Light-Activated Synthetic Rotary Motors in Lipid Membranes Induce Shape Changes Through Membrane Expansion.
Yusuf QutbuddinAinoa GuinartSvetozar GavrilovićKareem Al NahasBen L FeringaPetra SchwillePublished in: Advanced materials (Deerfield Beach, Fla.) (2024)
In biology, membranes are the key structures to separate and spatially organize cellular reaction systems. Their rich dynamics and transformations during the cell cycle are orchestrated by specific membrane-targeted molecular machineries many of which operate through energy dissipation. Likewise, man-made molecular rotary motors powered by light have previously shown drastic effects on cellular systems, but their physical roles on and within lipid membranes remain largely unexplored. Here we systematically investigate the impact of rotary molecular motors on well-defined biological membrane systems, focusing on supported lipid bilayers (SLBs) and giant unilamellar vesicles (GUVs). Notably, we observe dramatic mechanical transformations of these systems upon motor irradiation, indicative of motor-induced membrane expansion. We systematically explore the influence of several factors on this phenomenon, such as motor concentration and membrane composition, and find that in particular, membrane fluidity plays a crucial role in motor-induced deformations. At the same time, only minor contributions from local heating and singlet oxygen generation are observed. Most remarkably, we find that membrane area expansion under the influence of the motors continues as long as irradiation is maintained, and the system stays out-of-equilibrium. Overall, this research contributes to a comprehensive understanding of how molecular motors interact with biological membranes, elucidating the multifaceted factors that govern membrane responses and shape transitions in the presence of these remarkable molecular machines, thereby supporting their future applications in chemical biology. This article is protected by copyright. All rights reserved.