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 membranecentered 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 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.
Results and DiscussionThe fission yeasts Schizosaccharomyces pombe and Schizosaccharomyces japonicus show remarkable differences in fundamental membrane-centered processes such as establishment of polarity and mitotic nuclear envelope (NE) remodeling [1, 2]. The different strategies of managing the NE have been linked to the distinct regulation of lipid synthesis during the cell cycle in the two species [3, 4].To analyze membrane lipid compositions of the two sister species, we performed shotgun ESI-MS/MS analysis of total cellular lipid extracts (Supplemental Table 1).3