It is easy to note, while looking for the most conserved proteins, an under-representation of early conserved membrane proteins. This fact suggests that the emergence of membrane proteins may have followed the emergence of pre-cellular RNA/protein organisms. However, the nearly universal conservation of complex, membrane-embedded molecular machines, such as general protein secretory pathway elements and the F- and V-type ATP-synthases in modern cellular life forms, indicates that the L.U.C.A. might possess some kind of hydrophobic layer although not necessarily a full-fledged cellular organization based on lipid biosynthesis.The energetics of first living forms had to have been based on phosphate transfer reactions, since all the organisms were depending on nucleotides-triphosphate as energy source for anabolic reactions, synthesized mostly by ATP-synthases. Likely, the ancestral ATP-synthases, the smallest existing rotary engines, evolved from the connection of a membrane hexameric helicases (like the RNA-helicase Rho) with a membrane pore, and proceeded through the stages of RNA and protein translocases pumping sodium ions along with other sodium-pumps, such as the sodium-transporting pyrophosphatase and the sodium-transporting decarboxylase (present both in bacteria and archaea, antedating therefore the divergence of the three domains of life). Concerning the formation of a pore into the membrane, a helical hairpin, upon an succeeding interaction with a double-layer, might spread on its surface and then reassemble within the membrane in such a way that the non-polar side chains would interact with the hydrophobic lipid phase. More hairpins, then, would tend to aggregate, leading to the formation of water-filled pores. This arrangement is retained by the membrane embedded ring of the ATP-synthases, while the described mechanism of spontaneous protein insertion into the membrane (without translocon machinery) is still used by certain bacterial toxins and related proteins. Unlike other sodium-pumps, this common ancestor of the F/V-ATP-synthases would be potentially able to translocate sodium ions in both directions, thus resulting a reversal of the rotation in a sodium-driven synthesis of ATP. It is probable that the fulfillment of this event marked the birth of membrane bioenergetics, when the ancient sodium-pumps, together with the ancestral F/V-type ATP synthases, completed the first bioenergetic cycle. At a later stage, there would have been a transition towards a proton driven bioenergetics with the evolution of tighter membranes (possessing two-chains lipids for instance), where proton transfer could have been chemically coupled to redox reactions, thus enabling the creation of efficient redox- and light-driven generators of a proton motive force. The second possibility for the formation of integral membrane proteins would be the creation of membrane pores from large amphiphilic proteins, which might undergo “inside-out” rearrangements after binding to lipid bilayers. The second universally conserved membrane protein, SecY, exemplifies this kind of protein architecture. Starting from the pores that were built up of amphiphilic stretches of amino acids, such integral membrane proteins could evolve via the combined effect of multiple replacements of polar amino acids and gene duplications, ultimately yielding multi-helix hydrophobic bundles. Then, these multi-helix bundles could enable the controlled insertion of hydrophobic bundles into the membrane (with the aid of other proteins), as in the case of the conserved translocon SecY. Therefore, a plausible scenario of membrane evolution should include an evolutionary scenario for the emergence of integral membrane proteins, in parallel with the cellular lipid synthesis: in this way it suggests a co-evolution between inner cellular biochemical pathways, and the membrane system (the latter is a system because it consists of lipid bilayer plus different kinds of embedded proteins). Such co-evolutionary process, as above anticipated, brought about an increase in the ion-tightness of the membrane, and a transition from amphiphilic, pore-forming proteins, towards highly hydrophobic integral membrane complexes, which are very efficient for specific functions. Unfortunately, a comparison between bacteria and archaea does not shed much light on the origin and evolution of biological membranes, since the two domains have diverged too early in the complexification of their membranes.
Koonin, E.V., Martin, W. (2005) On the origin of genomes and cells within inorganic compartments; Trends Genet., 21, 12: 647-54.