Possible roles of two quinone molecules in direct and indirect proton pumps of bovine heart NADH-quinone oxidoreductase (complex I)

Abstract

In many energy transducing systems which couple electron and proton transport, for example, bacterial photosynthetic reaction center, cytochrome bc(1)-complex (complex III) and E. coli quinol oxidase (cytochrome bo(3) complex), two protein-associated quinone molecules are known to work together. T. Ohnishi and her collaborators reported that two distinct semiquinone species also play important roles in NADH-ubiquinone oxidoreductase (complex I). They were called SQ(Nf) (fast relaxing semiquinone) and SQ(Ns) (slow relaxing semiquinone). It was proposed that Q(Nf) serves as a "direct" proton carrier in the semiquinone-gated proton pump (Ohnishi and Salerno, FEBS Letters 579 (2005) 4555), while Q(Ns) works as a converter between one-electron and two-electron transport processes. This communication presents a revised hypothesis in which Q(Nf) plays a role in a "direct" redox-driven proton pump, while Q(Ns) triggers an "indirect" conformation-driven proton pump. Q(Nf) and Q(Ns) together serve as (1e(-)/2e(-)) converter, for the transfer of reducing equivalent to the Q-pool.

Fig. 1

A scheme is to show the flows of electrons and protons in bovine heart complex I. Aarrows of direct pump and indirect pump indicate that these two pumps are driven by two kinds of ubiquinone species. At the end of the cycle, bc₁ indicates the coupling to complex III via Qpool.

Fig. 2

Schematic mechanisms of the (a)-(c) Q_Nf-gated “direct” proton pump which transports 2 protons, and (d)-(f) Q_Ns-induced conformation-driven “indirect” proton pump which also transports 2 protons.