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Co-evolution of primordial membranes and membrane proteins - PubMed

Review

Co-evolution of primordial membranes and membrane proteins

Armen Y Mulkidjanian et al. Trends Biochem Sci. 2009 Apr.

Abstract

Studies of the past several decades have provided major insights into the structural organization of biological membranes and mechanisms of many membrane molecular machines. However, the origin(s) of the membrane(s) and membrane proteins remains enigmatic. We discuss different concepts of the origin and early evolution of membranes with a focus on the evolution of the (im)permeability to charged molecules such as proteins, nucleic acids and small ions. Reconstruction of the evolution of F-type and A/V-type membrane ATPases (ATP synthases), which are either proton- or sodium-dependent, might help us to understand not only the origin of membrane bioenergetics but also of membranes themselves. We argue that evolution of biological membranes occurred as a process of co-evolution of lipid bilayers, membrane proteins and membrane bioenergetics.

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Figures

Figure 1
Figure 1. Structure and evolutionary relationships of F-type and A/V-type ATPases

(a) modern F- and V-type ATPases; the minimal, prokaryotic sets of subunits are depicted; in the case of those V-ATPase subunits that are differently denoted in prokaryotes and eukaryotes, double notation is used: eukaryotic/prokaryotic. The subunits that form the membrane-bound FO and VO parts, respectively, are denoted by italic letters. The remaining subunits form the detachable, protruding F1 and V1 parts of the enzymes. Orthologous subunits are shown by the same colours and shapes, and non-homologous but functionally analogous subunits of the central stalk are shown by different colours and shapes. The a subunits that show structural similarity but might not be homologous [52] are shown by distinct but similar colours. For further details, see main text, Box 1 and ref. [52]. (b) membrane rotor subunits of the F-type and V-type, Na+-translocating ATP synthases; left, undecamer of c subunits of the Na+-translocating F-type ATP synthase of Ilyobacter tartaricus (PDB entry 1YCE [48]); right, decamer of K subunits of the Na+-translocating V-type ATP synthase of Enterococcus hirae (PDB entry 2BL2 [49]); both rings are tilted to expose the internal pore; in I. tartaricus, Na+ ions (purple) crosslink the neighbouring subunits, whereas in E. hirae the Na+ ions are bound by four-helical bundles that evolved via a subunit duplication (see also [50]). The subunits and residues that are superimposed on the panel below are highlighted, with subunit A of I. tartaricus shown in green and subunit B shown in ice-blue. (c) structural superposition of the Na+-binding sites of the F-type and A/V-type ATPases; in both structures, major coordinating bonds to the Na+ ion are provided by the principal ligand (Glu65A in I. tartaricus and Glu139 in E. hirae); other bonds come from a conserved glutamine (Gln32A in I. tartaricus and Gln110 in E. hirae), a hydroxy group of Ser66B in I. tartaricus and Thr64 in E. hirae and a backbone carbonyl (Val63B in I. tartaricus and Leu61 in E. hirae); in E. hirae a direct bond is provided by Gln65, whereas the corresponding residue in the I. tartaricus c-subunit, Thr67 apparently binds Na+ ion through a water molecule (T. Meier, personal communication); the remaining, sixth bond is provided, most likely, by an unseen water molecule [50]; note the superposition, in addition to the Na+ ligands, of non-ligating tyrosine residues (Tyr70B in I. tartaricus and Tyr68 in E. hirae) that are located beneath the Na+ ion and stabilize the principal Glu ligand [40]. The figure was produced using the VMD software package [78].

Figure 2
Figure 2. Insertion of a folded, water-soluble, α-helical hairpin into the membrane via an “inside-out” transition

Blue, hydrophilic surfaces of α-helices; yellow, their hydrophobic surfaces. (a) A soluble α -helical hairpin. (b) The α-helical hairpin spreads on the membrane surface by interacting with the lipid bilayer. (c) The proteins turn “inside-out”, aggregate and insert into the membrane forming a pore.

Figure 3
Figure 3. The proposed scenario for the evolution of membranes and membrane enzymes - from separate RNA helicases and primitive membrane pores, via membrane RNA and protein translocases, to the F- and V-type ATPases

Reproduced with permission from ref. [50]. The scheme shows the proposed transition from primitive, porous membranes that were leaky both to Na+ and H+ (dotted lines), via membranes that were Na+-tight but H+-leaky (dashed lines) to the modern-type membranes that are impermeable to both H+ and Na+ (solid lines). The brown dashed contour around one of the modern bacteria emphasizes that the membrane pores in the outer membranes of gram-negative bacteria, although formed not by α-helices but by β-barrels, can be considered as a recapitulation of the primordial membrane architecture. The common ancestor of the F- and V-ATPases possessed a Na+-binding site, the structure of which can be inferred from the superposition shown in Fig. 1 (c). The question mark indicates the ambiguity of the placement of the LUCA on the scheme. Regardless of whether LUCA was a modern-type cell or a consortium of replicating, membrane-bounded entities, it either had porous membranes so that the common ancestor of the F- and V-type ATPases either operated as a polymer translocase, with Na+ ions performing a structural role, or had membranes that were tight to sodium but permeable to protons; in this case the LUCA could possess sodium-dependent energetics (see main text and [50] for details).

Figure B1
Figure B1. Proton-dependent bioenergetics compared to sodium-dependent bioenergetics

Two halves of bacterial cells are shown with elements of sodium bioenergetics depicted to the left and elements of proton bioenergetics shown to the right. Blue spheres denote sodium ions, and red spheres denote protons. Blue arrows indicate sodium transfer steps, red arrows indicate proton transfer steps, dashed black arrows indicate electron transfer steps. The numbers of translocated H+ or Na+ ions are given per one electron. Patterned shapes denote redox modules. A dashed red line outside the proton-tight membrane indicates the interfacial electrostatic barrier for protons that confines them to the membrane surface, the checked strip indicates the higher atom density in the midplain of a proton-tight membrane. The scale of redox potentials (left) emphasizes that the Na+-pump NQR uses a redox span of only ∼0.4 V, whereas the full-fledged chain of redox-driven proton pumps can use the whole biochemically relevant redox span of 1.2 V. Abbreviations: PP, membrane pyrophosphatase; DC, membrane Na+-transporting decarboxylase; NQR, Na+-translocating NADH:ubiquinone oxidoreductase; NDH1, NADH:ubiquinone oxidoreductase of type 1; bc1, cytochrome bc1 complex; c, cytochrome c; COX, cytochrome oxidase.

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