Table of Contents Author Guidelines Submit a Manuscript
International Journal of Microbiology
Volume 2014, Article ID 873081, 16 pages
http://dx.doi.org/10.1155/2014/873081
Review Article

Response Mechanisms of Bacterial Degraders to Environmental Contaminants on the Level of Cell Walls and Cytoplasmic Membrane

1Department of Biochemical Technology, Faculty of Chemical and Food Technology, Institute of Biotechnology and Food Science, Slovak University of Technology, Radlinského 9, 812 37 Bratislava, Slovakia
2Water Research Institute, Nábrežie arm. gen. L. Svobodu 5, 812 49 Bratislava, Slovakia

Received 14 February 2014; Revised 12 May 2014; Accepted 27 May 2014; Published 26 June 2014

Academic Editor: Hugh W. Morgan

Copyright © 2014 Slavomíra Murínová and Katarína Dercová. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Tříska, G. Kuncová, M. Macková et al., “Isolation and identification of intermediates from biodegradation of low chlorinated biphenyls (DELOR-103),” Chemosphere, vol. 54, no. 6, pp. 725–733, 2004. View at Google Scholar
  2. R. Tandlich, B. Vrana, S. Payne, K. Dercová, and S. Balaz, “Biodegradation mechanism of biphenyl by a strain of Pseudomonas stutzeri,” Journal of Environmental Science and Health A: Toxic/Hazardous Substances and Environmental Engineering, vol. 46, no. 4, pp. 337–344, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. H. J. Heipieper, F. J. Weber, J. Sikkema, H. Keweloh, and J. A. M. de Bont, “Mechanisms of resistance of whole cells to toxic organic solvents,” Trends in Biotechnology, vol. 12, no. 10, pp. 409–415, 1994. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Šajbidor, “Effect of some environmental factors on the content and composition of microbial membrane lipids,” Critical Reviews in Biotechnology, vol. 17, no. 2, pp. 87–103, 1997. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Čertík and E. Breierová, “Adaptation responses of yeasts to environmental stress,” Chemical Letters, vol. 96, pp. 154–160, 2002. View at Google Scholar
  6. T. J. Denich, L. A. Beaudette, H. Lee, and J. T. Trevors, “Effect of selected environmental and physico-chemical factors on bacterial cytoplasmic membranes,” Journal of Microbiological Methods, vol. 52, no. 2, pp. 149–182, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Čertík, K. Dercová, Z. Sejáková, M. Finďová, and T. Jakubík, “Effect of polyaromatic hydrocarbons (PAHs) on the membrane lipids of bacterial cell,” Biologia, vol. 58, no. 6, pp. 1111–1117, 2003. View at Google Scholar
  8. F. J. Weber, S. Isken, and J. A. M. De Bont, “Cis/trans isomerization of fatty adds as a defence mechanism of Pseudomonas putida strains to toxic concentrations of toluene,” Microbiology, vol. 140, no. 8, pp. 2013–2017, 1994. View at Publisher · View at Google Scholar · View at Scopus
  9. I. Barák and K. Muchová, “The role of lipid domains in bacterial cell processes,” International Journal of Molecular Sciences, vol. 14, no. 2, pp. 4050–4065, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. D. E. Vance and J. Vance, Biochemistry of Lipids, Lipoproteins and Membranes, Elsevier Science BV, 1996.
  11. T. Kobayashi, A. Ohta, and I. Shibuya, “Membrane phospholipid synthesis in Escherichia coli: alteration by glycerol and physiological consequences in a pss mutant,” Journal of Biochemistry, vol. 99, no. 5, pp. 1393–1400, 1986. View at Google Scholar · View at Scopus
  12. W. Dowhan, M. Bogdanov, and E. Mileykovskaya, “Functional roles of lipids in membranes,” in Biochemistry of Lipids, Lipoproteins and Membranes, D. E. Vance and J. E. Vance, Eds., Elsevier, Amsterdam, The Netherlands, 2008. View at Google Scholar
  13. J. M. Berg, J. L. Tymoczko, and L. Stryer, Biochemistry, WH Freeman and Company, New York, NY, USA, 2006.
  14. P. De Weer, “A century of thinking about cell membranes,” Annual Review of Physiology, vol. 62, pp. 919–926, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. B. A. Lewis and D. M. Engelman, “Lipid bilayer thickness varies linearly with acyl chain length in fluid phosphatidylcholine vesicles,” Journal of Molecular Biology, vol. 166, no. 2, pp. 211–217, 1983. View at Publisher · View at Google Scholar · View at Scopus
  16. P. J. L. Werten, H. W. Rémigy, B. L. de Groot et al., “Progress in the analysis of membrane protein structure and function,” The FEBS Letters, vol. 529, no. 1, pp. 65–72, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. K. Simons and W. L. C. Vaz, “Model systems, lipid rafts, and cell membranes,” Annual Review of Biophysics and Biomolecular Structure, vol. 33, pp. 269–295, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. N. Beales, “Adaptation of microorganisms to cold temperatures, weak acid preservatives, low pH, and osmotic stress: a review,” Comprehensive Reviews in Food Science, vol. 3, pp. 1–20, 2004. View at Google Scholar
  19. J. Sikkema, J. A. M. de Bont, and B. Poolman, “Mechanisms of membrane toxicity of hydrocarbons,” Microbiological Reviews, vol. 59, no. 2, pp. 201–222, 1995. View at Google Scholar · View at Scopus
  20. H.-. Heipieper, R. Diefenbach, and H. Keweloh, “Conversion of cis unsaturated fatty acids to trans, a possible mechanism for the protection of phenol-degrading Pseudomonas putida P8 from substrate toxicity,” Applied and Environmental Microbiology, vol. 58, no. 6, pp. 1847–1852, 1992. View at Google Scholar · View at Scopus
  21. J. Sikkema, J. A. M. de Bont, and B. Poolman, “Interactions of cyclic hydrocarbons with biological membranes,” Journal of Biological Chemistry, vol. 269, no. 11, pp. 8022–8028, 1994. View at Google Scholar · View at Scopus
  22. P. Jurkiewicz, A. Olzyńska, L. Cwiklik et al., “Biophysics of lipid bilayers containing oxidatively modified phospholipids: insights from fluorescence and EPR experiments and from MD simulations,” Biochimica et Biophysica Acta—Biomembranes, vol. 1818, no. 10, pp. 2388–2402, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. S. K. B. Ghorbal, A. Chatti, M. M. Sethom et al., “Changes in membrane fatty acid composition of Pseudomonas aeruginosa in response to UV-C radiations,” Current Microbiology, vol. 67, no. 1, pp. 112–117, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. R. Diefenbach, H.J. Heipieper, and H. Keweloh, “The conversion of cis into trans unsaturated fatty acids in Pseudomonas putita P8: evidence for a role in the regulation of membrane fluidity,” Applied Microbiology and Biotechnology, vol. 38, no. 3, pp. 382–387, 1992. View at Google Scholar · View at Scopus
  25. H. J. Heipieper, F. Meinhardt, and A. Segura, “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 Microbiology Letters, vol. 229, no. 1, pp. 1–7, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Mrozik, S. Łabuzek, and Z. Piotrowska-Seget, “Changes in fatty acid composition in Pseudomonas putida and Pseudomonas stutzeri during naphthalene degradation,” Microbiological Research, vol. 160, no. 2, pp. 149–157, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Pepi, H. J. Heipieper, J. Fischer, M. Ruta, M. Volterrani, and S. E. Focardi, “Membrane fatty acids adaptive profile in the simultaneous presence of arsenic and toluene in Bacillus sp. ORAs2 and Pseudomonas sp. ORAs5 strains,” Extremophiles, vol. 12, no. 3, pp. 343–349, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Zorádová, H. Dudášová, L. Lukáčová, K. Dercová, and M. Čertík, “The effect of poly-chlorinated biphenyls (PCBs) on the membrane lipids of Pseudomonas stutzeri,” International Biodeterioration and Biodegradation, vol. 65, pp. 1019–1023, 2011. View at Google Scholar
  29. M. M. Donato, A. S. Jurado, M. C. Antunes-Madeira, and V. M. C. Madeira, “Effects of a lipophilic environmental pollutant (DDT) on the phospholipid and fatty acid contents of Bacillus stearothermophilus,” Archives of Environmental Contamination and Toxicology, vol. 33, no. 4, pp. 341–349, 1997. View at Publisher · View at Google Scholar · View at Scopus
  30. L. E. Nielsen, D. R. Kadavy, S. Rajagopal, R. Drijber, and K. W. Nickerson, “Survey of extreme solvent tolerance in gram-positive cocci: Membrane fatty acid changes in Staphylococcus haemolyticus grown in toluene,” Applied and Environmental Microbiology, vol. 71, no. 9, pp. 5171–5176, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Yamashita, M. Satoi, Y. Iwasa et al., “Utilization of hydrophobic bacterium Rhodococcus opacus B-4 as whole-cell catalyst in anhydrous organic solvents,” Applied Microbiology and Biotechnology, vol. 74, no. 4, pp. 761–767, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Torres, S. L. M. Pera, A. Pandey, and G. R. Castro, “Study on the effects of organic solvent stress on Bacillus lichenifomis S-86,” in Current Topics on Bioprocesses in Food Industry, L. V. Rao, A. Pandey, C. Larroche, and C. G. Dussap, Eds., pp. 1–13, Asiatech Publishers, New Delhi, India, 2009. View at Google Scholar
  33. S. Torres, A. Pandey, and G. R. Castro, “Organic solvent adaptation of Gram positive bacteria: applications and biotechnological potentials,” Biotechnology Advances, vol. 29, no. 4, pp. 442–452, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. C. C. C. R. de Carvalho, A. A. R. L. da Cruz, M. Pons et al., “Mycobacterium sp., Rhodococcus erythropolis, and Pseudomonas putida behavior in the presence of organic solvents,” Microscopy Research and Technique, vol. 64, no. 3, pp. 215–222, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. C. C. C. R. de Carvalho, V. Fatal, S. S. Alves, and M. M. R. Da Fonseca, “Adaptation of Rhodococcus erythropolis cells to high concentrations of toluene,” Applied Microbiology and Biotechnology, vol. 76, no. 6, pp. 1423–1430, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. P. Fernandes, M. P. C. Marques, F. Carvalho, and C. C. C. R. de Carvalho, “Organic-solvent tolerant gram-positive bacteria: applications and mechanisms of tolerance,” in Organic Solvents: Properties, Toxocoty, and Industrial Effects, R. E. Carter, Ed., pp. 89–104, Nova Science, New York, NY, USA, 2011. View at Google Scholar
  37. K. Trautwein, S. Kühner, L. Wöhlbrand et al., “Solvent stress response of the denitrifying bacterium “Aromatoleum aromaticum” strain EbN1,” Applied and Environmental Microbiology, vol. 74, no. 8, pp. 2267–2274, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. I. Duldhardt, J. Gaebel, L. Chrzanowski et al., “Adaptation of anaerobically grown Thauera aromatica, Geobacter sulfurreducens and Desulfococcus multivorans to organic solvents on the level of membrane fatty acid composition,” Microbial Biotechnology, vol. 3, no. 2, pp. 201–209, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Segura, E. Duque, G. Mosqueda, J. L. Ramos, and F. Junker, “Multiple responses of Gram-negative bacteria to organic solvents,” Environmental Microbiology, vol. 1, no. 3, pp. 191–198, 1999. View at Publisher · View at Google Scholar · View at Scopus
  40. K. Dercová, M. Čertík, A. Maľová, and Z. Sejáková, “Effect of chlorophenols on the membrane lipids of bacterial cells,” International Biodeterioration and Biodegradation, vol. 54, pp. 251–254, 2004. View at Google Scholar
  41. H. Y. Oh, J. O. Lee, and O. B. Kim, “Increase of organic solvent tolerance of Escherichia coli by the deletion of two regulator genes, fadR and marR,” Applied Microbiology and Biotechnology, vol. 96, no. 6, pp. 1619–1627, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Mrozik, S. Łabuzek, and Z. Piotrowska-Seget, “Changes in whole cell-derived fatty acids induced by naphthalene in bacteria from genus Pseudomonas,” Microbiological Research, vol. 159, no. 1, pp. 87–95, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. H. Keweloh, R. Diefenbach, and H. J. Rehm, “Increase of phenol tolerance of Escherichia coli by alterations of the fatty acid composition of the membrane lipids,” Archives of Microbiology, vol. 157, no. 1, pp. 49–53, 1991. View at Google Scholar · View at Scopus
  44. J. A. Gutiérrez, P. Nichols, and L. Couperwhite, “Changes in whole cell-derived fatty acids induced by benzene and occurrence of the unusual 16:1ω6c in Rhodococcus sp. 33,” FEMS Microbiology Letters, vol. 176, no. 1, pp. 213–218, 1999. View at Publisher · View at Google Scholar · View at Scopus
  45. F. J. Weber and J. A. M. de Bont, “Adaptation mechanisms of microorganisms to the toxic effects of organic solvents on membranes,” Biochimica et Biophysica Acta—Reviews on Biomembranes, vol. 1286, no. 3, pp. 225–245, 1996. View at Publisher · View at Google Scholar · View at Scopus
  46. J. R. Hazel and E. E. Williams, “The role of alternations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment,” Progress in Lipid Research, vol. 29, no. 3, pp. 167–227, 1990. View at Publisher · View at Google Scholar · View at Scopus
  47. J. E. Cronan Jr., “Phospholipid modifications in bacteria,” Current Opinion in Microbiology, vol. 5, no. 2, pp. 202–205, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. N. Kabelitz, P. M. Santos, and H. J. Heipieper, “Effect of aliphatic alcohols on growth and degree of saturation of membrane lipids in Acinetobacter calcoaceticus,” FEMS Microbiology Letters, vol. 220, no. 2, pp. 223–227, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. H. J. Heipieper and J. A. M. de Bont, “Adaptation of Pseudomonas putida S12 to ethanol and toluene at the level of fatty acid composition of membranes,” Applied and Environmental Microbiology, vol. 60, no. 12, pp. 4440–4444, 1994. View at Google Scholar · View at Scopus
  50. R. Y.-Y. Chiou, R. D. Phillips, P. Zhao, M. P. Doyle, and L. R. Beuchat, “Ethanol-mediated variations in cellular fatty acid composition and protein profiles of two genotypically different strains of Escherichia coli O157:H7,” Applied and Environmental Microbiology, vol. 70, no. 4, pp. 2204–2210, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. H. Keweloh and H. J. Heipieper, “Trans unsaturated fatty acids in bacteria,” Lipids, vol. 31, no. 2, pp. 129–137, 1996. View at Publisher · View at Google Scholar · View at Scopus
  52. H. J. Heipieper, G. Neumann, N. Kabelitz, M. Kastner, and H. H. Richnow, “Carbon isotope fractionation during cis-trans isomerization of unsaturated fatty acids in Pseudomonas putida,” Applied Microbiology and Biotechnology, vol. 66, no. 3, pp. 285–290, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. H. J. Heipieper, G. Meulenbeld, Q. van Oirschot, and J. A. M. de Bont, “Effect of environmental factors on the trans/cis ratio of unsaturated fatty acids in Pseudomonas putida S12,” Applied and Environmental Microbiology, vol. 62, no. 8, pp. 2773–2777, 1996. View at Google Scholar · View at Scopus
  54. R. Holtwick, H. Keweloh, and F. Meinhardt, “Cis/trans isomerase of unsaturated fatty acids of Pseudomonas putida P8: evidence for a heme protein of the cytochrome c type,” Applied and Environmental Microbiology, vol. 65, no. 6, pp. 2644–2649, 1999. View at Google Scholar · View at Scopus
  55. A. Von Wallbrunn, H. H. Richnow, G. Neumann, F. Meinhardt, and H. J. Heipieper, “Mechanism of cis-trans isomerization of unsaturated fatty acids in Pseudomonas putida,” Journal of Bacteriology, vol. 185, no. 5, pp. 1730–1733, 2003. View at Publisher · View at Google Scholar · View at Scopus
  56. H. J. Heipieper, P. de Waard, P. van der Meer et al., “Regiospecific effect of 1-octanol on cis-trans isomerization of unsaturated fatty acids in the solvent-tolerant strain pseudomonas putida S12,” Applied Microbiology and Biotechnology, vol. 57, no. 4, pp. 541–547, 2001. View at Publisher · View at Google Scholar · View at Scopus
  57. V. Pedrotta and B. Witholt, “Isolation and characterization of the cis-trans-unsaturated fatty acid isomerase of Pseudomonas oleovorans gpo12,” Journal of Bacteriology, vol. 181, no. 10, pp. 3256–3261, 1999. View at Google Scholar · View at Scopus
  58. F. Junker and J. L. Ramos, “Involvement of the cis/trans isomerase Cti in solvent resistance of Pseudomonas putida DOT-T1E,” Journal of Bacteriology, vol. 181, no. 18, pp. 5693–5700, 1999. View at Google Scholar · View at Scopus
  59. N. Morita, A. Shibahara, K. Yamamoto, K. Shinkai, G. Kajimoto, and H. Okuyama, “Evidence for cis-trans isomerization of a double bond in the fatty acids of the psychrophilic bacterium Vibrio sp. strain ABE-1,” Journal of Bacteriology, vol. 175, no. 3, pp. 916–918, 1993. View at Google Scholar · View at Scopus
  60. R. Diefenbach and H. Keweloh, “Synthesis of trans unsaturated fatty acids in Pseudomonas putida P8 by direct isomerization of the double bond of lipids,” Archives of Microbiology, vol. 162, no. 1-2, pp. 120–125, 1994. View at Publisher · View at Google Scholar · View at Scopus
  61. I. S. Kim, H. Lee, and J. T. Trevors, “Effects of 2,2′,5,5′-tetrachlorobiphenyl and biphenyl on cell membranes of Ralstonia eutropha H850,” FEMS Microbiology Letters, vol. 200, no. 1, pp. 17–24, 2001. View at Publisher · View at Google Scholar · View at Scopus
  62. A. Mrozik, M. Cycoń, and Z. Piotrowska-Seget, “Changes of FAME profiles as a marker of phenol degradation in different soils inoculated with Pseudomonas sp. CF600,” International Biodeterioration and Biodegradation, vol. 64, no. 1, pp. 86–96, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. L. Shabala and T. Ross, “Cyclopropane fatty acids improve Escherichia coli survival in acidified minimal media by reducing membrane permeability to H+ and enhanced ability to extrude H+,” Research in Microbiology, vol. 159, no. 6, pp. 458–461, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. N. Loffhagen, C. Härtig, and W. Babel, “Suitability of the trans/cis ratio of unsaturated fatty acids in Pseudomonas putida NCTC 10936 as an indicator of the acute toxicity of chemicals,” Ecotoxicology and Environmental Safety, vol. 50, no. 1, pp. 65–71, 2001. View at Publisher · View at Google Scholar · View at Scopus
  65. N. E. Chihib, Y. Tierny, P. Mary, and J. P. Hornez, “Adaptational changes in cellular fatty acid branching and unsaturation of Aeromonas species as a response to growth temperature and salinity,” International Journal of Food Microbiology, vol. 102, no. 1, pp. 113–119, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. A. Kaur, A. Chaudhary, R. Choudhary, and R. Kaushik, “Phospholipid fatty acid—a bioindicator of environment monitoring and assessment in soil ecosystem,” Current Science, vol. 89, no. 7, pp. 1103–1112, 2005. View at Google Scholar · View at Scopus
  67. A. Mrozik, Z. Piotrowska-Seget, and S. Łabuzek, “FAMEs profiles of phenol-degrading Pseudomonas stutzeri introduced into soil,” International Biodeterioration and Biodegradation, vol. 62, no. 3, pp. 319–324, 2008. View at Publisher · View at Google Scholar · View at Scopus
  68. J. L. Ramos, E. Duque, M. Gallegos et al., “Mechanisms of solvent tolerance in gram-negative bacteria,” Annual Review of Microbiology, vol. 56, pp. 743–768, 2002. View at Publisher · View at Google Scholar · View at Scopus
  69. B. Perly, I. C. P. Smith, and H. C. Jarrell, “Effects of the replacement of a double bond by a cyclopropane ring in phosphatidylethanolamines: A 2H NMR study of phase transitions and molecular organization,” Biochemistry, vol. 24, no. 4, pp. 1055–1063, 1985. View at Publisher · View at Google Scholar · View at Scopus
  70. D. W. Grogan and J. E. Cronan Jr., “Cyclopropane ring formation in membrane lipids of bacteria,” Microbiology and Molecular Biology Reviews, vol. 61, no. 4, pp. 429–441, 1997. View at Google Scholar · View at Scopus
  71. I. V. Tsitko, G. M. Zaitsev, A. G. Lobanok, and M. S. Salkinoja-Salonen, “Effect of aromatic compounds on cellular fatty acid composition of Rhodococcus opacus,” Applied and Environmental Microbiology, vol. 65, no. 2, pp. 853–855, 1999. View at Google Scholar · View at Scopus
  72. T. Kaneda, “Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance,” Microbiological Reviews, vol. 55, no. 2, pp. 288–302, 1991. View at Google Scholar · View at Scopus
  73. M. Unell, N. Kabelitz, J. K. Jansson, and H. J. Heipieper, “Adaptation of the psychrotroph Arthrobacter chlorophenolicus A6 to growth temperature and the presence of phenols by changes in the anteiso/iso ratio of branched fatty acids,” FEMS Microbiology Letters, vol. 266, no. 2, pp. 138–143, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. I. Duldhardt, I. Nijenhuis, F. Schauer, and H. J. Heipieper, “Anaerobically grown Thauera aromatica, Desulfococcus multivorans, Geobacter sulfurreducens are more sensitive towards organic solvents than aerobic bacteria,” Applied Microbiology and Biotechnology, vol. 77, no. 3, pp. 705–711, 2007. View at Publisher · View at Google Scholar · View at Scopus
  75. T. Romantsov, Z. Guan, and J. M. Wood, “Cardiolipin and the osmotic stress responses of bacteria,” Biochimica et Biophysica Acta, vol. 1788, no. 10, pp. 2092–2100, 2009. View at Publisher · View at Google Scholar · View at Scopus
  76. J. L. Ramos, E. Duque, J. Rodríguez-Herva et al., “Mechanisms for solvent tolerance in bacteria,” Journal of Biological Chemistry, vol. 272, no. 7, pp. 3887–3890, 1997. View at Publisher · View at Google Scholar · View at Scopus
  77. M. Schlame, “Cardiolipin synthesis for the assembly of bacterial and mitochondrial membranes,” Journal of Lipid Research, vol. 49, no. 8, pp. 1607–1620, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. F. Prossnigg, A. Hickel, G. Pabst, and K. Lohner, “Packing behaviour of two predominant anionic phospholipids of bacterial cytoplasmic membranes,” Biophysical Chemistry, vol. 150, no. 1–3, pp. 129–135, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. S. Nichols-Smith, S. Teh, and T. L. Kuhl, “Thermodynamic and mechanical properties of model mitochondrial membranes,” Biochimica et Biophysica Acta: Biomembranes, vol. 1663, no. 1-2, pp. 82–88, 2004. View at Publisher · View at Google Scholar · View at Scopus
  80. T. H. Haines and N. A. Dencher, “Cardiolipin: a proton trap for oxidative phosphorylation,” The FEBS Letters, vol. 528, no. 1-3, pp. 35–39, 2002. View at Publisher · View at Google Scholar · View at Scopus
  81. H. Palsdottir and C. Hunte, “Lipids in membrane protein structures,” Biochimica et Biophysica Acta—Biomembranes, vol. 1666, no. 1-2, pp. 2–18, 2004. View at Publisher · View at Google Scholar · View at Scopus
  82. P. Bernal, J. Muñoz-Rojas, A. Hurtado, J. L. Ramos, and A. Segura, “A Pseudomonas putida cardiolipin synthesis mutant exhibits increased sensitivity to drugs related to transport functionality,” Environmental Microbiology, vol. 9, no. 5, pp. 1135–1145, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. A. von Wallbrunn, H. Heipieper, and F. Meinhardt, “Cis/trans isomerisation of unsaturated fatty acids in a cardiolipin synthase knock-out mutant of Pseudomonas putida P8,” Applied Microbiology and Biotechnology, vol. 60, no. 1-2, pp. 179–185, 2003. View at Publisher · View at Google Scholar · View at Scopus
  84. P. Fernandes, B. S. Ferreira, and J. M. S. Cabral, “Solvent tolerance in bacteria: role of efflux pumps and cross-resistance with antibiotics,” International Journal of Antimicrobial Agents, vol. 22, no. 3, pp. 211–216, 2003. View at Publisher · View at Google Scholar · View at Scopus
  85. I. T. Paulsen, M. H. Brown, and R. A. Skurray, “Proton-dependent multidrug efflux systems,” Microbiological Reviews, vol. 60, no. 4, pp. 575–608, 1996. View at Google Scholar · View at Scopus
  86. H. Bolhuis, H. W. van Veen, B. Poolman, A. J. M. Driessen, and W. N. Konings, “Mechanisms of multidrug transporters,” FEMS Microbiology Reviews, vol. 21, no. 1, pp. 55–84, 1997. View at Publisher · View at Google Scholar · View at Scopus
  87. J. P. Sarathy, V. Dartois, and E. J. D. Lee, “The role of transport mechanisms in Mycobacterium Tuberculosis drug resistance and tolerance,” Pharmaceuticals, vol. 5, no. 11, pp. 1210–1235, 2012. View at Publisher · View at Google Scholar · View at Scopus
  88. C. Alvarez-Ortega, J. Olivares, and J. L. Martínez, “RND multidrug efflux pumps: what are they good for?” Frontiers in Microbiology, vol. 4, no. 7, pp. 1–11, 2013. View at Publisher · View at Google Scholar · View at Scopus
  89. A. Rojas, E. Duque, G. Mosqueda et al., “Three efflux pumps are required to provide efficient tolerance to toluene in Pseudomonas putida DOT-T1E,” Journal of Bacteriology, vol. 183, no. 13, pp. 3967–3973, 2001. View at Publisher · View at Google Scholar · View at Scopus
  90. S. Geng, J. Fang, K. B. Turner, S. Daunert, and Y. Wei, “Accumulation and efflux of polychlorinated biphenyls in Escherichia coli,” Analytical and Bioanalytical Chemistry, vol. 403, no. 8, pp. 2403–2409, 2012. View at Publisher · View at Google Scholar · View at Scopus
  91. A. Segura, A. Rojas, A. Hurtado, M. Huertas, and J. L. Ramos, “Comparative genomic analysis of solvent extrusion pumps in Pseudomonas strains exhibiting different degrees of solvent tolerance,” Extremophiles, vol. 7, no. 5, pp. 371–376, 2003. View at Publisher · View at Google Scholar · View at Scopus
  92. J. F. Muller, The role of multidrug efflux pumps in the stress response of Pseudomonas aeruginosa to organic contamination, [Ph.D. thesis], Virginia Polytechnic Institute, Blacksburg, Va, USA, 2006.
  93. K. Poole, “Multidrug efflux pumps and antimicrobial resistance in Pseudomonas aeruginosa and related organisms,” Journal of Molecular Microbiology and Biotechnology, vol. 3, no. 2, pp. 255–263, 2001. View at Google Scholar · View at Scopus
  94. C. Hunte and S. Richers, “Lipids and membrane protein structures,” Current Opinion in Structural Biology, vol. 18, no. 4, pp. 406–411, 2008. View at Publisher · View at Google Scholar · View at Scopus
  95. M. A. Baboshin and L. A. Golovleva, “Aerobic bacterial degradation of polycyclic aromatic hydrocarbons (PAHs) and its kinetic aspects,” Microbiology, vol. 81, no. 6, pp. 639–650, 2012. View at Publisher · View at Google Scholar · View at Scopus
  96. S. Kim, S. Seung-Youl, K. Kyung-Wook, H. Eun-Mi, and O. Kye-Heon, “Proteomic analysis of the benzoate degradation pathway in Acinetobacter sp. KS-1,” Research in Microbiology, vol. 154, pp. 697–703, 2003. View at Google Scholar
  97. L. Agulló, B. Cámara, P. Martínez, V. Latorre, and M. Seeger, “Response to (chloro)biphenyls of the polychlorobiphenyl-degrader Burkholderia xenovorans LB400 involves stress proteins also induced by heat shock and oxidative stress,” FEMS Microbiology Letters, vol. 267, no. 2, pp. 167–175, 2007. View at Publisher · View at Google Scholar · View at Scopus
  98. P. Martínez, L. Agulló, M. Hernández, and M. Seeger, “Chlorobenzoate inhibits growth and induces stress proteins in the PCB-degrading bacterium Burkholderia xenovorans LB400,” Archives of Microbiology, vol. 188, no. 3, pp. 289–297, 2007. View at Publisher · View at Google Scholar · View at Scopus
  99. S. T. Hossain, I. Mallick, and S. K. Mukherjee, “Cadmium toxicity in Escherichia coli: cell morphology, Z-ring formation and intracellular oxidative balance,” Ecotoxicology and Environmental Safety, vol. 86, pp. 54–59, 2012. View at Publisher · View at Google Scholar · View at Scopus
  100. T. Coba de la Peña, F. J. Redondo, M.F. Fillat, M. M. Lucas, and J. J. Pueyo, “Flavodoxin overexpression confers tolerance to oxidative beneficial soil improves survival in the presence of the herbicides paraquat and atrazine,” Journal of Applied Microbiology, vol. 115, no. 1, pp. 236–246, 2013. View at Google Scholar
  101. S. Runkel, H. C. Wells, and G. Rowley, “Living with stress: a lesson from the enteric pathogen Salmonella enterica,” Advances in Applied Microbiology, vol. 83, pp. 87–144, 2013. View at Publisher · View at Google Scholar · View at Scopus
  102. D. J. Gage and F. C. Neidhardt, “Adaptation of Escherichia coli to the uncoupler of oxidative phosphorylation 2,4-dinitrophenol,” Journal of Bacteriology, vol. 175, no. 21, pp. 7105–7108, 1993. View at Google Scholar · View at Scopus
  103. L. A. Lambert, K. Abshire, D. Blankenhorn, and J. Slonczewski, “Proteins induced in Escherichia coli by benzoic acid,” Journal of Bacteriology, vol. 179, no. 23, pp. 7595–7599, 1997. View at Google Scholar · View at Scopus
  104. Y.-S. Cho, S.-H. Park, C.-K. Kim, and K.-H. Oh, “Induction of stress shock proteins DnaK and GroEL by phenoxyherbicide 2,4-D in Burkholderia sp. YK-2 isolated from rice field,” Current Microbiology, vol. 41, no. 1, pp. 33–38, 2000. View at Publisher · View at Google Scholar · View at Scopus
  105. M. Hecker and U. Völker, “General stress response of Bacillus subtilis and other bacteria,” Advances in Microbial Physiology, vol. 44, pp. 35–91, 2001. View at Publisher · View at Google Scholar
  106. J. E. Visick and S. Clarke, “Repair, retold, recycle: how bacteria can deal with spontaneous and environmental damage to proteins,” Molecular Microbiology, vol. 16, no. 5, pp. 835–845, 1995. View at Publisher · View at Google Scholar · View at Scopus
  107. P. M. Santos, D. Benndorf, and I. Sá-Correia, “Insights into Pseudomonas putida KT2440 response to phenol-induced stress by quantitative proteomics,” Proteomics, vol. 4, no. 9, pp. 2640–2652, 2004. View at Publisher · View at Google Scholar · View at Scopus
  108. A. Segura, P. Godoy, P. van Dillewijn et al., “Proteomic analysis reveals the participation of energy- and stress-related proteins in the response of Pseudomonas putida DOT-T1E to toluene,” Journal of Bacteriology, vol. 187, no. 17, pp. 5937–5945, 2005. View at Publisher · View at Google Scholar · View at Scopus
  109. H. Keweloh, G. Weyrauch, and H.-W. Rehm, “Phenol-induced membrane changes in free and immobilized Escherichia coli,” Applied Microbiology and Biotechnology, vol. 33, no. 1, pp. 66–71, 1990. View at Google Scholar · View at Scopus
  110. I. C. Sutcliffe, “Cell envelope composition and organisation in the genus Rhodococcus,” Antonie van Leeuwenhoek, vol. 74, no. 1–3, pp. 49–58, 1998. View at Publisher · View at Google Scholar · View at Scopus
  111. C. E. Barry III and K. Mdluli, “Drug sensitivity and environmental adaptation of mycobacterial cell wall components,” Trends in Microbiology, vol. 4, no. 7, pp. 275–281, 1996. View at Publisher · View at Google Scholar · View at Scopus
  112. H. Marrakchi, M.-A. Lanéelle, and M. Daffé, “Mycolic acids: structures, biosynthesis, and beyond,” Chemistry and Biology, vol. 21, no. 1, pp. 67–85, 2014. View at Google Scholar
  113. R. Benz, “Uptake of solutes through bacterial outer membranes,” in Bacterial Cell Wall, J. M. Ghuysen and R. Hakenbeck, Eds., pp. 397–420, Elsevier Science BV., Amsterdam, The Netherlands, 1994. View at Google Scholar
  114. H. C. Pinkart, J. W. Wolfram, R. Rogers, and D. C. White, “Cell envelope changes in solvent-tolerant and solvent-sensitive Pseudomonas putida strains following exposure to o-xylene,” Applied and Environmental Microbiology, vol. 62, no. 3, pp. 1129–1132, 1996. View at Google Scholar · View at Scopus
  115. S. Isken and J. A. M. de Bont, “Bacteria tolerant to organic solvents,” Extremophiles, vol. 2, no. 3, pp. 229–238, 1998. View at Publisher · View at Google Scholar · View at Scopus
  116. S. A. Makin and T. J. Beveridge, “The influence of A-band and B-band lipopolysaccharide on the surface characteristics and adhesion of Pseudomonas aeruginosa to surfaces,” Microbiology, vol. 142, no. 2, pp. 299–307, 1996. View at Publisher · View at Google Scholar · View at Scopus
  117. S. Kim and F. Picardal, “Microbial growth on dichlorobiphenyls chlorinated on both rings as a sole carbon and energy source,” Applied and Environmental Microbiology, vol. 67, no. 4, pp. 1953–1955, 2001. View at Publisher · View at Google Scholar · View at Scopus
  118. B. Witholt, M.-J. De Smet, J. Kingma et al., “Bioconversions of aliphatic compounds by Pseudomonas oleovorans in multiple bioreactors: Background and economic potential,” Trends in Biotechnology, vol. 8, no. 2, pp. 46–52, 1990. View at Publisher · View at Google Scholar · View at Scopus
  119. F. P. Chávez, F. Gordillo, and C. A. Jerez, “Adaptive responses and cellular behaviour of biphenyl-degrading bacteria toward polychlorinated biphenyls,” Biotechnology Advances, vol. 24, no. 3, pp. 309–320, 2006. View at Publisher · View at Google Scholar · View at Scopus
  120. D. Halter, C. Casiot, H. J. Heipieper et al., “Surface properties and intracellular speciation revealed an original adaptive mechanism to arsenic in the acid mine drainage bio-indicator Euglena mutabilis,” Applied Microbiology and Biotechnology, vol. 93, no. 4, pp. 1735–1744, 2012. View at Publisher · View at Google Scholar · View at Scopus
  121. T. Baumgarten, J. Vazquez, C. Bastisch et al., “Alkanols and chlorophenols cause different physiological adaptive responses on the level of cell surface properties and membrane vesicle formation in Pseudomonas putida DOT-T1E,” Applied Microbiology and Biotechnology, vol. 93, no. 2, pp. 837–845, 2012. View at Publisher · View at Google Scholar · View at Scopus
  122. J. M. Diver, T. Schollaardt, H. R. Rabin, C. Thorson, and L. E. Bryan, “Persistence mechanisms in Pseudomonas aeruginosa from cystic fibrosis patients undergoing ciprofloxacin therapy,” Antimicrobial Agents and Chemotherapy, vol. 35, no. 8, pp. 1538–1546, 1991. View at Publisher · View at Google Scholar · View at Scopus
  123. R. Aono and H. Kobayashi, “Cell surface properties of organic solvent-tolerant mutants of Escherichia coli K12,” Applied and Environmental Microbiology, vol. 63, no. 9, pp. 3637–3642, 1997. View at Google Scholar · View at Scopus
  124. S. Isken and J. A. M. De Bont, “Active efflux of toluene in a solvent-resistant bacterium,” Journal of Bacteriology, vol. 178, no. 20, pp. 6056–6058, 1996. View at Google Scholar · View at Scopus
  125. A. S. Rudolph, J. H. Crowe, and L. M. Crowe, “Effects of three stabilizing agents—proline, betaine, and trehalose—on membrane phospholipids,” Archives of Biochemistry and Biophysics, vol. 245, no. 1, pp. 134–143, 1986. View at Publisher · View at Google Scholar · View at Scopus
  126. Ł. Chrzanowski, L. Y. Wick, R. Meulenkamp, M. Kaestner, and H. J. Heipieper, “Rhamnolipid biosurfactants decrease the toxicity of chlorinated phenols to Pseudomonas putida DOT-T1E,” Letters in Applied Microbiology, vol. 48, no. 6, pp. 756–762, 2009. View at Publisher · View at Google Scholar · View at Scopus
  127. D. R. Johnson, E. Coronado, S. K. Moreno-Forero, H. J. Heipieper, and J. van der Meer, “Transcriptome and membrane fatty acid analyses reveal different strategies for responding to permeating and non-permeating solutes in the bacterium Sphingomonas wittichii,” BMC Microbiology, vol. 11, pp. 250–256, 2011. View at Publisher · View at Google Scholar · View at Scopus
  128. C. C. C. R. de Carvalho, “Adaptation of Rhodococcus erythropolis cells for growth and bioremediation under extreme conditions,” Research in Microbiology, vol. 163, no. 2, pp. 125–136, 2012. View at Publisher · View at Google Scholar · View at Scopus
  129. A. Kulp and M. J. Kuehn, “Biological Functions and biogenesis of secreted bacterial outer membrane vesicles,” Annual Review of Microbiology, vol. 64, pp. 163–184, 2010. View at Publisher · View at Google Scholar · View at Scopus
  130. L. M. Mashburn-Warren and M. Whiteley, “Special delivery: vesicle trafficking in prokaryotes,” Molecular Microbiology, vol. 61, no. 4, pp. 839–846, 2006. View at Publisher · View at Google Scholar · View at Scopus
  131. H. Kobayashi, K. Uematsu, H. Hirayama, and K. Horikoshi, “Novel toluene elimination system in a toluene-tolerant microorganism,” Journal of Bacteriology, vol. 182, no. 22, pp. 6451–6455, 2000. View at Publisher · View at Google Scholar · View at Scopus
  132. T. J. Beveridge, S. A. Makin, J. L. Kadurugamuwa, and Z. S. Li, “Interactions between biofilms and the environment,” The FEMS Microbiology Reviews, vol. 20, no. 3-4, pp. 291–303, 1997. View at Publisher · View at Google Scholar · View at Scopus
  133. C. C. C. R. De Carvalho, L. Y. Wick, and H. J. Heipieper, “Cell wall adaptations of planktonic and biofilm Rhodococcus erythropolis cells to growth on C5 to C16 n-alkane hydrocarbons,” Applied Microbiology and Biotechnology, vol. 82, no. 2, pp. 311–320, 2009. View at Publisher · View at Google Scholar · View at Scopus
  134. G. Neumann, Y. Veeranagouda, T. B. Karegoudar et al., “Cells of Pseudomonas putida and Enterobacter sp. adapt to toxic organic compounds by increasing their size,” Extremophiles, vol. 9, no. 2, pp. 163–168, 2005. View at Publisher · View at Google Scholar · View at Scopus
  135. Z. Zahir, K. D. Seed, and J. J. Dennis, “Isolation and characterization of novel organic solvent-tolerant bacteria,” Extremophiles, vol. 10, no. 2, pp. 129–138, 2006. View at Publisher · View at Google Scholar · View at Scopus
  136. J. Fischer, U. Kappelmeyer, M. Kastner, F. Schauer, and H. J. Heipieper, “The degradation of bisphenol A by the newly isolated bacterium Cupriavidus basilensis JF1 can be enhanced by biostimulation with phenol,” International Biodeterioration and Biodegradation, vol. 64, no. 4, pp. 324–330, 2010. View at Publisher · View at Google Scholar · View at Scopus
  137. L. Cao, Y. Gao, G. Wu et al., “Cloning of three 2,3-dihydroxybiphenyl-1,2-dioxygenase genes from Achromobacter sp. BP3 and the analysis of their roles in the biodegradation of biphenyl,” Journal of Hazardous Materials, vol. 261, pp. 246–252, 2013. View at Publisher · View at Google Scholar · View at Scopus
  138. S. Zorádová-Murínová, H. Dudášová, L. Lukáčová et al., “Adaptation mechanisms of bacteria during the degradation of polychlorinated biphenyls in the presence of natural and synthetic terpenes as potential degradation inducers,” Applied Microbiology and Biotechnology, vol. 94, pp. 1375–1385, 2012. View at Google Scholar
  139. H. Dudášová, L. Lukáčová, S. Murínová, and K. Dercová, “Effects of plant terpenes on biodegradation of polychlorinated biphenyls (PCBs),” International Biodeterioration & Biodegradation, vol. 69, pp. 23–27, 2012. View at Publisher · View at Google Scholar
  140. B. S. Hernandez, S.-. Koh, M. Chial, and D. D. Focht, “Terpene-utilizing isolates and their relevance to enhanced biotransformation of polychlorinated biphenyls in soil,” Biodegradation, vol. 8, no. 3, pp. 153–158, 1997. View at Publisher · View at Google Scholar · View at Scopus
  141. E. K. Dzantor, J. E. Woolston, and B. Momen, “PCB dissipation and microbial community analysis in rhizosphere soil under substrate amendment conditions,” International Journal of Phytoremediation, vol. 4, no. 4, pp. 283–295, 2002. View at Publisher · View at Google Scholar · View at Scopus
  142. S. H. Kwon, M. H. Hong, J. H. Choi et al., “Bioremediation of aroclor 1242 by a consortium culture in marine sediment microcosm,” Biotechnology and Bioprocess Engineering, vol. 13, no. 6, pp. 730–737, 2008. View at Publisher · View at Google Scholar · View at Scopus
  143. S. Murínová, K. Dercová, and S. Murínová, “Bacterial cell membrane adaptation responses on stress caused with the environmental pollutants,” Acta Chimica Slovaca, vol. 6, no. 1, pp. 106–114, 2013. View at Google Scholar
  144. M. M. Tajkarimi, S. A. Ibrahim, and D. O. Cliver, “Antimicrobial herb and spice compounds in food,” Food Control, vol. 21, no. 9, pp. 1199–1218, 2010. View at Publisher · View at Google Scholar · View at Scopus
  145. A. Elaissi, K. H. Salah, S. Mabrouk, K. M. Larbi, R. Chemli, and F. Harzallah-Skhiri, “Antibacterial activity and chemical composition of 20 Eucalyptus species' essential oils,” Food Chemistry, vol. 129, no. 4, pp. 1427–1434, 2011. View at Publisher · View at Google Scholar · View at Scopus
  146. A. K. Tyagi and A. Malik, “Antimicrobial potential and chemical composition of Mentha piperita oil in liquid and vapour phase against food spoiling microorganisms,” Food Control, vol. 22, no. 11, pp. 1707–1714, 2011. View at Publisher · View at Google Scholar · View at Scopus
  147. P. M. Furneri, L. Mondello, G. Mandalari et al., “In vitro antimycoplasmal activity of citrus bergamia essential oil and its major components,” European Journal of Medicinal Chemistry, vol. 52, pp. 66–69, 2012. View at Publisher · View at Google Scholar · View at Scopus
  148. M. Mendez, R. Rodríguez, J. Ruiz et al., “Antibacterial activity of plant extracts obtained with alternative organics solvents against food-borne pathogen bacteria,” Industrial Crops and Products, vol. 37, no. 1, pp. 445–450, 2012. View at Publisher · View at Google Scholar · View at Scopus