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Delineating the Rules for Structural Adaptation of Membrane-Associated Proteins to Evolutionary Changes in Membrane Lipidome

Research output: Contribution to journalArticle

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

Original languageEnglish
Pages (from-to)367-380.e8
JournalCurrent Biology
Volume30
Issue number3
Early online date16 Jan 2020
DOIs
Accepted/In press13 Nov 2019
E-pub ahead of print16 Jan 2020
Published3 Feb 2020

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Abstract

Membrane 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 yeasts Schizosaccharomyces pombe and Schizosaccharomyces japonicus. We show that, unlike S. pombe that generates membranes where both glycerophospholipid acyl tails are predominantly 16–18 carbons long, S. japonicus synthesizes unusual “asymmetrical” glycerophospholipids where the tails differ in length by 6–8 carbons. This results in stiffer bilayers with distinct lipid packing properties. Retroengineered S. pombe synthesizing the S.-japonicus-type phospholipids exhibits unfolded protein response and downregulates secretion. Importantly, our protein sequence comparisons and domain swap experiments support the hypothesis 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. Makarova et al. show that membranes of related fission yeasts S. pombe and S. japonicus are made of structurally distinct phospholipids because of the difference in fatty acid synthase activities. Bioinformatics and retro-engineering experiments reveal that evolutionary changes in lipid metabolism require adaptation of the membrane-associated proteome.

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