Review
Co-evolution of primordial membranes and membrane proteins

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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.

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

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