Delineating the rules for structural adaptation of membrane-associated proteins to evolutionary changes in membrane lipidome

Author:

Makarova Maria,Peter Maria,Balogh Gabor,Glatz Attila,MacRae James I.,Mora Nestor Lopez,Booth Paula,Makeyev Eugene,Vigh Laszlo,Oliferenko SnezhanaORCID

Abstract

SummaryMembrane function is fundamental to life. Each species explores membrane lipid diversity within a genetically predefined range of possibilities. How membrane lipid composition in turn defines the functional space available for evolution of membrane-centered processes remains largely unknown. We address this fundamental question using related fission yeastsSchizosaccharomyces pombeandSchizosaccharomyces japonicus. We show that unlikeS. pombethat generates membranes where both glycerophospholipid acyl tails are predominantly 16-18 carbons long,S. japonicussynthesizes unusual ‘asymmetrical’ glycerophospholipids where the tails differ in length by 6-8 carbons. This results in stiffer bilayers with distinct lipid packing properties. RetroengineeredS. pombesynthesizing theS. japonicus-type phospholipids exhibits unfolded protein response and downregulates secretion. Importantly, our protein sequence comparisons and domain swap experiments indicate that transmembrane helices co-evolve with membranes, suggesting that, on the evolutionary scale, changes in membrane lipid composition may necessitate extensive adaptation of the membrane-associated proteome.

Publisher

Cold Spring Harbor Laboratory

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