The multicollisional, obstructed, long-range diffusional nature of mitochondrial electron transport

Abstract

Data are presented which reveal that ubiquinone (Q)-mediated electron transport is a multicollisional, obstructed, long-range diffusion process, where factors that affect the rate of lateral diffusion also affect the rate of electron transport. Based on fluorescence recovery after photobleaching measurements, it was concluded that Q-mediated electron transport occurs by the random collision of redox components which are independent lateral diffusants, each greater than 86% mobile and diffusing in a common pool. The diffusion process of Q-mediated electron transport is 1) multicollisional since the transfers of reducing equivalents between appropriate redox partners occur with less than 100% collision efficiency; 2) obstructed since its maximal rate as well as the rates of diffusion of all redox components involved vary as a function of the membrane protein density; and 3) long-range since the diffusion of all redox components is protein density-dependent, and the diffusion distance required for Q to catalyze the transfer of a reducing equivalent from Complex II to III must be, on average, greater than 37.6 nm. These findings and other theoretical treatments reveal that measurements of short-range diffusion (less than 10 nm), in which collisions between appropriate redox partners do not occur, on average, and which are not affected by membrane protein density, are irrelevant to the collisional process of electron transport. Thus, the data show that the maximum electron transport rate is dependent on both the diffusion rate and the concentration of the redox components. Sucrose was found to inhibit both the mobility of redox components as well as their electron transport rates. Data presented on the relationships between membrane viscosity, rates of lateral and rotational diffusion, and mobile fractions of redox components do not support rotationally immobile aggregates in the functional inner membrane. The high degree of unsaturated phospholipids and the absence of cholesterol in the bilayer of the native inner membrane reflect a requirement for a low resistance to motion of the redox components to compensate for the multicollisional, obstructive nature of their catalytically important collisions in this membrane. These findings support the Random Collision Model of electron transport in which the diffusion and concentration of redox components limit the maximum rate of electron transport.