Evolution of permease diversity and energy-coupling mechanisms: An introduction

Abstract

In this Forum, a number of apparently unrelated permeases are discussed which couple different forms of energy to solute transport. While the energy-coupling mechanisms utilized by the different permease classes are clearly distinct, it is proposed, based on structural comparisons, that many of these permeases possess transmembrane, hydrophobic domains which are evolutionarily related. Carriers may have arisen from transmembrane pore-forming proteins, and the protein constituents or domains which are specifically responsible for energy coupling may have had distinct origins. Thus, complex permeases may possess mosaic structures. The mechanistic implications of this proposal are presented. Five distinct mechanisms are known to be responsible for the transport of hydrophilic organic molecules across the cytoplasmic membranes of living cells: (1) facilitated diffusion mediated by non-specific pore-forming integral membrane proteins, such as the glycerol facilitator of Escherichia coli; (2) facilitated diffusion catalysed by single-species stereospecific facilitators, such as the glucose carrier of the human red blood cell; (3) chemiosmotically-coupled active transport catalysed by two-species facilitators, such as the lactose:H + or the melibiose:Na + symporter of E. coli; (4) chemically driven active transport catalysed, for example, by the multicomponent periplasmic binding-protein-dependent transport systems such as the maltose, histidine or oligopeptide permease of enteric bacteria; and (5) group translocation catalysed by the bacterial phosphoenolpyruvate-dependent, sugar-phosphorylating phosphotransferase system (Saier and Boyden, 1984; Saier, 1985). Mutants analyses and sequence comparisons as well as functional consideration