Crystallization as a selection force at the polymerization of nucleotides in a prebiotic context
Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
37664611
PubMed Central
PMC10470394
DOI
10.1016/j.isci.2023.107600
PII: S2589-0042(23)01677-2
Knihovny.cz E-zdroje
- Klíčová slova
- Biochemistry, Biological sciences, Natural sciences,
- Publikační typ
- časopisecké články MeSH
Accumulation and selection of nucleotides is one of the most challenging problems surrounding the origin of the first RNA molecules on our planet. In the current work we propose that guanosine 3',5' cyclic monophosphate could selectively crystallize upon evaporation of an acidic prebiotic pool containing various other nucleotides. The conditions of the evaporative crystallization are fully compatible with the subsequent acid catalyzed polymerization of this cyclic nucleotide reported in earlier studies and may be relevant in a broad range of possible prebiotic environments. Albeit cytidine 3',5' cyclic monophosphate has the ability to selectively accumulate under the same conditions, its crystal structure is not likely to support polymer formation.
Institute of Biophysics of the Czech Academy of Sciences Královopolská 135 61200 Brno Czech Republic
TESCAN Brno s r o Libušina třída 1 62300 Brno Czech Republic
University of Wrocław Faculty of Chemistry 14 F Joliot Curie 50 383 Wrocław Poland
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Yu L., Reutzel-Edens S.M., Mitchell C.A. Crystallization and polymorphism of conformationally flexible molecules: problems, patterns, and strategies. Org. Process Res. Dev. 2000;4:396–402. doi: 10.1021/op000028v. DOI
Tang N., Wang X., Du W., Zhang L., Xiang J., Wang S., Cheng P., Zhu L., Yin Q. Conformational flexibility and crystallization: the case of furosemide. Cryst. Growth Des. 2019;19:2050–2059. doi: 10.1021/acs.cgd.8b01407. DOI
Bensouissi A., Roge B., Mathlouthi M. Effect of conformation and water interactions of sucrose, maltitol, mannitol and xylitol on their metastable zone width and ease of nucleation. Food Chem. 2010;122:443–446. doi: 10.1016/j.foodchem.2009.03.075. DOI
Hursthouse M.B., Huth L.S., Threlfall T.L. Why do organic compounds crystallise well or badly or ever so slowly? Why is crystallisation nevertheless such a good purification technique? Org. Process Res. Dev. 2009;13:1231–1240. doi: 10.1021/op900169b. DOI
Powner M.W., Zheng S.L., Szostak J.W. Multicomponent assembly of proposed DNA precursors in water. J. Am. Chem. Soc. 2012;134:13889–13895. doi: 10.1021/ja306176n. PubMed DOI PMC
Marinova V., Wood G.P.F., Marziano I., Salvalaglio M. Dynamics and thermodynamics of ibuprofen conformational isomerism at the crystal/solution interface. J. Chem. Theor. Comput. 2018;14:6484–6494. doi: 10.1021/acs.jctc.8b00702. PubMed DOI
Smith G.P., Fraccia T.P., Todisco M., Zanchetta G., Zhu C., Hayden E., Bellini T., Clark N.A. Backbone-free duplex-stacked monomer nucleic acids exhibiting Watson–Crick selectivity. Proc. Natl. Acad. Sci. USA. 2018;115:E7658–E7664. doi: 10.1073/pnas.1721369115. PubMed DOI PMC
Jia T.Z., Bellini T., Clark N., Fraccia T.P. A liquid crystal world for the origins of life. Emerg. Top. Life Sci. 2022;6:557–569. doi: 10.1042/etls20220081. PubMed DOI
Deamer D. Liquid crystalline nanostructures: organizing matrices for non-enzymatic nucleic acid polymerization. Chem. Soc. Rev. 2012;41:5375–5379. doi: 10.1039/C2CS35042D. PubMed DOI
Himbert S., Chapman M., Deamer D.W., Rheinstädter M.C. Organization of nucleotides in different environments and the formation of pre-polymers. Sci. Rep. 2016;6 doi: 10.1038/srep31285. PubMed DOI PMC
Nakata M., Zanchetta G., Chapman B.D., Jones C.D., Cross J.O., Pindak R., Bellini T., Clark N.A. End-to-end stacking and liquid crystal condensation of 6- to 20-base pair DNA duplexes. Science. 2007;318:1276–1279. doi: 10.1126/science.1143826. PubMed DOI
Todisco M., Fraccia T.P., Smith G.P., Corno A., Bethge L., Klussmann S., Paraboschi E.M., Asselta R., Colombo D., Zanchetta G., et al. Nonenzymatic polymerization into long linear RNA templated by liquid crystal self-assembly. ACS Nano. 2018;12:9750–9762. doi: 10.1021/acsnano.8b05821. PubMed DOI
Hassenkam T., Deamer D. Visualizing RNA polymers produced by hot wet-dry cycling. Sci. Rep. 2022;12 doi: 10.1038/s41598-022-14238-2. PubMed DOI PMC
Ferris J.P., Hill A.R., Liu R., Orgel L.E. Synthesis of long prebiotic oligomers on mineral surfaces. Nature. 1996;381:59–61. doi: 10.1038/381059a0. PubMed DOI
Martra G., Deiana C., Sakhno Y., Barberis I., Fabbiani M., Pazzi M., Vincenti M. The formation and self-assembly of long prebiotic oligomers produced by the condensation of unactivated amino acids on oxide surfaces. Angew. Chem. Int. Ed. 2014;53:4671–4674. doi: 10.1002/anie.201311089. PubMed DOI
Hansma H.G. Possible origin of life between mica sheets. J. Theor. Biol. 2010;266:175–188. doi: 10.1016/j.jtbi.2010.06.016. PubMed DOI
Sakhno Y., Battistella A., Mezzetti A., Jaber M., Georgelin T., Michot L., Lambert J.-F. One step up the ladder of prebiotic complexity: formation of nonrandom linear polypeptides from binary systems of amino acids on silica. Chem. Eur J. 2019;25:1275–1285. doi: 10.1002/chem.201803845. PubMed DOI
Olasagasti F., Rajamani S. Lipid-assisted polymerization of nucleotides. Life. 2019;9:83. doi: 10.3390/life9040083. PubMed DOI PMC
Toppozini L., Dies H., Deamer D.W., Rheinstädter M.C. Adenosine monophosphate forms ordered arrays in multilamellar lipid matrices: insights into assembly of nucleic acid for primitive life. PLoS One. 2013;8 doi: 10.1371/journal.pone.0062810. PubMed DOI PMC
Rajamani S., Vlassov A., Benner S., Coombs A., Olasagasti F., Deamer D. Lipid-assisted synthesis of RNA-like polymers from mononucleotides. Orig. Life Evol. Biosph. 2008;38:57–74. doi: 10.1007/s11084-007-9113-2. PubMed DOI
Hulshof J., Ponnamperuma C. Prebiotic condensation reactions in an aqueous medium: a review of condensing agents. Orig. Life. 1976;7:197. doi: 10.1007/BF00926938. PubMed DOI
Kruse F.M., Teichert J.S., Trapp O. Prebiotic nucleoside synthesis: the selectivity of simplicity. Chem. Eur J. 2020;26:14776–14790. doi: 10.1002/chem.202001513. PubMed DOI PMC
Pasek M.A., Gull M., Herschy B. Phosphorylation on the early earth. Chem. Geol. 2017;475:149–170. doi: 10.1016/j.chemgeo.2017.11.008. DOI
Yadav M., Kumar R., Krishnamurthy R. Chemistry of abiotic nucleotide synthesis. Chem. Rev. 2020;120:4766–4805. doi: 10.1021/acs.chemrev.9b00546. PubMed DOI
Benner S.A., Kim H.-J., Carrigan M.A. Asphalt, water, and the prebiotic synthesis of ribose, ribonucleosides, and RNA. Acc. Chem. Res. 2012;45:2025–2034. doi: 10.1021/ar200332w. PubMed DOI
Benner S.A., Kim H.J., Yang Z. Setting the stage: the history, chemistry, and geobiology behind RNA. Cold Spring Harbor Perspect. Biol. 2012;4:a003541. doi: 10.1101/cshperspect.a003541. PubMed DOI PMC
Kaupp G. Waste-free synthesis and production all across chemistry with the benefit of self-assembled crystal packings. J. Phys. Org. Chem. 2008;21:630–643. doi: 10.1002/poc.1340. DOI
de Herrera A.G., Markert T., Trixler F. Temporal nanofluid environments induce prebiotic condensation in water. Commun. Chem. 2023;6:69. doi: 10.1038/s42004-023-00872-y. PubMed DOI PMC
Hassenkam T., Damer B., Mednick G., Deamer D. AFM images of viroid-sized rings that self-assemble from mononucleotides through wet–dry cycling: implications for the origin of life. Life. 2020;10:321. https://www.mdpi.com/2075-1729/10/12/321# PubMed PMC
DeGuzman V., Vercoutere W., Shenasa H., Deamer D. Generation of oligonucleotides under hydrothermal conditions by non-enzymatic polymerization. J. Mol. Evol. 2014;78:251–262. doi: 10.1007/s00239-014-9623-2. PubMed DOI
Da Silva L., Maurel M.C., Deamer D. Salt-promoted synthesis of RNA-like molecules in simulated hydrothermal conditions. J. Mol. Evol. 2015;80:86–97. doi: 10.1007/s00239-014-9661-9. PubMed DOI
Wunnava S., Dirscherl C.F., Výravský J., Kovařík A., Matyášek R., Šponer J., Braun D., Šponer J.E. Acid-catalyzed RNA-oligomerization from 3’,5’-cGMP. Chem. Eur J. 2021;27:17581–17585. doi: 10.1002/chem.202103672. PubMed DOI PMC
Mungi C.V., Bapat N.V., Hongo Y., Rajamani S. Formation of abasic oligomers in nonenzymatic polymerization of canonical nucleotides. Life. 2019;9:57. doi: 10.3390/life9030057. PubMed DOI PMC
Verlander M.S., Lohrmann R., Orgel L.E. Catalysts for self-polymerization of adenosine cyclic 2', 3'-phosphate. J. Mol. Evol. 1973;2:303–316. doi: 10.1007/bf01654098. PubMed DOI
Tapiero C.M., Nagyvary J. Prebiotic formation of cytidine nucleotides. Nature. 1971;231:42–43. doi: 10.1038/231042a0. PubMed DOI
Costanzo G., Pino S., Ciciriello F., Di Mauro E. Generation of long RNA chains in water. J. Biol. Chem. 2009;284:33206–33216. doi: 10.1074/jbc.M109.041905. PubMed DOI PMC
Costanzo G., Saladino R., Botta G., Giorgi A., Scipioni A., Pino S., Di Mauro E. Generation of RNA molecules by a base-catalysed click-like reaction. Chembiochem. 2012;13:999–1008. doi: 10.1002/cbic.201200068. PubMed DOI
Morasch M., Mast C.B., Langer J.K., Schilcher P., Braun D. Dry polymerization of 3 ', 5 '-cyclic GMP to long strands of RNA. Chembiochem. 2014;15:879–883. doi: 10.1002/cbic.201300773. PubMed DOI
Dass A.V., Wunnava S., Langlais J., von der Esch B., Krusche M., Ufer L., Chrisam N., Dubini R.C.A., Gartner F., Angerpointner S., et al. RNA oligomerisation without added catalyst from 2′,3′-cyclic nucleotides by drying at air-water interfaces. ChemSystemsChem. 2023;5 doi: 10.1002/syst.202200026. DOI
Dirscherl C.F., Ianeselli A., Tetiker D., Matreux T., Queener R.M., Mast C.B., Braun D. A heated rock crack captures and polymerizes primordial DNA and RNA. Phys. Chem. Chem. Phys. 2023;25:3375–3386. doi: 10.1039/D2CP04538A. PubMed DOI
Tekin E., Salditt A., Schwintek P., Wunnava S., Langlais J., Saenz J., Tang D., Schwille P., Mast C., Braun D. Prebiotic foam environments to oligomerize and accumulate RNA. Chembiochem. 2022;23 doi: 10.1002/cbic.202200423. PubMed DOI PMC
Shabarova Z., Bogdanov A. VCH Verlagsgesellshaft); 1994. Advanced Organic Chemistry of Nucleic Acids.
Šponer J.E., Šponer J., Výravský J., Šedo O., Zdráhal Z., Costanzo G., Di Mauro E., Wunnava S., Braun D., Matyášek R., Kovařík A. Nonenzymatic, template-free polymerization of 3’,5’ cyclic guanosine monophosphate on mineral surfaces. ChemSystemsChem. 2021;3 doi: 10.1002/syst.202100017. DOI
Šponer J.E., Šponer J., Giorgi A., Di Mauro E., Pino S., Costanzo G. Untemplated nonenzymatic polymerization of 3 ',5 ' cGMP: a plausible route to 3 ',5 '-linked oligonucleotides in primordia. J. Phys. Chem. B. 2015;119:2979–2989. doi: 10.1021/acs.jpcb.5b00601. PubMed DOI
Šponer J.E., Šponer J., Di Mauro E. New evolutionary insights into the non-enzymatic origin of RNA oligomers. Wiley Interdiscip. Rev. RNA. 2017;8 doi: 10.1002/wrna.1400. PubMed DOI
Usher D.A., Yee D. Geometry of the dry-state oligomerization of 2',3'-cyclic phosphates. J. Mol. Evol. 1979;13:287–293. doi: 10.1007/bf01731369. PubMed DOI
Chandrasekhar S., Naik T.R.R., Nayak S.K., Row T.N.G. Crystal structure of an intermolecular 2:1 complex between adenine and thymine. Evidence for both Hoogsteen and 'quasi-Watson-Crick' interactions. Bioorg. Med. Chem. Lett. 2010;20:3530–3533. doi: 10.1016/j.bmcl.2010.04.131. PubMed DOI
Katz L., Tomita K., Rich A. The crystal structure of the intermolecular complex 9-ethyladenine: 1-methyl-5-bromouracil. Acta Crystallogr. 1966;21:754–764. doi: 10.1107/S0365110X66003815. PubMed DOI
Sakore T.D., Tavale S.S., Sobell H.M. Base-pairing configurations between purines and pyrimidines in the solid state: I. Crystal and molecular structure of a 1:2 purine-pyrimidine hydrogen-bonded complex: 9-ethyladenine-1-methyl-5-iodouracil. J. Mol. Biol. 1969;43:361–374. doi: 10.1016/0022-2836(69)90346-5. PubMed DOI
Fujita S., Takenaka A., Sasada Y. Model for interactions of amino acid side chains with Watson-Crick base pair of guanine and cytosine: crystal structure of 9-(2-carbamoylethyl)guanine and 1-methylcytosine complex. Biochemistry. 1985;24:508–512. doi: 10.1021/bi00323a039. PubMed DOI
O'Brien E.J. Crystal structures of two complexes containing guanine and cytosine derivatives. Acta Crystallogr. 1967;23:92–106. doi: 10.1107/S0365110X67002191. PubMed DOI
Ślepokura K.A. Purine 3’:5’-cyclic nucleotides with the nucleobase in a syn orientation: cAMP, cGMP and cIMP. Acta Crystallogr. C. 2016;72:465–479. doi: 10.1107/S2053229616006999. PubMed DOI
Chwang A.K., Sundaralingam M. The crystal and molecular structure of guanosine 3’,5’-cyclic monophosphate (cyclic GMP) sodium tetrahydrate. Acta Crystallogr. B. 1974;30:1233–1240. doi: 10.1107/S0567740874004602. DOI
Zirbel C.L., Šponer J.E., Šponer J., Stombaugh J., Leontis N.B. Classification and energetics of the base-phosphate interactions in RNA. Nucleic Acids Res. 2009;37:4898–4918. doi: 10.1093/nar/gkp468. PubMed DOI PMC
Westhof E., Fritsch V. RNA folding: beyond Watson–Crick pairs. Structure. 2000;8:R55–R65. doi: 10.1016/S0969-2126(00)00112-X. PubMed DOI
Fraccia T.P., Smith G.P., Zanchetta G., Paraboschi E., Yi Y., Walba D.M., Dieci G., Clark N.A., Bellini T. Abiotic ligation of DNA oligomers templated by their liquid crystal ordering. Nat. Commun. 2015;6:6424. doi: 10.1038/ncomms7424. PubMed DOI PMC
Gellert M., Lipsett M.N., Davies D.R. Helix formation by guanylic acid. Proc. Natl. Acad. Sci. USA. 1962;48:2013–2018. doi: 10.1073/pnas.48.12.2013. PubMed DOI PMC
Chantot J.F., Sarocchi M.T., Guschlbauer W. Physico-chemical properties of nucleosides. 4. Gel formation by quanosine and its analogues. Biochimie. 1971;53:347–354. doi: 10.1016/s0300-9084(71)80101-3. PubMed DOI
Albert A., Brown D.J. Purine studies. Part I. Stability to acid and alkali. Solubility. Ionization. Comparison with pteridines. J. Chem. Soc. 1954:2060–2071. doi: 10.1039/JR9540002060. DOI
Schroeder R., Barta A., Semrad K. Strategies for RNA folding and assembly. Nat. Rev. Mol. Cell Biol. 2004;5:908–919. doi: 10.1038/nrm1497. PubMed DOI
Costanzo G., Šponer J.E., Šponer J., Cirigliano A., Benedetti P., Giliberti V., Polito R., Di Mauro E. Sustainability and chaos in the abiotic polymerization of 3’,5’ cyclic guanosine monophosphate: the role of aggregation. ChemSystemsChem. 2021;3 doi: 10.1002/syst.202000056. DOI
Soukup G.A., Breaker R.R. Relationship between internucleotide linkage geometry and the stability of RNA. RNA. 1999;5:1308–1325. doi: 10.1017/s1355838299990891. PubMed DOI PMC
Parthasarathy R., Srikrishnan T. Cytidine cyclic (3′, 5′) monophosphate: cyclic nucleotide with a non-characteristic ribose ring conformation. Nucleosides Nucleotides. 1997;16:1967–1981. doi: 10.1080/07328319708002548. DOI
Sheldrick G.M. SHELXT - Integrated space-group and crystal-structure determination. Acta Crystallogr. A. 2015;71:3–8. doi: 10.1107/S2053273314026370. PubMed DOI PMC
Sheldrick G.M. Crystal structure refinement with SHELXL. Acta Crystallogr. C. 2015;71:3–8. doi: 10.1107/S2053229614024218. PubMed DOI PMC
Degen T., Sadki M., Bron E., König U., Nénert G. The HighScore suite. Powder Diffr. 2014;29:S13–S18. doi: 10.1017/S0885715614000840. DOI
Brandenburg K. 2022. DIAMOND Version 4.6.8, Crystal Impact GbR.
CrysAlisPro Software System. Rigaku Oxford Diffraction; 2020.
Groom C.R., Bruno I.J., Lightfoot M.P., Ward S.C. The Cambridge Structural Database. Acta Crystallogr. B. 2016;72:171–179. doi: 10.1107/s2052520616003954. PubMed DOI PMC