Cryo-EM and MD infer water-mediated proton transport and autoinhibition mechanisms of V<sub>o</sub> complex.

Roh, Soung-Hun; Shekhar, Mrinal; Pintilie, Grigore; Chipot, Christophe; Wilkens, Stephan; Singharoy, Abhishek; Chiu, Wah · Sci Adv · 2020

basic_science · Level V

Where this comes from

Abstract

Rotary vacuolar adenosine triphosphatases (V-ATPases) drive transmembrane proton transport through a V<sub>o</sub> proton channel subcomplex. Despite recent high-resolution structures of several rotary ATPases, the dynamic mechanism of proton pumping remains elusive. Here, we determined a 2.7-Å cryo-electron microscopy (cryo-EM) structure of yeast V<sub>o</sub> proton channel in nanodisc that reveals the location of ordered water molecules along the proton path, details of specific protein-lipid interactions, and the architecture of the membrane scaffold protein. Moreover, we uncover a state of V<sub>o</sub> that shows the <i>c</i>-ring rotated by ~14°. Molecular dynamics simulations demonstrate that the two rotary states are in thermal equilibrium and depict how the protonation state of essential glutamic acid residues couples water-mediated proton transfer with <i>c</i>-ring rotation. Our cryo-EM models and simulations also rationalize a mechanism for inhibition of passive proton transport as observed for free V<sub>o</sub> that is generated as a result of V-ATPase regulation by reversible disassembly in vivo.