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Prebiotic Chemistry and Chemical Evolution of Nucleic Acids pp 175–197Cite as

The Origin of the Ionized Linker: Geochemical Predestination for Phosphate?

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Part of the book series: Nucleic Acids and Molecular Biology ((NUCLEIC,volume 35))

Abstract

A major event in the origin of life on the earth must have been the formation of self-replicating polymers [e.g., Gilbert (Nature 319(6055):618, 1986)]. It is likely that any robust self-replicating polymer would have needed an ionized linker to slow hydrolysis and prevent diffusion. In modern life, the ionized linker is phosphate. In this chapter, I consider other alternatives to phosphate as linkers prior to the evolution of modern RNA/DNA. From a chemical and geological perspective phosphate is suggested to be the most likely molecule capable of performing the key activities of an ionized linker within a nucleic acid.

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References

  • Achbergerová L, Nahálka J (2011) Polyphosphate-an ancient energy source and active metabolic regulator. Microb Cell Factories 10(1):63

    Article  CAS  Google Scholar 

  • Anders E, Grevesse N (1989) Abundances of the elements: meteoritic and solar. Geochim Cosmochim Acta 53(1):197–214

    Article  CAS  Google Scholar 

  • Bean HD, Anet FA, Gould IR, Hud NV (2006) Glyoxylate as a backbone linkage for a prebiotic ancestor of RNA. Orig Life Evol Biosph 36(1):39–63

    Article  CAS  PubMed  Google Scholar 

  • Benner SA (2011) Comment on “A bacterium that can grow by using arsenic instead of phosphorus”. Science 332:1149

    Article  CAS  PubMed  Google Scholar 

  • Benner SA, Sismour AM (2005) Synthetic biology. Nat Rev Genet 6(7):533–543

    Article  CAS  PubMed  Google Scholar 

  • Benner SA, Kim HJ, Carrigan MA (2012) Asphalt, water, and the prebiotic synthesis of ribose, ribonucleosides, and RNA. Acc Chem Res 45(12):2025–2034

    Article  CAS  PubMed  Google Scholar 

  • Blackmond DG (2010) The origin of biological homochirality. Cold Spring Harb Perspect Biol 2(5):a002147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borden J, Crans DC, Florián J (2006) Transition state analogues for nucleotidyl transfer reactions: structure and stability of pentavalent vanadate and phosphate ester dianions. J Phys Chem B 110(30):14988–14999

    Article  CAS  PubMed  Google Scholar 

  • Bornscheuer UT, Kazlauskas RJ (2004) Catalytic promiscuity in biocatalysis: using old enzymes to form new bonds and follow new pathways. Angew Chem Int Ed 43(45):6032–6040

    Article  CAS  Google Scholar 

  • Bryant DE, Marriott KE, Macgregor SA, Kilner C, Pasek MA, Kee TP (2010) On the prebiotic potential of reduced oxidation state phosphorus: the H-phosphinate–pyruvate system. Chem Commun 46(21):3726–3728

    Article  CAS  Google Scholar 

  • Burcar B, Pasek M, Gull M, Cafferty BJ, Velasco F, Hud NV, Menor-Salván C (2016) Darwin’s warm little pond: a one-pot reaction for prebiotic phosphorylation and the mobilization of phosphate from minerals in a urea-based solvent. Angew Chem Int Ed 55(42):13249–13253

    Article  CAS  Google Scholar 

  • Cafferty BJ, Fialho DM, Khanam J, Krishnamurthy R, Hud NV (2016a) Spontaneous formation and base pairing of plausible prebiotic nucleotides in water. Nat Commun 7

    Google Scholar 

  • Cafferty BJ, Musetti C, Kim K, Horowitz ED, Krishnamurthy R, Hud NV (2016b) Small molecule-mediated duplex formation of nucleic acids with ‘incompatible’backbones. Chem Commun 52(31):5436–5439

    Article  CAS  Google Scholar 

  • Callahan MP, Smith KE, Cleaves HJ, Ruzicka J, Stern JC, Glavin DP et al (2011) Carbonaceous meteorites contain a wide range of extraterrestrial nucleobases. Proc Natl Acad Sci 108(34):13995–13998

    Article  PubMed  Google Scholar 

  • Cech TR, Bass BL (1986) Biological catalysis by RNA. Annu Rev Biochem 55(1):599–629

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Wang L, Deng Z (2010) Twenty years hunting for sulfur in DNA. Protein Cell 1(1):14–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Graaf RM, Schwartz AW (2005) Thermal synthesis of nucleoside H-phosphonates under mild conditions. Orig Life Evol Biosph 35(1):1–10

    Article  CAS  PubMed  Google Scholar 

  • De Graaf RM, Visscher J, Schwartz AW (1998) Prebiotic chemistry of phosphonic acids: products derived from phosphonoacetaldehyde in the presence of formaldehyde. Orig Life Evol Biosph 28(3):271–282

    Google Scholar 

  • Elias M, Wellner A, Goldin-Azulay K, Chabriere E, Vorholt JA, Erb TJ, Tawfik DS (2012) The molecular basis of phosphate discrimination in arsenate-rich environments. Nature 491(7422):134–137

    Article  CAS  PubMed  Google Scholar 

  • Erb TJ, Kiefer P, Hattendorf B, Günther D, Vorholt JA (2012) GFAJ-1 is an arsenate-resistant, phosphate-dependent organism. Science 337(6093):467–470

    Article  CAS  PubMed  Google Scholar 

  • Fekry MI, Tipton PA, Gates KS (2011) Kinetic consequences of replacing the internucleotide phosphorus atoms in DNA with arsenic. ACS Chem Biol 6(2):127–130

    Article  CAS  PubMed  Google Scholar 

  • Fox SW (1969) Self-ordered polymers and propagative cell-like systems. Naturwissenschaften 56(1):1–9

    Article  CAS  PubMed  Google Scholar 

  • Gilbert W (1986) Origin of life: The RNA world. Nature 319(6055)

    Google Scholar 

  • Goldhaber MB, Orr WL (1995) Kinetic controls on thermochemical sulfate reduction as a source of sedimentary H2S. ACS Symp Ser 612:412–425

    Article  CAS  Google Scholar 

  • Gulick A (1955) Phosphorus as a factor in the origin of life. Am Sci 43(3):479–489

    CAS  Google Scholar 

  • Gull M, Mojica MA, Fernández FM, Gaul DA, Orlando TM, Liotta CL, Pasek MA (2015) Nucleoside phosphorylation by the mineral schreibersite. Sci Rep 5:17198–17198. https://doi.org/10.1038/srep17198

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guthrie JP (1978) Hydrolysis of esters of oxy acids: pKa values for strong acids; Brønsted relationship for attack of water at methyl; free energies of hydrolysis of esters of oxy acids; and a linear relationship between free energy of hydrolysis and pKa holding over a range of 20 pK units. Can J Chem 56(17):2342–2354

    Article  CAS  Google Scholar 

  • Hud NV, Cafferty BJ, Krishnamurthy R, Williams LD (2013) The origin of RNA and “my grandfather’s axe”. Chem Biol 20(4):466–474

    Article  CAS  PubMed  Google Scholar 

  • Hughes MF (2002) Arsenic toxicity and potential mechanisms of action. Toxicol Lett 133(1):1–16

    Article  CAS  PubMed  Google Scholar 

  • Kamerlin SC, Sharma PK, Prasad RB, Warshel A (2013) Why nature really chose phosphate. Q Rev Biophys 46(1):1

    Article  CAS  PubMed  Google Scholar 

  • Klemperer WG, Marquart TA, Yaghi OM (1992) New directions in polyvanadate chemistry: from cages and clusters to baskets, belts, bowls, and barrels. Angew Chem Int Ed Engl 31(1):49–51

    Article  Google Scholar 

  • Lopez V, Stevens T, Lindquist RN (1976) Vanadium ion inhibition of alkaline phosphatase-catalyzed phosphate ester hydrolysis. Arch Biochem Biophys 175(1):31–38

    Article  CAS  PubMed  Google Scholar 

  • Martin AR, Barvik I, Luvino D, Smietana M, Vasseur JJ (2011) Dynamic and programmable DNA-templated boronic ester formation. Angew Chem Int Ed 50(18):4193–4196

    Article  CAS  Google Scholar 

  • Martin AR, Mohanan K, Luvino D, Floquet N, Baraguey C, Smietana M, Vasseur JJ (2009) Expanding the borononucleotide family: synthesis of borono-analogues of dCMP, dGMP and dAMP. Org Biomol Chem 7(21):4369–4377

    Article  CAS  PubMed  Google Scholar 

  • Martin AR, Vasseur JJ, Smietana M (2013) Boron and nucleic acid chemistries: merging the best of both worlds. Chem Soc Rev 42(13):5684–5713

    Article  CAS  PubMed  Google Scholar 

  • Menor-Salván C, Ruiz-Bermejo D, Guzmán MI, Osuna-Esteban S, Veintemillas-Verdaguer S (2009) Synthesis of pyrimidines and triazines in ice: implications for the prebiotic chemistry of nucleobases. Chem Eur J 15(17):4411–4418

    Article  CAS  PubMed  Google Scholar 

  • Merck Index (1996) 12th ed. Merck, Whitehouse Station, NJ, p 152

    Google Scholar 

  • Miller SL (1953) A production of amino acids under possible primitive earth conditions. Science 117(3046):528–529

    Article  CAS  Google Scholar 

  • Miller SL, Urey HC (1959) Organic compound synthesis on the primitive earth. Science 130(3370):245–251

    Article  CAS  PubMed  Google Scholar 

  • Mitchell MC, Taylor RJ, Kee TP (1998) On the hydrolysis of dimethyl-H-phosphonate. An 18O-labelling and 31P-NMR study. Polyhedron 17(4):433–442

    Article  CAS  Google Scholar 

  • Mohammed FS, Chen K, Mojica M, Conley M, Napoline JW, Butch C, Pollet P, Krishnamurthy R, Liotta CL (2017) A plausible prebiotic origin of glyoxylate: nonenzymatic transamination reactions of glycine with formaldehyde. Synlett 28(01):93–97

    CAS  Google Scholar 

  • Mukhopadhyay R, Rosen BP, Phung LT, Silver S (2002) Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiol Rev 26(3):311–325

    Article  CAS  PubMed  Google Scholar 

  • Nelson KE, Levy M, Miller SL (2000) Peptide nucleic acids rather than RNA may have been the first genetic molecule. Proc Natl Acad Sci 97(8):3868–3871

    Article  CAS  PubMed  Google Scholar 

  • Niemi R, Vepsäläinen J, Taipale H, Järvinen T (1999) Bisphosphonate prodrugs: synthesis and in vitro evaluation of novel acyloxyalkyl esters of clodronic acid. J Med Chem 42(24):5053–5058

    Article  CAS  PubMed  Google Scholar 

  • O'Neill MA, Warrenfeltz D, Kates K, Pellerin P, Doco T, Darvill AG, Albersheim P (1996) Rhamnogalacturonan-II, a pectic polysaccharide in the walls of growing plant cell, forms a dimer that is covalently cross-linked by a borate ester in vitro conditions for the formation and hydrolysis of the dimer. J Biol Chem 271(37):22923–22930

    Article  CAS  PubMed  Google Scholar 

  • Orgel LE (2004) Prebiotic chemistry and the origin of the RNA world. Crit Rev Biochem Mol Biol 39(2):99–123

    Article  CAS  Google Scholar 

  • Ossenkamp GC, Kemmitt T, Johnston JH (2001) New approaches to surface-alkoxylated silica with increased hydrolytic stability. Chem Mater 13(11):3975–3980

    Article  CAS  Google Scholar 

  • Pabis A, Duarte F, Kamerlin SC (2016) Promiscuity in the enzymatic catalysis of phosphate and sulfate transfer. Biochemistry 55(22):3061–3081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pasek MA (2017) Schreibersite on the early earth: scenarios for prebiotic phosphorylation. Geosci Front 8:329–335

    Article  CAS  Google Scholar 

  • Pasek M, Block K (2009) Lightning-induced reduction of phosphorus oxidation state. Nat Geosci 2(8):553–556

    Article  CAS  Google Scholar 

  • Pasek MA, Dworkin JP, Lauretta DS (2007) A radical pathway for organic phosphorylation during schreibersite corrosion with implications for the origin of life. Geochim Cosmochim Acta 71(7):1721–1736

    Article  CAS  Google Scholar 

  • Pasek MA, Harnmeijer JP, Buick R, Gull M, Atlas Z (2013) Evidence for reactive reduced phosphorus species in the early Archean ocean. Proc Natl Acad Sci 110(25):10089–10094

    Article  PubMed  Google Scholar 

  • Pasek M, Herschy B, Kee TP (2015) Phosphorus: a case for mineral-organic reactions in prebiotic chemistry. Orig Life Evol Biosph 45(1–2):207–218

    Article  CAS  PubMed  Google Scholar 

  • Pasek MA, Kee TP, Bryant DE, Pavlov AA, Lunine JI (2008) Production of potentially prebiotic condensed phosphates by phosphorus redox chemistry. Angew Chem Int Ed 47(41):7918–7920

    Article  CAS  Google Scholar 

  • Pasek MA, Lauretta DS (2005) Aqueous corrosion of phosphide minerals from iron meteorites: a highly reactive source of prebiotic phosphorus on the surface of the early Earth. Astrobiology 5(4):515–535

    Article  CAS  PubMed  Google Scholar 

  • Pawlowska R, Korczynski D, Nawrot B, Stec WJ, Chworos A (2016) The α-thio and/or β-γ-hypophosphate analogs of ATP as cofactors of T4 DNA ligase. Bioorg Chem 67:110–115

    Article  CAS  PubMed  Google Scholar 

  • Peyser JR, Ferris JP (2001) The rates of hydrolysis of thymidyl-3′, 5′-thymidine-H-phosphonate: the possible role of nucleic acids linked by diesters of phosphorous acid in the origins of life. Orig Life Evol Biosph 31(4):363–380

    Article  CAS  PubMed  Google Scholar 

  • Powner MW, Gerland B, Sutherland JD (2009) Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459(7244):239–242

    Article  CAS  PubMed  Google Scholar 

  • Prusiner SB (1991) Molecular biology of prion diseases. Science 252(5012):1515–1523

    Article  CAS  PubMed  Google Scholar 

  • Reaves ML, Sinha S, Rabinowitz JD, Kruglyak L, Redfield RJ (2012) Absence of detectable arsenate in DNA from arsenate-grown GFAJ-1 cells. Science 337(6093):470–473

    Article  CAS  PubMed  Google Scholar 

  • Ricardo A, Carrigan MA, Olcott AN, Benner SA (2004) Borate minerals stabilize ribose. Science 303(5655):196–196

    Article  CAS  PubMed  Google Scholar 

  • Rochette EA, Bostick BC, Li G, Fendorf S (2000) Kinetics of arsenate reduction by dissolved sulfide. Environ Sci Technol 34(22):4714–4720

    Article  CAS  Google Scholar 

  • Schoepp-Cothenet B, Nitschke W, Barge LM, Ponce A, Russell MJ, Tsapin AI (2011) Comment on “A bacterium that can grow by using arsenic instead of phosphorus”. Science 332:1149

    Article  CAS  PubMed  Google Scholar 

  • Steinberg H, Hunter DL (1957) Preparation and rate of hydrolysis of boric acid esters. Ind Eng Chem 49(2):174–181

    Article  CAS  Google Scholar 

  • Sugiyama M, Hong Z, Whalen LJ, Greenberg WA, Wong CH (2006) Borate as a phosphate ester mimic in aldolase-catalyzed reactions: practical synthesis of L-fructose and L-Iminocyclitols. Adv Synth Catal 348(18):2555–2559

    Article  CAS  Google Scholar 

  • Takeno, N. (2005). Atlas of Eh-pH diagrams. Geological survey of Japan open file report, 419, p 102

    Google Scholar 

  • Tracey AS, Gresser MJ (1988) The characterization of primary, secondary, and tertiary vanadate alkyl esters by 51V nuclear magnetic resonance spectroscopy. Can J Chem 66(10):2570–2574

    Article  CAS  Google Scholar 

  • Tracey AS, Galeffi B, Mahjour S (1988) Vanadium (V) oxyanions. The dependence of vanadate alkyl ester formation on the pKa of the parent alcohols. Can J Chem 66(9):2294–2298

    Article  CAS  Google Scholar 

  • Taylor SR, McLennan SM (1995) The geochemical evolution of the continental crust. Rev Geophys 33(2):241–265

    Article  Google Scholar 

  • Van Mooy BA, Rocap G, Fredricks HF, Evans CT, Devol AH (2006) Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments. Proc Natl Acad Sci 103(23):8607–8612

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Li ZJ, Ying HJ (2009) Solubility of adenosine 5′-monophosphate in different solvents from (288.15 to 330.15) K. J Chem Eng Data 55(2):992–993

    Article  CAS  Google Scholar 

  • Wang L, Chen S, Xu T, Taghizadeh K, Wishnok JS, Zhou X et al (2007) Phosphorothioation of DNA in bacteria by dnd genes. Nat Chem Biol 3(11):709–710

    Article  CAS  PubMed  Google Scholar 

  • Wanty RB, Goldhaber MB (1992) Thermodynamics and kinetics of reactions involving vanadium in natural systems: accumulation of vanadium in sedimentary rocks. Geochim Cosmochim Acta 56(4):1471–1483

    Article  CAS  Google Scholar 

  • Watson JD, Crick FHC (1953) Molecular structure of nucleic acids: a structure for deoxyribose nucleic acid. Nature 171:737–738

    Article  CAS  PubMed  Google Scholar 

  • Westheimer FH (1987) Why nature chose phosphates. Science 235(4793):1173–1178

    Article  CAS  PubMed  Google Scholar 

  • White HB (1976) Coenzymes as fossils of an earlier metabolic state. J Mol Evol 7(2):101–104

    Article  CAS  PubMed  Google Scholar 

  • Williams NH, Wyman P (2001) Base catalysed phosphate diester hydrolysis. Chem Commun (14):1268–1269

    Google Scholar 

  • Wolfe-Simon F, Blum JS, Kulp TR, Gordon GW, Hoeft SE, Pett-Ridge J et al (2011) A bacterium that can grow by using arsenic instead of phosphorus. Science 332(6034):1163–1166

    Article  CAS  PubMed  Google Scholar 

  • Wohlgemuth R, Liese A, Streit W (2017) Biocatalytic phosphorylations of metabolites: past, present, and future. Trends Biotechnol 35(5):452–465

    Google Scholar 

  • Wuggenig F, Hammerschmidt F (1998) Enzymes in organic chemistry VI [1]. Enantioselective hydrolysis of 1-chloroacetoxycycloalkylmethylphosphonates with lipase AP 6 from Aspergillus niger and chemoenzymatic synthesis of chiral, nonracemic 1-aminocyclohexyl-methylphosphonic acids. Monatsh Chem Chem Mon 129(4):423–436

    CAS  Google Scholar 

  • Xie X, Liang J, Pu T, Xu F, Yao F, Yang Y et al (2012) Phosphorothioate DNA as an antioxidant in bacteria. Nucleic Acids Res 40(18):9115–9124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamagata Y (1999) Prebiotic formation of ADP and ATP from AMP, calcium phosphates and cyanate in aqueous solution. Orig Life Evol Biosph 29(5):511–520

    Article  CAS  PubMed  Google Scholar 

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  1. School of Geosciences, University of South Florida, Tampa, FL, USA

    Matthew A. Pasek

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Correspondence to Matthew A. Pasek .

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  1. NSF-NASA Center for Chemical Evolution, School of Chemistry and Biochemistry, Georgia Institute of Technology, Atlanta, GA, USA; Unidad de Bioquímica y Biología Molecular, Dept. Biologia de Sistemas, Universidad de Alcala, Madrid, Spain

    César Menor-Salván

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Pasek, M.A. (2018). The Origin of the Ionized Linker: Geochemical Predestination for Phosphate?. In: Menor-Salván , C. (eds) Prebiotic Chemistry and Chemical Evolution of Nucleic Acids. Nucleic Acids and Molecular Biology, vol 35. Springer, Cham. https://doi.org/10.1007/978-3-319-93584-3_6

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