Directed Assembly of Proteopolymer Membrane Arrays with Light Driven Transport Performance

Abstract

Photoconversion membrane proteins (MPs) are Nature's nanoengineering feats for renewable energy management. Harnessing their functions in synthetic systems could help understand, predict, and ultimately control matter and energy at the nanoscale. However, the fragile and often labile nature of lipid bilayers is incompatible with a broad range of engineered conditions. A knowledge gap exists on how to design robust synthetic nanomembranes as lipid-bilayer-mimics to support MP functions, and how to direct hierarchical MP reconstitution into those membranes to form 2-D or 3-D ordered proteomembrane arrays. Here we show that proteorhodopsin, a photoconversion MP that uses light energy to perform proton pumping across its supporting matrix, spontaneously reconstitute into a series of amphiphilic block copolymer membranes via a charge-interaction-directed reconstitution mechanism, even when the polymer membranes are in an entangled or frozen (i.e., glassy) state with far superior stability than lipid bilayers. Our structural and function assays suggest that proteorhodopsin is not enslaved by fluidic or lipid-based membrane environment. Rather, well-defined synthetic nanomembranes, with their tunable membrane moduli, act as allosteric regulators. Frozen polymer membranes with their greatly reduced fluidity and enhanced stability can still bear sufficient conformational freedom that rivals lipid-based biomembranes in supporting proteorhodopsin functions. We expect that versatile block copolymer designs exist to balance membrane fluidity and stability at the nanoscale. This modulates the conformational energetics of reconstituted MPs, and optimizes their stability and performance in synthetic systems.