Portasomes as Coupling Factors in Active Ion Transport and Oxidative Phosphorylation

Abstract

SYNOPSIS. We propose that particles, 7–15 nm in diameter, observed on the apical plasma membranes of cation transporting cells of insect midgut, salivary glands, and Malpighian tubules are modified F1-F coupling complexes such as those found on phosphorylating membranes of mitochondria, chloroplasts, and bacteria. We suggest the generic term, portasome, to describe all of these particles and point out that they are located on the side of the membrane which is electronegative and has the low cation concentration, i.e. , on the input side in each case. Biophysical evidence identifies the portasome bearing membrane as the ion transporting membrane in several insect epithelia, some of which exhibit ion modulated ATPase activity. The activity of a K+-modulated ATPase from Manduca sexta midgut is increased in portasome enriched plasma membrane fractions. We propose that portasomes orient the scalar hydrolysis of negatively charged MgATP2− to less negatively charged MgADP thereby eliminating the attraction of MgATP2− to K+ with the result that the K+ ions are ejected to the opposite side of the portasome bearing membrane. This mechanism explains the coupling of the scalar hydrolysis of ATP to the vectorial active transport of K+ which leads to the establishment of a K+ electrochemical gradient. The reverse process, but with an H+ ionophore replacing a K+ ionophore in the portasome, would provide a mechanism for coupling the vectorial flow of H+, driven by a proton electrochemical gradient, to scalar ATP synthesis and thereby provide a mechanism for oxidative phosphorylation. Electrogenic active potassium ion transport would appear to have evolved from oxidative phosphorylation.