Alpha-Linolenic Land and Eicosapentaenoic Ocean: Possible Reasons for Distinctions in the Fatty Acid Composition of Major Producers

We propose an ecological explanation of the prevalence of eicosapentaenoic acid (20:5n-3, EPA) in lipids of primary producers in aquatic ecosystems, such as diatoms, and of alpha-linolenic acid (18:3n-3, ALA) in lipids of primary producers in terrestrial ecosystems, specifically seed plants. Photosynthetic membranes are unique due to the presence of conical non-bilayer lipids—monogalactosyldiacylglycerols (MGDGs)—which are absent both in other plant cell membranes and in animal cell membranes. The non-bilayer properties—the ability to form an inverted conical shape—of MGDG molecules are conferred by the acyl chains of polyunsaturated fatty acids (PUFAs). When saturated chains are present, these molecules are transformed into regular cylindrical bilayer lipids. As structural lipids, MGDGs determine essential physical and chemical properties of membranes, which are often collectively referred to as fluidity. These properties include the 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 lineage, which distinguishes them from green plants, is their ability to photosynthesize 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 nonphotochemical quenching. These processes are several times faster than their counterparts in members of the green evolutionary lineage. The presence of a sufficient amount of conical non-bilayer structural lipids, specifically MGDGs, is crucial for the effective functioning of the XC, as it facilitates the solubilization of xanthophylls and the incorporation of deepoxidase 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.