Abstract
A rather efficient solvent adaptation mechanism enabling several gram-negative bacteria to tolerate and grow in the presence of membrane-disturbing compounds is the isomerization of cis- to trans-unsaturated membrane fatty acids. The degree of isomerization obviously depends on the toxicity and the concentration of membrane-affecting agents. Synthesis of trans-fatty acids comes about by direct isomerization of the respective cis-configuration of the double bond without shifting the position. The purpose of the conversion of the cis-configuration to trans is apparently the rapid adaptation of the membrane fluidity to rising temperature or the presence of toxic organic hydrocarbons.
The cis–trans-isomerase (Cti) is a constitutively expressed periplasmic enzyme that – to exert its action – necessitates neither ATP nor other cofactors, and consistently, is independent of de novo synthesis of lipids. A heme-binding site typical of cytochrome c-type proteins is present in the predicted Cti polypeptide indicating a reaction mechanism that renounces temporary saturation of the double bond. Due to its direct correlation with toxicity, cis–trans-isomerization is a potential biomarker for recording solvent stress or changes of other environmental conditions.
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References
Bernal P, Segura A, Ramos JL (2007) Compensatory role of the cis–trans-isomerase and cardiolipin synthase in the membrane fluidity of Pseudomonas putida DOT-T1E. Environ Microbiol 9:1658–1664
Chen Q, Janssen DB, Witholt B (1995) Growth on octane alters the membrane lipid fatty acids of Pseudomonas oleovorans due to the induction of alkB and synthesis of octanol. J Bacteriol 177:6894–6901
Cronan JE (2002) Phospholipid modifications in bacteria. Curr Opin Microbiol 5:202–205
Diefenbach R, Keweloh H (1994) Synthesis of trans unsaturated fatty acids in Pseudomonas putida P8 by direct isomerization of the double bond of lipids. Arch Microbiol 162:120–125
Diefenbach R, Heipieper HJ, 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
Guckert JB, Hood MA, White DC (1986) 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. Appl Environ Microbiol 52:794–801
Guckert JB, Ringelberg DB, White DC (1987) Biosynthesis of trans fatty acids from acetate in the bacterium Pseudomonas atlantica. Can J Microbiol 33:748–754
Guckert JB, Ringelberg DB, White DC, Hanson RS, Bratina BJ (1991) Membrane fatty acids as phenotypic markers in the polyphasic taxonomy of methylotrophs within the proteobacteria. J Gen Microbiol 137:2631–2641
Hara A, Syutsubo K, Harayama S (2003) Alcanivorax which prevails in oil-contaminated seawater exhibits broad substrate specificity for alkane degradation. Environ Microbiol 5:746–753
Hartig 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
Heipieper HJ, de Bont JAM (1994) Adaptation of Pseudomonas putida S12 to ethanol and toluene at the level of fatty acid composition of membranes. Appl Environ Microbiol 60:4440–4444
Heipieper HJ, Diefenbach R, Keweloh H (1992) Conversion of cis unsaturated fatty acids to trans, a possible mechanism for the protection of phenol-degrading Pseudomonas putida P8 from substrate toxicity. Appl Environ Microbiol 58:1847–1852
Heipieper HJ, Weber FJ, Sikkema J, Keweloh H, de Bont JAM (1994) Mechanisms behind resistance of whole cells to toxic organic solvents. Trends Biotechnol 12:409–415
Heipieper HJ, Loffeld B, Keweloh H, de Bont JAM (1995) The cis/trans isomerization of unsaturated fatty acids in Pseudomonas putida S12: an indicator for environmental stress due to organic compounds. Chemosphere 30:1041–1051
Heipieper HJ, Meulenbeld G, VanOirschot Q, De Bont JAM (1996) Effect of environmental factors on the trans/cis ratio of unsaturated fatty acids in Pseudomonas putida S12. Appl Environ Microbiol 62:2773–2777
Heipieper HJ, de Waard P, van der Meer P, Killian JA, Isken S, de Bont JAM, Eggink G, de Wolf FA (2001) Regiospecific effect of 1-octanol on cis-trans isomerization of unsaturated fatty acids in the solvent-tolerant strain Pseudomonas putida S12. Appl Microbiol Biotechnol 57:541–547
Heipieper HJ, 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
Heipieper HJ, Neumann G, Cornelissen S, Meinhardt F (2007) Solvent-tolerant bacteria for biotransformations in two-phase fermentation systems. Appl Microbiol Biotechnol 74:961–973
Holtwick R, Meinhardt F, Keweloh H (1997) Cis–trans isomerization of unsaturated fatty acids: cloning and sequencing of the cti gene from Pseudomonas putida P8. Appl Environ Microbiol 63:4292–4297
Holtwick R, Keweloh H, Meinhardt F (1999) cis/trans isomerase of unsaturated fatty acids of Pseudomonas putida P8: evidence for a heme protein of the cytochrome c type. Appl Environ Microbiol 65:2644–2649
Ingram LO (1977) Changes in lipid composition of Escherichia coli resulting from growth with organic solvents and with food additives. Appl Environ Microbiol 33:1233–1236
Isken S, de Bont JAM (1998) Bacteria tolerant to organic solvents. Extremophiles 2:229–238
Isken S, Santos P, de Bont JAM (1997) Effect of solvent adaptation on the antibiotic resistance in Pseudomonas putida S12. Appl Microbiol Biotechnol 48:642–647
Junker F, Ramos JL (1999) Involvement of the cis/trans isomerase Cti in solvent resistance of Pseudomonas putida DOT-T1E. J Bacteriol 181:5693–5700
Kabelitz N, Santos PM, Heipieper HJ (2003) Effect of aliphatic alcohols on growth and degree of saturation of membrane lipids in Acinetobacter calcoaceticus. FEMS Microbiol Lett 220:223–227
Keweloh H, Heipieper HJ (1996) Trans unsaturated fatty acids in bacteria. Lipids 31:129–137
Kiran MD, Prakash JSS, Annapoorni S, Dube S, Kusano T, Okuyama H, Murata N, Shivaji S (2004) Psychrophilic Pseudomonas syringae requires trans-monounsaturated fatty acid for growth at higher temperature. Extremophiles 8:401–410
Kiran MD, 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
Loffhagen N, Hartig C, Geyer W, Voyevoda M, Harms H (2007) Competition between cis, trans and cyclopropane fatty acid formation and its impact on membrane fluidity. Eng Life Sci 7:67–74
MacDonald PM, Sykes BD, McElhaney RN (1985) Flourine-19 nuclear magnetic resonance studies of lipid fatty acyl chain order and dynamics in Acholeplasma laidlawii b membranes: a direct comparsion of the effects of cis and trans cyclopropane ring and double-bond substituents on orientational order. Biochemistry 24:4651–4659
Morita N, Shibahara A, Yamamoto K, Shinkai K, Kajimoto G, Okuyama H (1993) Evidence for cis–trans isomerization of a double bond in the fatty acids of the psychrophilic bacterium Vibrio sp. strain ABE-1. J Bacteriol 175:916–918
Neumann G, Kabelitz N, Zehnsdorf A, Miltner A, Lippold H, Meyer D, Schmid A, Heipieper HJ (2005) 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 71:6606–6612
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
Okuyama H, Ueno A, Enari D, Morita N, Kusano T (1998) Purification and characterization of 9-hexadecenoic acid cis–trans isomerase from Pseudomonas sp strain E-3. Arch Microbiol 169:29–35
Pedrotta V, Witholt B (1999) Isolation and characterization of the cis–trans-unsaturated fatty acid isomerase of Pseudomonas oleovorans GPo12. J Bacteriol 181:3256–3261
Ramos JL, Gallegos MT, Marques S, Ramos-Gonzalez MI, Espinosa-Urgel M, Segura A (2001) Responses of gram-negative bacteria to certain environmental stressors. Curr Opin Microbiol 4:166–171
Ramos JL, Duque E, Gallegos MT, Godoy P, Ramos-Gonzalez MI, Rojas A, Teran W, Segura A (2002) Mechanisms of solvent tolerance in gram-negative bacteria. Annu Rev Microbiol 56:743–768
Roach C, Feller SE, Ward JA, Shaikh SR, Zerouga M, Stillwell W (2004) Comparison of cis and trans fatty acid containing phosphatidylcholines on membrane properties. Biochemistry 43:6344
Seelig J, Waespe-Šarcevic N (1978) Molecular order in cis and trans unsaturated phospholipid bilayers. Biochemistry 17:3310–3315
Segura A, Duque E, Mosqueda G, Ramos JL, Junker F (1999) Multiple responses of gram-negative bacteria to organic solvents. Environ Microbiol 1:191–198
Sikkema J, de Bont JA, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59:201–222
Suutari M, Laakso S (1994) Microbial fatty acids and thermal adaptation. Crit Rev Microbiol 20:285–328
Von Wallbrunn A, Heipieper HJ, 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
Von Wallbrunn A, Richnow HH, Neumann G, Meinhardt F, Heipieper HJ (2003) Mechanism of cis–trans isomerization of unsaturated fatty acids in Pseudomonas putida. J Bacteriol 185:1730–1733
Weber FJ, de Bont JAM (1996) Adaptation mechanisms of microorganisms to the toxic effects of organic solvents on membranes. Biochim Biophys Acta 1286:225–245
Zhang YM, Rock CO (2008) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6:222–233
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Heipieper, H.J., Fischer, J., Meinhardt, F. (2018). Cis–Trans Isomerase of Unsaturated Fatty Acids: An Immediate Bacterial Adaptive Mechanism to Cope with Emerging Membrane Perturbation Caused by Toxic Hydrocarbons. In: Krell, T. (eds) Cellular Ecophysiology of Microbe: Hydrocarbon and Lipid Interactions. Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-50542-8_49
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