Ancient Systems of Na+/K+ Homeostasis as Predecessors of Membrane Bioenergetics

Date

Mar 1, 2017

Time

11:00 AM - 12:00 PM

Speaker

Armen Y. Mulkidjanian

Affiliation

School of Physics, University of Osnabrueck, Germany; School of Bioengineering and Bioinformatics and A.N. Belozersky Institute of Physico-chemical Biology, Lomonosov Moscow State University, Russia

Language

en

Main Topic

Biologie

Other Topics

Biologie

Host

Marino Zerial & Yannis Kalaidzidis

Description

It is well known that the cytoplasm of living cells, generally, contains more potassium ions than sodium ions. It is also well established that prevalence of K+ ions is crucial for the activity of numerous (nearly) universal key enzymes, including those components of the translation system that even preceded the Last Universal Cellular Ancestor (LUCA) [1]. The inhibitory effect of Na+ on many of these ubiquitous K+-dependent enzymes does not seem compatible with the evolution of the ancestral cellular systems in marine environments with high sodium levels. Based on the data on the prevalence of potassium over sodium in cellular tissues, Archibald Macallum suggested, as early as in 1926, that the first cells might have emerged in K+-rich habitats [2]. Different, albeit complementary, scenarios have been recently proposed for the primordial K+-rich environments based on experimental data and theoretical considerations [1,3]. Specifically, building on the observation that the [K+]/[Na+] ratio is much greater than unity at vapor-dominated zones of inland geothermal systems, we argued that the first cells could have emerged in the pools and puddles at the periphery of primordial anoxic geothermal fields, where the elementary composition of the condensed vapor would resemble the internal milieu of modern cells [1]. Marine environments generally show a [K+]/[Na+] << 1.0. Therefore, to invade such environments, while maintaining the cytoplasmic [K+]/[Na+] ratio over unity, primordial cells needed ion-tight membranes and means to extrude sodium ions. The foray into marine, Na+-rich habitats was likely to drive the evolution of diverse redox-, light-, chemically-, or osmotically-dependent sodium export pumps as well as the increase of membrane tightness [4,5]. At some point, under the conditions of high salinity of the primordial ocean, one of such pumps, the Na+-translocating rotary ATPase, could change the direction of rotation and start to synthesize ATP at the expense of the transmembrane sodium potential, thus launching the membrane bioenergetics. In a rotary ATP synthase the energy of sequentially translocated ions is stored stepwise in the elastic deformation of the enzyme until enough energy to drive ATP synthesis is accumulated [6]. Hence, the rotary ATP synthase is a unique machine that can synthesize ATP by accumulating small portions of energy, which could be harvested by diverse redox- or light-driven ion translocases [5,7]. Furthermore, the rotary ATP synthases could be driven even by expelling “garbage” out of the cell - when the expelled cation(s) is/are accompanied with anionic forms of the end-products of cell fermentation, such as acetate or lactate [8,9]. Hence, on the primordial anoxic Earth, where organic acids should have been the end-products in most of prokaryotic fermentation pathways, a part of the ATP stock could be synthesized (almost) “for free” [5]. After the oxygenation of the atmosphere, the enzymes of membrane bioenergetics gradually became decoupled from the machinery responsible for maintaining the Na+/K+ disequilibrium. On one hand, prokaryotic membranes became largely impermeable not only to sodium ions but also to protons, and the proton-dependent bioenergetics, more beneficial under oxidizing conditions [10], became prevalent. On the other hand, the ancestors of eukaryotes, on one hand, evolved a specialized, extremely efficient enzyme to maintain the Na+/K+ disequilibrium, namely the Na+/K+ ATPase, and, on the other hand, recruited &#945;-proteobacteria as energy-converting machines, future mitochondria. Still, eukaryotic cells harbor a plethora of Na+-coupled membrane enzymes, including the G-protein coupled receptors [11], as relics of the primordial Na+-exporting machinery.

Last modified: Mar 2, 2017, 8:55:53 AM