Alpha-linolenic land and eicosapentaenoic ocean: possible reasons for distinctions in the fatty acid composition of major producers
M. I. Gladyshev1,2, V. E. Guseynova2, N. N. Sushchik1,2
1Krasnoyarsk Science Centre of the Siberian Branch of Russian Academy of Science, Institute of Biophysics, Krasnoyarsk, Russia
2Siberian Federal University, Krasnoyarsk, Russia
Keywords: eicosapentaenoic acid, alpha-linolenic acid, monogalactosyldiacylglycerols, conical non-bilayer lipids, light and temperature adaptation, xanthophyll cycle, photosynthetic membranes
Abstract
An ecological explanation is proposed for the prevalence of eicosapentaenoic acid (20:5n-3, EPA) in the lipids of primary producers in aquatic ecosystems, such as diatoms, and of alpha-linolenic acid (18:3n-3, ALA) in the lipids of primary producers in terrestrial ecosystems, specifically seed plants. Photosynthetic membranes are unique due to the presence of conical non-bilayer lipids, monogalactosyldiacylglycerols (MGDG), which are absent in both other plant cell membranes and animal cell membranes. The non-bilayer properties - specifically, the ability to form an inverted conical shape - of MGDG molecules are conferred by the acyl chains of polyunsaturated fatty acids (PUFA). When saturated chains are present, these molecules transform into regular cylindrical bilayer lipids. As structural lipids, MGDG determine essential physical and chemical properties of membranes, often collectively referred to as “fluidity”. These properties include molecular rotation rate, diffusion, permeability, free volume, packing defects, lateral pressure, and curvature stress, all of which influence the effectiveness of membrane protein function. The primary ecological feature of diatoms and other marine and freshwater algae of the “red” evolutionary line, which distinguishes them from green plants, is their ability to photosynthesise under rapid changes in light intensity. This occurs both during their circulation in the mixed surface layer of the water column and throughout the tidal cycle in the littoral zone. The common strategies for light adaptation in green plants - such as changes in chloroplast morphology and alterations in the number and structure of light-harvesting complexes and their antennae - are too slow for these dynamic conditions. Instead, light adaptation in diatoms is achieved through the rapid operation of the xanthophyll cycle (XC) and non-photochemical quenching. These processes occur several times faster than their counterparts in members of the “green” evolutionary line. The presence of a sufficient amount of conical non-bilayer structural lipids, specifically MGDG, is crucial for the effective functioning of the XC, as it facilitates the solubilization of xanthophylls and the incorporation of de-epoxidase into the membrane. It is likely that EPA within MGDG in diatoms plays a key role in the rapid operation of the XC by conferring the structural lipid molecules with the necessary inverted conical shape. This shape cannot be fully achieved by the less unsaturated shorter chain of ALA.
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