Evolution of membrane bioenergetics

By combining structural and phylogenetic analyses, we have earlier clarified the evolutionary relationships among membrane enzymes that couple the transmembrane transfer of protons or sodium ions with the synthesis/hydroly-sis of ATP. A comparison of the structures of the sodium-dependent bacterial and archaeal ATPases revealed nearly identical sets of amino acids involved in sodium binding. Phylogenetic analysis showed that the sodium-dependent ATPases are scattered among proton-dependent ATPases in both the archaeal and bacterial branches of the phylo-genetic tree [1–3]. Barring convergent emergence of the same set of amino acid ligands in several lineages, these findings indicate that the common ancestor of rotary ATPases should have possessed a sodium-binding site. A focused search for primitive sodium-translocating ATPases/ATP synthases among microbial genomes identified an atypical form of a rotary ATPase that is present in a number of phylogenetically diverse marine, halotolerant and pathogenic bacteria and archaea [4]. In complete ge-nomes, representatives of this form (referred to here as an N-ATPase) are always present as second copies, in addition to the typical proton-translocating ATP synthases. Since the N-ATPases carry a full set of sodium-binding residues , we suggested that these enzymes are relict sodium-translocating ATPases that likely confer on their hosts the ability to extrude sodium ions [4]. Recently this prediction has been experimentally confirmed [5]. Concurrently, Lahti et al. have shown that the sodium-translocating membrane pyrophosphatases were evolutionary predecessors of their proton-translocating counterparts [6]. Based on this body of evidence, we suggest that the use of sodium gradient for ATP synthesis is the ancestral modality of membrane bioenergetics that should have been used by the Last Universal Cellular Ancestor (LUCA). Generally, the evolution of membrane bioenergetics seems to have followed the overall trend of progressive seques-tration of protocells from the environment. The first ATP synthases likely evolved from protein translocases [7] within primitive, sodium-impermeable but proton-permeable cell membranes that harboured a set of sodium-transporting enzymes. The more structurally demanding proton-tight membranes, which could accommodate proton-specific pumps, appear to emerge later, independently in bacteria and archaea.