates a decrease of the fatty acid saturation degree in Acinetobacter calcoaceticus. Arch Microbiol 171, 166-172.
22. Härtig, C., Loffhagen, N. & Harms, H. (2005). Formation of trans fatty acids is not involved in growth-linked membrane adaptation of Pseudomonas putida. Appl Environ Microbiol 71, 1915-1922.
23. Heipieper, H. J., Weber, F. J., Sikkema, J., Keweloh, H. & de Bont, J. A. M. (1994). Mechanisms of resistance of whole cells to toxic organic solvents. Trends Biotechnol 12, 409-415.
24. Heipieper, H. J., Meinhardt, F. & Segura, A. (2003). The cis-trans isomerase of unsaturated fatty acids in Pseudomonas and Vibrio: biochemistry, molecular biology and physiological function of a unique stress adaptive mechanism. FEMS Microbiol Lett 229, 1-7.
25. Henderson, R. & Tocher, D. (1992). Thin layer chromatography. In Lipid Analysis: A Practical Approach, pp. 65-112. Edited by R. Hamilton & S. Hamilton. Oxford: Oxford University Press.
26. Ingram, L. O. (1976). Adaptation of membrane lipids to alcohols. J Bacteriol 125, 670-678.
27. Jones, M. V., Herd, T. M. & Christie, H. J. (1989). Resistance of Pseudomonas aeruginosa to amphoteric and quaternary ammonium biocides. Microbios 58, 49-61.
28. Kaneda, T. (1977). Fatty acids of the genus Bacillus: an example of branched-chain preference. Bacteriol Rev 41, 391-418.
29. Keweloh, H., Diefenbach, R. & Rehm, H. J. (1991). Increase of phenol tolerance of Escherichia coli by alterations of the fatty acid composition of the membrane lipids. Arch Microbiol 157, 49-53.
30. Kiran, M. D., Annapoorni, S., Suzuki, I., Murata, N. & Shivaji, S. (2005). Cis-trans isomerase gene in psychrophilic Pseudomonas syringae is constitutively expressed during growth and under conditions of temperature and solvent stress. Extremophiles 9, 117- 125.
31. Konopásek, I., Strzalka, K. & Svobodová, J. (2000). Cold shock in Bacillus subtilis: different effects of benzyl alcohol and ethanol on the membrane organisation and cell adaptation. Biochim Biophys Acta 1464, 18-26.
32. Lakowicz, J. R. (1999). Principles of Fluorescence Spectroscopy, 2nd edn. New York: Kluwer.
33. Liffourrena, A. S., López, F. G., Salvano, M. A., Domenech, C. E. & Lucchesi, G. I. (2008). Degradation of tetradecyltrimethylammonium by Pseudomonas putida A ATCC 12633 restricted by accumulation of trimethylamine is alleviated by addition of Al 3+ ions. J Appl Microbiol 104, 396-402.
34. Litman, B. J. & Barenholz, Y. (1982). Fluorescent probe: diphenylhexatriene. Methods Enzymol 81, 678-685.
35. Loffeld, B. & Keweloh, H. (1996). cis/trans isomerization of unsaturated fatty acids as possible control mechanism of membrane fluidity in Pseudomonas putida P8. Lipids 31, 811-815.
36. López, C. S., Alice, A. F., Heras, H., Rivas, E. A. & Sánchez-Rivas, C. (2006). Role of anionic phospholipids in the adaptation of Bacillus subtilis to high salinity. Microbiology 152, 605-616.
37. Loughlin, M. F., Jones, M. V. & Lambert, P. A. (2002). Pseudomonas aeruginosa cells adapted to benzalkonium chloride show resistance to other membrane-active agents but not to clinically relevant antibiotics. J Antimicrob Chemother 49, 631-639.
38. Lucchesi, G. I., Lisa, T. A. & Domenech, C. E. (1989). Choline and betaine as inducer agents of Pseudomonas aeruginosa phospholipase C activity in high phosphate medium. FEMS Microbiol Lett 57, 335-338.
39. Matsumoto, K. (2001). Dispensable nature of phosphatidylglycerol in Escherichia coli: dual roles of anionic phospholipids. Mol Microbiol 39, 1427-1433.
40. McDonnell, G. & Russell, A. D. (1999). Antiseptics and disinfectants: activity, action, and resistance. Clin Microbiol Rev 12, 147-179.
41. Méchin, L., Dubois-Brissonnet, F., Heyd, B. & Leveau, J. Y. (1999). Adaptation of Pseudomonas aeruginosa ATCC 15442 to didecyldimethylammonium bromide induces changes in membrane fatty acid composition and in resistance of cells. J Appl Microbiol 86, 859-866.
42. Morrison, W. R. & Smith, L. M. (1964). Preparation of fatty acid methyl esters and dimethylacetals from lipids with boron fluoride- methanol. J Lipid Res 5, 600-608.
43. Mrozik, A., Piotrowska-Seget, Z. & Łabuzek, S. (2004). Changes in whole cell-derived fatty acids induced by naphthalene in bacteria from genus Pseudomonas. Microbiol Res 159, 87-95.
44. Mykytczuk, N. C. S., Trevors, J. T., Leduc, L. G. & Ferroni, G. D. (2007). Fluorescence polarization in studies of bacterial cytoplasmic membrane fluidity under environmental stress. Prog Biophys Mol Biol 95, 60-82.
45. Nelson, K. E., Weinel, C., Paulsen, I. T., Dodson, R. J., Hilbert, H., Martins dos Santos, V. A. P., Fouts, D. E., Gill, S. R., Pop, M. & other authors (2002). Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ Microbiol 4, 799-808.
46. Neumann, G., Kabelitz, N. & Heipieper, H. J. (2003). The regulation of the cis-trans isomerase (cti) of unsaturated fatty acids in Pseudomonas putida: correlation between cti activity and K+-uptake systems. Eur J Lipid Sci Technol 105, 585-589.
47. Nikaido, H. (1994). Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science 264, 382-388.
48. Nishihara, T., Okamoto, T. & Nishiyama, N. (2000). Biodegradation of didecyldimethylammonium chloride by Pseudomonas fluorescens TN4 isolated from activated sludge. J Appl Microbiol 88, 641-647.
49. Okuyama, H., Okajima, N., Sasaki, S., Higashi, S. & Murata, N. (1991). The cis/trans isomerization of the double bond of a fatty acid as a strategy for adaptation to changes in ambient temperature in the psychrophilic bacterium, Vibrio sp. strain ABE-1. Biochim Biophys Acta 1084, 13-20.
50. Paulucci, N. S., Medeot, D. B., Dardanelli, M. S. & de Lema, M. G. (2011). Growth temperature and salinity impact fatty acid composition and degree of unsaturation in peanut-nodulating rhizobia. Lipids 46, 435-441.
51. Pini, C. V., Bernal, P., Godoy, P., Ramos, J. L. & Segura, A. (2009). Cyclopropane fatty acids are involved in organic solvent tolerance but not in acid stress resistance in Pseudomonas putida DOT-T1E. Microb Biotechnol 2, 253-261.
52. Pinkart, H. C., Wolfram, J. W., Rogers, R. & White, D. C. (1996). Cell envelope changes in solvent-tolerant and solvent-sensitive Pseudomonas putida strains following exposure to o-xylene. Appl Environ Microbiol 62, 1129-1132.
53. Ramos, J. L., Duque, E., Rodríguez-Herva, J. J., Godoy, P., Haïdour, A., Reyes, F. & Fernández-Barrero, A. (1997). Mechanisms for solvent tolerance in bacteria. J Biol Chem 272, 3887-3890.
54. Ramos, J. L., Duque, E., Gallegos, M. T., Godoy, P., Ramos- Gonzalez, M. I., Rojas, A., Teran, W. & Segura, A. (2002). Mechanisms of solvent tolerance in Gram-negative bacteria. Annu Rev Microbiol 56, 743-768.
55. Russell, N. J. (1984). Mechanisms of thermal adaptation in bacteria: blueprints for survival. Trends Biochem Sci 9, 108-112.
56. Schweizer, H. P. (2004). Fatty acid biosynthesis and biologically significant acyl transfer reactions in Pseudomonads. In Pseudomonas: Biosynthesis of Macromolecules and Molecular Metabolism, pp. 83-109. Edited by J. L. Ramos. New York: Kluwer.
57. Sikkema, J., Weber, F. J., Heipieper, H. J. & de Bont, J. A. M. (1994). Cellular toxicity of lipophilic compounds: mechanisms, implications, and adaptations. Biocatalysis 10, 113-122.
58. Sikkema, J., de Bont, J. A. M. & Poolman, B. (1995). Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59, 201-222.
59. Takenaka, S., Tonoki, T., Taira, K., Murakami, S. & Aoki, K. (2007). Adaptation of Pseudomonas sp. strain 7-6 to quaternary ammonium compounds and their degradation via dual pathways. Appl Environ Microbiol 73, 1797-1802.
60. To, M. S., Favrin, S., Romanova, N. & Griffiths, M. W. (2002). Postadaptational resistance to benzalkonium chloride and subsequent physicochemical modifications of Listeria monocytogenes. Appl Environ Microbiol 68, 5258-5264.
61. Trevors, J. T. (2003). Fluorescent probes for bacterial cytoplasmic membrane research. J Biochem Biophys Methods 57, 87-103.
62. van Ginkel, C. G., van Dijk, J. B. & Kroon, A. G. M. (1992). Metabolism of hexadecyltrimethylammonium chloride in Pseudomonas strain B1. Appl Environ Microbiol 58, 3083-3087.
63. von Wallbrunn, A., Heipieper, H. J. & Meinhardt, F. (2002). Cis/trans isomerisation of unsaturated fatty acids in a cardiolipin synthase knock-out mutant of Pseudomonas putida P8. Appl Microbiol Biotechnol 60, 179-185.
64. Zhao, T. & Sun, G. (2007). Antimicrobial finishing of wool fabric with quaternary aminopyridinium salts. J Appl Polym Sci 103, 482-486.
65. Zhu, K., Choi, K. H., Schweizer, H. P., Rock, C. O. & Zhang, Y. M. (2006). Two aerobic pathways for the formation of unsaturated fatty acids in Pseudomonas aeruginosa. Mol Microbiol 60, 260-273.