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Expansion of the “Sodium World” through Evolutionary Time and Taxonomic Space

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Abstract

In 1986, Vladimir Skulachev and his colleagues coined the term “Sodium World” for the group of diverse organisms with sodium (Na)-based bioenergetics. Albeit only few such organisms had been discovered by that time, the authors insightfully noted that “the great taxonomic variety of organisms employing the Na-cycle points to the ubiquitous distribution of this novel type of membrane-linked energy transductions”. Here we used tools of bioinformatics to follow expansion of the Sodium World through the evolutionary time and taxonomic space. We searched for those membrane protein families in prokaryotic genomes that correlate with the use of the Na-potential for ATP synthesis by different organisms. In addition to the known Na-translocators, we found a plethora of uncharacterized protein families; most of them show no homology with studied proteins. In addition, we traced the presence of Na-based energetics in many novel archaeal and bacterial clades, which were recently identified by metagenomic techniques. The data obtained support the view that the Na-based energetics preceded the proton-dependent energetics in evolution and prevailed during the first two billion years of the Earth history before the oxygenation of atmosphere. Hence, the full capacity of Na-based energetics in prokaryotes remains largely unexplored. The Sodium World expanded owing to the acquisition of new functions by Na-translocating systems. Specifically, most classes of G-protein-coupled receptors (GPCRs), which are targeted by almost half of the known drugs, appear to evolve from the Na-translocating microbial rhodopsins. Thereby the GPCRs of class A, with 700 representatives in human genome, retained the Na-binding site in the center of the transmembrane heptahelical bundle together with the capacity of Na-translocation. Mathematical modeling showed that the class A GPCRs could use the energy of transmembrane Na-potential for increasing both their sensitivity and selectivity. Thus, GPCRs, the largest protein family coded by human genome, stem from the Sodium World, which encourages exploration of other Na-dependent enzymes of eukaryotes.

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Abbreviations

COG:

Cluster of Orthologous Groups of proteins

GPCR:

G protein-coupled receptor

GTDB:

Genome Taxonomy Database

LUCA:

Last Universal Cellular Ancestor

MR:

microbial rhodopsin

NaR:

Na+-translocating rhodopsin

NQR:

Na+-translocating NADH:quinone oxidoreductase

pmf :

proton-motive force

PRC:

photochemical reaction center

RNF:

Na+-translocating ferredoxin:NAD(H) oxidoreductase

smf :

sodium-motive force

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Acknowledgements

We are particularly thankful to Vladimir Skulachev for his long-lasting interest in our work. We gratefully acknowledge helpful discussions with Drs. Alexander V. Bogachev, Pavel Dibrov, Michael Y. Galperin, Johann Klare, Eugene V. Koonin, Kira S. Makarova, Heinz-Juergen Steinhoff, Natalia Voskoboynikova, and Yuri V. Wolf.

Funding

This work was financially supported by the Deutsche Forschungsgemeinschaft, the German Academic Exchange Service (DAAD), the EvoCell Program of the Osnabrueck University, the Development Program of the Lomonosov Moscow State University (supercomputers “Chebyshev” and “Lomonosov”), and by the Russian Science Foundation (project no. 17-14-01314).

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Authors and Affiliations

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

    M. I. Kozlova, D. N. Shalaeva & A. Y. Mulkidjanian

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

    M. I. Kozlova, D. V. Dibrova & A. Y. Mulkidjanian

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

    I. M. Bushmakin, J. D. Belyaeva & A. Y. Mulkidjanian

  4. Semenov Institute of Chemical Physics, Russian Academy of Sciences, 119991, Moscow, Russia

    D. A. Cherepanov

Authors
  1. M. I. Kozlova
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  2. I. M. Bushmakin
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  3. J. D. Belyaeva
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  4. D. N. Shalaeva
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  5. D. V. Dibrova
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  6. D. A. Cherepanov
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  7. A. Y. Mulkidjanian
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Correspondence to A. Y. Mulkidjanian.

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The authors declare no conflict of interest in financial or any other sphere. This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

We dedicate this paper to Professor Vladimir P. Skulachev on the occasion of his 85th birthday and in appreciation of his discovery of the Sodium World.

Supplementary file 1

10541_2020_2100_MOESM1_ESM.pdf

BLAST search results; proteolipid sequence of the N-ATPase of Synechococcus sp. PCC 73109 was used as a query against all cyanobacterial sequences. The first 64 hits represent proteolipid subunits of typical N-ATPases. 53 of them have whole sets of Na+ ligands.

Supplementary file 2

10541_2020_2100_MOESM2_ESM.xlsx

Proteolipid subunits in genomes of novel cyanobacteria-related lineages Sericytochromatia, Melainabacteria, Saganbacteria, and Margulisbacteria.

Supplementary file 3

10541_2020_2100_MOESM3_ESM.pdf

BLAST search results; proteolipid sequence of the N-ATPase of Synechococcus sp. PCC 73109 was used as a query against all Oscillatoriales sequences. The first 14 hits represent typical N-ATPases. 11 of them have whole sets of Na+ ligands.

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Kozlova, M.I., Bushmakin, I.M., Belyaeva, J.D. et al. Expansion of the “Sodium World” through Evolutionary Time and Taxonomic Space. Biochemistry Moscow 85, 1518–1542 (2020). https://doi.org/10.1134/S0006297920120056

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  • DOI: https://doi.org/10.1134/S0006297920120056

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