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Ancient systems of sodium/potassium homeostasis as predecessors of membrane bioenergetics

  • Special Issue Honoring 80th Anniversary of Academician V. P. Skulachev Guest Editors D. B. Zorov and B. V. Chernyak
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Abstract

Cell cytoplasm of archaea, bacteria, and eukaryotes contains substantially more potassium than sodium, and potassium cations are specifically required for many key cellular processes, including protein synthesis. This distinct ionic composition and requirements have been attributed to the emergence of the first cells in potassium-rich habitats. Different, albeit complementary, scenarios have been proposed for the primordial potassium-rich environments based on experimental data and theoretical considerations. Specifically, building on the observation that potassium prevails over sodium in the vapor of inland geothermal systems, we have argued that the first cells could emerge 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. Marine and freshwater environments generally contain more sodium than potassium. Therefore, to invade such environments, while maintaining excess of potassium over sodium in the cytoplasm, primordial cells needed means to extrude sodium ions. The foray into new, sodium-rich habitats was the likely driving force behind the evolution of diverse redox-, light-, chemically-, or osmotically-dependent sodium export pumps and the increase of membrane tightness. Here we present a scenario that details how the interplay between several, initially independent sodium pumps might have triggered the evolution of sodium-dependent membrane bioenergetics, followed by the separate emergence of the proton-dependent bioenergetics in archaea and bacteria. We also discuss the development of systems that utilize the sodium/potassium gradient across the cell membranes.

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Abbreviations

KREEP:

Potassium [K], Rare Earth Elements and Phosphorus

LUCA:

Last Universal Cellular Ancestor

P-loop:

phosphate-binding loop — amino acid sequence (in nucleotide-binding proteins) also known as a Walker A-motif

Δψ:

transmembrane potential

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Authors and Affiliations

  1. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119992, Moscow, Russia

    D. V. Dibrova & A. Y. Mulkidjanian

  2. National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland, 20894, USA

    M. Y. Galperin & E. V. Koonin

  3. School of Physics, Osnabrueck University, 49069, Osnabrueck, Germany

    A. Y. Mulkidjanian

  4. School of Bioengineering and Bioinformatics, Lomonosov Moscow State University, 119992, Moscow, Russia

    A. Y. Mulkidjanian

Authors
  1. D. V. Dibrova
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  2. M. Y. Galperin
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  3. E. V. Koonin
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  4. A. Y. Mulkidjanian
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Correspondence to A. Y. Mulkidjanian.

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We dedicate this paper to Professor Vladimir P. Skulachev on the occasion of his 80th birthday and in appreciation of his seminal contribution to the field of science that, many years ago, has been named bioenergetics at his suggestion.

Published in Russian in Biokhimiya, 2015, Vol. 80, No. 5, pp. 590–611.

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Dibrova, D.V., Galperin, M.Y., Koonin, E.V. et al. Ancient systems of sodium/potassium homeostasis as predecessors of membrane bioenergetics. Biochemistry Moscow 80, 495–516 (2015). https://doi.org/10.1134/S0006297915050016

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  • DOI: https://doi.org/10.1134/S0006297915050016

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