ReviewRegulation of the desaturation of fatty acids and its role in tolerance to cold and salt stress
Introduction
Fatty acids are the major constituents of membrane glycerolipids. Most of the fatty acids in biological membranes are desaturated, with one or more double bonds in their fatty-acyl chains. The physical properties of membrane lipids depend on the number of double bonds in the constituent fatty acids. Unsaturated fatty acids are synthesized from saturated fatty acids by fatty acid desaturases that convert single bonds to double bonds [1]. In a survey of genome sequences (from The Institute for Genomic Research), we found putative genes for fatty acid desaturases in many prokaryotes, especially in all sequenced strains of cyano-bacteria and in some strains of bacteria but not in archaea. However, we found no genes for fatty acid desaturases in most bacteria, such as Escherichia coli, which synthesizes unsaturated fatty acids via an anaerobic pathway [2••].
The extent of desaturation of individual fatty acids is regulated genetically and environmentally, and temperature is a critically important environmental factor that regulates the extent of desaturation 3., 4.. In response to a decrease in ambient temperature, almost all poikilothermal organisms, including cyanobacteria and bacteria, increase the level of their unsaturated fatty acids, maintaining the appropriate fluidity of membrane lipids regardless of the ambient temperature [5]. This acclimatizing response of membrane lipids is known as homeoviscous acclimation.
The cold-induced expression of genes for fatty acid desaturases (des genes) increases the extent of desaturation of fatty acids at low temperatures in cyanobacteria 3., 4., 6. and in Bacillus subtilis [7]. As it is unlikely that the expression of des genes is directly regulated by temperature, we postulated that a specific mechanism must exist for perception of a change in ambient temperature and transduction of the signal, with subsequent enhancement of the expression of des genes.
Details of the roles of unsaturated fatty acids have been studied in wild-type cyanobacteria and in mutant and transgenic derivatives. In previous studies, we have demonstrated that unsaturated fatty acids are important in maintenance of the photosystem II complex 3., 8. and the expression of des genes 4., 9., particularly at low temperatures. However, it remains to be determined, for example, whether the unsaturated fatty acids of membrane lipids have other important biological functions and whether they are also important in other prokaryotes.
This review summarizes the results of recent studies of cold-sensing histidine kinases and response regulators that transduce the ‘cold signal’ and regulate the expression of des genes in Synechocystis sp. PCC 6803 (referred to hereafter as Synechocystis) and B. subtilis. We also describe the important role of the unsaturated fatty acids in membrane lipids in the tolerance to cold and salt stress.
Section snippets
How is temperature perceived for regulation of the desaturation of fatty acids?
In considering possible mechanisms for the perception and transduction of cold signals and subsequent induction of the expression of des genes, we postulated that the cold sensor may be a histidine kinase [10••]. We produced a ‘knockout’ library of cells that lacked the activities of individual histidine kinases by systematically disrupting all the putative genes for histidine kinases in Synechocystis [11]. An analysis of the cold-responsive activity of the promoter of the desB gene for the ω3
Biological roles of polyunsaturated fatty acids
Analyses of model membranes that consist exclusively of polar glycerolipids have shown that the desaturation of constituent fatty acids fluidizes the membrane. However, biological membranes contain high levels of protein and, in particular, membrane-spanning intrinsic membrane proteins. These proteins might be expected to change the physical properties of lipids in biological membranes. We produced a mutant of Synechocystis with mutations in the fatty acid desaturases that contained only
Conclusions
The extensive studies of the regulation of fatty acid desaturation in prokaryotes have led to the identification of cold sensors that transduce signals that induce the expression of genes for fatty acid desaturases in Synechocystis and B. subtilis. Furthermore, FTIR has demonstrated that changes in the fluidity or molecular motion of membrane lipids are directly related to the level of unsaturated fatty acids in biological membranes. Finally, it has been shown that unsaturated fatty acids in
Acknowledgement
This work was supported, in part, by a Grant-in-Aid for Scientific Research (S; number 13854002) awarded to NM by the Ministry of Education, Science, Sports and Culture of Japan.
References and recommended reading
Papers of particular interest, published within the annual period of review,have been highlighted as:
• of special interest
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