Mechanisms Involved In Organic Solvent Resistance in Gram-Negative Bacteria

The high world interest given to the researches concerning the study of moderately halophilic solvent-tolerant bacteria isolated from marine polluted environments is due to their high biotechnological potential, and also to the perspective of their application in different remediation technologies. Using enrichment procedures, I isolated two moderately halophilic Gram-negative bacterial strains from seawater sample, which are tolerant to organic solvents. Cell tolerance, adhesion and cells viability of Aeromonas salmonicida IBBCt2 and Pseudomonas aeruginosa IBBCt3 in the presence of organic solvents depends not only on its physicochemical properties and its concentration, but also on the specific response of the cells, and the cellular response is not the same for these bacterial strains. n-hexane, n-heptane, propylbenzene, with log POW between 3.69 and 4.39, were less toxic for Aeromonas salmonicida IBBCt2 and Pseudomonas aeruginosa IBBCt3, compared with toluene, styrene, xylene isomers and ethylbenzene, with log POW between 2.64 and 3.17. The results indicated that Aeromonas salmonicida IBBCt2 is more susceptible to organic solvents than Pseudomonas aeruginosa IBBCt3. The mechanisms underlying solvent tolerance (e.g., the existance of the efflux pumps) in Aeromonas salmonicida IBBCt2 and Pseudomonas aeruginosa IBBCt3 it was also studied.





References:
[1] R. Aono, and H. Kobayashi, "Cell surface properties of organic solventtolerant
mutants of Escherichia coli K-12," Appl. Environ. Microbiol.,
vol. 63, pp. 3637-3642, 1997.
[2] S. Isken, and J. A. M. de Bont, "Bacteria tolerant to organic solvents,"
Extremophiles, vol. 2, pp. 229-238, 1998.
[3] 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," Appl. Environ. Microbiol., vol. 71, pp. 5171-5176, 2005.
[4] M. R. Smith, "The biodegradation of aromatic hydrocarbons by bacteria,"
Biodegrad., vol. 1, pp. 191-206, 1990.
[5] E. A. Nonino, "Where is the citrus industry going?," Perfum Flavor, vol.
22, pp. 53-58, 1997.
[6] K. Shirai, "Catechol production from benzene through reaction with
resting and immobilized cells of mutant strains of Pseudomonas," Agric.
Biol. Chem., vol. 51, pp. 121-128, 1987.
[7] R. O. Jenkins, G. M. Stephens, and H. Dalton, 1987, "Production of
toluene cisglycol by Pseudomonas putida in glucose feed-batch culture,"
Biotechnol. Bioeng., vol. 29, pp. 873-883.
[8] J. Sikkema, J. A. M. de Bont, and B. Poolman, "Interactions of cyclic
hydrocarbons with biological membranes," J. Biol. Chem., vol. 269, pp.
8022-8028, 1994.
[9] J. Sikkema, J. A. M. de Bont, and B. Poolman, "Mechanisms of
membrane toxicity of hydrocarbons," Microbiol. Rev., vol. 59, pp. 201-
222, 1995.
[10] J. L. Ramos, E. Duque, M. T. Gallegos, P. Godoy, M. I. Ramos-González,
A. Rojas, W. Terán, and A. Segura, "Mechanisms of solvent tolerance in
gram-negative bacteria," Annu. Rev. Microbiol., vol. 56, pp. 743-768,
2002.
[11] H. J. Heipieper, G. Neumann, S. Cornelissen, and F. Meinhardt, "Solventtolerant
bacteria for biotransformations in two-phase fermentation
systems," Appl. Microbiol. Biotechnol., vol. 74, pp. 961-973, 2007.
[12] A. Segura, E. Duque, G. Mosqueda, J. L. Ramos, and F. Junker, "Multiple
responses of Gram-negative bacteria to organic solvents," Environ.
Microbiol., vol. 1, pp. 191-198, 1999.
[13] A. Segura, P. Godoy, P. van Dillewijn, A. Hurtado, N. Arroyo, S.
Santacruz, and J. L. Ramos, "Proteomic analysis reveals the participation
of energy- and stress-related proteins in the response of Pseudomonas
putida DOT-T1E to toluene," J. Bacteriol., vol. 187, pp. 5937-5945,
2005.
[14] A. Segura, A. Hurtado, B. Rivera, and M. M. Lâzâroaie, "Isolation of new
toluene-tolerant marine strains of bacteria and characterization of their
solvent-tolerance properties," J. Appl. Microbiol., vol. 104, pp. 1408-
1416, 2008.
[15] E. Duque, J. J. Rodriguez-Herva, J. de la Torre, P. Dominguez-Cuevas, J.
Munoz-Rojas, and J. L. Ramos, "The RpoT regulon of Pseudomonas
putida DOT-T1E and its role in stress endurance against solvents," J.
Bacteriol., vol. 189, pp. 207-219, 2007.
[16] H. C. Pinkart, and D.C. White, "Phospholipid biosynthesis and solvent
tolerance in Pseudomonas putida strains," J. Bacteriol., vol. 179, pp.
4219-4226, 1997.
[17] M. I. Borges-Walmsley, K. S. McKeegan, and A. R. Walmsley, "Structure
and function of efflux pumps that confer resistance to drugs," Biochem.
J., vol. 376, pp. 313-338, 2003.
[18] K. Nishino, and A. Yamaguchi, "Role of histone-like protein H-NS in
multidrug resistance of Escherichia coli," J. Bacteriol., vol. 186, pp.
1423-1429, 2004.
[19] R. Margesin, and F. Schinner, "Biodegradation and bioremediation of
hydrocarbons in extreme environments," Appl. Microbiol. Biotechnol.,
vol. 56, pp. 650-663, 2001.
[20] M. T. García, E. Mellado, J. C. Ostos, and A. Ventosa, "Halomonas
organivorans sp. nov., a moderate halophile able to degrade aromatic
compounds," Int. J. of Syst. and Evol. Microbiol., vol. 54, pp. 1723-
1728, 2004.
[21] J. R. Haines, B. A. Wrenn, E. L. Holder, K. L. Strohmeier, R.T.
Herrington, and A. D. Venosa, "Measurement of hydrocarbon-degrading
microbial populations by a 96-well plate most-probable-number
procedure," J. Ind. Microbiol., vol. 16, pp. 36-41, 1996.
[22] W. E. Garthright, and R. J. Blodgett, "FDA's preferred MPN methods for
standard, large or unusual tests, with a spreadsheet," Food Microbiol.,
vol. 20, pp. 439-445, 2003.
[23] J. De Ley, "The quick approximation of DNA base composition from
absorbancy ratios," Antonie van Leeuwenhoek, vol. 33, pp. 203-208,
1976.
[24] J. L. Ramos, E. Duque, M. J. Huertas, and A. Haídour, "Isolation and
expansion of the catabolic potential of a Pseudomonas putida strain able
to grow in the presence of high concentrations of aromatic
hydrocarbons," J. Bacteriol., vol. 177, pp. 3911-3916, 1995.
[25] M. Rosenberg, D. Gutnick, and E. Rosenberg, "Adherence of bacteria to
hydrocarbons: a simple method for measuring cell-surface
hydrofobicity," FEMS Microbiol. Lett., vol. 9, pp. 29-33, 1980.
[26] J. L. Ramos, E. Duque J. J., Rodriguez-Hervas, P. Godoy, A. Haidour, F.
Reyes, and A. Fernández-Barrero, "Metabolism for solvent tolerance in
bacteria," J. Biol. Chem., vol. 272, pp. 3887-3890, 1997.
[27] J. Sambrook, E. F. Fritsch, and T. Maniatis, Molecular Cloning, A
Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold
Spring Harbor, New York, 1989.
[28] M. M. Bradford, "A rapid and sensitive method for the quantitation of
microgram quantities of protein utilizing the principle of protein-dye
binding," Anal. Biochem., vol. 72, pp. 248-254, 1976.
[29] L. G. Whyte, C. W. Greer, and W. E. Inniss, "Assessment of the
biodegradation potential of psychrotrophic microorganisms," Can. J.
Microbiol., vol. 42, pp. 99-106, 1995.
[30] R. H. Vreeland, C. D. Lichtfield, E. L. Martin, and E. Elliot, "Halomonas
elongata, a new genus and species of extremely salt-tolerant bacteria,"
Int. J. Syst. Bacteriol., vol. 30, pp. 485-495, 1980.
[31] J. D. Walker, and R. R. Colwell, "Enumeration of petroleum-degrading
microorganisms," Appl. Environ. Microbiol., vol. 31, pp. 198-207, 1976.
[32] G. Roubal, and R. M. Atlas, 1978, "Distribution of hydrocarbonutilizing
microorganisms and hydrocarbon biodegradation potentials in Alaskan
continental shelf areas," Appl. Environ. Microbiol., vol. 35, pp. 897-
905.
[33] M. A. Heitkamp, and C. E. Cerniglia, "Mineralization of polycyclic
aromatic hydrocarbons by a bacterium isolated from sediment below an
oil field," Appl. Environ. Microbiol., vol. 54, pp. 1612-1614, 1988.
[34] H.-G. Song, and R. Bartha, "Effects of jet fuel spills on the microbial
community of soil," Appl. Environ. Microbiol., vol. 56, pp. 646-651,
1990.
[35] Y. Shi, M. D. Zwolinski, M. E. Schreiber, J. M. Bahr, G. W. Sewell, and
W. J. Hickey, "Molecular analysis of microbial community structures in
pristine and contaminated aquifers: field and laboratory microcosm
experiments," Appl. Environ. Microbiol., vol. 65, pp. 2143-2150, 1999.
[36] S. Bordenave, M. S. Go├▒i-Urriza, P. Caumette, and R. Duran, "Effects of
heavy fuel oil on the bacterial community structure of a pristine
microbial mat," Appl. Environ. Microbiol., vol. 73, pp. 6089-6097,
2007.
[37] W. F. Röling, M. G. Milner, D. M. Jones, K. Lee, F. Daniel, R. J.
Swannell, and I. M. Head, "Robust hydrocarbon degradation and
dynamics of bacterial communities during nutrient-enhanced oil spill
bioremediation," Appl. Environ. Microbiol., vol. 68, pp. 5537-5548,
2002.
[38] R. Seshadri, S. W. Joseph, A. K. Chopra, J. Sha, J. Shaw, J. Graf, D. Haft,
M. Wu, Q. Ren, M. J. Rosovitz, R. Madupu, L. Tallon, M. Kim, S. Jin,
H. Vuong, O. C. Stine, A. Ali, A. J. Horneman, and J. F. Heidelberg,
"Genome sequence of Aeromonas hydrophila ATCC 7966T: jack of all
trades," J. Bacteriol., vol. 188, pp. 8272-8282, 2006.
[39] H. Nikaido, and H. I. Zgurskaya, "AcrAB and related multidrug efflux
pumps of Escherichia coli," J. Mol. Microbiol. Biotechnol., vol. 3, pp.
215-218, 2001.
[40] W. Terán, A. Felipe, A. Segura, A. Rojas, J. L. Ramos, and M.-T.
Gallegos, "Antibiotic-dependent induction of Pseudomonas putida
DOT-T1E TtgABC efflux pump is mediated by the drug binding
repressor TtgR," Antimicrob. Agents Chemother., vol. 47, pp. 3067-
3072, 2003.
[41] K. Poole, "Efflux-mediated antimicrobial resistance," J. Antimicrob.
Chemother., vol. 56, pp. 20-51, 2005.
[42] R. Aono, N. Tsukagoshi, and M. Yamamoto, "Involvement of outer
membrane protein TolC, a possible member of the mar-sox regulon, in
maintenance and improvement of organic solvent tolerance of
Escherichia coli K-12," J. Bacteriol., vol. 180, pp. 938-944, 1998.
[43] R. A. Al-Tahhan, T. R. Sandrin, A. A. Bodour, and R. M. Maier,
"Rhamnolipid-induced removal of lipopolysaccharide from
Pseudomonas aeruginosa: effect on cell surface properties and
interaction with hydrophobic substrates," Appl. Environ. Microbiol., vol.
66, pp. 3262-3268, 2000.
[44] A. Inoue, M. Yamamoto, and K. Horikoshi, "Pseudomonas putida which
can grow in the presence of toluene," Appl Environ Microbiol., vol. 57,
pp. 1560-1562, 1991.
[45] F. J. Weber, and J. A. M. de Bont, "Adaptation mechanisms of
microorganisms to the toxic effects of organic solvents on membranes,"
Biochim. Biophys. Acta, vol. 1286, pp. 225-245, 1996.
[46] G. Mosqueda, and J. L. Ramos, "A set of genes encoding a second
toluene efflux system in Pseudomonas putida DOT-T1.E is linked to the
tod genes for toluene metabolism," J. Bacteriol., vol. 182, pp. 937-943,
2000.
[47] K. Kim, L. Lee, K. Lee, and D. Lim, "Isolation and characterization of
toluene-sensitive mutants from the toluene-resistant bacterium Pseudomonas putida GM73," J. Bacteriol., vol. 180, pp. 3692-3696,
1998.
[48] A. Rojas, A. Segura, M. E. Guazzaroni, W. Teran, A. Hurtado, M. T.
Gallegos, and J. L. Ramos, "In vivo and in vitro evidence that TtgV is
the specific regulator of the TtgGHI multidrug and solvent efflux pump
of Pseudomonas putida," J. Bacteriol., vol. 185, pp. 4755-4763, 2003.
[49] G. Neumann, N. Kabelitz, A. Zehnsdorf, A. Miltner, H. Lippold, D.
Meyer, A. Schmid, and H. J. Heipieper, "Prediction of the adaptability of
Pseudomonas putida DOT-T1E to a second phase of a solvent for
economically sound two-phase biotransformations," Appl. Environ.
Microbiol., vol. 71, pp. 6606-6612, 2005.
[50] N. Meguro, Y. Kodama, M. T. Gallegos, and K. Watanabe, "Molecular
characterization of resistance-nodulation-division transporters from
solvent- and drug-resistant bacteria in petroleum-contaminated soil,"
Appl. Environ. Microbiol., vol. 71, pp. 580-586, 2005.
[51] J. G. Leahy, and R. R. Colwell, "Microbial degradation of hydrocarbons
in the environment," Microbiol. Rev., vol. 54, pp. 305-315, 1990.
[52] A. I. Okoh, "Biodegradation alternative in the cleanup of petroleum
hydrocarbon pollutants," Biotechnol. Molec. Biol. Rev., vol. 1, pp. 38-
50, 2006.
[53] I. Llamas, M. Argandona, E. Quesada, and A. del Moral, "Transposon
mutagenesis in Halomonas eurihalina," Res. Microbiol., vol. 151, pp.
13-18, 2000.
[54] G. Gauthier, M. Gauthier, and R. Christen, "Phylogenetic analysis of the
genera Alteromonas, Shewanella, and Moritella using genes coding for
small-subunit rRNA sequences and division of the genus Alteromonas
into two genera, Alteromonas (Emended) and Pseudoalteromonas gen.
nov., and proposal of twelve new species combinations," Int. J. of Syst.
Bacteriol., vol. 45, pp. 755-761, 1995.