Cellular membranes of the related fission yeast species differ in their dipole potential

Abstract

The dielectric environment and membrane dipole potential are key electrostatic properties of biological membranes, which modulate the function of membrane-associated proteins. If and how these properties are shaped by species-specific cellular lipid landscapes is a fundamental question. Here we use two related fission yeast species, S. pombe and S. japonicus, which exhibit remarkable differences in membrane lipid composition, to address this problem. S. pombe synthesizes membranes from largely unsaturated glycerophospholipids with 18- and 16-carbon long fatty acyl chains and the major fungal sterol ergosterol. Its relative S. japonicus produces abundant saturated asymmetrical glycerophospholipids that contain a medium chain fatty acyl C10:0 at the sn-2 position of the glycerol backbone. Alongside ergosterol, its membranes contain the sterol mimic diplopterol, produced by a horizontally transferred squalene hopene cyclase of a bacterial origin. Using fluorescence lifetime imaging of the solvatochromic dye di-4-ANEPPDHQ we show that S. pombe and S. japonicus exhibit comparable dielectric environment. Interestingly, dipole potential measurements using the voltage-sensitive probe di-8-ANEPPS show that S. japonicus membranes have higher dipole potential relative to S. pombe. The in vivo measurements of sterol- and diplopterol-lacking S. japonicus mutants supported by experiments with model membranes and S. pombe retroengineered to produce the C10-containing glycerophospholipids, indicate that both ergosterol and the saturated asymmetrical glycerophospholipids support high membrane dipole potential. Our results suggest that membrane physicochemical properties result from a combination of lipid composition, packing and interfacial electrostatics and point to possible avenues in exploring the evolutionary differences in membrane protein function.