Proton Currents and Local Energy Coupling in Thylakoids: A Survey

Summary

A survey of the experimental and conceptual basis of a microchemiosmotic interpretation of energy-dependent processes in thylakoids is presented. It assumes that protons circulate from their active transport points to their backflow ports in a heterogeneous medium, having a resistivity not only transversal, from membrane to isopotential bulk phase, but also lateral, in or on the membrane, an idea central to our hypothesis. Consequently, the proton electrochemical potential ΔμH at the H⁺-generators (redox carriers) is higher than ΔμH at H⁺-leaks (coupling factors and membrane pores), and the measured ΔμH is an average of local values. However, some flexibility in this microscopic coupling is possible, and a delocalized behaviour may sometimes be obtained by increasing the lumen volume (osmolarity decrease) and its conductivity (ionicity increase). A one-to-one link between primary and secondary pumps, as advocated by mosaic chemiosmosis, seems therefore improbable here.

The experimental procedure used in this investigation consisted in correlating electron flow, proton gradient (ΔpH, with or without Δψ), and phosphorylation rate in several conditions. To modulate ΔμH, H⁺ influx or efflux were adjusted by light or ionophore changes: contrary to the prediction of classical chemiosmosis, these two factors have no identical effects. Also, an increase of the distance between H⁺-translocators and coupling factors (SII chain vs. SI) lowers the phosphorylation efficiency of a given mean ΔμH, which is easily explained by a ΔμH drop along the lateral resistance mentioned above. Another approach was to compare redox control and phosphorylation in heavy water media, where proton circulation is hindered. Additional information given concerns possible occurrence of “scalar ATPases” and a quantitative estimate, at variable ΔpH, of proton flux across coupling factor, phosphorylating or not.