Lipids, proteins, and their interplay in the dynamics of temperature-stressed membranes of a cyanobacterium, Synechocystis PCC 6803.
Proper responses to low- and high-temperature stresses are essential for the survival of many organisms. It has been established that at low-temperature stress the sufficient microviscosity of the lipids is decisive in this respect. In many organisms, adapting the level of lipid unsaturation to the low growth temperature regulates this feature. At high-temperature stresses, however, there are no unequivocal results concerning the role of the lipids. In these temperature ranges, the lipids are all disordered and fluid and their physical parameters change slowly with increasing temperatures, while biological organisms give characteristic stress responses in rather narrow temperature ranges. Therefore, one may speculate that other membrane parameters/components, which change sharply in the range of the high-temperature stress, may give a signal to initiate the general response of the cells. For such a role, proteins are the trivial candidates. To reveal the role of the lipids and the proteins in these processes, we used a genetically engineered system, based on a cyanobacterium, Synechocystis PCC 6803. In the wild-type cells of this bacterium, by altering the growth temperature, the polyunsaturated lipid content of the cell membranes can be varied considerably (as required by the homeoviscous adaptation principle). In the case of desA(-)/desD(-) mutant cells, which can contain only monounsaturated fatty acyl chains in their lipids, homeoviscous adaptation of the lipids is not possible. Since desA(-)/desD(-) mutation affects only the lipids, additional perturbations (e.g., altered protein content) should minimally disturb the comparison of the lipid behaviors in wild-type and mutant cells. Infrared spectra of thylakoid and cytoplasmic membranes isolated from wild-type and mutant cells were recorded in 3 degrees C steps between 8 and 92 degrees C. By analyzing the rates of protein structural changes, hydrogen-deuterium exchange, in-membrane lipid disorder, and water-membrane interfacial order/hydration as functions of the temperature, we conclude that (i) the gel-to-liquid crystalline phase transition of the lipids correlates with the growth temperature in the wild-type cells but not in the desA(-)/desD(-) mutants, (ii) over the physiological temperature range, both protein and lipid dynamics are regulating/regulated, providing remarkably constant dynamics for both the thylakoid and cytoplasmic membrane, (iii) in the high-temperature stress region, protein structure and dynamics are changing sharply without any correlation with growth temperature and/or mutation, i.e., membrane protein stability does not seem to depend on the lipid composition of the membrane (this finding points to the possible primacy of proteins as initiators/targets of heat-shock alarms), and (iv) there are substantial differences between the dynamics of the proteins of the thylakoid and cytoplasmic membranes, reflecting their different protein complexes and lipid-to-protein ratios.
Laczkó-Dobos
Hajnalka
H
Institute of Plant Biology, Biological Research Center, Hungarian Academy of Sciences, Temesvári krt. 62, POB 521, H-6701 Szeged, Hungary.
Szalontai
Balázs
B
D001426:Bacterial Proteins / Q000737:chemistry* / Q000378:metabolism; D002462:Cell Membrane / Q000378:metabolism*; D008563:Membrane Lipids / Q000737:chemistry* / Q000378:metabolism; D008565:Membrane Proteins / Q000737:chemistry* / Q000378:metabolism; D008954:Models, Biological; D009154:Mutation; D017550:Spectroscopy, Fourier Transform Infrared; D046939:Synechocystis / Q000145:classification / Q000378:metabolism*; D013696:Temperature; D013816:Thermodynamics; D020524:Thylakoids / Q000378:metabolism
D001426:Bacterial Proteins; D008563:Membrane Lipids; D008565:Membrane Proteins