The random collision model and a critical assessment of diffusion and collision in mitochondrial electron transport

This review focuses on our studies over the past ten years which reveal that the mitochondrial inner membrane is a fluid-state rather than a solid-state membrane and that all membrane proteins and redox components which catalyze electron transport and ATP synthesis are in constant and independent diffusional motion. The studies reviewed represent the experimental basis for therandom collision model of electron transport. We present five fundamental postulates upon which the random collision model of mitochondrial electron transport is founded: (1) All redox components areindependent lateral diffusants; (2) Cytochromec diffuses primarily inthree dimensions; (3) Electron transport is adiffusion-coupled kinetic process; (4) Electron transport is amulticollisional, obstructed, long-range diffusional process; (5) The rates of diffusion of the redox components have a direct influence on the overall kinetic process of electron transport and can berate limiting, as indiffusion control. The experimental rationales and the results obtained in testing each of the five postulates of the random collision model are presented. In addition, we offer the basic concepts, criteria and experimental strategies that we believe are essential in considering the significance of the relationship between diffusion and electron transport. Finally, we critically explore and assess other contemporary studies on the diffusion of inner membrane components related to electron transport including studies on: rotational diffusion, immobile fractions, complex formation, dynamic aggregates, and rates of diffusion. Review of all available data confirms the random collision model and no data appear to exist that contravene it. It is concluded that mitochondrial electron transport is a diffusion-based random collision process and that diffusion has an integral and controlling affect on electron transport.