Mineral-Organic Interactions in Prebiotic Synthesis

The Discontinuous Synthesis Model for the Formation of RNA in Naturally Complex Geological Environments
  • Steven A. Benner
  • Hyo-Joong Kim
  • Elisa BiondiEmail author
Part of the Nucleic Acids and Molecular Biology book series (NUCLEIC, volume 35)


A common criticism of “prebiotic chemistry research” is that it is done with starting materials that are too pure, in experiments that are too directed, to get results that are too scripted, under conditions that could never have existed on Earth. Planetary scientists in particular remark that these experiments often arise simply because a chemist has a “cool idea” and then pursues it without considering external factors, especially geological and planetary context. A growing literature addresses this criticism and is reviewed here. We assume a model where RNA emerged spontaneously from a prebiotic environment on early Earth, giving the planet its first access to Darwinism. This “RNA First Hypothesis” is not driven by the intrinsic prebiotic accessibility; quite the contrary, RNA is a “prebiotic chemist’s nightmare.” However, by assuming models for the accretion of the Earth, the formation of the Moon, and the acquisition of Earth’s “late veneer,” a reasonable geological model can be envisioned to deliver the organic precursors needed to form the nucleobases and ribose of RNA. A geological model having an environment with dry arid land under a carbon dioxide atmosphere receiving effluent from serpentinizing igneous rocks allows their conversion to nucleosides and nucleoside phosphates. Mineral elements including boron and molybdenum prevent organic material from devolving to form “tars” along the way. And dehydration and activation allows the formation of oligomeric RNA that can be stabilized by adsorption on available minerals.


  1. Abramov O, Mojzsis SJ (2009) Microbial habitability of the Hadean Earth during the late heavy bombardment. Nature 459:419–422PubMedCrossRefPubMedCentralGoogle Scholar
  2. Agricola G (1530) Quarzum. In: Bermannus, Sive De Re Metallica, in Aedibus Frobenianis. Basileae, p 129Google Scholar
  3. Allègre CJ, Manhès G, Göpel G (2008) The major differentiation of the Earth at ∼4.45 Ga. Earth Planet Sci Lett 267:386–398CrossRefGoogle Scholar
  4. Andreani M, Munoz M, Marcaillou C et al (2013) μXANES study of iron redox state in serpentine during oceanic serpentinization. Lithos 178:70–83CrossRefGoogle Scholar
  5. Anet FA (2004) The place of metabolism in the origin of life. Curr Opin Chem Biol 8:654–659PubMedCrossRefPubMedCentralGoogle Scholar
  6. Anumukonda LN, Young A, Lynn DG et al (2011) Adenine synthesis in a model prebiotic reaction: connecting origin of life chemistry with biology. J Chem Educ 88:1698–1701PubMedPubMedCentralCrossRefGoogle Scholar
  7. Appayee C, Breslow R (2014) Deuterium studies reveal a new mechanism for the formose reaction involving hydride shifts. J Am Chem Soc 136:3720–3723PubMedCrossRefGoogle Scholar
  8. Bach W, Paulick H, Garrido CJ et al (2006) Unravelling the sequence of serpentinization reactions: petrography, mineral chemistry, and petrophysics of serpentinites from MAR 15_N (ODP Leg 209, Site 1274). Geophys Res Lett 33:L13306CrossRefGoogle Scholar
  9. Bada JL, Chalmers JH, Cleaves HJ (2016) Is formamide a geochemically plausible prebiotic solvent? Phys Chem Chem Phys 18:20085–20090PubMedCrossRefGoogle Scholar
  10. Becker H (2006) Highly siderophile element composition of the Earth’s primitive upper mantle: constraints from new data on peridotite massifs and xenoliths. Geochim Cosmochim Acta (17):4528–4550Google Scholar
  11. Becker S, Thoma I, Deutsch A et al (2016) A high-yielding, strictly regioselective prebiotic purine nucleoside formation pathway. Science 352(6287):833–836PubMedCrossRefGoogle Scholar
  12. Bell EA, Boehnke P, Harrison TM et al (2015) Potentially biogenic carbon preserved in a 4.1 billion-year-old zircon. Proc Natl Acad Sci U S A 112(47):14518–14521PubMedPubMedCentralCrossRefGoogle Scholar
  13. Benner SA (2009) The life, the universe and the scientific method. FfAME Press, .Gainesville, 312 pp.Google Scholar
  14. Benner SA (2013) Synthesis as a route to knowledge. Biol Theory 8:357–367CrossRefGoogle Scholar
  15. Benner SA (2017a) Detecting Darwinism from molecules in the Enceladus plumes, Jupiter’s moons, and other planetary water lagoons. Astrobiology 17(9):840–851PubMedPubMedCentralCrossRefGoogle Scholar
  16. Benner SA (2017b) Uniting natural history with the molecular sciences. The ultimate multidisciplinarity. Acc Chem Res 50:498–502PubMedCrossRefGoogle Scholar
  17. Benner SA, Kim HJ (2015) The case for a Martian origin for Earth life. In: Hoover RB, Levin GV, Rozanov, AY, Wickramasinghe NC (eds) Instruments, methods, and missions for astrobiology XVII, SPIE Optical Engineering+ Applications, 9606, 96060CGoogle Scholar
  18. Benner SA, Ellington AD, Tauer A (1989) Modern metabolism as a palimpsest of the RNA world. Proc Natl Acad Sci U S A 86:7054–7058PubMedPubMedCentralCrossRefGoogle Scholar
  19. Benner SA, Devine KG, Matveeva LN et al (2000) The missing organic molecules on Mars. Proc Natl Acad Sci U S A 97:2425–2430PubMedPubMedCentralCrossRefGoogle Scholar
  20. Benner SA, Caraco MD, Thomson JM et al (2002) Planetary biology. Paleontological, geological, and molecular histories of life. Science 293:864–868CrossRefGoogle Scholar
  21. Benner SA, Bains W, Seager S (2013) Models and standards of proof in cross-disciplinary science: the case of arsenic DNA. Astrobiology 13:510–513PubMedCrossRefGoogle Scholar
  22. Benner SA, Karalkar NB, Hoshika S et al (2016) Alternative Watson-Crick synthetic genetic systems. Synthetic Biology. Cold Spring Harb Perspect Biol 8(11). doi:
  23. Bernal JD (1951) The physical basis of life. Routledge and Kegan Paul, LondonGoogle Scholar
  24. Berndt ME, Allen DE, Seyfried WE (1996) Reduction of CO2 during serpentinization of olivine at 300 °C and 500 bar. Geology 24(4):351–354CrossRefGoogle Scholar
  25. Biondi E, Branciamore S, Maurel MC et al (2007a) Montmorillonite protection of an UV-irradiated hairpin ribozyme. Evolution of the RNA world in a mineral environment. BMC Evol Biol 7(Suppl 2):S2PubMedPubMedCentralCrossRefGoogle Scholar
  26. Biondi E, Branciamore S, Fusi L et al (2007b) Catalytic activity of a hammerhead ribozyme in a clay mineral environment: implications for the RNA World. Gene 389:10–18PubMedCrossRefGoogle Scholar
  27. Biondi E, Howell L, Benner SA (2016) Opal adsorbs and stabilizes RNA – a hierarchy of prebiotic silica minerals. Syn Lett 27:A–EGoogle Scholar
  28. Biondi E, Furukawa Y, Kwai J et al (2017) Adsorption of RNA on mineral surfaces and mineral precipitates. Beilstein J Org Chem 13:393–404PubMedPubMedCentralCrossRefGoogle Scholar
  29. Blöchl E, Keller M, Wächtershäuser G et al (1992) Reactions depending on iron sulfide and linking geochemistry with biochemistry. Proc Natl Acad Sci U S A 89(17):8117–8120PubMedPubMedCentralCrossRefGoogle Scholar
  30. Boehnken P, Harrison TM (2016) Illusory late heavy bombardments. Proc Natl Acad Sci U S A 113(39):10802–10806CrossRefGoogle Scholar
  31. Boily JF, Persson P, Sjöberg S (2000a) Benzenecarboxylate complexation at the goethite-water interface: I. A mechanistic description of pyromellitate surface complexes from the combined evidence of infrared spectroscopy, potentiometry, adsorption data and surface complexation modeling. Langmuir 16:5719–5729CrossRefGoogle Scholar
  32. Boily JF, Persson P, Sjöberg S (2000b) Benzenecarboxylate surface complexation at the goethite (α-FeOOH)/water interface: II. Linking IR spectroscopic observations to mechanistic surface complexation models for phthalate, trimellitate, and pyromellitate. Geochim Cosmochim Acta 64(20):3453–3470CrossRefGoogle Scholar
  33. Bonner WA, Kavasmaneck PR, Martin FS et al (1974) Asymmetric adsorption of alanine by quartz. Science 186(4159):143–144PubMedCrossRefGoogle Scholar
  34. Bonner WA, Kavasmaneck PR, Martin FS et al (1975) Asymmetric adsorption by quartz: a model for the prebiotic origin of optical activity. Orig Life 6(3):367–376PubMedCrossRefGoogle Scholar
  35. Borisov AA (2016) Mutual interaction of redox pairs in silicate melts: equilibria involving metallic phases. Petrology 24(2):117CrossRefGoogle Scholar
  36. Brandes JA, Boctor NZ, Cody GD et al (1998) Abiotic nitrogen reduction on the early Earth. Nature 395(6700):365–367PubMedCrossRefPubMedCentralGoogle Scholar
  37. Brasser R, Mojzsis SJ (2017) A colossal impact enriched Mars’ mantle with noble metals. Geophys Res Lett.
  38. Brasser R, Mojzsis SJ, Werner SC et al (2016) Late veneer and late accretion to the terrestrial planets. Earth Planet Sci Lett 455:85–93CrossRefGoogle Scholar
  39. Bregestovski PD (2015) “RNA World”, a highly improbable scenario of the origin and early evolution of life on Earth. J Evol Biochem Physiol 51:72–84CrossRefGoogle Scholar
  40. Burcar BT, Barge LM, Trail D et al (2015) RNA oligomerization in laboratory analogues of alkaline hydrothermal vent systems. Astrobiology 15:509–522PubMedCrossRefPubMedCentralGoogle Scholar
  41. Burcar BT, Pasek M, Gull M et al (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):13249–13253CrossRefGoogle Scholar
  42. Burton FG, Neuman MW, Neuman WF (1969) On the possible role of crystals in the origins of life. I. The adsorption of nucleosides, nucleotides and pyrophosphate by apatite crystals. Biosystems 3(1):20–26CrossRefGoogle Scholar
  43. Butlerov A (1861) Bildung einer zuckerartigen Substanz durch Synthese. Ann Chem 120:295–298CrossRefGoogle Scholar
  44. Cairns-Smith AG (1977) Takeover mechanisms and early biochemical evolution. Biosystems 9(2–3):105–109PubMedCrossRefPubMedCentralGoogle Scholar
  45. Cairns-Smith AG (1982) Genetic takeover and the mineral origins of life. Cambridge University Press, CambridgeGoogle Scholar
  46. Cairns-Smith AG (2005) Sketches for a mineral genetic material. Elements 1:157–161CrossRefGoogle Scholar
  47. Calvin M, Calvin GI (1964) Atom to Adam. Am Sci 52:163Google Scholar
  48. Cech TR (2000) The ribosome is a ribozyme. Science 289(5481):878–879PubMedCrossRefPubMedCentralGoogle Scholar
  49. Cech TR, Bass BL (1986) Biological catalysis by RNA. Annu Rev Biochem 55:599–629PubMedCrossRefGoogle Scholar
  50. Chapman CR, Cohen BA, Grinspoon DH (2007) What are the real constraints on the existence and magnitude of the late heavy bombardment? Icarus 189(1):233–245CrossRefGoogle Scholar
  51. Cherniak DJ, Hanchar JM, Watson EB (1997) Rare-earth diffusion in zircon. Chem Geol 134:289–301CrossRefGoogle Scholar
  52. Cleaves HJ (2008) The prebiotic geochemistry of formaldehyde. Precambrian Res 164:111–118CrossRefGoogle Scholar
  53. Cody GD (2004) Transition metal sulfides and the origins of metabolism. Geophysical Laboratory, Carnegie Institution of Washington, Washington, DC, pp 569–599Google Scholar
  54. Cody GD (2005) Geochemical connections to primitive metabolism. Elements 1:139–143CrossRefGoogle Scholar
  55. Cody GD, Boctor NZ, Filley T et al (2000) The primordial synthesis of carbonylated iron-sulfur clusters and the synthesis of pyruvate. Science 289:1339–1339CrossRefGoogle Scholar
  56. Cody GD, Boctor NZ, Hazen RM et al (2001) Geochemical roots of autotrophic carbon fixation: Hydrothermal experiments in the system citric acid, H2O-(±FeS)-(±NiS). Geochim Cosmochim Acta 65(20):3557–3576CrossRefGoogle Scholar
  57. Cody GD, Boctor NZ, Brandes JA et al (2004) Assaying the catalytic potential of transition metal sulfides for abiotic carbon fixation. Geochim Cosmochim Acta 68(10):2185–2196CrossRefGoogle Scholar
  58. Cohen BA, Swindle TD, Kring DA (2000) Support for the lunar cataclysm hypothesis from lunar meteorite impact melt ages. Science 290:1754–1756PubMedCrossRefPubMedCentralGoogle Scholar
  59. Condie KC (2018) A planet in transition: the onset of plate tectonics on Earth between 3 and 2 Ga. Geosci Front 9(1):51–60Google Scholar
  60. Cox PA (1989) The elements: their origin, abundance, and distribution. Oxford University Press, OxfordGoogle Scholar
  61. da Silva JAL, Holm NG (2014) Borophosphates and silicophosphates as plausible contributors to the emergence of life. J Colloid Interface Sci 431:250–254PubMedCrossRefPubMedCentralGoogle Scholar
  62. Dal Negro A, Ungaretti L (1971) Refinement of the crystal structure of aragonite. Am Mineral 56:768–772Google Scholar
  63. Danielson LR, Righter K, Newville M et al (2011) Molybdenum valence in basaltic silicate melts: effects of temperature and pressure. In: 42nd Lunar and planetary science conference, 2609Google Scholar
  64. Dauphas N, Schauble EA (2016) Mass fractionation laws, mass-independent effects, and isotopic anomalies. Annu Rev Earth Planet Sci 44:709–783CrossRefGoogle Scholar
  65. Dauphas N, Chen J, Papanastassiou D (2015) Testing Earth–Moon isotopic homogenization with calcium-48. In: Lunar and planetary science conference XXXXVI, 2436Google Scholar
  66. Day JM, Walker RJ (2015) Highly siderophile element depletion in the Moon. Earth Planet Sci Lett 423:114–124CrossRefGoogle Scholar
  67. Decher G, Lehr B, Lowack K et al (1994) New nanocomposite films for biosensors – layer-by-layer adsorbed films of polyelectrolytes, proteins or DNA. Biosens Bioelectron 9:677–684CrossRefGoogle Scholar
  68. Decker P, Schweer H, Pohlamnn R (1982) Bioids: X. Identification of formose sugars, presumable prebiotic metabolites, using capillary gas chromatography/gas chromatography—mas spectrometry of n-butoxime trifluoroacetates on OV-225. J Chromatogr A 244:281–291CrossRefGoogle Scholar
  69. Dyson F (1985) Origin of life. Cambridge University Press, CambridgeGoogle Scholar
  70. Ehlmann BL, Mustard JF, Murchie SL et al (2008) Orbital identification of carbonate-bearing rocks on Mars. Science 322:1828–1832PubMedCrossRefPubMedCentralGoogle Scholar
  71. Ertem G, Ferris JP (1996) Synthesis of RNA oligomers on heterogeneous templates. Nature 379(6562):238–240PubMedCrossRefPubMedCentralGoogle Scholar
  72. Ertem G, Ferris JP (1997) Template-directed synthesis using the heterogeneous templates produced by montmorillonite catalysis. A possible bridge between the prebiotic and RNA worlds. J Am Chem Soc 119(31):7197–7201PubMedCrossRefPubMedCentralGoogle Scholar
  73. Ertem G, Ertem MC, McKay CP et al (2017) Shielding biomolecules from effects of radiation by Mars analogue minerals and soils. Int J Astrobiol 16(03):280–285CrossRefGoogle Scholar
  74. Eschenmoser A (1997) Towards a chemical etiology of nucleic acid structure. Orig Life Evol Biosph 27(5–6):535–553PubMedCrossRefPubMedCentralGoogle Scholar
  75. Evgenii K, Wolfram T (2000) The role of quartz in the origin of optical activity on earth. Orig Life Evol Biosph 30(5):431–434PubMedCrossRefPubMedCentralGoogle Scholar
  76. Feely RA, Trefry JH, Lebon GT et al (1998) The relationship between P/Fe and V/Fe ratios in hydrothermal precipitates and dissolved phosphate in seawater. Geophys Res Lett 25:2253–2256CrossRefGoogle Scholar
  77. Feigl F (1937) Qualitative analysis by spot tests. Nordemann, New York, p 400Google Scholar
  78. Ferris JP (2005) Mineral catalysis and prebiotic synthesis: montmorillonite-catalyzed formation of RNA. Elements 1(3):145–149CrossRefGoogle Scholar
  79. Ferris JP, Ertem G (1992) Oligomerization of ribonucleotides on montmorillonite: reaction of the 5′-phosphorimidazolide of adenosine. Science 257(5075):1387–1389PubMedCrossRefPubMedCentralGoogle Scholar
  80. Ferris JP, Ertem G (1993) Montmorillonite catalysis of RNA oligomer formation in aqueous solution. A model for the prebiotic formation of RNA. J Am Chem Soc 115(26):12270–12275PubMedCrossRefPubMedCentralGoogle Scholar
  81. Ferris JP, Sanchez RA, Orgel LE (1968) Studies in prebiotic synthesis: III. Synthesis of pyrimidines from cyanoacetylene and cyanate. J Mol Biol 33(3):693–704PubMedCrossRefGoogle Scholar
  82. Feynman R (1974) Cargo cult science. Caltech commencement address. Reproduced in “Surely You’re Joking, Mr. Feynman”. Norton, New YorkGoogle Scholar
  83. Fiore M, Strazewski P (2016) Prebiotic lipidic amphiphiles and condensing agents on the early Earth. Life 6.
  84. Fox SW (1965) A theory of macromolecular and cellular origins. Nature 205:328PubMedCrossRefGoogle Scholar
  85. Fuchs LH (1969) The phosphate mineralogy of meteorites. In: Meteorite research. Springer, Dordrecht, pp 683–695Google Scholar
  86. Fyfe WS, Bischoff JL (1965) The calcite-aragonite problem. In Pray LC, Murray RC (eds), Dolomitization and limestone diagenesis: a symposium. Society of Economic Paleontologists and Mineralogists, Special Publication, 13, pp 3–13Google Scholar
  87. Galison PL (1987) How experiments end. University of Chicago Press, ChicagoGoogle Scholar
  88. Genda H, Fujita T, Kobayashi H et al (2017) Impact erosion model for gravity-dominated planetesimals. Icarus 294:234–246CrossRefGoogle Scholar
  89. Goldschmidt VM (1952) Geochemical aspects of the origin of complex organic molecules on the earth, as precursors to organic life. New Biol 12:97–105Google Scholar
  90. Grasby SE (2003) Naturally precipitating vaterite (μ-CaCO3) spheres: Unusual carbonates formed in an extreme environment. Geochim Cosmochim Acta 67:1659–1666CrossRefGoogle Scholar
  91. Grosjean M, Geyh MA, Messerli B et al (1995) Late-glacial and early Holocenelake sediments, groundwater formation and climate in the Atacama altiplano 22–241S. J Paleolimnol 14:241–252CrossRefGoogle Scholar
  92. Guerrier-Takada C, Gardiner K, Marsh T et al (1983) The RNA moiety of ribonuclease-P is the catalytic subunit of the enzyme. Cell 35:849–857PubMedCrossRefGoogle Scholar
  93. Gull M, Mojica MA, Fernández FM et al (2015) Nucleoside phosphorylation by the mineral schreibersite. Sci Rep 5:17198. Scholar
  94. Hamano K, Abe Y, Genda H (2013) Emergence of two types of terrestrial planet on solidification of magma ocean. Nature 497:607–610PubMedCrossRefGoogle Scholar
  95. Hanczyc MM, Fujikawa SM, Szostak JW (2003) Experimental models of primitive cellular compartments: encapsulation, growth, and division. Science 302(5645):618–622PubMedPubMedCentralCrossRefGoogle Scholar
  96. Harman CE, Kasting JF, Wolf ET (2013) Atmospheric production of glycolaldehyde under hazy prebiotic conditions. Orig Life Evol Biosph 43:77–98PubMedCrossRefGoogle Scholar
  97. Hartmann WK (1975) Lunar “cataclysm”: a misconception? Icarus 24(2):181–187CrossRefGoogle Scholar
  98. Hazen RM (2005) Genesis. The scientific quest for life’s origins. Joseph Henry Press, Washington, DCGoogle Scholar
  99. Hazen RM, Papineau D, Bleeker W et al (2008) Mineral evolution. Am Mineral 93(11–12):1693–1720CrossRefGoogle Scholar
  100. Hedenquist JW, Arribas A, Gonzalez-Urien E (2000) Exploration for epithermal gold deposits. Rev Econ Geol 13:45–77Google Scholar
  101. Herdewijn P (2001) TNA as a potential alternative to natural nucleic acids. Angew Chem Int Ed 40(12):2249–2251CrossRefGoogle Scholar
  102. Holland H (1984) The chemical evolution of the atmosphere and oceans. Princeton University Press, Princeton, 598 pGoogle Scholar
  103. Holm NG, Ertem G, Ferris JP (1993) The binding and reactions of nucleotides and polynucleotides on iron oxide hydroxide polymorphs. Orig Life Evol Biosph 23(3):195–215PubMedCrossRefGoogle Scholar
  104. Huber C, Wächtershäuser G (1997) Activated acetic acid by carbon fixation on (Fe,Ni)S under primordial conditions. Science 276(5310):245–247PubMedCrossRefGoogle Scholar
  105. Huber C, Wächtershäuser G (1998) Peptides by activation of amino acids with CO on (Ni,Fe)S surfaces: implications for the origin of life. Science 281(5377):670–671PubMedCrossRefPubMedCentralGoogle Scholar
  106. Huber C, Eisenreich W, Hecht S et al (2003) A possible primordial peptide cycle. Science 301(5635):938–940PubMedCrossRefGoogle Scholar
  107. Huber C, Kraus F, Hanzlik M et al (2012) Elements of metabolic evolution. Chem Eur J 18(7):2063–2080PubMedCrossRefGoogle Scholar
  108. Hud NV, Jain SS, Li X et al (2007) Addressing the problems of base pairing and strand cyclization in template-directed synthesis. Chem Biodivers 4(4):768–783PubMedCrossRefGoogle Scholar
  109. Hyeon C, Dima RI, Thirumalai D (2006) Size, shape, and flexibility of RNA structures. J Chem Phys 125(19):194905PubMedCrossRefGoogle Scholar
  110. Ichida JK, Zou K, Horhota A et al (2005) An in vitro selection system for TNA. J Am Chem Soc 127(9):2802–2803PubMedPubMedCentralCrossRefGoogle Scholar
  111. Inoue T, Orgel LE (1982) Oligomerization of (guanosine 5′-phosphor)-2-methylimidazolide on poly (C): an RNA polymerase model. J Mol Biol 162(1):201–217PubMedCrossRefPubMedCentralGoogle Scholar
  112. Islam S, Bučar DK, Powner MW (2017) Prebiotic selection and assembly of proteinogenic amino acids and natural nucleotides from complex mixtures. Nat Chem 9:584–589CrossRefGoogle Scholar
  113. Izgu EC, Oh SS, Szostak JW (2016) Synthesis of activated 3′-amino-3′-deoxy-2-thio-thymidine, a superior substrate for the nonenzymatic copying of nucleic acid templates. Chem Commun 52(18):3684–3686CrossRefGoogle Scholar
  114. Javoy M, Kaminski E, Guyot F et al (2010) The chemical composition of the Earth: enstatite chondrite models. Earth Planet Sci Lett 293:259–268CrossRefGoogle Scholar
  115. Jermann TM, Opitz JG, Stackhouse J et al (1995) Reconstructing the evolutionary history of the artiodactyl ribonuclease superfamily. Nature 374:57–59PubMedCrossRefPubMedCentralGoogle Scholar
  116. Jones LC, Rosenbauer R, Goldsmith JI et al (2010) Carbonate control of H2 and CH4 production in serpentinization systems at elevated P-Ts. Geophys Res Lett 37:L14306Google Scholar
  117. Joyce GF, Orgel LE (1999) Prospects for understanding the origin of the RNA world. In: Gestland RF, Cech RTR, Atkins JF (eds) The RNA World, 2nd edn. Cold Spring Harbor Press, Cold Spring Harbor, NY, pp 49–78Google Scholar
  118. Keefe AD, Miller SL (1996) Was ferrocyanide a prebiotic reagent? Orig Life Evol Biosph 26(2):111–129PubMedCrossRefPubMedCentralGoogle Scholar
  119. Kim HJ, Benner SA (2010) Comment on “The silicate-mediated formose reaction: bottom-up synthesis of sugar silicates”. Science 329(5994):902-aGoogle Scholar
  120. Kim HJ, Benner, SA (2017) Prebiotic stereoselective synthesis of purine and noncanonical pyrimidine nucleotide from nucleobases and phosphorylated carbohydrates. Proc Natl Acad Sci U S A (on line)Google Scholar
  121. Kim HJ, Ricardo A, Illangkoon HI et al (2011) Synthesis of carbohydrates in mineral-guided prebiotic cycles. J Am Chem Soc 133:9457–9468PubMedCrossRefGoogle Scholar
  122. Kim HJ, Furukawa Y, Kakegawa T et al (2016) Evaporite borate-containing mineral ensembles make phosphate available and regiospecifically phosphorylate ribonucleosides: borate as a multifaceted problem solver in prebiotic chemistry. Angew Chem 55:15816–15820CrossRefGoogle Scholar
  123. Kring DA, Cohen BA (2002) Cataclysmic bombardment throughout the inner solar system 3.9–4.0Ga. J Geophys Res 107(E2):4-1–4-6CrossRefGoogle Scholar
  124. Kruijer TS, Kleine T, Fischer-Gödde M et al (2015) Lunar tungsten isotopic evidence for the late veneer. Nature 5:534–537CrossRefGoogle Scholar
  125. Lahav N (1994) Minerals and the origin of life – hypotheses and experiments in heterogeneous chemistry. Heterog Chem Rev 1:159–179Google Scholar
  126. Lahav N, White D, Chang S (1978) Peptide formation in the prebiotic era: thermal condensation of glycine in fluctuating clay environments. Science 201(435 O):67–69Google Scholar
  127. Lambert JB, Gurusamy-Thangavelu SA, Ma KBA (2010a) The silicate-mediated formose reaction: bottom-up synthesis of sugar silicates. Science 327:984–986PubMedCrossRefGoogle Scholar
  128. Lambert JB, Gurusamy-Thangavelu SA, Ma KBA (2010b) Response to comment on “The silicate-mediated formose reaction: bottom-up synthesis of sugar silicates”. Science 329(5994):902-bGoogle Scholar
  129. Lapen TJ, Righter M, Brandon AD et al (2010) A younger age for ALH84001 and its geochemical link to shergottite sources in Mars. Science 328:347–351PubMedCrossRefGoogle Scholar
  130. Larralde R, Robertson MP, Miller SL (1995) Rates of decomposition of ribose and other sugars. Implications for chemical evolution. Proc Natl Acad Sci U S A 92:8158–8160PubMedPubMedCentralCrossRefGoogle Scholar
  131. Lehman N (2003) A case for the extreme antiquity of recombination. J Mol Evol 56:770–777PubMedCrossRefPubMedCentralGoogle Scholar
  132. Leman LJ, Orgel LE, Ghadiri MR (2006) Amino acid dependent formation of phosphate anhydrides in water mediated by carbonyl sulfide. J Am Chem Soc 128(1):20–21PubMedCrossRefPubMedCentralGoogle Scholar
  133. Levy M, Miller SL (1998) The stability of the RNA bases: implications for the origin of life. Proc Natl Acad Sci U S A 95:7933–7938PubMedPubMedCentralCrossRefGoogle Scholar
  134. Levy M, Miller SL, Oró J (1999) Production of guanine from NH4CN polymerizations. J Mol Evol 49:165–168PubMedCrossRefPubMedCentralGoogle Scholar
  135. Li L, Prywes N, Tam CP et al (2017) Enhanced nonenzymatic RNA copying with 2-aminoimidazole activated nucleotides. J Am Chem Soc 139(5):1810–1813PubMedCrossRefPubMedCentralGoogle Scholar
  136. Lincoln TA, Joyce GF (2009) Self-sustained replication of an RNA enzyme. Science 323:1229–1232PubMedPubMedCentralCrossRefGoogle Scholar
  137. Löb W (1913) Uber das Verhalten des Formamids unter der Wirkung der stillen Entladung Ein Beitrag zur Frage der Stickstoff-Assimilation. Ber Dtsch Chem Ges 46:684–697CrossRefGoogle Scholar
  138. Lohrmann R (1972) Formation of urea and guanidine by irradiation of ammonium cyanide. J Mol Evol 1:263–269PubMedCrossRefPubMedCentralGoogle Scholar
  139. Maher KA, Stevenson DJ (1988) Impact frustration of the origin of life. Nature 331:612–614PubMedCrossRefPubMedCentralGoogle Scholar
  140. Malaterre C (2013) Synthetic biology and synthetic knowledge. Biol Theory 8:346–356CrossRefGoogle Scholar
  141. Mann U, Frost DJ, Rubie DC et al (2012) Partitioning of Ru Rh Pd Re Ir and Pt between liquid metal and silicate at high pressures and high temperatures – Implications for the origin of highly siderophile element concentrations in the Earth’s mantle. Geochim Cosmochim Acta 84:593–613CrossRefGoogle Scholar
  142. Marchi S, Bottke WF, Cohen BE et al (2013) High-velocity collisions from the lunar cataclysm recorded in asteroidal meteorites. Nat Geosci 6:303–307CrossRefGoogle Scholar
  143. Markovitch O, Lancet D (2014) Multispecies population dynamics of prebiotic compositional assemblies. J Theor Biol 357:26–34PubMedCrossRefPubMedCentralGoogle Scholar
  144. Maslen EN, Streltsov VA, Streltsova NR (1993) X-ray study of the electron density in calcite, CaCO3. Acta Cryst B49:636–641CrossRefGoogle Scholar
  145. McCauley JW, Roy R (1974) Controlled nucleation and crystal growth of various CaCO3 phases by the silica gel technique. Am Mineral 59:947–963Google Scholar
  146. McCollom TM (2013) Miller-Urey and beyond: What have we learned about prebiotic organic synthesis reactions in the past 60 years? Annu Rev Earth Planet Sci 41:207–229CrossRefGoogle Scholar
  147. McCollom TM, Seewald JS (2001) A reassessment of the potential for reduction of dissolved CO2 to hydrocarbons during serpentinization of olivine. Geochim Cosmochim Acta 65(21):3769–3778CrossRefGoogle Scholar
  148. Miller SL (1953) A production of amino acids under possible primitive earth conditions. Science 117:528–529PubMedCrossRefPubMedCentralGoogle Scholar
  149. Miyakawa S, Cleaves HJ, Miller SL (2002) The cold origin of life: B. Implications based on pyrimidines and purines produced from frozen ammonium cyanide solutions. Orig Life Evol Biosph 32:209–218PubMedCrossRefPubMedCentralGoogle Scholar
  150. Mojzsis SJ, Arrhenius G, McKeegan KD et al (1996) Evidence for life on Earth before 3,800 million years ago. Nature 384(6604):55–59PubMedCrossRefPubMedCentralGoogle Scholar
  151. Molster FJ, Lim TL, Sylvester RJ et al (2001) The complete ISO spectrum of NGC 6302. Astron Astrophys 372:165–172CrossRefGoogle Scholar
  152. Morbidelli A, Marchi S, Bottke WF et al (2012) A sawtooth-like timeline for the first billion years of lunar bombardment. Earth Planet Sci Lett 355-356:144–151CrossRefGoogle Scholar
  153. Müller J, Fabricius F (1978) Lüneburgite [Mg3(PO4)2B2O(OH)4 × 6 H2O] in Upper Miocene sediments of the Eastern Mediterranean Sea. Init Rep DSDP 42:661–664. Scholar
  154. Mutschler H, Wochner A, Holliger P (2015) Freeze-thaw cycles as drivers of complex ribozyme assembly. Nat Chem 7:502–508PubMedPubMedCentralCrossRefGoogle Scholar
  155. Neveu M, Kim HJ, Benner SA (2013) The “Strong” RNA World hypothesis. Fifty years old. Astrobiology 13:391–403PubMedCrossRefGoogle Scholar
  156. Nishiyama T, Kagami Y, Yamauchi T et al (2013) Assembly of stimulus-sensitive gel particles with DNA-dye complexes. Polym J 45:659–664CrossRefGoogle Scholar
  157. Okafor CD, Lanier KA, Petrov AS et al (2017) Iron mediates catalysis of nucleic acid processing enzymes: support for Fe (II) as a cofactor before the great oxidation event. Nucleic Acids Res 45:3634–3642PubMedPubMedCentralCrossRefGoogle Scholar
  158. Orgel LE (2000a) A simpler nucleic acid. Science 290(5495):1306–1307PubMedCrossRefGoogle Scholar
  159. Orgel LE (2000b) Self-organizing biochemical reactions. Proc Natl Acad Sci U S A 97:12503–12507PubMedPubMedCentralCrossRefGoogle Scholar
  160. Oró JJ (1965) Investigation of organo-chemical evolution. In: Mamikunian G, Briggs MH (eds) Current aspects of exobiology. Pergamon Press, Oxford, pp 13–39CrossRefGoogle Scholar
  161. Parsons I, Lee MR, Smith JV (1998) Biochemical evolution II: origin of life in tubular microstructures on weathered feldspar surfaces. Proc Natl Acad Sci 95(26):15173–15176PubMedCrossRefPubMedCentralGoogle Scholar
  162. Pasek MA (2016) Schreibersite on the early earth: scenarios for prebiotic phosphorylation. Geosci Front 8(2):329–335CrossRefGoogle Scholar
  163. Pearce BKD, Pudritz RE (2015) Seeding the pregenetic Earth: meteoritic abundances of nucleobases and potential reaction pathways. Astrophys J 807:85–94CrossRefGoogle Scholar
  164. Pearce BKD, Pudritz RE, Semenov DA et al (2017) Origin of the RNA world: the fate of nucleobases in warm little ponds. Proc Natl Acad Sci U S A.
  165. Petrus L, Petrusová M, Hricovíniová Z (2001) The Bilik reaction. In: Stutz AE (ed) Topics in current chemistry: glycoscience, epimerisation, isomerisation and rearrangment reactions of carbohydrates, vol 215. Springer, Berlin, pp 15–41Google Scholar
  166. Piccoli PM, Candela P (2002) Apatite in igneous systems. Rev Miner Geochem 48:255–292CrossRefGoogle Scholar
  167. Pinto J, Gladstone G, Yung Y (1980) Photochemical production of formaldehyde in Earth’s primitive atmosphere. Science 210:183–185PubMedCrossRefPubMedCentralGoogle Scholar
  168. Powner MW, Gerland B, Sutherland JD (2009) Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459:239–242PubMedCrossRefGoogle Scholar
  169. Puchtel IS, Walker RJ, Touboul M et al (2014) Insights into early Earth from the Pt–Re–Os isotope and highly siderophile element abundance systematics of Barberton komatiites. Geochim Cosmochim Acta 125:394–413CrossRefGoogle Scholar
  170. Qin L, Alexander CMD, Carlson RW (2010) Contributors to chromium isotope variation of meteorites. Geochim Cosmochim Acta 74:1122–1145CrossRefGoogle Scholar
  171. Ricardo A, Carrigan MA, Olcott AN et al (2004) Borate minerals stabilize ribose. Science 303:196PubMedCrossRefGoogle Scholar
  172. Rich A (1962) On the problems of evolution and biochemical information transfer. In: Kasha M, Pullmann B (eds) Horizons in biochemistry. Academic Press, NY, pp 103–126Google Scholar
  173. Richter Y, Fischer B (2003) Characterization and elucidation of coordination requirements of adenine nucleotides complexes with Fe (II) ions. Nucleosides Nucleotides Nucleic Acids 22(9):1757–1780PubMedCrossRefPubMedCentralGoogle Scholar
  174. Righter K, Yang H, Costin G et al (2008) Oxygen fugacity in the Martian mantle controlled by carbon: New constraints from the nakhlite MIL 03346. Meteorit Planet Sci 43:1709–1723CrossRefGoogle Scholar
  175. Righter K, Danielson LR, Pando KM et al (2015) Highly siderophile element (HSE) abundances in the mantle of Mars are due to core formation at high pressure and temperature. Meteorit Planet Sci 50:604–631CrossRefGoogle Scholar
  176. Rosing MT (1999) 13C-Depleted carbon microparticles in >3700-Ma sea-floor sedimentary rocks from West Greenland. Science 283:674–676PubMedCrossRefGoogle Scholar
  177. Rubie DC, Jacobson SA, Morbidelli A et al (2015a) Accretion and differentiation of the terrestrial planets with implications for the compositions of early-formed Solar System bodies and accretion of water. Icarus 248:89–108CrossRefGoogle Scholar
  178. Rubie DC, Nimmo F, Melosh HJ (2015b) Formation of the Earth’s core. In: Schubert G (ed) Treatise on geophysics, vol 9: Evolution of the Earth, 2nd edn. Elsevier, Oxford, pp 43–79Google Scholar
  179. Russell MJ, Hall AJ (1997) The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front. J Geol Soc 154(3):377–402CrossRefGoogle Scholar
  180. Russell MJ, Martin W (2004) The rocky roots of the acetyl-CoA pathway. Trends Biochem Sci 29(7):358–363PubMedCrossRefGoogle Scholar
  181. Russell MJ, Daniel RM, Hall AJ et al (1994) A hydrothermally precipitated catalytic iron sulphide membrane as a first step toward life. J Mol Evol 39(3):231–243CrossRefGoogle Scholar
  182. Sahai N, Kaddour H, Dalai P (2016) The transition from geochemistry to biogeochemistry. Elements 12(6):389–394CrossRefGoogle Scholar
  183. Saladino R, Ciambecchini U, Crestini C et al (2003) One-pot TiO2-catalyzed synthesis of nucleic bases and acyclonucleosides from formamide: implications for the origin of life. Chembiochem 4:514–521PubMedCrossRefGoogle Scholar
  184. Saladino R, Barontini M, Cossetti C et al (2011) The effects of borate minerals on the synthesis of nucleic acid bases, amino acids and biogenic carboxylic acids from formamide. Orig Life Evol Biosph 41:317–330PubMedCrossRefGoogle Scholar
  185. Sanchez RA, Orgel LE (1970) Studies in prebiotic synthesis: V. Synthesis and photoanomerization of pyrimidine nucleosides. J Mol Biol 47:531–543PubMedCrossRefGoogle Scholar
  186. Sanchez RA, Ferris JP, Orgel LE (1966) Cyanoacetylene in prebiotic synthesis. Science 154:784–785PubMedCrossRefGoogle Scholar
  187. Santos AR, Agee CB, McCubbin FM et al (2013) Apatite and merrillite from Martian meteorite NWA 7034. In: Lunar and planetary science conference 44, 2601Google Scholar
  188. Schoonen M, Smirnov A (2016) Staging life in an early warm ‘seltzer’ ocean. Elements 12(6):395–400CrossRefGoogle Scholar
  189. Schoonen M, Smirnov A, Cohn C (2004) A perspective on the role of minerals in prebiotic synthesis. Ambio 33(8):539–551PubMedCrossRefGoogle Scholar
  190. Sekimoto K, Takayama M (2012) Formation of hydrogen cyanide HCN under limited discharge conditions in non-reduced ambient air. ESCAMPIG XXI, Viana do Castelo, Portugal, 10–14 JulyGoogle Scholar
  191. Shapiro R (1995) The prebiotic role of adenine: a critical analysis. Orig Life Evol Biosph 25:83–98PubMedCrossRefGoogle Scholar
  192. Shapiro R (1999) Prebiotic cytosine synthesis: a critical analysis and implications for the origin of life. Proc Natl Acad Sci U S A 96:4396–4401PubMedPubMedCentralCrossRefGoogle Scholar
  193. Shapiro R (2007) A simpler origin for life. Sci Am 296:46–53PubMedCrossRefGoogle Scholar
  194. Sleep NH, Meibom A, Fridriksson T et al (2004) H2-rich fluids from serpentinization: geochemical and biotic implications. Proc Natl Acad Sci U S A 101:12818–12823PubMedPubMedCentralCrossRefGoogle Scholar
  195. Sleep NH, Bird DK, Pope EC (2011) Serpentinite and the dawn of life. Philos Trans R Soc B 366:2857–2869CrossRefGoogle Scholar
  196. Smith JV (1998) Biochemical evolution. I. Polymerization on internal, organophilic silica surfaces of dealuminated zeolites and feldspars. Proc Natl Acad Sci U S A 95(7):3370–3375PubMedPubMedCentralCrossRefGoogle Scholar
  197. Smith JV, Arnold FP, Parsons I et al (1999) Biochemical evolution III: polymerization on oganophilic silica-rich surfaces, crystal-chemical modeling, formation of first cells, and geological clues. Proc Natl Acad Sci U S A 96(7):3479–3485PubMedPubMedCentralCrossRefGoogle Scholar
  198. Stephenson JD, Hallis LJ, Nagashima K et al (2013) Boron enrichment in Martian clay. PLoS One 8(6):e64624PubMedPubMedCentralCrossRefGoogle Scholar
  199. Stephenson JD, Popović M, Bristow TF et al (2016) Evolution of ribozymes in the presence of a mineral surface. RNA 22:1893–1901PubMedPubMedCentralGoogle Scholar
  200. Stober W, Fink A, Bohn E (1968) Controlled growth of monodisperse silica spheres in micron size range. J Colloid Interface Sci 26:62–69CrossRefGoogle Scholar
  201. Summers DP, Chang S (1993) Prebiotic ammonia from reduction of nitrite by iron (II) on the early Earth. Nature 365(6447):630–633PubMedCrossRefPubMedCentralGoogle Scholar
  202. Sutherland JD (2016) The origin of life. Out of the blue. Angew Chem Int Ed 55(1):104–121CrossRefGoogle Scholar
  203. Taves DR (1963) Similarity of octacalcium phosphate and hydroxyapatite structures. Nature 200(4913):1312–1313CrossRefGoogle Scholar
  204. Taves DR, Reedy RC (1969) A structural basis for the transphosphorylation of nucleotides with hydroxyapatite. Calcif Tissue Int 3(1):284–292CrossRefGoogle Scholar
  205. Tera F, Papanastassiou DA, Wasserburg GJ (1974) Isotopic evidence for a terminal lunar cataclysm. Earth Planet Sci Lett 22(1):1–21CrossRefGoogle Scholar
  206. Touboul M, Puchtel IS, Walker RJ (2012) 182W evidence for long term preservation of early mantle differentiation products. Science 335:1065–1069PubMedCrossRefPubMedCentralGoogle Scholar
  207. Touboul M, Liu J, O’Neil J et al (2014) New insights into the Hadean mantle revealed by 182 W and highly siderophile element abundances of supracrustal rocks from the Nuvvuagittuq greenstone belt, Quebec Canada. Chem Geol 383:63–75CrossRefGoogle Scholar
  208. Trail D, Watson EB, Tailby ND (2011) The oxidation state of Hadean magmas and implications for early Earth’s atmosphere. Nature 480(7375):79–82PubMedCrossRefPubMedCentralGoogle Scholar
  209. Van Vleck JH (1928) The correspondence principle in the statistical interpretation of quantum mechanics. Proc Natl Acad Sci U S A 14(2):178–188PubMedPubMedCentralCrossRefGoogle Scholar
  210. Wächtershäuser G (1988a) Before enzymes and templates: theory of surface metabolism. Microbiol Rev 52(4):452–484PubMedPubMedCentralGoogle Scholar
  211. Wächtershäuser G (1988b) Pyrite formation, the first energy source for life: a hypothesis. Syst Appl Microbiol 10(3):207–210CrossRefGoogle Scholar
  212. Wächtershäuser G (1990a) Evolution of the first metabolic cycles. Proc Natl Acad Sci U S A 87(1):200–204PubMedPubMedCentralCrossRefGoogle Scholar
  213. Wächtershäuser G (1990b) The case for the chemoautotrophic origin of life in an iron-sulfur world. Orig Life Evol Biosph 20(2):173–176CrossRefGoogle Scholar
  214. Wächtershäuser G (1993) The cradle chemistry of life: on the origin of natural products in a pyrite-pulled chemoautotrophic origin of life. Pure Appl Chem 65(6):1343–1348CrossRefGoogle Scholar
  215. Warren PH (2011) Stable-isotopic anomalies and the accretionary assemblage of the Earth and Mars: a subordinate role for carbonaceous chondrites. Earth Planet Sci Lett 311:93–100CrossRefGoogle Scholar
  216. Weber AL (1995) Prebiotic polymerization: oxidative polymerization of 2,3-dimercapto-l-propanol on the surface of iron(III) hydroxide oxide. Orig Life Evol Biosph 25(1–3):53–60PubMedCrossRefGoogle Scholar
  217. Willbold M, Elliot T, Moorbath S (2011) The tungsten isotopic composition of the Earth’s mantle before the terminal bombardment. Nature 477:195–198PubMedCrossRefGoogle Scholar
  218. Willbold M, Mojzsis SJ, Chen HW et al (2015) Tungsten isotope composition of the Acasta Gneiss Complex. Earth Planet Sci Lett 419:168–177CrossRefGoogle Scholar
  219. Young ED, Kohl IE, Warren PH et al (2016) Oxygen isotopic evidence for vigorous mixing during the Moon-forming giant impact. Science 351:493–496PubMedCrossRefGoogle Scholar
  220. Yuasa S, Flory D, Basile B et al (1984) Abiotic synthesis of purines and other heterocyclic compounds by the action of electrical discharges. J Mol Evol 21:76–80PubMedCrossRefGoogle Scholar
  221. Zhang J, Dauphas N, Davis AM et al (2012) The proto-Earth as a significant source of lunar material. Nat Geosci 5:251–255CrossRefGoogle Scholar
  222. Zhang S, Blain JC, Zielinska D et al (2013) Fast and accurate nonenzymatic copying of an RNA-like synthetic genetic polymer. Proc Natl Acad Sci U S A 110(44):17732–17737PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Steven A. Benner
    • 1
    • 2
    • 3
  • Hyo-Joong Kim
    • 1
    • 2
    • 3
  • Elisa Biondi
    • 1
    • 2
    • 3
    Email author
  1. 1.The Westheimer Institute for Science and TechnologyGainesvilleUSA
  2. 2.Firebird Biomolecular Sciences LLCAlachuaUSA
  3. 3.The Foundation for Applied Molecular EvolutionAlachuaUSA

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