Effect of Environmental Factors on the trans/cis Ratio of Unsaturated Fatty Acids in Pseudomonas putida S12
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1 APPLIED AND ENVIRONMENTAL MICROBIOLOGY, Aug. 1996, p Vol. 62, No /96/$ Copyright 1996, American Society for Microbiology Effect of Environmental Factors on the trans/cis Ratio of Unsaturated Fatty Acids in Pseudomonas putida S12 HERMANN J. HEIPIEPER,* GERWIN MEULENBELD, QUIRIEN VAN OIRSCHOT, AND JAN A. M. DE BONT Division of Industrial Microbiology, Department of Food Science, Wageningen Agricultural University, 6700 EV Wageningen, The Netherlands Received 22 January 1996/Accepted 15 May 1996 The membrane reactions of Pseudomonas putida S12 to environmental stress were investigated. Cells reacted to the addition of six different heavy metals with an increase in the ratio of trans to cis unsaturated fatty acids. A correlation among the increase in the trans/cis ratio, the toxic effects of the heavy metals, and nonspecific permeabilization of the cytoplasmic membrane, as indicated by an efflux of potassium ions, was measured. Cells previously adapted to toxic concentrations of toluene exhibited increased tolerance to all applied concentrations of zinc compared with nonadapted cells. Cells exposed to different temperatures grew optimally at 30 C. The degree of saturation of the membrane fatty acids of these cells decreased with decreasing temperature. An increase in the trans/cis ratio of unsaturated fatty acids took place only at higher temperatures. Osmotic stress, expressed as reduced water activity, was obtained by using different types of solutes. Only in the presence of toxic concentrations of sodium chloride or sucrose did the trans/cis ratio increase. At no applied water activity a significant effect of glycerol on the trans/cis ratio was measured. When cells were exposed to different phs, a distinct optimum cis/trans isomerase activity was measured at phs between 4.0 and 5.0, whereas at higher or lower phs no reaction occurred. This optimum coincided with a loss of viability between ph 4 and 5. The isomerization of cis unsaturated fatty acids to trans unsaturated fatty acids is a mechanism used by Pseudomonas putida cells to adapt their membranes to organic solvents (10, 23, 24, 44). Because of the steric differences between the two configurations of the unsaturated fatty acids, the conversion of cis unsaturated fatty acids into trans unsaturated fatty acids reduces the membrane fluidity and acts against the increase in fluidity caused by organic compounds (12, 27, 40). The isomerization system has not been described in detail yet, but it is known to be constitutively present in the cytoplasmic membrane of the bacteria (13, 28). This system does not need any energy supply, is activated in the absence of de novo synthesis of lipids (23), and also functions in resting cells and isolated membranes (13, 24). The trans fatty acids are formed by direct isomerization of the complementary cis configuration of the double bond without a shift of the position (13, 28). Recently, it was found that this isomerization can be used as an indicator to measure the toxicity of organic compounds. A correlation among the hydrophobicity of organic solvents, the toxic potential of the solvents, and changes in the trans/cis ratios of membrane lipids was observed (26). Fatty acid profiles are important markers for ecological investigations of the soil microflora (19, 47). Therefore, a possible application of this indicator is measurement of toxicity and environmental stress, e.g., during in situ bioremediation processes. Previously, Guckert et al. (19) suggested that the trans/cis ratio of unsaturated fatty acids could be used as an index for starvation or stress in environmental samples. The measurement of toxic effects based on fatty acid profiles may have advantages in determining toxicity in situations in which growth-dependent tests cannot be performed (e.g., in natural habitats). * Corresponding author. Mailing address: Division of Industrial Microbiology, Department of Food Science, Wageningen Agricultural University, P.O. Box 8129, 6700 EV Wageningen, The Netherlands. Phone: Fax: A potential problem for the biodegradation of contaminants in natural environments is the effect of unfavorable physiochemical conditions (environmental factors) on the microflora (42). Environmental factors may also have an effect on the cis-trans isomerase. Therefore, we investigated the influence of several environmental factors on the cis-trans isomerase system for unsaturated fatty acids in P. putida S12. As the most important environmental factors we chose temperature, ph, reduced water activity (a w ) (osmotic stress), and heavy metals. Heavy metals are potential cocontaminants of organic pollutants. In the United States, 37% of all sites polluted with organic compounds also contain toxic inorganic contaminants, such as heavy metals (41). MATERIALS AND METHODS Microorganism and culture conditions. P. putida S12 was previously isolated as a styrene-degrading organism (21). This strain was cultivated in a minimal medium as described by Hartmans et al. (20) with 15 mm glucose as the sole carbon source. Cells were grown in 100-ml shake cultures in a horizontally shaking water bath at 30 C. Measurement of growth and growth inhibition. An inoculum from an overnight culture was transferred to fresh medium. After 3 h of exponential growth, the toxins were added. Cell growth was measured by monitoring the turbidity (optical density at 560 nm) of each cell suspension with a spectrophotometer. Growth inhibition in the presence of different phs and heavy metals was measured by determining the viable-cell numbers (number of CFU); cells were diluted in 50 mm sodium phosphate buffer (ph 7.0) and plated onto agar plates containing glucose-yeast extract medium (5.0 g of glucose per liter, 3.5 g of yeast extract per liter, 15.0 g of agar per liter). The MIC was defined as the lowest concentration of a heavy metal which caused no increase or a small decrease in survival (expressed as CFU) 2 h after the compound was added or the ph was changed. The a w of the medium was decreased by adding glycerol, sodium chloride, or sucrose. Concentrations for solutes corresponding to the a w used in this study were obtained from the work of Scott (39). The medium a w was standardized, with an a w of 1.0 defined as the a w of a solution containing 46.5 mm dissolved solutes. The average results of three identical experiments are shown below, and the standard deviation was less than 6%. Preparation of resting cells. A 100-ml portion of exponentially growing cells was harvested by centrifugation and suspended in the same volume of 50 mm sodium phosphate buffer (ph 7.0) supplemented with 15 mm glucose. Experi- 2773
2 2774 HEIPIEPER ET AL. APPL. ENVIRON. MICROBIOL. TABLE 1. Effects of heavy metals on growth and cis/trans isomerization of fatty acids of P. putida S12 Heavy metal a MIC (mm) b TC max (mm) c Highest trans/cis value FIG. 1. Effect of ZnCl 2 on growth (F), the trans/cis ratio of unsaturated fatty acids ( ), and the K content ({) ofp. putida S12. The K content of cells was determined 1 h after the addition of zinc. dw, dry weight. ments were started 45 min after the cells were suspended, when growth had stopped completely. Lipid extraction and transesterification. Cell suspensions (100 ml; about cells) were centrifuged 3 h after the toxic agents were added and then washed with saline. The lipids were extracted with chloroform-methanol-water as described by Bligh and Dyer (4). Fatty acid methyl esters were prepared by incubating preparations for 15 min at 95 C in boron trifluoride-methanol by the method of Morrison and Smith (35). The fatty acid methyl esters were extracted with hexane. Determination of fatty acid composition. Fatty acid analysis was performed by using gas chromatography (50-m CP-Sil 88 capillary column; temperature program, 160 to 220 C). The instrument used was a model CP-9000 gas chromatograph (Chrompack-Packard) equipped with a flame ionization detector. The fatty acids were identified with the aid of standards. The relative amounts of the fatty acids were determined from the peak areas of the methyl esters by using a Chromatopac model C-R6A integrator (Shimadsu, Kyoto, Japan). Replicate determinations indicated that the relative errors ([standard deviation/mean] 100%) of the values were 2 to 5%. The degree of saturation of the membrane fatty acids was defined as the ratio between the two saturated fatty acids (16:0 and 18:0) and the unsaturated fatty acids (16:1trans, 16:1cis, 18:1trans, and 18:1cis) of strain S12. In all cases the average results of three identical experiments are shown below, and the standard deviation was less than 5%; even smaller changes in the fatty acid composition were reproducible. Measurement of cellular K content. Samples (1 ml) were withdrawn before and after the toxins were added. Cells were separated from the supernatant by rapid centrifugation. The cell pellets were disrupted in 5% (wt/vol) trichloroacetic acid, and debris was removed by centrifugation. The released K in the supernatant was measured by flame photometry with a model PFP 7 flame photometer (Jenway, Ltd., Dunmow, Essex, United Kingdom). All experiments were carried out three times, and the averages of the results are shown below; the standard deviations were less than 5%. RESULTS Effects of heavy metals. Cells of P. putida S12 were grown on glucose, and during the exponential growth phase six different heavy metals were added at different concentrations. Figure 1 shows the growth inhibition and the trans/cis ratio of unsaturated fatty acids after ZnCl 2 was added. A MIC for ZnCl 2 of about 3 mm was measured. The trans/cis ratio exhibited a strong increase at toxic concentrations of the metal, and the maximum value (0.8) was observed at 6 mm. Table 1 shows the data for all other heavy metals investigated. Growth inhibition caused by the other heavy metals investigated gave results similar to the results obtained with zinc when the compounds were added at the effective toxic concentrations (data not shown). Nickel and copper had only very small effects on the trans/cis ratio. For all of the heavy metals tested the concentration which resulted in the highest trans/cis ratio was slightly higher than the MIC. No significant Zinc (Zn 2 ) Cadmium (Cd 2 ) Chrome (Cr 3 ) Cobalt (Co 2 ) Copper (Cu 2 ) Nickel (Ni 2 ) Calcium (Ca 2 ) 0.07 Magnesium (Mg 2 ) 0.07 Manganese (Mn 2 ) 0.07 Control 0.06 a All metals were added in the chloride salt form. b MIC was defined as the concentration which resulted in no increase in survival (expressed in CFU) 2 h after the heavy metal was added. c TC max, concentration which resulted in the highest value for the trans/cis ratio. changes in the levels of saturation of the fatty acids were observed (data not shown). One of the first indications of membrane damage in bacteria is an efflux of potassium ions, which is also caused by heavy metals (16, 32, 46). Therefore, we measured the effect of Zn 2 on the cytoplasmic potassium concentrations. The cells exhibited a concentration-dependent efflux of potassium. At concentrations of zinc which still allowed growth (up to 2.5 mm), the cells were able to restore the cellular K content. Figure 1 shows the cellular potassium concentrations 1 h after zinc was added. After this all possible cellular reactions to compensate for the loss of K (e.g., enhanced uptake) had taken place (24, 25). A relationship between growth inhibition caused by different concentrations of zinc and a loss of cellular K content was observed. At concentrations above the MIC for zinc under these conditions (3 mm) a total loss of cellular potassium occurred. Cells previously adapted to toxic toluene concentrations (400 mg/liter) (45) exhibited increased tolerance to all concentrations of zinc applied compared with nonadapted cells (Fig. 2). Under these conditions the MIC was 4 mm, compared with 3 mm for the nonadapted cells. Effect of temperature on growth and membrane composition of P. putida S12. Cells of P. putida S12 were grown exponen- FIG. 2. Growth of toluene-adapted cells (F) and nonadapted cells (E) inthe presence of ZnCl 2. Whereas nonadapted cells were precultivated on glucose, toluene-adapted cells were taken from a chemostat culture where they grew under steady-state conditions in the presence of 400 mg of toluene per liter. Both types of cells were grown in mineral medium for 2 h before different concentrations of zinc were added.
3 VOL. 62, 1996 ADAPTATION OF P. PUTIDA TO ENVIRONMENTAL STRESS 2775 FIG. 3. Effects of different temperatures on growth rates (F), degrees of saturation of membrane lipids (ç), and trans/cis ratios of unsaturated fatty acids ( ) ofp. putida S12. The exponentially growing cells were preincubated at 30 C for 3 h and then incubated for 3 h at different temperatures in shaken water baths before they were harvested for membrane lipid extraction. tially at 30 C for 3 h and then transferred to shaking water baths at different temperatures. Figure 3 shows the growth rates, degrees of saturation, and trans/cis ratios of the membrane fatty acids of cells incubated for 3 h at different temperatures. The optimum growth temperature was 30 C. The degree of saturation decreased with decreasing temperature. An increase in the trans/cis ratio of unsaturated fatty acids took place only at high temperatures (35, 40, and 45 C); no effect on the trans/cis ratio was observed at lower temperatures. Effects of reduced a w. Reduced a w values were obtained by using different types of solutes added to growing cells during the exponential growth phase. Growth was inhibited by each of the different solutes in a specific manner and stopped at a w values of 0.98, 0.975, and 0.96 for sucrose, sodium chloride, and glycerol, respectively. Figure 4 shows the effects of the three solutes on the trans/cis ratio. Only in the presence of toxic concentrations of sodium chloride or sucrose did the trans/cis ratio increase. Regardless of the a w generated by glycerol, no significant variation in the trans/cis ratio was observed. The degree of saturation of the fatty acids did not change significantly after the addition of any a w -reducing compound (data not shown). Effect of ph. Figure 5 shows both the trans/cis ratios of (energized) resting cells of P. putida S12 and their levels of survival when they were incubated for 2 h at different phs. As expected, no significant changes in the degree of saturation FIG. 4. Effect of reducing the a w on the cis/trans isomerization. As described by Scott (39), NaCl (F), sucrose ( ), and glycerol (ç) were added to growing cells at concentrations that resulted in the a w values indicated. FIG. 5. Effects of different phs on survival (ç) and on the trans/cis ratio ( ) of unsaturated fatty acids of P. putida S12. Octanol (F) was added at a concentration of 2.5 mm to cultures which had been preincubated for 1 h at different phs. occurred under these conditions at any ph (data not shown). A distinct optimum trans/cis ratio was measured between ph 4.0 and 5.0, whereas at higher and lower phs no reaction occurred. This optimum coincided with a loss of viability between ph 4 and 5, but at high phs no relationship between viability and increase in trans/cis ratio was observed. As a control, the ph-dependent response of the isomerization system was measured by adding octanol at a concentration of 2.5 mm, which is known to cause a strong increase in the trans/cis ratio (26). Under these conditions optimum cis/trans isomerization occurred at ph 7. A trans/cis ratio of 1.11 was found at this ph for doubly challenged cells; this value was much higher than the value resulting from a ph change alone (0.45). No octanol-triggered activity was found at phs lower than 4.0 and higher than 10.0 (Fig. 5). DISCUSSION Cells adapted to toxic concentrations of toluene have been shown to be more resistant to ethanol than nonadapted cells are (23). However, the finding that these cells were also more resistant to zinc was surprising. The toxicities of toluene and ethanol are based on the same mode of action; both increase the fluidity of membranes, leading to nonspecific permeabilization (40). The action of heavy metals has not been investigated in detail, but these elements are known to have no direct influence on the fluidity of phospholipids (9, 22) like ethanol or toluene does. Still, it has often been stated that the classical stress response of heat shock proteins is induced not only by increases in temperature but also by organic solvents and heavy metals (5, 17, 34). The observation that the maximum trans/cis ratio was measured at concentrations of heavy metals which were a bit higher than the MICs was also true for all organic compounds investigated (26). The mode of action of heavy metals is still not understood in detail, but these elements seem to interact with membrane proteins, where they exchange with the normally present two- or threefold-charged metals, leading to disturbance of the protein activities and/or conformations (14, 15, 36). The effect on membrane proteins is also shown by the effect of zinc on the cellular potassium content. Up to the highest concentration at which the cells are still able to grow, the cellular K concentration is relatively high. However, concentrations greater than the MIC result in a complete loss of
4 2776 HEIPIEPER ET AL. APPL. ENVIRON. MICROBIOL. potassium. This is in contrast to the cellular potassium levels in the presence of phenols, where a total loss was not observed (24, 25). The difference in the modes of action of the two groups of toxins seems to be the reason. Whereas aromatic compounds have a direct influence on the membrane lipid bilayer, increasing its fluidity and thereby causing an increase in permeability, heavy metals which have no influence on lipid fluidity act directly on membrane channels and transport systems. Gadd et al. (16), who tested the efflux of K to assess heavy metal toxicity, even observed that glucose (an energy source) had a positive influence on the potassium efflux caused by heavy metals in Saccharomyces cerevisiae. The heavy metals are transported into cells via energy-dependent cation transport systems, which leads to an efflux of the ions (e.g., K ) that are normally transported by this system. The time course of such processes is very fast, and this leads to a complete breakdown of the potassium gradient across the cytoplasmic membrane. Normally, the cells react by increasing uptake of K to compensate for this efflux. However, at high heavy metal concentrations they are no longer able to restore these gradients. An optimum growth temperature of 30 C for this bacterium was expected. Also, decreases in the degree of saturation of the membrane lipids with decreasing temperatures have often been described previously (18, 31, 33, 37). The fact that cis/ trans isomerization took place only at temperatures above 30 C supports the theory that the activation of the constitutively present cis/trans isomerization system is related to increases in membrane fluidity (e.g., increases caused by an increase in temperature) (12). The cis/trans isomerization is not generally activated in the presence of any kind of stress which reduces the ability to grow, especially in the presence of changes in the environment which disrupt the membrane and lead to an increase in membrane fluidity or membrane permeability. The observation that even at very low temperatures changes in the degree of saturation occurred is proof that the absence of cis/trans isomerization is not due to a slower reaction speed at lower temperatures but that no activation of the system took place. Bacteria which have only the anaerobic pathway of fatty acid biosynthesis, like P. putida, are not able to change the fatty acid composition of membrane phospholipids postbiosynthetically (28). Therefore, growth is necessary to change the ratio between saturated and unsaturated fatty acids, and under these conditions the cis/trans isomerization should also work after activation. Cells exposed to osmotic stress caused by different compounds reacted in the presence of sodium chloride and sucrose with an increase in the trans/cis ratio, whereas glycerol caused no response. To explain this behavior, diffusive properties have to be taken into consideration. Sodium chloride and sucrose cannot diffuse across the cytoplasmic membrane (11), while equilibration of a glycerol gradient across biological membranes is extraordinarily fast (1, 11). Thus, there seems to be a relationship to the classical bacterial responses to osmotic stress. Bacteria normally react to osmotic stress first by taking up potassium ions, and this is followed by accumulation or biosynthesis of compatible solutes (11). For the latter process an increase in the cytoplasmic concentration of K seems to be the main signal (7, 11). For glycerol it is known that this process leads to neither an accumulation of potassium nor an uptake or synthesis of compatible solutes. Both of these responses take place in the presence of NaCl and sucrose. The finding that glycerol, in contrast to the other two compounds tested, did not activate the cis/trans isomerization system seems to present an interesting parallel between the two stress response systems. The fact that optimum cis/trans isomerization occurs in a distinct ph range (between ph 3.5 and 5.0) is hard to explain. A reaction to any kind of ph stress would mean that the cells should react at both very low and very high phs, which was not observed. Lower phs in particular have no direct influence on the phase transition of phospholipid bilayers (8, 22, 43). Hauser (22) found that phospholipid bilayers exhibited enhanced fluidity (the transition temperature of phospholipids was reduced) with increasing ph. Therefore, the reaction of this system in the presence of lower phs cannot be explained by a classical increase in bilayer fluidity. However, one explanation for the fact that increases in the trans/cis ratio occurred only at low phs could be that K uptake systems were activated during ph adaptation of bacteria. Neutrophilic bacteria (like Escherichia coli and P. putida) regulate their cytoplasmic phs by activating the K uptake systems at external phs below 6.5 (3, 6, 29, 30), whereas they activate a potassium efflux system at external phs above 7.5 (6, 29). From the results of this work it can be concluded that the cis/trans isomerization is analogous to responses to other stress conditions, as indicated very recently by the work of Pinkart et al. (38). A good indicator of this theory is the parallels between the responses of this system to reductions in a w and ph and the activation of potassium uptake systems which occur under exactly the same conditions. Perhaps the activation of K uptake systems is a key signal for many cellular stress responses (7). The exact mechanisms of activation and induction of these systems are still unknown, but recently it has been postulated that the signal for the induction of the kdp K uptake system in E. coli is related to the specific rate of transmembrane K influx (2). If this rate is decreased by a loss of potassium caused by solvents or other conditions, induction occurs. In fact, all other factors or groups of compounds which activate the cis/ trans isomerization system in P. putida are known to be also activators or inducers of the K uptake systems; these factors include organic solvents (24, 25), heavy metals (16; also this study), NaCl, sucrose (11; also this study), an increase in temperature (12), and phs between 3.5 and 5.0 (6, 29; also this study). One difference between the role of K uptake in the activation of the cis/trans isomerization system and the activation of other reactions is that for the accumulation or biosynthesis of compatible solutes an increase in the cellular potassium content is necessary (7). The cis/trans isomerase seems to be activated just by the signal which increases K uptake (e.g., under conditions like the presence of organic solvents, which causes a loss of potassium that has to be compensated for). The other main difference is that the cis/trans isomerase does not need any energy source and is active even in growth situations in which all other energy-dependent mechanisms cannot function. On the one hand, the results of this study can lead to a better understanding of the still unknown mechanisms which activate the cis/trans isomerization system. On the other hand, they could show that some environmental factors also have an effect on the trans/cis ratio of unsaturated fatty acids. 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