Prebiotic chemists often study how modern biopolymers, e.g., peptides and nucleic acids, could have originated in the primitive environment, though most contemporary biomonomers don't spontaneously oligomerize under mild conditions without activation or catalysis. However, life may not have originated using the same monomeric components that it does presently. There may be numerous non-biological (or "xenobiological") monomer types that were prebiotically abundant and capable of facile oligomerization and self-assembly. Many modern biopolymers degrade abiotically preferentially via processes which produce thermodynamically stable ring structures, e.g. diketopiperazines in the case of proteins and 2', 3'-cyclic nucleotide monophosphates in the case of RNA. This weakness is overcome in modern biological systems by kinetic control, but this need not have been the case for primitive systems. We explored here the oligomerization of a structurally diverse set of prebiotically plausible xenobiological monomers, which can hydrolytically interconvert between cyclic and acyclic forms, alone or in the presence of glycine under moderate temperature drying conditions. These monomers included various lactones, lactams and a thiolactone, which varied markedly in their stability, propensity to oligomerize and apparent modes of initiation, and the oligomeric products of some of these formed self-organized microscopic structures which may be relevant to protocell formation.

Blue Marble Space Institute for Science 1001 4th Ave Suite 3201 Seattle WA 98154 USA

Department of Physical Chemistry University of Chemistry and Technology Prague Technicka 5 16628 Prague 6 Dejvice Czech Republic

Earth Life Science Institute Tokyo Institute of Technology 2 12 1 IE 1 Ookayama Meguro ku Tokyo 152 8550 Japan

Indian Institute of Science Education and Research Dr Homi Bhabha Road Pashan Pune Maharashtra 411 008 India

Institute for Advanced Study 1 Einstein Drive Princeton NJ 08540 USA

Space Science Center Institute of Climate Change Level 3 Research Complex National University of Malaysia UKM 43600 Bangi Selangor Malaysia

Zobrazit více v PubMed

Oparin AI. Proischogdenie zhizni. Moscow: Moscovsky Robotchii; 1924.

Haldane, J. B. S. The Origin of Life. The Rationalist Annual 3–10 (1929).

Miller SL, Orgel LE. The Origins of Life on the Earth. Upper Saddle River: Prentice-Hall; 1974.

Lowe CU, Rees MW, Markham R. Synthesis of complex organic compounds from simple precursors: Formation of amino-acids, amino-acid polymers, fatty acids and purines from ammonium cyanide. Nature. 1963;199:219–222. doi: 10.1038/199219a0. PubMed DOI

Ferris JP, Joshi PC, Edelson EH, Lawless JG. HCN: A plausible source of purines, pyrimidines and amino acids on the primitive earth. J. Mol. Evol. 1978;11:293–311. doi: 10.1007/BF01733839. PubMed DOI

Orgel LE. The origin of life - a review of facts and speculations. Trends Biochem. Sci. 1998;23:491–495. doi: 10.1016/S0968-0004(98)01300-0. PubMed DOI

Bernstein M. Prebiotic materials from on and off the early Earth. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2006;361:1689–1702. doi: 10.1098/rstb.2006.1913. PubMed DOI PMC

Cleaves HJ, Lazcano A. The origin of biomolecules. In: Zaikowski L, Friedrich JM, Seidel SR, editors. Chemical Evolution II: From Origins of Life to Modern Society. Oxford: Oxford University Press; 2009. pp. 17–43.

Brack A. From interstellar amino acids to prebiotic catalytic peptides: A review. Chem. Biodivers. 2007;4:665–679. doi: 10.1002/cbdv.200790057. PubMed DOI

Patel BH, Percivalle C, Ritson DJ, Duffy CD, Sutherland JD. Common origins of RNA, protein and lipid precursors in a cyanosulfidic protometabolism. Nat. Chem. 2015;7:301. doi: 10.1038/nchem.2202. PubMed DOI PMC

Schwartz AW, Bakker CG. Was adenine the first purine? Science. 1989;245:1102–1104. doi: 10.1126/science.11538344. PubMed DOI

Johnson AP, et al. The Miller volcanic spark discharge experiment. Science. 2008;322:404. doi: 10.1126/science.1161527. PubMed DOI

Cleaves HJ. Prebiotic chemistry: What we know, what we don’t. Evol. Educ. Outreach. 2012;5:342–360. doi: 10.1007/s12052-012-0443-9. DOI

Schwartz AW. Intractable mixtures and the origin of life. Chem. Biodivers. 2007;4:656–664. doi: 10.1002/cbdv.200790056. PubMed DOI

Schmitt-Kopplin P, et al. High molecular diversity of extraterrestrial organic matter in Murchison meteorite revealed 40 years after its fall. Proc. Natl. Acad. Sci. 2010;107:2763–2768. doi: 10.1073/pnas.0912157107. PubMed DOI PMC

Guttenberg N, Virgo N, Chandru K, Scharf C, Mamajanov I. Bulk measurements of messy chemistries are needed for a theory of the origins of life. Philos. Trans. R. Soc. A. Math. Phys. Eng. Sci. 2017;375:2. PubMed PMC

Segré D, Ben-Eli D, Lancet D. Compositional genomes: Prebiotic information transfer in mutually catalytic noncovalent assemblies. Proc. Natl. Acad. Sci. 2000;97:4112–4117. doi: 10.1073/pnas.97.8.4112. PubMed DOI PMC

Hunding A, et al. Compositional complementarity and prebiotic ecology in the origin of life. BioEssays. 2006;28:399–412. doi: 10.1002/bies.20389. PubMed DOI

Shapiro R. Small molecule interactions were central to the origin of life. Q. Rev. Biol. 2006;81:105–125. doi: 10.1086/506024. PubMed DOI

Kuriyan J, Konforti B, Wemmer D. The Molecules of Life: Physical and Chemical Principles. New York: Garland Science; 2012.

Dunn IS. Searching for molecular solutions: empirical discovery and its future. New York: John Wiley & Sons; 2010.

Ross DS, Deamer D. Dry/wet cycling and the thermodynamics and kinetics of prebiotic polymer synthesis. Life. 2016;6:2. doi: 10.3390/life6030028. PubMed DOI PMC

Imai E, Honda H, Hatori K, Brack A, Matsuno K. Elongation of oligopeptides in a simulated submarine hydrothermal system. Science. 1999;283:831–833. doi: 10.1126/science.283.5403.831. PubMed DOI

Cleaves HJ, Aubrey AD, Bada JL. An evaluation of the critical parameters for abiotic peptide synthesis in submarine hydrothermal systems. Orig. Life Evol. Biosph. 2009;39:109–126. doi: 10.1007/s11084-008-9154-1. PubMed DOI

Schneider-Bernloehr H, Lohrmann R, Orgel LE, Sulston J, Weimann BJ. Partial resolution of DL-adenosine by template synthesis. Science. 1968;162:809–810. doi: 10.1126/science.162.3855.809. PubMed DOI

Weimann BJ, Lohrmann R, Orgel LE, Schneider-Bernloehr H, Sulston JE. Template-directed synthesis with adenosine-5’-phosphorimidazolide. Science. 1968;161:387. doi: 10.1126/science.161.3839.387. PubMed DOI

Fox SW, Harada K. Thermal copolymerization of amino acids to a product resembling protein. Science. 1958;128:1214. doi: 10.1126/science.128.3333.1214. PubMed DOI

Ferris JP, Hill AR, Jr, Liu R, Orgel LE. Synthesis of long prebiotic oligomers on mineral surfaces. Nature. 1996;381:59–61. doi: 10.1038/381059a0. PubMed DOI

Surman AJ, et al. Environmental control programs the emergence of distinct functional ensembles from unconstrained chemical reactions. Proc. Natl. Acad. Sci. 2019;116:5387–5392. doi: 10.1073/pnas.1813987116. PubMed DOI PMC

Campbell TD, et al. Prebiotic condensation through wet–dry cycling regulated by deliquescence. Nat. Commun. 2019;10:4508. doi: 10.1038/s41467-019-11834-1. PubMed DOI PMC

Meggy AB. The free energy of formation of the amide bond in polyamides. J. Appl. Chem. 1954;4:154–159. doi: 10.1002/jctb.5010040402. DOI

Frey PA, Arabshahi A. Standard free energy change for the hydrolysis of the alpha, beta-phosphoanhydride bridge in ATP. Biochemistry. 1995;34:11307–11310. doi: 10.1021/bi00036a001. PubMed DOI

Vallentyne JR. Biogeochemistry of organic matter—II Thermal reaction kinetics and transformation products of amino compounds. Geochim. Cosmochim. Acta. 1964;28:157–188. doi: 10.1016/0016-7037(64)90147-4. DOI

White RH. Hydrolytic stability of biomolecules at high temperatures and its implication for life at 250 degrees C. Nature. 1984;310:430–432. doi: 10.1038/310430a0. PubMed DOI

Cleaves HJ, II, Chalmers JH. Extremophiles may be irrelevant to the origin of life. Astrobiology. 2004;4:1–9. doi: 10.1089/153110704773600195. PubMed DOI

Hall HK. Structural effects on the polymerization of lactams. J. Am. Chem. Soc. 1958;80:6404–6409. doi: 10.1021/ja01556a059. DOI

Hall HK, Schneider AK. Polymerization of cyclic esters, urethans, ureas and imides. J. Am. Chem. Soc. 1958;80:6409–6412. doi: 10.1021/ja01556a060. DOI

Li S, Vert M. Biodegradation of Aliphatic Polyesters. In: Scott G, editor. Degradable Polymers: Principles and Applications. Berlin: Springer; 2002. pp. 71–131.

Dechy-Cabaret O, Martin-Vaca B, Bourissou D. Controlled ring-opening polymerization of lactide and glycolide. Chem. Rev. 2004;104:6147–6176. doi: 10.1021/cr040002s. PubMed DOI

Verlander MS, Lohrmann R, Orgel LE. Catalysts for the self-polymerization of adenosine cyclic 2’, 3'-phosphate. J. Mol. Evol. 1973;2:303–316. doi: 10.1007/BF01654098. PubMed DOI

Verlander MS, Orgel LE. Analysis of high molecular weight material from the polymerization of adenosine cyclic 2’, 3'-phosphate. J. Mol. Evol. 1974;3:115–120. doi: 10.1007/BF01796557. PubMed DOI

Sawai H, Lohrmann R, Orgel LE. Prebiotic peptide-formation in the solid state. II. Reaction of glycine with adenosine 5’-triphosphate and P1, P2-diadenosine-pyrophosphate. J. Mol. Evol. 1975;6:165–184. doi: 10.1007/BF01732354. PubMed DOI

Chandru K, Mamajanov I, Cleaves HJ, 2nd, Jia TZ. Polyesters as a model system for building primitive biologies from non-biological prebiotic chemistry. Life. 2020;10:1–6. doi: 10.3390/life10010006. PubMed DOI PMC

Joyce GF, Schwartz AW, Miller SL, Orgel LE. The case for an ancestral genetic system involving simple analogues of the nucleotides. Proc. Natl. Acad. Sci. USA. 1987;84:4398–4402. doi: 10.1073/pnas.84.13.4398. PubMed DOI PMC

Hud NV, Cafferty BJ, Krishnamurthy R, Williams LD. The origin of RNA and ‘my grandfather’s axe’. Chem. Biol. 2013;20:466–474. doi: 10.1016/j.chembiol.2013.03.012. PubMed DOI

Nelson KE, Levy M, Miller SL. Peptide nucleic acids rather than RNA may have been the first genetic molecule. Proc. Natl. Acad. Sci. USA. 2000;97:3868–3871. doi: 10.1073/pnas.97.8.3868. PubMed DOI PMC

Egholm M, Buchardt O, Nielsen PE, Berg RH. Peptide nucleic acids (PNA). Oligonucleotide analogs with an achiral peptide backbone. J. Am. Chem. Soc. 1992;114:1895–1897. doi: 10.1021/ja00031a062. DOI

Nelson KE. The Prebiotic Synthesis of the Components of Peptide Nucleic Acid. San Diego: University of California; 1998.

Brunelle DJ. Ring-Opening Polymerization. Oxford: Oxford University Press; 1993.

Corbett PT, et al. Dynamic combinatorial chemistry. Chem. Rev. 2006;106:3652–3711. doi: 10.1021/cr020452p. PubMed DOI

Chandru K, et al. Simple prebiotic synthesis of high diversity dynamic combinatorial polyester libraries. Commun. Chem. 2018;1:30. doi: 10.1038/s42004-018-0031-1. DOI

Ellis GP. The Maillard Reaction. In: Wolfrom ML, editor. Advances in Carbohydrate Chemistry. New York: Academic Press; 1959. pp. 63–134. PubMed

Lavado N, et al. Prebiotic-like condensations of cyanamide and glyoxal: Revisiting intractable biotars. Chem. Eur. J. 2016;22:13632–13642. doi: 10.1002/chem.201601999. PubMed DOI

Forsythe JG, et al. Ester-mediated amide bond formation driven by wet–dry cycles: A possible path to polypeptides on the prebiotic earth. Angew. Chem. Int. Ed Engl. 2015;54:9871–9875. doi: 10.1002/anie.201503792. PubMed DOI PMC

Compton RG, Bamford CH, Tipper CFH. Ester Formation and Hydrolysis and Related Reactions. Amsterdam: Elsevier; 1972.

Szostak JW, Bartel DP, Luisi PL. Synthesizing life. Nature. 2001;409:387–390. doi: 10.1038/35053176. PubMed DOI

Mann S. Systems of creation: The emergence of life from nonliving matter. Acc. Chem. Res. 2012;45:2131–2141. doi: 10.1021/ar200281t. PubMed DOI

Jia TZ, et al. Membraneless polyester microdroplets as primordial compartments at the origins of life. Proc. Natl. Acad. Sci. 2019;116:15830–15835. doi: 10.1073/pnas.1902336116. PubMed DOI PMC

Mariscal C, et al. Hidden concepts in the history and philosophy of origins-of-life studies: A workshop report. Origin Life Evol. Biospheres. 2019;49:111–145. doi: 10.1007/s11084-019-09580-x. PubMed DOI

Preiner M, et al. The future of origin of life research: bridging decades-old divisions. Life. 2020;10:2. doi: 10.3390/life10030020. PubMed DOI PMC

Rich, A. In Chemical Evolution and the Origin of Life (eds. Buvet, R., Ponnamperuma, C.) (1971)

Peltzer ET, Bada JL, Schlesinger G, Miller SL. The chemical conditions on the parent body of the Murchison meteorite: Some conclusions based on amino, hydroxy and dicarboxylic acids. Adv. Space Res. 1984;4:69–74. doi: 10.1016/0273-1177(84)90546-5. PubMed DOI

Miller, S. L. & Van Trump, J. E. The Strecker Synthesis in the Primitive Ocean. in Origin of Life (ed. Wolman, Y.) 135–141 (Dordrecht, 1981).

Peltzer ET, Bada JL. α-Hydroxycarboxylic acids in the Murchison meteorite. Nature. 1978;272:443–444. doi: 10.1038/272443a0. DOI

Pizzarello S, Wang Y, Chaban GM. A comparative study of the hydroxy acids from the Murchison, GRA 95229 and LAP 02342 meteorites. Geochim. Cosmochim. Acta. 2010;74:6206–6217. doi: 10.1016/j.gca.2010.08.013. DOI

Parker ET, Cleaves HJ, Bada JL. Quantitation of α-hydroxy acids in complex prebiotic mixtures via liquid chromatography/tandem mass spectrometry. Mass Spectrometry. 2016;2:2. PubMed

Cooper GW, Cronin JR. Linear and cyclic aliphatic carboxamides of the Murchison meteorite: Hydrolyzable derivatives of amino acids and other carboxylic acids. Geochim. Cosmochim. Acta. 1995;59:1003–1015. doi: 10.1016/0016-7037(95)00018-6. PubMed DOI

Martins Z. The nitrogen heterocycle content of meteorites and their significance for the origin of life. Life. 2018;8:2. doi: 10.3390/life8030028. PubMed DOI PMC

Parker ET, et al. Primordial synthesis of amines and amino acids in a 1958 Miller H2S-rich spark discharge experiment. Proc. Natl. Acad. Sci. 2011;108:5526. doi: 10.1073/pnas.1019191108. PubMed DOI PMC

Cleaves HJ, II, et al. Amino acids generated from hydrated titan tholins: comparison with Miller–Urey electric discharge products. Icarus. 2014;237:182–189. doi: 10.1016/j.icarus.2014.04.042. DOI

Rodriguez-Garcia M, et al. Formation of oligopeptides in high yield under simple programmable conditions. Nat. Commun. 2015;6:8385. doi: 10.1038/ncomms9385. PubMed DOI PMC

Chandru K, Obayashi Y, Kaneko T, Kobayashi K. Formation of amino acid condensates partly having peptide bonds in a simulated submarine hydrothermal environment. Viva Origino. 2014;41:24–28.

Killops S, Killops V. Introduction to Organic Geochemistry. Hoboken: Blackwell Publishing Ltd.; 2004.

Labadie M, Cohere G, Brechenmacher C. Recherches sur l’évolution pré-biologique. II Etude morphologique des microsphérules obtenues à partir du cyanure d'ammonium. C. r. Séanc. Soc. Biol. 1967;161:1689–1693. PubMed

Folsome CE, Allen RD, Ichinose NK. Organic microstructures as products of Miller-Urey electrical discharges. Precambrian Res. 1975;2:263–275. doi: 10.1016/0301-9268(75)90012-1. DOI

Surman AJ, et al. Environmental control programs the emergence of distinct functional ensembles from unconstrained chemical reactions. Proc. Natl. Acad. Sci. USA. 2019;116:5387–5392. doi: 10.1073/pnas.1813987116. PubMed DOI PMC

Cleaves HJ, Butch C, Burger PB, Goodwin J, Meringer M. One among millions: The chemical space of nucleic acid-like molecules. J. Chem. Inf. Model. 2019;59:4266–4277. doi: 10.1021/acs.jcim.9b00632. PubMed DOI

Cleaves HJ, James Cleaves H, Bada JL. The Prebiotic Chemistry of Alternative Nucleic Acids. Dordrecht: Genesis-In Beginning. Springer; 2012. pp. 3–33.

Teichert JS, Kruse FM, Trapp O. Direct prebiotic pathway to DNA nucleosides. Angew. Chem. Int. Ed. 2019;58:9944–9947. doi: 10.1002/anie.201903400. PubMed DOI

Rodriguez LE, House CH, Smith KE, Roberts MR, Callahan MP. Nitrogen heterocycles form peptide nucleic acid precursors in complex prebiotic mixtures. Sci. Rep. 2019;9:9281. doi: 10.1038/s41598-019-45310-z. PubMed DOI PMC

Chandru K, Imai E, Kaneko T, Obayashi Y, Kobayashi K. Survivability and abiotic reactions of selected amino acids in different hydrothermal system simulators. Origin. Life Evol. Biospheres. 2013;43:99–108. doi: 10.1007/s11084-013-9330-9. PubMed DOI

Mungi CV, Bapat NV, Hongo Y, Rajamani S. Formation of abasic oligomers in nonenzymatic polymerization of canonical nucleotides. Life. 2019;9:2. doi: 10.3390/life9030057. PubMed DOI PMC

Mamajanov I, Cody GD. Protoenzymes: The case of hyperbranched polyesters. Philos. Trans. R. Soc. Lond. A. 2017;375:20160357. PubMed PMC

Pross A. What is Life? How chemistry becomes biology. Oxford: Oxford University Press; 2012. p. 256.

Pascal R. Kinetic barriers and the self-organization of life. Isr. J. Chem. 2015;55:865–874. doi: 10.1002/ijch.201400193. DOI

Strohalm M, Hassman M, Košata B, Kodíček M. mMass data miner: An open source alternative for mass spectrometric data analysis. Rapid Commun. Mass Spectrom. 2008;22:905–908. doi: 10.1002/rcm.3444. PubMed DOI

Strohalm M, Kavan D, Novák P, Volný M, Havlícek V. mMass 3: A cross-platform software environment for precise analysis of mass spectrometric data. Anal. Chem. 2010;82:4648–4651. doi: 10.1021/ac100818g. PubMed DOI

Niedermeyer THJ, Strohalm M. mMass as a software tool for the annotation of cyclic peptide tandem mass spectra. PLoS ONE. 2012;7:e44913. doi: 10.1371/journal.pone.0044913. PubMed DOI PMC

The interplay between peptides and RNA is critical for protoribosome compartmentalization and stability