Landing Proteins on Graphene Trampoline Preserves Their Gas-Phase Folding on the Surface

Abstract

Molecule-surface collisions are known to initiate dynamics that lead to products inaccessible by thermal chemistry. These collision dynamics, however, have mostly been examined on bulk surfaces, leaving vast opportunities unexplored for molecular collisions on nanostructures, especially on those that exhibit mechanical properties radically different from those of their bulk counterparts. Probing energy-dependent dynamics on nanostructures, particularly for large molecules, has been challenging due to their fast time scales and high structural complexity. Here, by examining the dynamics of a protein impinging on a freestanding, single-atom-thick membrane, we discover <i>molecule-on-trampoline</i> dynamics that disperse the collision impact away from the incident protein within a few picoseconds. As a result, our experiments and <i>ab initio</i> calculations show that cytochrome c retains its gas-phase folded structure when it collides onto freestanding single-layer graphene at low energies (∼20 meV/atom). The <i>molecule-on-trampoline</i> dynamics, expected to be operative on many freestanding atomic membranes, enable reliable means to transfer gas-phase macromolecular structures onto freestanding surfaces for their single-molecule imaging, complementing many bioanalytical techniques.