Bacteria tolerant to organic solvents

Abstract The toxic effects that organic solvents have on whole cells is an important drawback in the application of these solvents in environmental biotechnology and in the production of fine chemicals by whole-cell biotransformations. Hydrophobic organic solvents, such as toluene, are toxic for living organisms because they accumulate in and disrupt cell membranes. The toxicity of a compound correlates with the logarithm of its partition coefficient with octanol and water (log Pow). Substances with a log Pow value between 1 and 5 are, in general, toxic for whole cells. However, in recent years different bacterial strains have been isolated and characterized that can adapt to the presence of organic solvents. These strains grow in the presence of a second phase of solvents previously believed to be lethal. Different mechanisms contributing to the solvent tolerance of these strains have been found. Alterations in the composition of the cytoplasmic and outer membrane have been described. These adaptations suppress the effects of the solvents on the membrane stability or limit the rate of diffusion into the membrane. Furthermore, changes in the rate of the biosynthesis of the phospholipids were reported to accelerate repair processes. In addition to these adaptation mechanisms compensating the toxic effect of the organic solvents, mechanisms do exist that actively decrease the amount of the toxic solvent in the cells. An efflux system actively decreasing the amount of solvents in the cell has been described recently. We review here the current knowledge about exceptional strains that can grow in the presence of toxic solvents and the mechanisms responsible for their survival.

[1]  P. Davidson,et al.  Antimicrobial Activity of Non-Halogenated Phenolic Compounds. , 1981, Journal of food protection.

[2]  T. Kudo,et al.  Isolation of toluene-resistant mutants from Pseudomonas putida PpG1 (ATCC 17453) , 1991 .

[3]  D. Janssen,et al.  Growth on octane alters the membrane lipid fatty acids of Pseudomonas oleovorans due to the induction of alkB and synthesis of octanol , 1995, Journal of bacteriology.

[4]  H. Nikaido,et al.  Prevention of drug access to bacterial targets: permeability barriers and active efflux. , 1994, Science.

[5]  R. Farías,et al.  Inhibitory action of a non-metabolizable fatty acid on the growth of Escherichia coli: role of metabolism and outer membrane integrity , 1977, Journal of bacteriology.

[6]  H. Heipieper,et al.  The cis/trans isomerisation of unsaturated fatty acids in Pseudomonas putida S12: An indicator for environmental stress due to organic compounds , 1995 .

[7]  H. Ishikawa,et al.  Organic-Solvent-Tolerant Bacterium Which Secretes Organic-Solvent-Stable Lipolytic Enzyme , 1994, Applied and environmental microbiology.

[8]  L. Ingram.  Microbial tolerance to alcohols: role of the cell membrane , 1986 .

[9]  P. Rangel,et al.  Effects of cyclohexane, an industrial solvent, on the yeast Saccharomyces cerevisiae and on isolated yeast mitochondria , 1990, Applied and environmental microbiology.

[10]  K. Horikoshi,et al.  Isolation of a benzene-tolerant bacterium and its hydrocarbon degradation , 1993 .

[11]  C. Cartwright,et al.  Ethanol dissipates the proton-motive force across the plasma membrane of Saccharomyces cerevisiae , 1986 .

[12]  S. Aust,et al.  Pollutant degradation by white rot fungi. , 1994, Reviews of environmental contamination and toxicology.

[13]  A. Matin,et al.  Unique and overlapping pollutant stress proteins of Escherichia coli , 1992, Applied and environmental microbiology.

[14]  Gerben J. Zylstra,et al.  Identification and Molecular Characterization of an Efflux Pump Involved in Pseudomonas putida S12 Solvent Tolerance* , 1998, The Journal of Biological Chemistry.

[15]  H. Terada,et al.  The local anesthetic tetracaine destabilizes membrane structure by interaction with polar headgroups of phospholipids. , 1992, Biochimica et biophysica acta.

[16]  M. Shinitzky,et al.  Glucose transport through cell membranes of modified lipid fluidity. , 1981, Biochemistry.

[17]  K. Horikoshi,et al.  Degradation of polyaromatic hydrocarbons by organic solvent-tolerant bacteria from deep sea. , 1995, Bioscience, biotechnology, and biochemistry.

[18]  B. Poolman,et al.  Interactions of cyclic hydrocarbons with biological membranes. , 1994, The Journal of biological chemistry.

[19]  L. Ingram.  Changes in lipid composition of Escherichia coli resulting from growth with organic solvents and with food additives , 1977, Applied and environmental microbiology.

[20]  KT 2442 to 2-Chlorophenol . of the Response of Pseudomonas putida Two-Dimensional Gel Electrophoresis Analysis , 1995 .

[21]  Bradley G. Mehrtens,et al.  Correlation of carotenoid production, decreased membrane fluidity, and resistance to oleic acid killing in Staphylococcus aureus 18Z , 1991, Infection and immunity.

[22]  L. Ingram,et al.  Ethanol tolerance in bacteria. , 1990, Critical reviews in biotechnology.

[23]  J. Ramos,et al.  Isolation and expansion of the catabolic potential of a Pseudomonas putida strain able to grow in the presence of high concentrations of aromatic hydrocarbons , 1995, Journal of bacteriology.

[24]  J. Bollag,et al.  Microbial metabolism of aromatic compounds under anaerobic conditions , 1986 .

[25]  F. Jüttner,et al.  Anoxic hypolimnion is a significant source of biogenic toluene , 1986, Nature.

[26]  P. Seeman,et al.  The membrane actions of anesthetics and tranquilizers. , 1972, Pharmacological reviews.

[27]  J. D. de Bont,et al.  Cis/trans isomerization of fatty acids as a defence mechanism of Pseudomonas putida strains to toxic concentrations of toluene. , 1994, Microbiology.

[28]  B. Poolman,et al.  Mechanisms of membrane toxicity of hydrocarbons. , 1995, Microbiological reviews.

[29]  M. Turner,et al.  Correlation of biocatalytic activity in an organic-aqueous two-liquid phase system with solvent concentration in the cell membrane. , 1990, Enzyme and microbial technology.

[30]  F J Weber,et al.  Adaptation mechanisms of microorganisms to the toxic effects of organic solvents on membranes. , 1996, Biochimica et biophysica acta.

[31]  D B Kell,et al.  Solvent selection for whole cell biotransformations in organic media. , 1995, Critical reviews in biotechnology.

[32]  K. Horikoshi,et al.  A benzene-tolerant bacterium utilizing sulfur compounds isolated from deep sea , 1993 .

[33]  K. Horikoshi,et al.  A Pseudomonas thrives in high concentrations of toluene , 1989, Nature.

[34]  S. Levy,et al.  Role of the acrAB locus in organic solvent tolerance mediated by expression of marA, soxS, or robA in Escherichia coli , 1997, Journal of bacteriology.

[35]  A. Klibanov,et al.  Cloning of an organic solvent-resistance gene in Escherichia coli: the unexpected role of alkylhydroperoxide reductase. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[36]  D. Clark,et al.  Altered phospholipid composition in mutants of Escherichia coli sensitive or resistant to organic solvents. , 1979, Journal of general microbiology.

[37]  H. Kobayashi,et al.  Cell surface properties of organic solvent-tolerant mutants of Escherichia coli K-12 , 1997, Applied and environmental microbiology.

[38]  K. Horikoshi,et al.  Pseudomonas putida Which Can Grow in the Presence of Toluene , 1991, Applied and environmental microbiology.

[39]  K. Horikoshi,et al.  Estimation of solvent-tolerance of bacteria by the solvent parameter log P , 1991 .

[40]  B. Poolman,et al.  Effects of the membrane action of tetralin on the functional and structural properties of artificial and bacterial membranes , 1992, Journal of bacteriology.

[41]  J. Ramos,et al.  Mechanisms for Solvent Tolerance in Bacteria* , 1997, The Journal of Biological Chemistry.

[42]  M. V. van Loosdrecht,et al.  Influence of interfaces on microbial activity. , 1990, Microbiological reviews.

[43]  K. Kobayashi,et al.  Overexpression of the robA gene increases organic solvent tolerance and multiple antibiotic and heavy metal ion resistance in Escherichia coli , 1995, Applied and environmental microbiology.

[44]  Masahiro Ito,et al.  Isolation of Novel Toluene-Tolerant Strain of Pseudomonas aeruginosa , 1992 .

[45]  J. D. de Bont,et al.  Active efflux of toluene in a solvent-resistant bacterium , 1996, Journal of bacteriology.

[46]  Mark R. Smith.  The physiology of aromatic hydrocarbon degrading bacteria , 1994 .

[47]  M. Hood,et al.  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 , 1986, Applied and environmental microbiology.

[48]  J. Tramper,et al.  Toxicity of homologous series of organic solvents for the gram‐positive bacteria Arthrobacter and Nocardia Sp. and the gram‐negative bacteria Acinetobacter and Pseudomonas Sp. , 1993, Biotechnology and bioengineering.

[49]  C. Laane,et al.  Optimization of biocatalysis in organic media. , 1987 .

[50]  T. Kudo,et al.  Production of 3-Vinylcatechol and Physiological Properties of Pseudomonas LF-3, Which Can Assimilate Styrene in a Two-phase (Solvent-Aqueous) System , 1997 .

[51]  F. Meinhardt,et al.  cis-trans isomerization of unsaturated fatty acids: cloning and sequencing of the cti gene from Pseudomonas putida P8 , 1997, Applied and environmental microbiology.

[52]  J. Kingma,et al.  The effect of toluene on the structure and permeability of the outer and cytoplasmic membranes of Escherichia coli. , 1978, Biochimica et biophysica acta.

[53]  B A Neilan,et al.  A Rhodococcus species that thrives on medium saturated with liquid benzene. , 1997, Microbiology.

[54]  A. Peña,et al.  Effects of P-Pinene on Yeast Membrane Functions , 2022 .

[55]  H. Heipieper,et al.  Influence of phenols on growth and membrane permeability of free and immobilized Escherichia coli , 1991, Applied and environmental microbiology.

[56]  K. Shirai.  Catechol Production from Benzene through Reaction with Resting and Immobilized Cells of a Mutant Strain of Pseudomonas , 1987 .

[57]  J. D. de Bont,et al.  Effect of solvent adaptation on the antibiotic resistance in Pseudomonas putida S12 , 1997, Applied Microbiology and Biotechnology.

[58]  H. Heipieper,et al.  Conversion of cis unsaturated fatty acids to trans, a possible mechanism for the protection of phenol-degrading Pseudomonas putida P8 from substrate toxicity , 1992, Applied and environmental microbiology.

[59]  M. Kobayashi,et al.  soxRS gene increased the level of organic solvent tolerance in Escherichia coli. , 1995, Bioscience, biotechnology, and biochemistry.

[60]  H. Nikaido.  Multidrug efflux pumps of gram-negative bacteria , 1996, Journal of bacteriology.

[61]  A. M. George,et al.  Multidrug resistance in enteric and other gram-negative bacteria. , 1996, FEMS microbiology letters.

[62]  H. Nakajima,et al.  Cloning of organic solvent tolerance gene ostA that determines n-hexane tolerance level in Escherichia coli , 1994, Applied and environmental microbiology.

[63]  S J Singer,et al.  Membrane fluidity and cellular functions. , 1975, Advances in experimental medicine and biology.

[64]  H. Heipieper,et al.  Adaptation of Pseudomonas putida S12 to ethanol and toluene at the level of fatty acid composition of membranes , 1994, Applied and environmental microbiology.

[65]  K. Lewis,et al.  Bacterial resistance to uncouplers , 1994, Journal of bioenergetics and biomembranes.

[66]  C. Woldringh.  Effects of Toluene and Phenethyl Alcohol on the Ultrastructure of Escherichia coli , 1973, Journal of bacteriology.

[67]  Sergio Riva,et al.  Role of solvents in the control of enzyme selectivity in organic media , 1995 .

[68]  I. Paulsen,et al.  Proton-dependent multidrug efflux systems , 1996, Microbiological reviews.

[69]  T. Komatsu,et al.  A toluene-tolerant mutant of Pseudomonas aeruginosa lacking the outer membrane protein F. , 1995, Bioscience, biotechnology, and biochemistry.

[70]  K. Horikoshi,et al.  Preparation of Organic Solvent-tolerant Mutants from Escherichia coli K-12 , 1991 .

[71]  J. Dolfing,et al.  Effects of octane on the fatty acid composition and transition temperature of Pseudomonas oleovorans membrane lipids during growth in two-liquid-phase continuous cultures , 1995 .

[72]  L. Ingram.  Adaptation of membrane lipids to alcohols , 1976, Journal of bacteriology.

[73]  T. Kudo,et al.  Physiological properties of two Pseudomonas mendocina strains which assimilate styrene in a two-phase (solvent-aqueous) system under static culture conditions , 1997 .

[74]  L. Ingram,et al.  Effects of ethanol on the Escherichia coli plasma membrane , 1984, Journal of bacteriology.

[75]  D. White,et al.  Phospholipid biosynthesis and solvent tolerance in Pseudomonas putida strains , 1997, Journal of bacteriology.

[76]  G. Stephens,et al.  Production of toluene cis‐glycol by Pseudomonas putida in glucose feb‐batch culture , 1987, Biotechnology and bioengineering.

[77]  J. Monti,et al.  Effects of dolichol on membrane permeability. , 1987, Biochimica et biophysica acta.

[78]  K. Kobayashi,et al.  Organic solvent tolerance and antibiotic resistance increased by overexpression of marA in Escherichia coli , 1997, Applied and environmental microbiology.

[79]  R. Rogers,et al.  Physiological properties of a Pseudomonas strain which grows with p-xylene in a two-phase (organic-aqueous) medium , 1992, Applied and environmental microbiology.

[80]  D. White,et al.  Cell Envelope Changes in Solvent-Tolerant and Solvent-Sensitive Pseudomonas putida Strains following Exposure to o-Xylene , 1996, Applied and environmental microbiology.

[81]  W. Hugo.  Phenols: a review of their history and development as antimicrobial agents. , 1978, Microbios.

[82]  E. A. Nonino.  Where is the citrus industry going , 1997 .

[83]  K. Horikoshi,et al.  Effects of Organic Solvents on Growth of Escherichia coli K-12 , 1994 .

[84]  L. K. Bowles,et al.  Effects of butanol on Clostridium acetobutylicum , 1985, Applied and environmental microbiology.

[85]  H. Ishikawa,et al.  Organic solvent-tolerant bacterium which secretes an organic solvent-stable proteolytic enzyme , 1995, Applied and environmental microbiology.

[86]  F. Narberhaus,et al.  Induction of heat shock proteins during initiation of solvent formation in Clostridium acetobutylicum , 2022 .

[87]  H. Nikaido,et al.  Mycobacterial cell wall: structure and role in natural resistance to antibiotics. , 1994, FEMS microbiology letters.

[88]  A. Driessen,et al.  Effect of cholesterol on the branched-chain amino acid transport system of Streptococcus cremoris , 1988, Journal of bacteriology.

[89]  K. Horikoshi,et al.  Effective Isolation and Identification of Toluene-tolerant Pseudomonas Strains , 1992 .

[90]  H. Wang,et al.  Chemical permeabilization of cells for intracellular product release. , 1990, Bioprocess technology.

[91]  A. Cremieux,et al.  Antibacterial activity of phenolic compounds and aromatic alcohols. , 1990, Research in microbiology.

[92]  F. Neidhardt,et al.  Adaptation of Escherichia coli to the uncoupler of oxidative phosphorylation 2,4-dinitrophenol , 1993, Journal of bacteriology.

[93]  M. Kobayashi,et al.  A close correlation between improvement of organic solvent tolerance levels and alteration of resistance toward low levels of multiple antibiotics in Escherichia coli. , 1995, Bioscience, biotechnology, and biochemistry.

[94]  R. Jackson,et al.  Effects of Toluene on Escherichia coli , 1965, Journal of bacteriology.