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Why Nature Chose Potassium

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Abstract

The presence of most of the atoms involved in the building up of living cells can be explained by their intrinsic physico-chemical properties. Yet, the involvement of the alkali metal potassium cation (K+) is somewhat of a mystery for most scenarios of origins of life, as this element is less abundant than its sodium counterpart in sea water, the original medium bathing the majority of proposed sites as the cradle of life. Potassium is involved in key processes that could as well have been fulfilled by sodium (such as maintenance of an electrochemical potential or homeostatic osmolarity). However, K+ is also required for the setup of a functional translation machinery, as well as for a fairly enigmatic metabolic pathway involving the usually toxic metabolite methylglyoxal. Here we discuss the possibility that potassium has been selected because of some of its idiosyncratic properties or whether it is just the outcome of the accidental place where life was born. Specific physico-chemical properties of the K+ ion would argue in favour of positive selection in the course of life’s evolution. By contrast, the latter explanation would require that life originated on potassium-rich environments, possibly continental but yet of unknown location, making K+ presence just a frozen accident of evolution.

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References

  • Abousaab A, Lang F (2016) Up-regulation of excitatory amino acid transporters EAAT3 and EAAT4 by lithium sensitive glycogen synthase kinase GSK3ss. Cell Physiol Biochem 40:1252–1260

    CAS  PubMed  Google Scholar 

  • Adams E, Miyazaki T, Saito S, Uozumi N, Shin R (2019a) Cesium inhibits plant growth primarily through reduction of potassium influx and accumulation in Arabidopsis. Plant Cell Physiol 60:63–76

    PubMed  Google Scholar 

  • Adams E, Miyazaki T, Shin R (2019b) Contribution of KUPs to potassium and cesium accumulation appears complementary in Arabidopsis. Plant Signal Behav 14:1554468

    PubMed  Google Scholar 

  • Ali MK, Li X, Tang Q, Liu X, Chen F, Xiao J, Ali M, Chou SH, He J (2017) Regulation of inducible potassium transporter KdpFABC by the KdpD/KdpE two-component system in Mycobacterium smegmatis. Front Microbiol 8:570

    PubMed  PubMed Central  Google Scholar 

  • Allaman I, Belanger M, Magistretti PJ (2015) Methylglyoxal, the dark side of glycolysis. Front Neurosci 9:23

    PubMed  PubMed Central  Google Scholar 

  • Altendorf K, Siebers A, Epstein W (1992) The KDP ATPase of Escherichia coli. Ann N Y Acad Sci 671:228–243

    CAS  PubMed  Google Scholar 

  • Anand B, Surana P, Prakash B (2010) Deciphering the catalytic machinery in 30S ribosome assembly GTPase YqeH. PLoS ONE 5:e9944

    PubMed  PubMed Central  Google Scholar 

  • Ash MR, Maher MJ, Guss JM, Jormakka M (2011) The structure of an N11A mutant of the G-protein domain of FeoB. Acta Crystallogr, Sect F: Struct Biol Cryst Commun 67:1511–1515

    CAS  Google Scholar 

  • Auffinger P, Bielecki L, Westhof E (2004) Symmetric K+ and Mg2+ ion-binding sites in the 5S rRNA loop E inferred from molecular dynamics simulations. J Mol Biol 335:555–571

    CAS  PubMed  Google Scholar 

  • Auffinger P, D’Ascenzo L, Ennifar E (2016) Sodium and potassium interactions with nucleic acids. Met Ions Life Sci 16:167–201

    CAS  PubMed  Google Scholar 

  • Bada JL, Bigham C, Miller SL (1994) Impact melting of frozen oceans on the early Earth: implications for the origin of life. Proc Natl Acad Sci USA 91:1248–1250

    CAS  PubMed  Google Scholar 

  • Ball P (2017) Water is an active matrix of life for cell and molecular biology. Proc Natl Acad Sci USA 114:13327–13335

    CAS  PubMed  Google Scholar 

  • Ball P, Hallsworth JE (2015) Water structure and chaotropicity: their uses, abuses and biological implications. Phys Chem Chem Phys 17:8297–8305

    CAS  PubMed  Google Scholar 

  • Barreto L, Canadell D, Valverde-Saubi D, Casamayor A, Arino J (2012) The short-term response of yeast to potassium starvation. Environ Microbiol 14:3026–3042

    CAS  PubMed  Google Scholar 

  • Biggin PC, Smith GR, Shrivastava I, Choe S, Sansom MS (2001) Potassium and sodium ions in a potassium channel studied by molecular dynamics simulations. Biochim Biophys Acta 1510:1–9

    CAS  PubMed  Google Scholar 

  • Blasic JR, Worcester DL, Gawrisch K, Gurnev P, Mihailescu M (2015) Pore hydration states of KcsA potassium channels in membranes. J Biol Chem 290:26765–26775

    CAS  PubMed  PubMed Central  Google Scholar 

  • Boel G, Danot O, de Lorenzo V, Danchin A (2019) Omnipresent Maxwell’s demons orchestrate information management in living cells. Microb Biotechnol 12:210–242

    PubMed  PubMed Central  Google Scholar 

  • Brown BM, Nguyen HM, Wulff H (2019) Recent advances in our understanding of the structure and function of more unusual cation channels. F1000Res 1:8

    Google Scholar 

  • Caetano-Anolles G, Kim KM, Caetano-Anolles D (2012) The phylogenomic roots of modern biochemistry: origins of proteins, cofactors and protein biosynthesis. J Mol Evol 74:1–34

    CAS  PubMed  Google Scholar 

  • Capera J, Serrano-Novillo C, Navarro-Perez M, Cassinelli S, Felipe A (2019) The potassium channel odyssey: mechanisms of traffic and membrane arrangement. Int J Mol Sci 20:734

    CAS  PubMed Central  Google Scholar 

  • Cases I, Perez-Martin J, de Lorenzo V (1999) The IIANtr (PtsN) protein of Pseudomonas putida mediates the C source inhibition of the σ54-dependent Pu promoter of the TOL plasmid. J Biol Chem 274:15562–15568

    CAS  PubMed  Google Scholar 

  • Cases I, Lopez JA, Albar JP, De Lorenzo V (2001) Evidence of multiple regulatory functions for the PtsN (IIA(Ntr)) protein of Pseudomonas putida. J Bacteriol 183:1032–1037

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cavalazzi B, Barbieri R, Gomez F, Capaccioni B, Olsson-Francis K, Pondrelli M, Rossi AP, Hickman-Lewis K, Agangi A, Gasparotto G, Glamoclija M, Ori GG, Rodriguez N, Hagos M (2019) The Dallol geothermal area, northern Afar (Ethiopia)-an exceptional planetary field analog on Earth. Astrobiology 19:553–578

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chandrangsu P, Loi VV, Antelmann H, Helmann JD (2018) The role of bacillithiol in Gram-positive Firmicutes. Antioxid Redox Signal 28:445–462

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chang TM, Cooper RJ, Williams ER (2013) Locating protonated amines in clathrates. J Am Chem Soc 135:14821–14830

    CAS  PubMed  Google Scholar 

  • Chen G, Kennedy SD, Qiao J, Krugh TR, Turner DH (2006) An alternating sheared AA pair and elements of stability for a single sheared purine-purine pair flanked by sheared GA pairs in RNA. Biochemistry 45:6889–6903

    CAS  PubMed  PubMed Central  Google Scholar 

  • Collins KD (1997) Charge density-dependent strength of hydration and biological structure. Biophys J 72:65–76

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cooper RJ, Chang TM, Williams ER (2013) Hydrated alkali metal ions: spectroscopic evidence for clathrates. J Phys Chem A 117:6571–6579

    CAS  PubMed  Google Scholar 

  • Corrigan RM, Bellows LE, Wood A, Grundling A (2016) ppGpp negatively impacts ribosome assembly affecting growth and antimicrobial tolerance in Gram-positive bacteria. Proc Natl Acad Sci USA 113:E1710–E1719

    CAS  PubMed  Google Scholar 

  • Danchin A (1989) Homeotopic transformation and the origin of translation. Prog Biophys Mol Biol 54:81–86

    CAS  PubMed  Google Scholar 

  • Danchin A (2017a) Coping with inevitable accidents in metabolism. Microb Biotechnol 10:57–72

    PubMed  Google Scholar 

  • Danchin A (2017b) From chemical metabolism to life: the origin of the genetic coding process. Beilstein J Org Chem 13:1119–1135

    CAS  PubMed  PubMed Central  Google Scholar 

  • Danchin A, Fang G (2016) Unknown unknowns: essential genes in quest for function. Microb Biotechnol 9:530–540

    PubMed  PubMed Central  Google Scholar 

  • Deamer D (2017) Conjecture and hypothesis: the importance of reality checks. Beilstein J Org Chem 13:620–624

    CAS  PubMed  PubMed Central  Google Scholar 

  • Delemotte L (2018) Opening leads to closing: allosteric crosstalk between the activation and inactivation gates in KcsA. J Gen Physiol 150:1356–1359

    CAS  PubMed  PubMed Central  Google Scholar 

  • Deuschle M, Limbrunner S, Rother D, Wahler S, Chavarria M, de Lorenzo V, Kremling A, Pfluger-Grau K (2015) Interplay of the PtsN (EIIANtr) protein of Pseudomonas putida with its target sensor kinase KdpD. Environ Microbiol Rep 7:899–907

    CAS  PubMed  Google Scholar 

  • Deutscher J, Ake FM, Derkaoui M, Zebre AC, Cao TN, Bouraoui H, Kentache T, Mokhtari A, Milohanic E, Joyet P (2014) The bacterial phosphoenolpyruvate:carbohydrate phosphotransferase system: regulation by protein phosphorylation and phosphorylation-dependent protein-protein interactions. Microbiol Mol Biol Rev 78:231–256

    PubMed  PubMed Central  Google Scholar 

  • Dever TE, Ivanov IP (2018) Roles of polyamines in translation. J Biol Chem 293:18719–18729

    CAS  PubMed  Google Scholar 

  • Dibrova DV, Galperin MY, Koonin EV, Mulkidjanian AY (2015) Ancient systems of sodium/potassium homeostasis as predecessors of membrane bioenergetics. Biochemistry 80:495–516

    CAS  PubMed  Google Scholar 

  • Dickmanns A, Zschiedrich CP, Arens J, Parfentev I, Gundlach J, Hofele R, Neumann P, Urlaub H, Gorke B, Ficner R, Stulke J (2018) Structural basis for the regulatory interaction of the methylglyoxal synthase MgsA with the carbon flux regulator Crh in Bacillus subtilis. J Biol Chem 293:5781–5792

    CAS  PubMed  PubMed Central  Google Scholar 

  • Diskowski M, Mikusevic V, Stock C, Hanelt I (2015) Functional diversity of the superfamily of K+ transporters to meet various requirements. Biol Chem 396:1003–1014

    CAS  PubMed  Google Scholar 

  • Douglas KT, Bunni MA, Baindur SR (1990) Thallium in biochemistry. Int J Biochem 22:429–438

    CAS  PubMed  Google Scholar 

  • Dubina MV, Vyazmin SY, Boitsov VM, Nikolaev EN, Popov IA, Kononikhin AS, Eliseev IE, Natochin YV (2013) Potassium ions are more effective than sodium ions in salt induced peptide formation. Orig Life Evol Biosph 43:109–117

    CAS  PubMed  PubMed Central  Google Scholar 

  • Epstein E (1973) Mechanisms of ion transport through plant cell membranes. Int Rev Cytol 34:123–168

    CAS  Google Scholar 

  • Epstein W (2016) The KdpD sensor kinase of Escherichia coli responds to several distinct signals to turn on expression of the Kdp transport system. J Bacteriol 198:212–220

    CAS  PubMed  Google Scholar 

  • Erickson AI, Sarsam RD, Fisher AJ (2015) Crystal structures of Mycobacterium tuberculosis CysQ, with substrate and products bound. Biochemistry 54:6830–6841

    CAS  PubMed  Google Scholar 

  • Faisal Tarique K, Arif Abdul Rehman S, Gourinath S (2014) Structural elucidation of a dual-activity PAP phosphatase-1 from Entamoeba histolytica capable of hydrolysing both 3′-phosphoadenosine 5′-phosphate and inositol 1,4-bisphosphate. Acta Crystallogr D Biol Crystallogr 70:2019–2031

    CAS  PubMed  Google Scholar 

  • Fan Y, Gaffney BL, Jones RA (2005) RNA GG x UU motif binds K+ but not Mg2+. J Am Chem Soc 127:17588–17589

    CAS  PubMed  Google Scholar 

  • Ferguson GP, Munro AW, Douglas RM, McLaggan D, Booth IR (1993) Activation of potassium channels during metabolite detoxification in Escherichia coli. Mol Microbiol 9:1297–1303

    CAS  PubMed  Google Scholar 

  • Ferguson GP, Totemeyer S, MacLean MJ, Booth IR (1998) Methylglyoxal production in bacteria: suicide or survival? Arch Microbiol 170:209–218

    CAS  PubMed  Google Scholar 

  • Fislage M, Wauters L, Versees W (2016) Invited review: MnmE, a GTPase that drives a complex tRNA modification reaction. Biopolymers 105:568–579

    CAS  PubMed  Google Scholar 

  • Flaherty KM, DeLuca-Flaherty C, McKay DB (1990) Three-dimensional structure of the ATPase fragment of a 70 K heat-shock cognate protein. Nature 346:623–628

    CAS  PubMed  Google Scholar 

  • Francis BR (2013) Evolution of the genetic code by incorporation of amino acids that improved or changed protein function. J Mol Evol 77:134–158

    CAS  PubMed  Google Scholar 

  • Francis BR (2015) The hypothesis that the genetic code originated in coupled synthesis of proteins and the evolutionary predecessors of nucleic acids in primitive cells. Life 5:467–505

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fritz SE, Haque N, Hogg JR (2018) Highly efficient in vitro translation of authentic affinity-purified messenger ribonucleoprotein complexes. RNA 24:982–989

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garza-Ramos G, Mujica-Jimenez C, Munoz-Clares RA (2013) Potassium and ionic strength effects on the conformational and thermal stability of two aldehyde dehydrogenases reveal structural and functional roles of K+-binding sites. PLoS ONE 8:e54899

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gebala M, Johnson SL, Narlikar GJ, Herschlag D (2019) Ion counting demonstrates a high electrostatic field generated by the nucleosome. Elife 8:e44993

    PubMed  PubMed Central  Google Scholar 

  • Gehring PJ, Hammond PB (1967) The interrelationship between thallium and potassium in animals. J Pharmacol Exp Ther 155:187–201

    CAS  PubMed  Google Scholar 

  • Gohara DW, Di Cera E (2016) Molecular mechanisms of enzyme activation by monovalent cations. J Biol Chem 291:20840–20848

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goncalves CA, Rodrigues L, Bobermin LD, Zanotto C, Vizuete A, Quincozes-Santos A, Souza DO, Leite MC (2019) Glycolysis-derived compounds from astrocytes that modulate synaptic communication. Front Neurosci 12:1035

    PubMed  PubMed Central  Google Scholar 

  • Greie JC, Altendorf K (2007) The K + -translocating KdpFABC complex from Escherichia coli: a P-type ATPase with unique features. J Bioenerg Biomembr 39:397–402

    CAS  PubMed  Google Scholar 

  • Gruber R, Horovitz A (2016) Allosteric mechanisms in chaperonin machines. Chem Rev 116:6588–6606

    CAS  PubMed  Google Scholar 

  • Gumz ML, Rabinowitz L, Wingo CS (2015) An integrated view of potassium homeostasis. N Engl J Med 373:1787–1788

    PubMed  Google Scholar 

  • Gundlach J, Herzberg C, Hertel D, Thurmer A, Daniel R, Link H, Stulke J (2017) Adaptation of Bacillus subtilis to life at extreme potassium limitation. MBio 8:e00861-17

    PubMed  PubMed Central  Google Scholar 

  • Gundlach J, Commichau FM, Stulke J (2018) Perspective of ions and messengers: an intricate link between potassium, glutamate, and cyclic di-AMP. Curr Genet 64:191–195

    CAS  PubMed  Google Scholar 

  • Gundlach J, Kruger L, Herzberg C, Turdiev A, Poehlein A, Tascon I, Weiss M, Hertel D, Daniel R, Hanelt I, Lee VT, Stulke J (2019) Sustained sensing in potassium homeostasis: cyclic di-AMP controls potassium uptake by KimA at the levels of expression and activity. J Biol Chem 294:9605–9614

    CAS  PubMed  Google Scholar 

  • Hagelueken G, Hoffmann J, Schubert E, Duthie FG, Florin N, Konrad L, Imhof D, Behrmann E, Morgner N, Schiemann O (2016) Studies on the X-ray and solution structure of FeoB from Escherichia coli BL21. Biophys J 110:2642–2650

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hagemann M (2011) Molecular biology of cyanobacterial salt acclimation. FEMS Microbiol Rev 35:87–123

    CAS  PubMed  Google Scholar 

  • Hamann K, Zimmann P, Altendorf K (2008) Reduction of turgor is not the stimulus for the sensor kinase KdpD of Escherichia coli. J Bacteriol 190:2360–2367

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hicks DB, Liu J, Fujisawa M, Krulwich TA (2010) F1F0-ATP synthases of alkaliphilic bacteria: lessons from their adaptations. Biochim Biophys Acta 1797:1362–1377

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ho CH, Tsay YF (2010) Nitrate, ammonium, and potassium sensing and signaling. Curr Opin Plant Biol 13:604–610

    CAS  PubMed  Google Scholar 

  • Hoque TS, Okuma E, Uraji M, Furuichi T, Sasaki T, Hoque MA, Nakamura Y, Murata Y (2012) Inhibitory effects of methylglyoxal on light-induced stomatal opening and inward K+ channel activity in Arabidopsis. Biosci Biotechnol Biochem 76:617–619

    CAS  PubMed  Google Scholar 

  • Hoque TS, Hossain MA, Mostofa MG, Burritt DJ, Fujita M, Tran LS (2016) Methylglyoxal: an emerging signaling molecule in plant abiotic stress responses and tolerance. Front Plant Sci 7:1341

    PubMed  PubMed Central  Google Scholar 

  • Hunt TS (1891) Potassium salts in sea-water. Nature 43:463–464

    Google Scholar 

  • Iacomino G, Picariello G, D’Agostino L (2012) DNA and nuclear aggregates of polyamines. Biochim Biophys Acta 1823:1745–1755

    CAS  PubMed  Google Scholar 

  • Iliopoulos I, Ananiadou S, Danchin A, Ioannidis JP, Katsikis PD, Ouzounis CA, Promponas VJ (2019) Hypothesis, analysis and synthesis, it’s all Greek to me. Elife. https://doi.org/10.7554/eLife.43514

    Article  PubMed  PubMed Central  Google Scholar 

  • Jakubowski H (2017) Homocysteine editing, thioester chemistry, coenzyme A, and the origin of coded peptide synthesis. Life 7:6

    PubMed Central  Google Scholar 

  • Jia B, Pu ZJ, Tang K, Jia X, Kim KH, Liu X, Jeon CO (2018) Catalytic, computational, and evolutionary analysis of the d-lactate dehydrogenases responsible for d-lactic acid production in lactic acid bacteria. J Agric Food Chem 66:8371–8381

    PubMed  Google Scholar 

  • Jiang T, Guo X, Yan J, Zhang Y, Wang Y, Zhang M, Sheng B, Ma C, Xu P, Gao C (2017) A bacterial multidomain NAD-independent d-lactate dehydrogenase utilizes flavin adenine dinucleotide and Fe-S clusters as cofactors and quinone as an electron acceptor for d-lactate oxidization. J Bacteriol 199:e00342-17

    PubMed  PubMed Central  Google Scholar 

  • Kashket ER (1979) Active transport of thallous ions by Streptococcus lactis. J Biol Chem 254:8129–8131

    CAS  PubMed  Google Scholar 

  • Kemnic TR, Coleman M (2019) Thallium Toxicity StatPearls review books (Internet). StatPearls Publishing, Treasure Island

    Google Scholar 

  • Klumpp S, Zhang Z, Hwa T (2009) Growth rate-dependent global effects on gene expression in bacteria. Cell 139:1366–1375

    PubMed  PubMed Central  Google Scholar 

  • Krymkiewicz N (1973) Reactions of methylglyoxal with nucleic acids. FEBS Lett 29:51–54

    CAS  PubMed  Google Scholar 

  • Kuhle B, Ficner R (2014) A monovalent cation acts as structural and catalytic cofactor in translational GTPases. EMBO J 33:2547–2563

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar A, Satpati P (2018) Principle of K+/Na+ selectivity in the active site of group II intron at various stages of self-splicing pathway. J Mol Gr Model 84:1–9

    CAS  Google Scholar 

  • Kwak JM, Murata Y, Baizabal-Aguirre VM, Merrill J, Wang M, Kemper A, Hawke SD, Tallman G, Schroeder JI (2001) Dominant negative guard cell K + channel mutants reduce inward-rectifying K+ currents and light-induced stomatal opening in Arabidopsis. Plant Physiol 127:473–485

    CAS  PubMed  PubMed Central  Google Scholar 

  • Landauer R (1961) Irreversibility and heat generation in the computing process. IBM J Res Dev 3:184–191

    Google Scholar 

  • Lartigue C, Glass JI, Alperovich N, Pieper R, Parmar PP, Hutchison CA 3rd, Smith HO, Venter JC (2007) Genome transplantation in bacteria: changing one species to another. Science 317:632–638

    CAS  PubMed  Google Scholar 

  • Laskowski M, Augustynek B, Kulawiak B, Koprowski P, Bednarczyk P, Jarmuszkiewicz W, Szewczyk A (2016) What do we not know about mitochondrial potassium channels? Biochim Biophys Acta 1857:1247–1257

    CAS  PubMed  Google Scholar 

  • Lee CR, Cho SH, Yoon MJ, Peterkofsky A, Seok YJ (2007) Escherichia coli enzyme IIANtr regulates the K+ transporter TrkA. Proc Natl Acad Sci USA 104:4124–4129

    CAS  PubMed  Google Scholar 

  • Lee J, Park YH, Kim YR, Seok YJ, Lee CR (2015) Dephosphorylated NPr is involved in an envelope stress response of Escherichia coli. Microbiology 161:1113–1123

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leonarski F, D’Ascenzo L, Auffinger P (2019) Nucleobase carbonyl groups are poor Mg(2 +) inner-sphere binders but excellent monovalent ion binders-a critical PDB survey. RNA 25:173–192

    CAS  PubMed  PubMed Central  Google Scholar 

  • Levy M, Miller SL, Brinton K, Bada JL (2000) Prebiotic synthesis of adenine and amino acids under Europa-like conditions. Icarus 145:609–613

    CAS  PubMed  Google Scholar 

  • Li Z, Pan Q, Xiao Y, Fang X, Shi R, Fu C, Danchin A, You C (2019) Deciphering global gene expression and regulation strategy in Escherichia coli during carbon limitation. Microb Biotechnol 12:360–376

    CAS  PubMed  Google Scholar 

  • Lightfoot HL, Hall J (2014) Endogenous polyamine function–the RNA perspective. Nucleic Acids Res 42:11275–11290

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lin JJ, Carey M (2012) In vitro transcription and immobilized template analysis of preinitiation complexes. Curr Protoc Mol Biol Chapter 97:12–14

    Google Scholar 

  • Linster CL, Van Schaftingen E, Hanson AD (2013) Metabolite damage and its repair or pre-emption. Nat Chem Biol 9:72–80

    CAS  PubMed  Google Scholar 

  • Lipmann F (1971) Attempts to map a process evolution of peptide biosynthesis. Science 173:875–884

    CAS  PubMed  Google Scholar 

  • Liu YB, Chen C, Chaudhry MT, Si MR, Zhang L, Wang Y, Shen XH (2014) Enhancing Corynebacterium glutamicum robustness by over-expressing a gene, mshA, for mycothiol glycosyltransferase. Biotechnol Lett 36:1453–1459

    CAS  PubMed  Google Scholar 

  • Locascio A, Andres-Colas N, Mulet JM, Yenush L (2019) Saccharomyces cerevisiae as a tool to investigate plant potassium and sodium transporters. Int J Mol Sci 20:2133

    PubMed Central  Google Scholar 

  • Lopez-Coronado JM, Belles JM, Lesage F, Serrano R, Rodriguez PL (1999) A novel mammalian lithium-sensitive enzyme with a dual enzymatic activity, 3′-phosphoadenosine 5′-phosphate phosphatase and inositol-polyphosphate 1-phosphatase. J Biol Chem 274:16034–16039

    CAS  PubMed  Google Scholar 

  • Lu M (2019) Structure and mechanism of the divalent anion/Na+ symporter. Int J Mol Sci 20:440

    PubMed Central  Google Scholar 

  • Luttmann D, Gopel Y, Gorke B (2012) The phosphotransferase protein EIIANtr modulates the phosphate starvation response through interaction with histidine kinase PhoR in Escherichia coli. Mol Microbiol 86:96–110

    PubMed  Google Scholar 

  • Luttmann D, Gopel Y, Gorke B (2015) Cross-talk between the canonical and the nitrogen-related phosphotransferase systems modulates synthesis of the KdpFABC potassium transporter in Escherichia coli. J Mol Microbiol Biotechnol 25:168–177

    PubMed  Google Scholar 

  • Manikas RG, Thomson E, Thoms M, Hurt E (2016) The K+-dependent GTPase Nug1 is implicated in the association of the helicase Dbp10 to the immature peptidyl transferase centre during ribosome maturation. Nucleic Acids Res 44:1800–1812

    PubMed  PubMed Central  Google Scholar 

  • Marcus Y (2014) Concentration dependence of ionic hydration numbers. J Phys Chem B 118:10471–10476

    CAS  PubMed  Google Scholar 

  • Markovich D (2012) Sodium-sulfate/carboxylate cotransporters (SLC13). Curr Top Membr 70:239–256

    CAS  PubMed  Google Scholar 

  • Maurer S (2017) The impact of salts on single chain amphiphile membranes and implications for the location of the origin of life. Life 7:44

    PubMed Central  Google Scholar 

  • Mechold U, Ogryzko V, Ngo S, Danchin A (2006) Oligoribonuclease is a common downstream target of lithium-induced pAp accumulation in Escherichia coli and human cells. Nucleic Acids Res 34:2364–2373

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mechold U, Fang G, Ngo S, Ogryzko V, Danchin A (2007) YtqI from Bacillus subtilis has both oligoribonuclease and pAp-phosphatase activity. Nucleic Acids Res 35:4552–4561

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meisel JD, Kim DH (2016) Inhibition of lithium-sensitive phosphatase BPNT-1 causes selective neuronal dysfunction in C. elegans. Curr Biol 26:1922–1928

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory Edition, Cold Spring Harbor

    Google Scholar 

  • Morgan JLW, Evans EGB, Zagotta WN (2019) Functional characterization and optimization of a bacterial cyclic nucleotide-gated channel. J Biol Chem 294:7503–7515

    CAS  PubMed  Google Scholar 

  • Mork-Morkenstein M, Heermann R, Gopel Y, Jung K, Gorke B (2017) Non-canonical activation of histidine kinase KdpD by phosphotransferase protein PtsN through interaction with the transmitter domain. Mol Microbiol 106:54–73

    PubMed  Google Scholar 

  • Mounce BC, Olsen ME, Vignuzzi M, Connor JH (2017) Polyamines and their role in virus infection. Microbiol Mol Biol Rev 81:e00029-17

    PubMed  PubMed Central  Google Scholar 

  • Mulkidjanian AY, Bychkov AY, Dibrova DV, Galperin MY, Koonin EV (2012) Origin of first cells at terrestrial, anoxic geothermal fields. Proc Natl Acad Sci USA 109:E821–E830

    CAS  PubMed  Google Scholar 

  • Muller M, Hopfner KP, Witte G (2015) c-di-AMP recognition by Staphylococcus aureus PstA. FEBS Lett 589:45–51

    PubMed  Google Scholar 

  • Muriel-Millan LF, Moreno S, Gallegos-Monterrosa R, Espin G (2017) Unphosphorylated EIIANtr induces ClpAP-mediated degradation of RpoS in Azotobacter vinelandii. Mol Microbiol 104:197–211

    CAS  PubMed  Google Scholar 

  • Natochin Y, Felitsyn S, Klimova E, Shakhmatova E (2012) K+/Na+ in the animal extracellular fluid at weathering of granitoids and problem of the origin of life. J Evolut Biochem Physiol 48:479–488

    CAS  Google Scholar 

  • Negoda A, Negoda E, Xian M, Reusch RN (2009) Role of polyphosphate in regulation of the Streptomyces lividans KcsA channel. Biochim Biophys Acta 1788:608–614

    CAS  PubMed  Google Scholar 

  • Negrerie M (2019) Iron transitions during activation of allosteric heme proteins in cell signaling. Metallomics 11:868–893

    CAS  PubMed  Google Scholar 

  • Nowak T, Suelter C (1981) Pyruvate kinase: activation by and catalytic role of the monovalent and divalent cations. Mol Cell Biochem 35:65–75

    CAS  PubMed  Google Scholar 

  • Oh YT, Kim J, Youn JH (2013) Role of pituitary in K+ homeostasis: impaired renal responses to altered K + intake in hypophysectomized rats. Am J Physiol Regul Integr Comp Physiol 304:R1166–R1174

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ohnishi J, Flugge UI, Heldt HW, Kanai R (1990) Involvement of Na in active uptake of pyruvate in mesophyll chloroplasts of some C4 plants: Na/pyruvate cotransport. Plant Physiol 94:950–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ozyamak E, Black SS, Walker CA, Maclean MJ, Bartlett W, Miller S, Booth IR (2010) The critical role of S-lactoylglutathione formation during methylglyoxal detoxification in Escherichia coli. Mol Microbiol 78:1577–1590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Page MJ, Di Cera E (2006) Role of Na+ and K+ in enzyme function. Physiol Rev 86:1049–1092

    CAS  PubMed  Google Scholar 

  • Papa S, Capitanio G, Papa F (2018) The mechanism of coupling between oxido-reduction and proton translocation in respiratory chain enzymes. Biol Rev Camb Philos Soc 93:322–349

    PubMed  Google Scholar 

  • Parthasarathy L, Vadnal RE, Parthasarathy R, Devi CS (1994) Biochemical and molecular properties of lithium-sensitive myo-inositol monophosphatase. Life Sci 54:1127–1142

    CAS  PubMed  Google Scholar 

  • Partono S, Lewin AS (1991) The rate and specificity of a group I ribozyme are inversely affected by choice of monovalent salt. Nucleic Acids Res 19:605–609

    CAS  PubMed  PubMed Central  Google Scholar 

  • Patching SG (2018) Recent developments in nucleobase cation symporter-1 (NCS1) family transport proteins from bacteria, archaea, fungi and plants. J Biosci 43:797–815

    CAS  PubMed  Google Scholar 

  • Patel S, Yenush L, Rodriguez PL, Serrano R, Blundell TL (2002) Crystal structure of an enzyme displaying both inositol-polyphosphate-1-phosphatase and 3′-phosphoadenosine-5′-phosphate phosphatase activities: a novel target of lithium therapy. J Mol Biol 315:677–685

    CAS  PubMed  Google Scholar 

  • Perez-Arellano I, Spinola-Amilibia M, Bravo J (2013) Human Drg1 is a potassium-dependent GTPase enhanced by Lerepo4. FEBS J 280:3647–3657

    CAS  PubMed  Google Scholar 

  • Pinhassi J, DeLong EF, Beja O, Gonzalez JM, Pedros-Alió C (2016) Marine bacterial and archaeal ion-pumping rhodopsins: genetic diversity, physiology, and ecology. Microbiol Mol Biol Rev 80:929–954

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pivovarov AS, Calahorro F, Walker RJ (2018) Na+/K+-pump and neurotransmitter membrane receptors. Invert Neurosci 19:1

    PubMed  PubMed Central  Google Scholar 

  • Posson DJ, Thompson AN, McCoy JG, Nimigean CM (2013) Molecular interactions involved in proton-dependent gating in KcsA potassium channels. J Gen Physiol 142:613–624

    CAS  PubMed  PubMed Central  Google Scholar 

  • Powell BS, Court DL, Inada T, Nakamura Y, Michotey V, Cui X, Reizer A, Saier MH Jr, Reizer J (1995) Novel proteins of the phosphotransferase system encoded within the rpoN operon of Escherichia coli. Enzyme IIANtr affects growth on organic nitrogen and the conditional lethality of an erats mutant. J Biol Chem 270:4822–4839

    CAS  PubMed  Google Scholar 

  • Prado S, Villarroya M, Medina M, Armengod ME (2013) The tRNA-modifying function of MnmE is controlled by post-hydrolysis steps of its GTPase cycle. Nucleic Acids Res 41:6190–6208

    CAS  PubMed  PubMed Central  Google Scholar 

  • Prochaska JX, Howk JC, Wolfe AM (2003) The elemental abundance pattern in a galaxy at z = 2.626. Nature 423:57–59

    CAS  PubMed  Google Scholar 

  • Rafay A, Majumdar S, Prakash B (2012) Exploring potassium-dependent GTP hydrolysis in TEES family GTPases. FEBS Open Bio 2:173–177

    PubMed  PubMed Central  Google Scholar 

  • Randich AM, Cuello LG, Wanderling SS, Perozo E (2014) Biochemical and structural analysis of the hyperpolarization-activated K+ channel MVP. Biochemistry 53:1627–1636

    CAS  PubMed  PubMed Central  Google Scholar 

  • Razi A, Davis JH, Hao Y, Jahagirdar D, Thurlow B, Basu K, Jain N, Gomez-Blanco J, Britton RA, Vargas J, Guarne A, Woodson SA, Williamson JR, Ortega J (2019) Role of Era in assembly and homeostasis of the ribosomal small subunit. Nucleic Acids Res. https://doi.org/10.1101/525360

    Article  PubMed  PubMed Central  Google Scholar 

  • Renart ML, Montoya E, Giudici AM, Poveda JA, Fernandez AM, Morales A, Gonzalez-Ros JM (2017) Selective exclusion and selective binding both contribute to ion selectivity in KcsA, a model potassium channel. J Biol Chem 292:15552–15560

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rhoads DB, Waters FB, Epstein W (1976) Cation transport in Escherichia coli. VIII. Potassium transport mutants. J Gen Physiol 67:325–341

    CAS  PubMed  Google Scholar 

  • Rimmer PB, Shorttle O (2019) Origin of life’s building blocks in carbon- and nitrogen-rich surface hydrothermal vents. Life 9:12

    PubMed Central  Google Scholar 

  • Rocha R, Teixeira-Duarte CM, Jorge JMP, Morais-Cabral JH (2019) Characterization of the molecular properties of KtrC, a second RCK domain that regulates a Ktr channel in Bacillus subtilis. J Struct Biol 205:34–43

    CAS  PubMed  Google Scholar 

  • Roussel G, Lindner E, White SH (2019) Stabilization of SecA ATPase by the primary cytoplasmic salt of Escherichia coli. Protein Sci 28:984–989

    CAS  PubMed  Google Scholar 

  • Roux B (2017) Ion channels and ion selectivity. Essays Biochem 61:201–209

    PubMed  PubMed Central  Google Scholar 

  • Rozov A, Khusainov I, El Omari K, Duman R, Mykhaylyk V, Yusupov M, Westhof E, Wagner A, Yusupova G (2019) Importance of potassium ions for ribosome structure and function revealed by long-wavelength X-ray diffraction. Nat Commun 10:2519

    PubMed  PubMed Central  Google Scholar 

  • Rubey WW (1951) Geologic history of sea water: an attempt to state the problem. GSA Bull 62:1111–1148

    CAS  Google Scholar 

  • Sato Y, Nanatani K, Hamamoto S, Shimizu M, Takahashi M, Tabuchi-Kobayashi M, Mizutani A, Schroeder JI, Souma S, Uozumi N (2014) Defining membrane spanning domains and crucial membrane-localized acidic amino acid residues for K+ transport of a Kup/HAK/KT-type Escherichia coli potassium transporter. J Biochem 155:315–323

    CAS  PubMed  Google Scholar 

  • Saxena SC, Salvi P, Kaur H, Verma P, Petla BP, Rao V, Kamble N, Majee M (2013) Differentially expressed myo-inositol monophosphatase gene (CaIMP) in chickpea (Cicer arietinum L.) encodes a lithium-sensitive phosphatase enzyme with broad substrate specificity and improves seed germination and seedling growth under abiotic stresses. J Exp Bot 64:5623–5639

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schramke H, Laermann V, Tegetmeyer HE, Brachmann A, Jung K, Altendorf K (2017) Revisiting regulation of potassium homeostasis in Escherichia coli: the connection to phosphate limitation. MicrobiologyOpen 6:e00438

    PubMed Central  Google Scholar 

  • Schulz S, Iglesias-Cans M, Krah A, Yildiz O, Leone V, Matthies D, Cook GM, Faraldo-Gomez JD, Meier T (2013) A new type of Na+-driven ATP synthase membrane rotor with a two-carboxylate ion-coupling motif. PLoS Biol 11:e1001596

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sekowska A, Kung HF, Danchin A (2000) Sulfur metabolism in Escherichia coli and related bacteria: facts and fiction. J Mol Microbiol Biotechnol 2:145–177

    CAS  PubMed  Google Scholar 

  • Shabala S (2017) Signalling by potassium: another second messenger to add to the list? J Exp Bot 68:4003–4007

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shalaeva DN, Cherepanov DA, Galperin MY, Golovin AV, Mulkidjanian AY (2018) Evolution of cation binding in the active sites of P-loop nucleoside triphosphatases in relation to the basic catalytic mechanism. Elife 7:e37373

    PubMed  PubMed Central  Google Scholar 

  • Shannon R (1976) Revised effective ionic radii and systematic studies of interatomic distances in halides and chalcogenides. Acta Crystallogr A 32:751–767

    Google Scholar 

  • Sheehan W (1976) A periodic chart. Chemistry 49:17–18

    CAS  Google Scholar 

  • Shiman R, Draper DE (2000) Stabilization of RNA tertiary structure by monovalent cations. J Mol Biol 302:79–91

    CAS  PubMed  Google Scholar 

  • Shin SM, Song SH, Lee JW, Kwak MK, Kang SO (2017) Methylglyoxal synthase regulates cell elongation via alterations of cellular methylglyoxal and spermidine content in Bacillus subtilis. Int J Biochem Cell Biol 91:14–28

    CAS  PubMed  Google Scholar 

  • Shin M, Mey AR, Payne SM (2019) Vibrio cholerae FeoB contains a dual nucleotide-specific NTPase domain essential for ferrous iron uptake. Proc Natl Acad Sci USA 116:4599–4604

    CAS  PubMed  Google Scholar 

  • Singh G, Verma R, Wagle S, Gadre SR (2017) Explicit hydration of ammonium ion by correlated methods employing molecular tailoring approach. Mol Phys 115:2708–2720

    CAS  Google Scholar 

  • Smathers CM, Robart AR (2019) The mechanism of splicing as told by group II introns: ancestors of the spliceosome. Biochim Biophys Acta Gene Regul Mech (in press)

  • Spiegelberg BD, De la Cruz J, Law TH, York JD (2005) Alteration of lithium pharmacology through manipulation of phosphoadenosine phosphate metabolism. J Biol Chem 280:5400–5405

    CAS  PubMed  Google Scholar 

  • Stahley MR, Adams PL, Wang J, Strobel SA (2007) Structural metals in the group I intron: a ribozyme with a multiple metal ion core. J Mol Biol 372:89–102

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stock C, Hielkema L, Tascon I, Wunnicke D, Oostergetel GT, Azkargorta M, Paulino C, Hanelt I (2018) Cryo-EM structures of KdpFABC suggest a K+ transport mechanism via two inter-subunit half-channels. Nat Commun 9:4971

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun J, Jeffryes JG, Henry CS, Bruner SD, Hanson AD (2017) Metabolite damage and repair in metabolic engineering design. Metab Eng 44:150–159

    CAS  PubMed  Google Scholar 

  • Svrckova M, Zatloukalova M, Dvorakova P, Coufalova D, Novak D, Hernychova L, Vacek J (2017) Na+/K+-ATPase interaction with methylglyoxal as reactive metabolic side product. Free Radic Biol Med 108:146–154

    CAS  PubMed  Google Scholar 

  • Szollosi A, Vieira-Pires RS, Teixeira-Duarte CM, Rocha R, Morais-Cabral JH (2016) Dissecting the molecular mechanism of nucleotide-dependent activation of the KtrAB K+ transporter. PLoS Biol 14:e1002356

    PubMed  PubMed Central  Google Scholar 

  • Tansel B (2012) Significance of thermodynamic and physical characteristics on permeation of ions during membrane separation: hydrated radius, hydration free energy and viscous effects. Sep Purif Technol 86:119–126

    CAS  Google Scholar 

  • Toledano E, Ogryzko V, Danchin A, Ladant D, Mechold U (2012) 3′-5′ Phosphoadenosine phosphate is an inhibitor of PARP-1 and a potential mediator of the lithium-dependent inhibition of PARP-1 in vivo. Biochem J 443:485–490

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tomar SK, Kumar P, Prakash B (2011) Deciphering the catalytic machinery in a universally conserved ribosome binding ATPase YchF. Biochem Biophys Res Commun 408:459–464

    CAS  PubMed  Google Scholar 

  • Varma S, Sabo D, Rempe SB (2008) K+/Na+ selectivity in K channels and valinomycin: over-coordination versus cavity-size constraints. J Mol Biol 376:13–22

    CAS  PubMed  Google Scholar 

  • Vasak M, Schnabl J (2016) Sodium and potassium ions in proteins and enzyme catalysis. Met Ions Life Sci 16:259–290

    CAS  PubMed  Google Scholar 

  • Verstraeten N, Fauvart M, Versees W, Michiels J (2011) The universally conserved prokaryotic GTPases. Microbiol Mol Biol Rev 75:507–542

    CAS  PubMed  PubMed Central  Google Scholar 

  • Viitanen PV, Lubben TH, Reed J, Goloubinoff P, O’Keefe DP, Lorimer GH (1990) Chaperonin-facilitated refolding of ribulosebisphosphate carboxylase and ATP hydrolysis by chaperonin 60 (groEL) are K+ dependent. Biochemistry 29:5665–5671

    CAS  PubMed  Google Scholar 

  • Vistoli G, De Maddis D, Cipak A, Zarkovic N, Carini M, Aldini G (2013) Advanced glycoxidation and lipoxidation end products (AGEs and ALEs): an overview of their mechanisms of formation. Free Radic Res 47(Suppl 1):3–27

    CAS  PubMed  Google Scholar 

  • Voigt J, Sander G, Nagel K, Parmeggiani A (1974) Effect of NH4 + and K+ on the activity of the ribosomal subunits in the EF-G- and EF-T-dependent GTR hydrolysis. Biochem Biophys Res Commun 57:1279–1286

    CAS  PubMed  Google Scholar 

  • Wang Y, Wu WH (2013) Potassium transport and signaling in higher plants. Annu Rev Plant Biol 64:451–476

    CAS  PubMed  Google Scholar 

  • Wang Y, Hall LM, Kujawa M, Li H, Zhang X, O’Meara M, Ichinose T, Wang JM (2019) Methylglyoxal triggers human aortic endothelial cell dysfunction via modulation of the KATP/MAPK pathway. Am J Physiol Cell Physiol 317:C68–C81

    CAS  PubMed  Google Scholar 

  • Weiner ID, Verlander JW (2010) Role of NH3 and NH4 + transporters in renal acid-base transport. Am J Physiol Renal Physiol 300:F11–F23

    PubMed  PubMed Central  Google Scholar 

  • Welchen E, Schmitz J, Fuchs P, Garcia L, Wagner S, Wienstroer J, Schertl P, Braun HP, Schwarzlander M, Gonzalez DH, Maurino VG (2016) d-lactate dehydrogenase links methylglyoxal degradation and electron transport through cytochrome c. Plant Physiol 172:901–912

    CAS  PubMed  PubMed Central  Google Scholar 

  • Westheimer FH (1987) Why nature chose phosphates. Science 235:1173–1178

    CAS  PubMed  Google Scholar 

  • Wheatley RW, Juers DH, Lev BB, Huber RE, Noskov SY (2015) Elucidating factors important for monovalent cation selectivity in enzymes: E. coli  β-galactosidase as a model. Phys Chem Chem Phys 17:10899–10909

    CAS  PubMed  Google Scholar 

  • Wilbanks SM, McKay DB (1995) How potassium affects the activity of the molecular chaperone Hsc70. II. Potassium binds specifically in the ATPase active site. J Biol Chem 270:2251–2257

    CAS  PubMed  Google Scholar 

  • Wolf S, Pfluger-Grau K, Kremling A (2015) Modeling the interplay of Pseudomonas putida EIIA with the potassium transporter KdpFABC. J Mol Microbiol Biotechnol 25:178–194

    CAS  PubMed  Google Scholar 

  • Wyllie S, Fairlamb AH (2011) Methylglyoxal metabolism in trypanosomes and leishmania. Semin Cell Dev Biol 22:271–277

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Li S, Konduru AS, Zhang S, Trower TC, Shi W, Cui N, Yu L, Wang Y, Zhu D, Jiang C (2012) Prolonged exposure to methylglyoxal causes disruption of vascular KATP channel by mRNA instability. Am J Physiol Cell Physiol 303:C1045–C1054

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang RL, Deng CY, Wei JW, He W, Li AN, Qian W (2018) A large-scale mutational analysis of two-component signaling systems of Lonsdalea quercina revealed that KdpD-KdpE regulates bacterial virulence against host poplar trees. Mol Plant Microbe Interact 31:724–736

    CAS  PubMed  Google Scholar 

  • Yenush L, Belles JM, Lopez-Coronado JM, Gil-Mascarell R, Serrano R, Rodriguez PL (2000) A novel target of lithium therapy. FEBS Lett 467:321–325

    CAS  PubMed  Google Scholar 

  • Zhang C, Li H, Wang J, Zhang B, Wang W, Lin H, Luan S, Gao J, Lan W (2017) The rice high-affinity K+ transporter OsHKT2;4 mediates Mg2+ homeostasis under high-Mg2+ conditions in transgenic Arabidopsis. Front Plant Sci 8:1823

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by AMAbiotics SAS as one of the background studies meant to place microbiomes in a functional perspective. The financial support from The Novo Nordisk Foundation (Grant NNF10CC1016517, and LiFe, NNF18OC0034818) and the Danish Council for Independent Research (SWEET, DFF-Research Project 8021-00039B) to P.I.N. is gratefully acknowledged.

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Danchin, A., Nikel, P.I. Why Nature Chose Potassium. J Mol Evol 87, 271–288 (2019). https://doi.org/10.1007/s00239-019-09915-2

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