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 remain 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 and 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 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.
Membrane evolution and the Last Universal Common AncestorA 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 molecular mechanisms of many membrane proteins, the origin (s) of biological membranes remain obscure [2][3][4][5].The conservation of a set of essential genes between two major domains of life, archaea and bacteria, leaves no reasonable doubt in the existence of some version of Last Universal Common Ancestor (LUCA), the prototypic organism that led to the three branches of cellular life, namely, Bacteria, Archaea, and Eukarya [6]. The standard model of evolution places the primary division of cellular life forms between Archaea and Bacteria (e.g., [7]). Rooting the "tree of life" is an extremely difficult problem, and alternatives to the standard model were proposed including rooting within the bacteria [8] or between prokaryotes and eukaryotes [9]. In this article, we stick to the standard model that, on the weight of the totality of evidence, especially, the fundamental differences between DNA replication systems [10] and the membrane structure and biogenesis pathways (see below), we consider to be most plausible.Under the standard model, the approach of choice for the reconstruction of the early evolution of a particular cellular system is to systematically compare its components in Bacteria and Archaea [11]. This approach yields informative results, especially, in the case of the translation