It has been four decades since formamide was first suggested to perform roles as a precursor and/or a solvent in prebiotic chemistry. However, little work has sought to integrate formamide into larger prebiotic schemes that might create prebiotic RNA, often proposed to have been the first Darwinian biopolymer. Here, we report that formamide can be used as a solvent to perform the Bílik reaction, which uses molybdenum(VI) oxo species as catalysts at near-neutral pH to rearrange branched carbohydrates to give linear carbohydrates; the branched carbohydrates are produced from formaldehyde (HCHO) in alkaline mixtures containing borate, whereas the linear carbohydrates are the precursors needed for ribonucleosides and ribonucleotides. Under conditions wherein the Bílik reaction does this rearrangement, carbohydrate reaction products do not require stabilization by borate. These results, therefore, connect aqueous and formamide-based processes for the prebiotic formation of RNA components. Based on data from Hadean zircons that show that the mantle of the early Earth was near the fayalite-quartz-magnetite fugacity, molybdenum in its 6+ oxidation state was likely available in the Hadean. Together, these allow us to conjecture a process that delivers ribonucleosides and ribonucleotides from hydrogen cyanide and HCHO from a Hadean atmosphere on a Hadean geosphere, without needing precisely timed transitions from one solvent system to the other.
Get full access to this article
View all access options for this article.
References
1.
AbeY., TakizawaT., and KuniedaT. (1980) Epimerization of aldoses catalyzed by dioxobis(2,4-pentanedionato-O,O')molybdenum(VI). An improved procedure for C-2 epimer preparation. Chem Pharm Bull, 28:1324–1326.
2.
AngyalS.J. (2001) The Lobry de Bruyn-Alberda Van Ekenstein transformation and related reactions. In Glycoscience: Epimerisation, Isomerisation and Rearrangement Reactions of Carbohydrates, edited by StützA.E., Springer, Berlin, Vol 215, pp 1–14.
3.
ArrheniusG., BladridgeK.K., Richards-GrossS., and SiegelJ.S. (1997) Glycolonitrile oligomerization: structure of isolated oxazolines, potential heterocycles on the early earth. J Org Chem, 62:5522–5525.
4.
BadaJ.L., ChalmersJ.H., and CleavesH.J. (2016) Is formamide a geochemically plausible prebiotic solvent?. Phys Chem Chem Phys, 18:20085–20090.
5.
BeckerS., ThomaI., DeutschA., GehrkeT., MayerP., ZipseH., and CarellT. (2016) A high-yielding, strictly regioselective prebiotic purine nucleoside formation pathway. Science, 352:833–836.
6.
BennerS.A., RicardoA., and CarriganM.A. (2004) Is there a common chemical model for life in the universe?. Curr Opin Chem Biol, 8:672–689.
7.
BennerS.A., KimH.J., and CarriganM.A. (2012) Asphalt, water, and the prebiotic synthesis of ribose, ribonucleosides, and RNA. Acc Chem Res, 45:2025–2034.
8.
BílikV. and CaplovicJ. (1973) Reactions of saccharides catalyzed by molybdate ions. VII. Preparation of l-ribose, d-, and l-lyxose. Chem Papers, 27:547–550.
9.
BílikV., JurčováE., and SutorisV. (1978a) Reactions of saccharides catalyzed by molybdate ions. XX. Preparation of epilactose and epimaltose. Chem Papers, 32:252–257.
10.
BílikV., PetrusL., and FarkasV. (1978b) Reactions of saccharides catalyzed by molybdate ions; Part XXVI. Preparation of D-[U-14C]-aldopentoses from any D-[U-14C]-aldopentose. Coll Czech Chem Comm, 43:1163–1166.
11.
BorisovA.A. (2016) Mutual interaction of redox pairs in silicate melts: equilibria involving metallic phases. Petrology, 24:117–126.
12.
BurcarB., PasekM., GullM., CaffertyB.J., VelascoF., HudN.V., and Menor‐SalvánC. (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, 55:13249–13253.
13.
CleavesH.J. (2008) The prebiotic geochemistry of formaldehyde. Precambrian Res, 164:111–118.
14.
GendaH., BrasserR., and MojzsisS.J. (2017) The terrestrial late veneer from core disruption of a lunar-sized impactor. Earth Planet Sci Lett, 480:25–32.
15.
GorshkovaR.P., IsakovV.V., KalmykovaE.N., and OvodovY.S. (1995) Structural studies of O-specific polysaccharide chains of the lipopolysaccharide from Yersinia enterocolitica serovar O:10. Carbohydr Res, 268:249–255.
16.
GottliebH.E., KotlyarV., and NudelmanA. (1997) NMR chemical shifts of common laboratory solvents as trace impurities. J Org Chem, 62:7512–7515.
17.
HayesM.L., PenningsN.J., SerianniA.S., and BarkerR. (1982) Epimerization of aldoses by molybdate involving a novel rearrangement of the carbon skeleton. J Am Chem Soc, 104:6764–6769.
18.
HazenR. (2017) Assessing the paleomineralogy of the Hadean Eon. In XVIIIth Conference of the International Society for the Study of the Origins of Life. San Diego, CA.
19.
HazenR.M., LiuX.-M., DownsR.T., GoldenJ., PiresA.J., GrewE.S., HystadG., EstradaC., and SverjenskyD.A. (2013) Mineral evolution: episodic metallogenesis, the supercontinent cycle, and the coevolving geosphere and biosphere. Econ Geol Spec Pub, 18:1–15.
20.
HiroshiN., TakeshiT., and MasahikoH. (1985) A process for the production of a d-ribose-containing solution. German Patent. DE3437571A1.
21.
JoyceG. and OrgelL.E. (1999) Prospects for understanding the origin of the RNA world. In The RNA World, 2nd ed., edited by GestlandR.F., CechT.R, and AtkinsJ.F., Cold Spring Harbor Press, Cold Spring Harbor, NY, pp 49–78.
22.
KeefeA.D. and MillerS.L. (1996) Was ferrocyanide a prebiotic reagent?. Orig Life Evol Biosph, 26:111–129.
23.
KimH.J. and BennerS.A. (2017) Prebiotic stereoselective synthesis of purine and noncanonical pyrimidine nucleotide from nucleobases and phosphorylated carbohydrates. Proc Natl Acad Sci U S A, 114:11315–11320.
24.
KimH.-J. and BennerS.A. (2018) A direct prebiotic synthesis of nicotinamide nucleotide. Chemistry, 24:581–584.
25.
KimH.-J., RicardoA., IllangkoonH.I., KimM.J., CarriganM.A., FryeF., and BennerS.A. (2011) Synthesis of carbohydrates in mineral-guided prebiotic cycles. J Am Chem Soc, 133:9457–9468.
26.
KimH.J., FurukawaY., KakegawaT., BitaA., ScoreiR., and BennerS.A. (2016) Evaporite borate-containing mineral ensembles make phosphate available and regiospecifically phosphorylate ribonucleosides: borate as a multifaceted problem solver in prebiotic chemistry. Angew Chem, 55:15816–15820.
27.
KrishnamurthyR., GunthaS., and EschenmoserA. (2000) Regioselective α‐phosphorylation of aldoses in aqueous solution. Angew Chem Int Ed, 39:2281–2285.
28.
KuaJ. and ThrushK.L. (2016) HCN, formamidic acid, and formamide in aqueous solution: a free-energy map. J Phys Chem B, 120:8175–8185.
29.
LapenT.J., RighterM., BrandonA.D., DebailleV., BeardB.L., ShaferJ.T., and PeslierA.H. (2010) A younger age for ALH84001 and its geochemical link to shergottite sources in Mars. Science, 328:347–351.
30.
LiebmanS.A., Pesce-RodriguezR.A., and MatthewsC.N. (1995) Organic analysis of hydrogen cyanide polymers: prebiotic and extraterrestrial chemistry. Adv Space Res, 15:71–80.
31.
NamI., NamH.G., and ZareR.N. (2018) Abiotic synthesis of purine and pyrimidine ribonucleosides in aqueous microdroplets. Proc Natl Acad Sci U S A, 115:36–40.
32.
NeveuM., KimH.-J., and BennerS.A. (2013) The “Strong” RNA World hypothesis. Fifty years old. Astrobiology, 13:391–403.
33.
PatelB.H., PercivalleC., RitsonD.J., DuffyC.D., and SutherlandJ.D. (2015) Common origins of RNA, protein and lipid precursors in a cyanosulfidic protometabolism. Nat Chem, 7:301–307.
34.
PetrušL., PetrusovaM., and HricoviniovaZ. (2001) The Bílik reaction. In Glycoscience: Epimerisation, Isomerisation and Rearrangement Reactions of Carbohydrates, edited by StützA.E., Springer, Berlin, pp 15–45.
35.
PownerM.W., GerlandB., and SutherlandJ.D. (2009) Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature, 459:239–242.
36.
RicardoA., CarriganA., OlcottA., and BennerS. (2004) Borate minerals stabilize ribose. Science, 303:196–196.
37.
RighterK., DanielsonL.R., PandoK.M., WilliamsJ., HumayunM., HervigR.L., and SharpT.G. (2015) Highly siderophile element (HSE) abundances in the mantle of Mars are due to core formation at high pressure and temperature. Meteorit Planet Sci, 50:604–631.
38.
RotelliL., Trigo-RodriguezJ.M., Moyano-CamberoC.E., CarotaE., BottaL., Di MauroE., and SaladinoR. (2016) The key role of meteorites in the formation of relevant prebiotic molecules in a formamide/water environment. Sci Rep, 6:38888.
39.
SaladinoR., CrestiniC., CostanzoG., NegriR., and Di MauroE. (2001) A possible prebiotic synthesis of purine, adenine, cytosine, and 4(3H)-pyrimidinone from formamide. Implications for the origin of life. Bioorg Med Chem, 9:1249–1253.
40.
SaladinoR., BarontiniM., CossettiC., Di MauroE., and CrestiniC. (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, 41:317–330.
41.
SaladinoR., CrestiniC., PinoS., CostanzoG., and Di MauroE. (2012) Formamide and the origin of life. Phys Life Rev, 9:84–104.
42.
SaladinoR., CarotaE., BottaG., KapralovM., TimoshenkoG.N., RozanovA.Y., KrasavinE., and DiMauroE. (2015) Meteorite-catalyzed syntheses of nucleosides and of other prebiotic compounds from formamide under proton irradiation. Proc Natl Acad Sci U S A, 112:7109–7110.
43.
SchoffstallA.M. (1976) Prebiotic phosphorylation of nucleosides in formamide. Orig Life Evol Biosph, 7:399–412.
44.
SchoffstallA.M. and LaingE.M. (1985) Phosphorylation mechanisms in chemical evolution. Orig Life Evol Biosph, 15:141–150.
45.
SchoffstallA.M., BartoR.J., and RamosD.L. (1982) Nucleoside and deoxynucleoside phosphorylation in formamide solutions. Orig Life Evol Biosph, 12:143–151.
46.
SleepN.H., BirdD.K., and PopeE.C. (2011) Serpentinite and the dawn of life. Phil Trans Royal Soc B, 366:2857–2869.
47.
TrailD., WatsonE.B., and TailbyN.D. (2011) The oxidation state of Hadean magmas and implications for early Earth's atmosphere. Nature, 480:79–82.
48.
UsuiT., YanagisawaS., OhguchiM., YoshinoM., KawabataR., KishimotoJ., AraiY., AidaK., WatanabeH., and HayaseF. (2007) Identification and determination of α-dicarbonyl compounds formed in the degradation of sugars. Biosci Biotechnol Biochem, 71:2465–2472.
49.
YamadaH., HirobeM., HigashiyamaK., TakahashiH., and SuzukiK.T. (1978a) Detection of carbon-13-nitrogen-15 coupled units in adenine derived from doubly labeled hydrogen cyanide or formamide. J Am Chem Soc, 100:4617–4618.
50.
YamadaH., HirobeM., HigashiyamaK., TakahashiH., and SuzukiK.T. (1978b) Reaction mechanism for purine ring formation as studied by carbon-13-nitrogen-15 coupling. Tetrahedron Lett, 42:4039–4042.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
