Energy coupling to potassium transport in Streptococcus faecalis. Interplay of ATP and the protonmotive force

Abstract

We have studied the mechanism by which metabolic energy is coupled to potassium accumulation by the fermentative bacterium, Streptococcus faecalis. In starving cells, K+ movements into the cells or out are very slow; even 42K+/K+ exchange requires concurrent metabolism of glucose or arginine. Metabolizing cells accumulate K+, establishing a concentration gradient of some 50,000. Accumulation is prevented by reagents that block or short circuit the proton circulation, but 42K+/K+ exchange persists. In glycolyzing cells whose proton pump has been blocked with N,N'-dicyclohexylcarbodiimide, net uptake of K+ can be induced by imposing an artificial membrane potential, interior negative. Net K+ efflux is also controlled by the interplay of ATP and the proton circulation. Addition of proton conductors to glycolyzing cells induces K+ efflux, but has no effect on starving cells; the rate of K+ efflux appears to be a function of the cells' ATP content. We conclude that K+ accumulation requires the cells to generate both a protonmotive force and ATP. K+ uptake is electrogenic and attains a concentration gradient far too steep to be in equilibrium with the membrane potential. We consider two alternative models for K+ transport: a primary ATP-driven pump regulated by the proton circulation or a secondary porter activated by ATP that mediates symport of K+ with H+.