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

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.

Comparative analysis of active sites in P-loop nucleoside triphosphatases suggests an ancestral activation mechanism

“…We have previously presented evidence suggesting that activating Arg resudues were 852 independently recruited, instead of K + ions, in diverse lineages of TRAFAC NTPases 853 (Dibrova et al, 2015;Mulkidjanian, et al, 2012b), which implies that the common ancestor 854 of TRAFAC NTPases was a K + -dependent enzyme with an Asp/Asn in the Gly13 position. 855 Accordingly, residues congruent to Asp/Asn could have remained in the Gly13 position even 856 in some TRAFAC NTPases that have lost the K + -dependence.…”

Transcriptomic analysis reveals how a lack of potassium ions increases Sulfolobus acidocaldarius sensitivity to pH changes

“…Potassium is the most abundant cation in the cytoplasm of all cells, reflecting its deep-rooted compatibility with cellular structures throughout evolution (Dibrova et al, 2015;Kuo et al, 2005). The role of potassium ions is suggested to have been retained as it would be too 'energetically demanding' to alter (Mulkidjanian et al, 2012).…”

Eukaryotic G protein-coupled receptors as descendants of prokaryotic sodium-translocating rhodopsins

“…From the comparison of the Na + -binding sites, the ancient state of this enzyme could be reconstructed as a Na + -exporting, ATP-driven pump, one of the ancient sodium export pumps that could keep the [K + ]/[Na + ] ratio in the cell cytoplasm over unity [ 43 – 46 ]. Since many key cellular systems, traceable to the Last Universal Cellular Ancestor (LUCA) and including the protein synthesis, are activated by K + ions and inhibited by Na + ions, even the primordial cells should have had systems for Na + export [ 46 – 48 ]. Our phylogenomic analysis even suggested that a particular family of rotary ATPases, that we dubbed N-ATPases, contains enzymes that still operate as Na + export pumps in modern organisms [ 49 ].…”