The proton-driven rotor of ATP synthase: ohmic conductance (10 fS), and absence of voltage gating

The membrane portion of F₀F₁-ATP synthase, F₀, translocates protons by a rotary mechanism. Proton conduction by F₀ was studied in chromatophores of the photosynthetic bacterium Rhodobacter capsulatus. The discharge of a light-induced voltage jump was monitored by electrochromic absorption transients to yield the unitary conductance of F₀. The current-voltage relationship of F₀ was linear from 7 to 70 mV. The current was extremely proton-specific (>10⁷) and varied only slightly (≈threefold) from pH 6 to 10. The maximum conductance was ≈10 fS at pH 8, equivalent to 6240 H⁺ s⁻¹ at 100-mV driving force, which is an order-of-magnitude greater than of coupled F₀F₁. There was no voltage-gating of F₀ even at low voltage, and proton translocation could be driven by ΔpH alone, without voltage. The reported voltage gating in F₀F₁ is thus attributable to the interaction of F₀ with F₁ but not to F₀ proper. We simulated proton conduction by a minimal rotary model including the rotating c-ring and two relay groups mediating proton exchange between the ring and the respective membrane surface. The data fit attributed pK values of ≈6 and ≈10 to these relays, and placed them close to the membrane/electrolyte interface.