Trends in Biochemical Sciences
ReviewCo-evolution of primordial membranes and membrane proteins
Section snippets
Membrane evolution and the last universal common ancestor
A topologically closed membrane is a ubiquitous feature of all cellular life forms. This membrane is not a simple lipid bilayer enclosing the innards of the cell: far from that, even in the simplest cells, the membrane is a biological device of a staggering complexity that carries diverse protein complexes mediating energy-dependent (and tightly regulated) import and export of metabolites and polymers [1]. Despite the growing understanding of the structural organization of membranes and
Origin and evolution of the F-type and A/V-type membrane ATPases
It is our belief that insights into the co-evolution of membranes and membrane proteins can be obtained from structural and phylogenetic analyses of the F- and A/V-type ATPases (for reviews, see Refs 27, 28, 29, 30, 31, 32). These are membrane enzymes that are ubiquitous in modern cellular life forms and so were conceivably present in the LUCA [16]; apparently, these ATPases require ion-impermeable (ion-tight) membranes for their function. Together with two unrelated classes of proteins, the
Emergence of integral membrane proteins
In the preceding section, we proposed that the common ancestor of the c-oligomers in the F- and V ATPases could initially function as a membrane pore. Such pores that could be required to enable passive exchange of ions, small molecules and even polymers between protocells and their environment 46, 54 also might represent a transition state in the evolution of integral membrane proteins. Integral membrane proteins contain long stretches of hydrophobic amino acid residues. By contrast, in
Co-evolution of membranes and membrane bioenergetics
Szathmáry [54] recently put forward a scenario of co-evolution of membranes and metabolism, in which evolution proceeded through progressive sequestration of protocells from the environment. Under this model, the gradual build-up of enzymatic pathways inside the protocell should be accompanied by a decrease in membrane permeability. Membrane-coupled energy-conversion reactions that collectively comprise the membrane bioenergetics (Box 2) are an essential part of cell metabolism; unlike other
Conclusions and outlook
The present scenario describes co-evolution of (i) lipid bilayers (from leaky to proton-tight), (ii) membrane proteins (from amphiphilic, pore-forming ones to highly hydrophobic integral membrane proteins) and (iii) membrane bioenergetics (from the relatively simple, sodium-dependent form to the sophisticated proton bioenergetics). The scenario favors the primitive ‘porous’ membranes as an intermediate step between membrane-less pre-cellular life forms and modern cells that are bounded by
Acknowledgements
Valuable discussions with A.A. Baykov, A.V. Bogachev, D.A. Cherepanov, P.A. Dibrov, P. Dimroth, A.V. Finkelstein, T. Haines, W. Junge, T. Krulwich, T. Meier, K.S. Makarova, D. Pogoryelov, V.P. Skulachev, H.-J. Steinhoff, J.E. Walker and Y.I. Wolf are greatly appreciated. We thank M. Kozlova for the help with Figure 1. This study was supported by grants to A.Y.M. from the Deutsche Forschungsgemeinschaft (www.dfg.de/en) and the Volkswagen Foundation (www.volkswagenstiftung.de) and by the
References (98)
Ancestral lipid biosynthesis and early membrane evolution
Trends Biochem. Sci.
(2004)- et al.
On the origin of genomes and cells within inorganic compartments
Trends Genet.
(2005) - et al.
The general protein secretory pathway: phylogenetic analyses leading to evolutionary conclusions
Biochim. Biophys. Acta
(2003) Features of V-ATPases that distinguish them from F-ATPases
FEBS Lett.
(2001)- et al.
ATP synthesis driven by proton transport in F1F0-ATP synthase
FEBS Lett.
(2003) Distribution of F- and A/V-type ATPases in Thermus scotoductus and other closely related species
Syst. Appl. Microbiol.
(2006)Primary sodium ion translocating enzymes
Biochim. Biophys. Acta
(1997)- et al.
Changing the ion binding specificity of the Escherichia coli H+-transporting ATP synthase by directed mutagenesis of subunit c
J. Biol. Chem.
(1995) - et al.
Transmembrane helices before, during, and after insertion
Curr. Opin. Struct. Biol.
(2005) - et al.
Pore-forming protein toxins: from structure to function
Prog. Biophys. Mol. Biol.
(2005)
Disparate proteins use similar architectures to damage membranes
Trends Biochem. Sci.
Principles of membrane protein assembly and structure
Prog. Biophys. Mol. Biol.
The past and present of the sodium energetics: may the sodium-motive force be with you
Biochim. Biophys. Acta
Do sterols reduce proton and sodium leaks through lipid bilayers?
Prog. Lipid Res.
The role of sodium ion transport in Escherichia coli energetics
Biochim. Biophys. Acta
Atomic snapshots of an RNA packaging motor reveal conformational changes linking ATP hydrolysis to RNA translocation
Cell
VMD: visual molecular dynamics
J. Mol. Graph.
The ATP synthase of Escherichia coli: structure and function of F0 subunits
Biochim. Biophys. Acta
Mechanics of coupling proton movements to c-ring rotation in ATP synthase
FEBS Lett.
Stoichiometry and localization of the stator subunits E and G in Thermus thermophilus H+-ATPase/synthase
J. Biol. Chem.
Stoichiometry of the peripheral stalk subunits E and G of yeast V1-ATPase determined by mass spectrometry
J. Biol. Chem.
The proton-driven rotor of ATP synthase: ohmic conductance (10 fS), and absence of voltage gating
Biophys. J.
Proton in the well and through the desolvation barrier
Biochim. Biophys. Acta
The Na+-translocating methyltransferase complex from methanogenic archaea
Biochim. Biophys. Acta
The multifarious couplings of energy transduction
Biochim. Biophys. Acta
On the functional proton current pathway of electron transport phosphorylation. An electrodic view
Biochim. Biophys. Acta
Protons @ interfaces: implications for biological energy conversion
Biochim. Biophys. Acta
Does arginine remain protonated in the lipid membrane? Insights from microscopic pKa calculations
Biophys. J.
Biomembranes: Molecular Structure and Function
Intracellular protein topogenesis
Proc. Natl. Acad. Sci. U. S. A.
The first living systems: a bioenergetic perspective
Microbiol. Mol. Biol. Rev.
The influence of environmental conditions, lipid composition, and phase behavior on the origin of cell membranes
Orig. Life Evol. Biosph.
The Last Universal Common Ancestor: emergence, constitution and genetic legacy of an elusive forerunner
Biol. Direct
Root of the universal tree of life based on ancient aminoacyl-tRNA synthetase gene duplications
Proc. Natl. Acad. Sci. U. S. A.
Rooting the tree of life by transition analyses
Biol. Direct
Where is the root of the universal tree of life?
Bioessays
Did DNA replication evolve twice independently?
Nucleic Acids Res.
Comparative genomics, minimal gene-sets and the last universal common ancestor
Nat. Rev. Microbiol.
Biosynthesis of ether-type polar lipids in archaea and evolutionary considerations
Microbiol. Mol. Biol. Rev.
On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells
Philos. Trans. R. Soc. Lond. B Biol. Sci.
The prokaryote-to-eukaryote transition reflected in the evolution of the V/F/A-ATPase catalytic and proteolipid subunits
J. Mol. Evol.
Did the last common ancestor have a biological membrane?
Biol. Direct
Chemistry and physics of primitive membranes
Top. Curr. Chem.
Stability of model membranes in extreme environments
Orig. Life Evol. Biosph.
Membrane properties of branched polyprenyl phosphates, postulated as primitive membrane constituents
Chem. Biodivers.
Obcells as proto-organisms: membrane heredity, lithophosphorylation, and the origins of the genetic code, the first cells, and photosynthesis
J. Mol. Evol.
Cell evolution and the problem of membrane topology
Nat. Rev. Mol. Cell Biol.
The lipid world
Orig. Life Evol. Biosph.
Synthesizing life
Nature
Cited by (126)
From building blocks to cells
2022, New Frontiers in AstrobiologyAn algal PIP-like aquaporin facilitates water transport and ionic conductance
2021, Biochimica et Biophysica Acta - BiomembranesPotassium physiology from Archean to Holocene: A higher-plant perspective
2021, Journal of Plant PhysiologyCitation Excerpt :Indeed, phylogenetic and biochemical analyses suggest that electrochemical Na+ gradients (ΔμNa+) were actively generated in the “last universal common ancestor” of all existing life, the prokaryotic LUCA, as well as its much later descendant LECA (the last universal eukaryotic ancestor; Margulis et al., 2006; Mulkidjanian et al., 2008; Weiss et al., 2016). Moreover, in this “sodium world” (or “sodium economy”, as it is sometimes called; Skulachev, 1988; Britto and Kronzucker, 2005; Mulkidjanian et al., 2009; Taylor et al., 2012), the generation of ΔμNa+, using ATP as an energy source, may have constituted the means by which membranes were electrochemically energized in the earliest true cells (Mulkidjanian et al., 2008, 2009; Rodríguez-Navarro and Benito, 2010; Lane and Martin, 2012; Poehlein et al., 2012; Dibrova et al., 2015). Considerable evidence suggests that an alternative, proton (H+)-based economy was only later established, via the independent (convergent) evolution of Na+ pumps into H+ pumps in multiple lineages (Mulkidjanian et al., 2008; a chloride-based economy is also possible, see Raven and Beardall, 2020).
Membrane proteins in magnetically aligned phospholipid polymer discs for solid-state NMR spectroscopy
2020, Biochimica et Biophysica Acta - BiomembranesGeneration of long-chain fatty acids by hydrogen-driven bicarbonate reduction in ancient alkaline hydrothermal vents
2024, Communications Earth and EnvironmentLightly counting membrane proteins in native nanodiscs
2024, Nature Nanotechnology