The emergence of mechanisms for phosphorylating organic and inorganic molecules is a key step en route to the earliest living systems. At the heart of all contemporary biochemical systems reside reactive phosphorus (P) molecules (such as adenosine triphosphate, ATP) as energy currency molecules to drive endergonic metabolic processes and it has been proposed that a predecessor of such molecules could have been pyrophosphate [P 2O 7 4？; PPi(V)]. Arguably the most geologically plausible route to PPi(V) is dehydration of orthophosphate, Pi(V), normally a highly endergonic process in the absence of mechanisms for activating Pi(V). One possible solution to this problem recognizes the presence of reactive-P containing mineral phases, such as schreibersite [(Fe,Ni) 3P] within meteorites whose abundance on the early Earth would likely have been significant during a putative Hadean-Archean heavy bombardment. Here, we propose that the reduced oxidation state P-oxyacid, H-phosphite [HPO 3 2？; Pi(III)] could have activated Pi(V) towards condensation via the intermediacy of the condensed oxyacid pyrophosphite [H 2P 2O 5 2？; PPi(III)]. We provide geologically plausible provenance for PPi(III) along with evidence of its ability to activate Pi(V) towards PPi(V) formation under mild conditions (80 °C) in water.
References
[1]
Harold, F.M. The Vital Force: A Study of Bioenergetics; W.H. Freeman: New York, NY, USA, 1986.
[2]
Dimroth, P.; Kaim, G.; Matthey, U. Crucial role of the membrane potential for ATP synthesis by F(1)F(0) synthases. J. Exp. Biol.？2000, 203, 51–59.
[3]
Bochud-Allemann, N.; Schneider, A. Mitochondrial substrate level phosphorylation is essential for growth of procyclic Trypanosoma brucei. J. Biol. Chem.？2002, 277, 32849–32854, doi:10.1074/jbc.M205776200.
[4]
Baltscheffsky, M.; Schultz, A.; Baltscheffsky, H. H+-proton-pumping inorganic pyrophosphatase: A tightly membrane-bound family. FEBS Lett.？1999, 452, 121–127, doi:10.1016/S0014-5793(99)00617-1.
[5]
Serrano, A.; Perez-Castineira, J.R.; Baltscheffsky, H.; Baltscheffsky, M. Proton-pumping inorganic pyrophosphatases in some archaea and other extremophilic prokaryotes. J. Bioenerg. Biomembr.？2004, 36, 127–133, doi:10.1023/B:JOBB.0000019604.49875.b3.
[6]
Serrano, A.; Perez-Castineira, J.R.; Baltscheffsky, M.; Baltscheffsky, H. H+-PPases: Yesterday, today and tomorrow. IUBMB Life？2007, 59, 76–83, doi:10.1080/15216540701258132.
[7]
Ernester, L. Molecular Mechanism in Bioenergetics; Elsevier: Amsterdam, The Netherlands, 1992.
[8]
Lipscomb, W.N.; Strater, N. Recent advances in zinc enzymology. Chem. Rev.？1996, 96, 2375–2433, doi:10.1021/cr950042j.
[9]
Pross, A. Toward a general theory of evolution: Extending Darwinian theory to inanimate matter. J. Syst. Chem.？2011, 2, 1–14, doi:10.1186/1759-2208-2-1.
[10]
Keefe, A.D.; Miller, S.L. Are polyphosphates or phosphate esters prebiotic reagents? J. Mol. Evol.？1995, 41, 693–702.
[11]
Eschenmoser, A. Etiology of potentially primordial biomolecular structures: From VitaminB12 to the nucleic acids and an inquiry into the chemistry of life’s origin: A retrospective. Angew. Chem. Int. Ed.？2011, 50, 12412–12472, doi:10.1002/anie.201103672.
[12]
Babich, L.; Hartog, A.F.; van der Horst, M.A.; Wever, R. Continuous-flow reactor-based enzymatic synthesis of phosphorylated compounds on a large scale. Chem. Eur. J.？2012, 18, 6604–6609, doi:10.1002/chem.201200101.
[13]
Holm, N.G.; Baltscheffsky, H. Links between hydrothermal environments, pyrophosphate, Na+ and early evolution. Orig. Life Evol. Biosph.？2011, 41, 483–493, doi:10.1007/s11084-011-9235-4.
[14]
Hill, A.; Orgel, L.E. Trimetaphosphate-induced addition of aspartic acid to oligo(glutamic acid)s. Helv. Chim. Acta？2002, 85, 4244–4254, doi:10.1002/hlca.200290009.
[15]
Yamagata, Y.; Watanabe, H.; Saitoh, M.; Namba, T. Volcanic production of polyphosphates and its relevance to prebiotic evolution. Nature？1991, 352, 516–519, doi:10.1038/352516a0.
[16]
Pasek, M.A.; Kee, T.P. On the Origin of Phosphorylated Biomolecules. In Origins of Life: The Primal Self Organization; Egel, R., Lankenau, D.-H., Mulkidjanian, A.-Y., Eds.; Springer Verlag: Berlin, Germany, 2011; pp. 57–83.
[17]
Hoskuldsson, A.; Sparks, R.S.J.; Carroll, M.R. Constraints on the dynamics of subglacial basalt eruptions from geologicaland geochemical observations at Kverkfj？ll, NE-Iceland. Bull. Volcanol.？2006, 68, 689–701, doi:10.1007/s00445-005-0043-4.
[18]
ólafsson, M.; Torfason, H.; Gr？nvold, K. Surface Exploration and Monitoring of Geothermal Activity in the Kverkfj？ll Geothermal Area, Central Iceland. In Proceedings of World Geothermal Congress, Beppu-Morioka, Japan, 28 May–10 June 2000; pp. 1539–1545.
[19]
Cousins, C.R.; Crawford, I.A.; Carrivick, J.; Gunn, M.; Harris, J.; Kee, T.; Karlsson, M.; Carmody, L.; Cockell, C.; Herschy, B.; et al. Glaciovolcanic hydrothermal environments in Iceland and implications for their detection on Mars. J. Volcanol. Geotherm. Res.？2013, 256, 61–77, doi:10.1016/j.jvolgeores.2013.02.009.
[20]
Blaser, B.; Worms, I.H.Z. Umanhydrisierungsreaktionen von P-O-P-Sauren,über die P-O-P-P-Saure. Anorg. Allgem. Chem.？1953, 301, 18–22, doi:10.1002/zaac.19593010104.
[21]
Madhurambal, G.; Subha, R.; Mojumdar, S.C. Crystallization and thermal characterization of calcium hydrogen phosphate dihydrate crystals. J. Therm. Anal. Calorim.？2009, 96, 73–76, doi:10.1007/s10973-008-9841-1.
[22]
Mesmer, R.E.; Carroll, R.L. The kinetics and mechanism of the hydrolysis of pyrophosphate. J. Am. Chem. Soc.？1966, 88, 1381–1387, doi:10.1021/ja00959a010.
[23]
Mulkidjanian, A.Y.; Bychkov, A.Y.; Dibrova, D.V.; Galperin, M.Y.; Koonin, E.V. Origin of first cells at terrestrial, anoxic geothermal fields. Proc. Natl. Acad. Sci. USA？2012, 109, E821–E830.
[24]
Pech, H.; Henry, A.; Khachikian, C.S.; Salmassi, T.M.; Hanrahan, G.; Foster, K.L. Detection of geothermal phosphite using high performanceliquid chromatography. Environ. Sci. Technol.？2009, 43, 7671–7675.
[25]
Pasek, M.A.; Lauretta, D.S. Aqueous corrosion of phosphide minerals from iron meteorites: A highly reactive source of prebiotic phosphorus on the surface of the early earth. Astrobiology？2005, 5, 515–535.
[26]
Bryant, D.E.; Kee, T.P. Direct evidence for the availability of reactive, water soluble phosphorus on the early Earth. H-Phosphinic acid from the Nantan meteorite. Chem. Commun.？2006, 22, 2344–2346.
[27]
Pasek, M.A.; Dworkin, J.P.; Lauretta, D.S. A radical pathway for organic phosphorylation during schreibersite corrosion with implications for the origin of life. Geochim. Cosmochim. Acta？2007, 71, 1721–1736, doi:10.1016/j.gca.2006.12.018.
[28]
Pasek, M.A.; Lauretta, D.S. Extraterrestrial flux of potentially prebiotic C, N, and P. Orig. Life Evol. Biosph.？2008, 38, 5–21, doi:10.1007/s11084-007-9110-5.
[29]
Bryant, D.E.; Greenfield, D.; Walshaw, R.D.; Evans, S.M.; Nimmo, A.E.; Smith, C.; Wang, L.; Pasek, M.A.; Kee, T.P. Electrochemical studies of iron meteorites: Phosphorus redox chemistry on the early Earth. Int. J. Astrobiol.？2009, 8, 27–36, doi:10.1017/S1473550408004345.
[30]
Benedix, G.K.; McCoy, T.J.; Kiel, K.; Love, S.G. A petrologic study of the IAB iron meteorites: Constraints on the formation of the IAB-Winonaite parent body. Meteorit. Planet. Sci.？2000, 35, 1127–1141, doi:10.1111/j.1945-5100.2000.tb01502.x.
[31]
Pasek, M.A.; Block, K. Lightning-induced reduction of phosphorus oxidation state. Nat. Geosci.？2009, 2, 553–556, doi:10.1038/ngeo580.
[32]
Chao, E.C.T.; Dwornik, E.J.; Littler, J. New data on the nickel-iron spherules from Southeast Asian tektites and their implications. Geochim. Cosmochim. Acta？1964, 28, 971–974, doi:10.1016/0016-7037(64)90044-4.
[33]
Kl？ck, W.; Palme, H.; Tobsehall, H.J. Trace elements in natural metallic iron from Disko Island, Greenland. Contrib. Mineral. Petrol.？1986, 93, 273–282.
[34]
Bryant, D.E.; Greenfield, D.; Walshaw, R.D.; Johnson, B.R.G.; Herschy, B.; Smith, C.; Pasek, M.A.; Telford, R.; Scowen, I.; Munshi, T.; et al. Hydrothermal modification of the Sikhote-Alin iron meteorite under low pH geothermal environments. A plausibly prebiotic route to activated phosphorus on the early Earth. Geochim. Cosmochim. Acta？2013, 109, 90–112, doi:10.1016/j.gca.2012.12.043.
[35]
Miller, S.L.; Parris, M. Synthesis of pyrophosphate under primitive earth conditions. Nature？1964, 204, 1248–1250, doi:10.1038/2041248a0.
[36]
Steinman, G.; Kenyon, D.H.; Calvin, M. Dehydration condensation in aqueous solution. Nature？1965, 206, 707–708, doi:10.1038/206707a0.
[37]
Beck, A.; Orgel, L.E. The formation of condensed phosphate in aqueous solution. Proc. Natl. Acad. Sci. USA？1965, 54, 664–667, doi:10.1073/pnas.54.3.664.
[38]
Weber, A.L. Formation of pyrophosphate, tripolyphosphate, and phosphorylimidazole with the thioester, N,S-diacetylcysteamine, as the condensing agent. J. Mol. Evol.？1981, 18, 24–29, doi:10.1007/BF01733208.
[39]
Weber, A.L. Formation of pyrophosphate on hydroxyapatite with thioesters as condensing agents. Biosystems？1982, 15, 183–189, doi:10.1016/0303-2647(82)90002-8.
[40]
Hermes-Lima, M.; Vieyra, A. Pyrophosphate formation from phospho(enol)pyruvate adsorbed onto precipitated orthosphosphate: A model for prebiotic catalysis of transphosphorylations. Orig. Life Evol. Biosph.？1989, 19, 143–152, doi:10.1007/BF01808148.
[41]
Hermes-Lima, M. Model for prebiotic pyrophosphate formation: Condensation of precipitated orthophosphate at low temperature in the absence of condensing or phosphorylating agents. J. Mol. Evol.？1990, 31, 353–358, doi:10.1007/BF02106049.
[42]
Keefe, A.D.; Miller, S.L. Potentially prebiotic syntheses of condensed phosphates. Orig. Life Evol. Biosph.？1996, 26, 15–25, doi:10.1007/BF01808157.
[43]
De Zwart, I.I.; Meade, S.J.; Pratt, A.J. Biomimetic phosphoryl transfer catalysed by iron(II)-mineral precipitates. Geochim. Cosmochim. Acta？2004, 68, 4093–4098, doi:10.1016/j.gca.2004.01.028.
