Evolutionary primacy of sodium bioenergetics

Abstract

BackgroundThe F- and V-type ATPases are rotary molecular machines that couple translocation of protons or sodium ions across the membrane to the synthesis or hydrolysis of ATP. Both the F-type (found in most bacteria and eukaryotic mitochondria and chloroplasts) and V-type (found in archaea, some bacteria, and eukaryotic vacuoles) ATPases can translocate either protons or sodium ions. The prevalent proton-dependent ATPases are generally viewed as the primary form of the enzyme whereas the sodium-translocating ATPases of some prokaryotes are usually construed as an exotic adaptation to survival in extreme environments.ResultsWe combine structural and phylogenetic analyses to clarify the evolutionary relation between the proton- and sodium-translocating ATPases. A comparison of the structures of the membrane-embedded oligomeric proteolipid rings of sodium-dependent F- and V-ATPases reveals nearly identical sets of amino acids involved in sodium binding. We show that the sodium-dependent ATPases are scattered among proton-dependent ATPases in both the F- and the V-branches of the phylogenetic tree.ConclusionBarring convergent emergence of the same set of ligands in several lineages, these findings indicate that the use of sodium gradient for ATP synthesis is the ancestral modality of membrane bioenergetics. Thus, a primitive, sodium-impermeable but proton-permeable cell membrane that harboured a set of sodium-transporting enzymes appears to have been the evolutionary predecessor of the more structurally demanding proton-tight membranes. The use of proton as the coupling ion appears to be a later innovation that emerged on several independent occasions.ReviewersThis article was reviewed by J. Peter Gogarten, Martijn A. Huynen, and Igor B. Zhulin. For the full reviews, please go to the Reviewers' comments section.

Membrane-integral pyrophosphatase subfamily capable of translocating both Na + and H +

“…In summary, we have characterized a unique subfamily of membrane-integral PPases that transport both Na + and H + ions in a noncompetitive manner and are widespread in the bacterial world. Our findings provide support for the hypothesis that selection pressure favors membrane H + coupling vs. Na + coupling in modern organisms (24)(25)(26)(27). Furthermore, we conclude that (i) changes in transport specificity can be achieved in different ways and require only minor rearrangements in protein structure; (ii) the evolutionary pathway from Na + to H + transport is not strictly unidirectional, and may involve recursions; (iii) Na + and H + transport proceed via highly similar mechanisms; and (iv) Na …”

Origin of first cells at terrestrial, anoxic geothermal fields

“…Therefore, they would require ion pumps capable of ejecting Na + ions out of the cell against large concentration backpressure. As argued previously on the basis of phylogenomic analysis of rotary ATPases, the interplay between several Na + pumps might have led to the emergence of membrane bioenergetics, initially in its ancestral, Na + -using form (38,131,132). The proposed terrestrial origin of the first cells implies that life started not as a planetary but as a local event, confined to a longlasting inland geothermal field or to a network of such fields at a continental volcanic system.…”

Na+-translocating Membrane Pyrophosphatases Are Widespread in the Microbial World and Evolutionarily Precede H+-translocating Pyrophosphatases

“…We further propose that the ancestor enzyme is possibly a Na ϩ pump. Thus, the evolution of a membrane PPase coupling ion specificity from Na ϩ to H ϩ parallels the scenario suggested for Na ϩ -and H ϩ -coupled F-and V-type ATP synthases/ATPases and adds support to the concept of global evolutionary primacy of Na ϩ -coupled bioenergetics (43)(44)(45)53). Further research is required to establish the physiological role of Na ϩ -PPase.…”