Effect of warm acclimation rate on fatty acid composition and phase transitions of Saccharina japonica (J.E. Areschoug) glycolipids

Saccharina japonica is a valuable commercial species and the most common object of mariculture. Temperature is a powerful factor determining the growth and development of macroalgae. Rational mariculture and an understanding of the dynamics of marine ecosystems require the study of the physicochemical basis of temperature adaptation. The key mechanism of this process is the redistribution of the fatty acid (FA) composition of polar lipids, maintaining the optimal liquid-crystalline state of the biomembrane lipid matrix. In the conditions of increasing ambient temperature variability, the rate of changes aimed at the thermal adaptation of ectothermic organisms, which include plants, becomes particularly important. However, to date, the effect of the temperature acclimation rate on ectothermic organisms has been little studied. The present paper aims to study the ability of S. japonica to adapt the physicochemical properties of the main polar lipids to elevated ambient temperature at different rates of seawater heating. Algae were collected in the Sea of Japan in winter at a water temperature of 4 °C and warmed to a summer temperature of 20 °C at rates of 16 °C/d (rapid acclimation) and 2 °C/d (slow acclimation). We isolated glycolipids monogalactosyldiacylglycerol (MGDG), digalactosyldiacylglycerol (DGDG) and sulfoquinovosyldiacylglycerol (SQDG) from acclimated algae as well as their thalli, collected in winter and summer, and studied their FA composition, the composition of molecular species and thermal transitions from crystalline state to liquid crystalline state, which is optimal for functioning of biomembranes, by GLC, HPLC-MS and differential scanning calorimetry (DSC), respectively. Statistical significance was analyzed using Student's t-test (p ≤ 0.05). The results of this study showed that rapid thermal acclimation caused an increase in the unsaturation index (UI) and the ratio of unsaturated/saturated FA of the main lipid of thylakoid membranes MGDG (See Table 1), in contrast to both acclimatization and acclimation changes in the FA composition of the remaining glycolipids DGDG and SQDG when a season changes from winter to summer (See Tables 2-3). The opposite character of changes in the unsaturation of the FA composition of MGDG compared with DGDG and SQDG was also preserved during slow thermal acclimation. Slow warming only strengthened this feature in MGDG, contributed to increasing the unsaturation of FA composition of DGDG as opposed to the effect of rapid acclimation or weakened its effect in SQDG. The ratio of n-3/n-6 polyunsaturated fatty acids (PUFAs), the decrease of which, that is, increase in the share of n-6 PUFAs in polar lipids of marine macrophytes during thermal acclimatization is important both for regulating the viscosity of membrane lipids, and for strengthening mediators derived from PUFAs in the physiologically active season. However, during thermal acclimation, the n-3/n-6 ratio of PUFAs changed a little in MGDG and SQDG of S. japonica regardless of the acclimation rate. Only in DGDG, the n-3/n-6 ratio of PUFAs decreased in accordance with the seasonal trend, especially at rapid acclimation. These changes in the FA composition of glycolipids were accompanied by equally ambiguous changes in their thermotropic behavior. Thermal acclimation caused the phase separation of MGDG, which was characterized by splitting of the peak of crystal - liquid crystal thermal transition of the glycolipid into the low and high temperature peaks, while the seasonal effect contributed to a decrease in the peak maximum temperature (T_max) to the low temperature region by 20°C (See Fig. 1a). Phase separation of MGDG was accompanied by an increase in the percentage of molecular PUFA/PUFA forms, as well as monounsaturated FA (MUFA)/PUFA, and a decrease in saturated FA (SFA)/ PUFA (See Table 4). However, the warming up of sea water at a rate of 16°C/d and 2°C/d was not enough to bring the profile of the thermogram acclimatization and acclimation closer to that of the summer sample. Similar acclimation changes, which had a character of the emerging trend of fitting the profile of thermograms, were observed in the DGDG and SQDG calorimetric transitions (See Fig. 1b, c), which were based not so much on the FA composition as a whole but on the composition of their molecular species/forms (See Tables 5-6). Consequently, an increase in seawater temperature from 4 °C to 20 °C at rates of 16 °C/d or 2 °C/d showed an ambiguous, stressful nature of the FA composition and calorimetric transitions of glycolipids from S. japonica during thermal acclimation. The low efficiency of molecular mechanisms underlying maintenance of the liquid crystalline state of the main polar lipids of S. japonica that is optimal for functioning of the membranes is probably due to cold-loving nature and absence of sharp temperature fluctuations in the natural habitats of this species of marine macroalgae. The paper contains 1 Figure, 6 Tables and 34 References.

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