The origin of the RNA world: Co-evolution of genes and metabolism
Abstract
Discoveries demonstrating that RNA can serve genetic, catalytic, structural, and regulatory roles have provided strong support for the existence of an RNA World that preceded the origin of life as we know it. Despite the appeal of this idea, it has been difficult to explain how macromolecular RNAs emerged from small molecules available on the early Earth. We propose here a mechanism by which mutual catalysis in a pre-biotic network initiated a progression of stages characterized by ever larger and more effective catalysts supporting a proto-metabolic network, and the emergence of RNA as the dominant macromolecule due to its ability to both catalyze chemical reactions and to be copied in a template-directed manner. This model suggests that many features of modern life, including the biosynthetic pathways leading to simple metabolites, the structures of organic and metal ion cofactors, homochirality, and template-directed replication of nucleic acids, arose long before the RNA World and were retained as pre-biotic systems became more sophisticated.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The origin of RNA and DNA is intimately linked with proto-metabolic reactions.
“In this view, present-day metabolism is a direct consequence of prebiotic chemistry, rather than an accidental by-product, and the origin of RNA and DNA is intimately linked with these proto-metabolic reactions (Copley et al., 2007).”
From The Astrobiology Primer v2.0 (2016) · cites this paper as Copley et al., 2007
Present-day metabolism is a direct consequence of prebiotic chemistry, rather than an accidental by-product.
“In this view, present-day metabolism is a direct consequence of prebiotic chemistry, rather than an accidental by-product, and the origin of RNA and DNA is intimately linked with these proto-metabolic reactions (Copley et al., 2007).”
From The Astrobiology Primer v2.0 (2016) · cites this paper as Copley et al., 2007
Cites
The Structural Basis of Ribosome Activity in Peptide Bond Synthesis
Nissen, P., Hansen, J., Ban, N., Moore, P. B., & Steitz, T. A. (2000) · Science · doi:10.1126/science.289.5481.920 · Cited by 2,269 · see citing works
Ibba, M., & Söll, D. G. (2000) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.69.1.617 · Cited by 1,461 · see citing works
Proline-catalyzed asymmetric reactions
List, B. (2002) · Tetrahedron · doi:10.1016/s0040-4020(02)00516-1 · Cited by 1,155 · see citing works
The antiquity of RNA-based evolution.
Joyce, G. F. (2002) · Nature · doi:10.1038/418214a · Cited by 1,070 · see citing works
Martin, W., & Russell, M. J. (2003) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2002.1183 · Cited by 856 · see citing works
Coenzymes as fossils of an earlier metabolic state
White, H. B. (1976) · Journal of Molecular Evolution · doi:10.1007/bf01732468 · Cited by 493 · see citing works
Volcanoes, Fluids, and Life at Mid-Ocean Ridge Spreading Centers
Kelley, D. S., Baross, J. A., & Delaney, J. R. (2002) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev.earth.30.091201.141331 · Cited by 463 · see citing works
Primordial Carbonylated Iron-Sulfur Compounds and the Synthesis of Pyruvate
Cody, G. D., Boctor, N. Z., Filley, T. R., Hazen, R. M., Scott, J. H., Sharma, A., & Yoder, H. S. (2000) · Science · doi:10.1126/science.289.5483.1337 · Cited by 441 · see citing works
A small catalytic RNA motif with Diels-Alderase activity
Seelig, B., & Jäschke, A. (1999) · Chemistry & Biology · doi:10.1016/s1074-5521(99)89008-5 · Cited by 322 · see citing works
Substrate-assisted catalysis of peptide bond formation by the ribosome
Weinger, J. S., Parnell, K. M., Dorner, S., Green, R., & Strobel, S. A. (2004) · Nature Structural & Molecular Biology · doi:10.1038/nsmb841 · Cited by 278 · see citing works
An amino acid as a cofactor for a catalytic polynucleotide
Roth, A., & Breaker, R. R. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.11.6027 · Cited by 239 · see citing works
Great Metalloclusters in Enzymology
Rees, D. C. (2002) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.71.110601.135406 · Cited by 220 · see citing works
Structural Evidence for a Two-Metal-Ion Mechanism of Group I Intron Splicing
Stahley, M. R., & Strobel, S. A. (2005) · Science · doi:10.1126/science.1114994 · Cited by 212 · see citing works
Hydrolytic stability of helical RNA: a selective advantage for the natural 3',5'-bond.
Usher, D. A., & McHale, A. H. (1976) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.73.4.1149 · Cited by 179 · see citing works
snRNAs as the catalysts of pre-mRNA splicing
Valadkhan, S. (2005) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2005.10.008 · Cited by 147 · see citing works
Evolution of Early Earth's Atmosphere, Hydrosphere, and Biosphere - Constraints from Ore Deposits
Kesler, S. E., & Ohmoto, H. (2006) · Geological Society of America eBooks · doi:10.1130/mem198 · Cited by 138 · see citing works
A mechanism for the association of amino acids with their codons and the origin of the genetic code
Copley, S. D., Smith, E., & Morowitz, H. J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0501049102 · Cited by 134 · see citing works
Self-citationRohatgi, R., Bartel, D. P., & Szostak, J. W. (1996) · Journal of the American Chemical Society · doi:10.1021/ja9537134 · Cited by 134 · see citing works
The Sugar Model: Catalysis by Amines and Amino Acid Products
Weber, A. L. (2001) · Origins of life and evolution of the biosphere · doi:10.1023/a:1006750423942 · Cited by 127 · see citing works
Segrè, D., Lancet, D., Kedem, O., & Pilpel, Y. (1998) · Origins of Life and Evolution of Biospheres · doi:10.1023/a:1006583712886 · Cited by 126 · see citing works
RNA-Catalyzed Amino Acid Activation
Kumar, R. K., & Yarus, M. (2001) · Biochemistry · doi:10.1021/bi010710x · Cited by 121 · see citing works
Random biochemical networks: the probability of self-sustaining autocatalysis
Mossel, E., & Steel, M. (2004) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2004.10.011 · Cited by 119 · see citing works
A tiny RNA that catalyzes both aminoacyl-RNA and peptidyl-RNA synthesis
Illangasekare, M., & Yarus, M. (1999) · RNA · doi:10.1017/s1355838299991264 · Cited by 104 · see citing works
Dipeptide seryl-histidine and related oligopeptides cleave DNA, protein, and a carboxyl ester
Li, Y., Zhao, Y., Hatfield, S., Wan, R., Zhu, Q., Li, X., McMills, M. C., Ma, Y., Li, J., Brown, K. L., et al. (2000) · Bioorganic & Medicinal Chemistry · doi:10.1016/s0968-0896(00)00208-x · Cited by 104 · see citing works
RNA-Catalyzed CoA, NAD, and FAD Synthesis from Phosphopantetheine, NMN, and FMN
Huang, F., Bugg, C. W., & Yarus, M. (2000) · Biochemistry · doi:10.1021/bi002061f · Cited by 102 · see citing works
A novel ribozyme with ester transferase activity
Jenne, A., & Famulok, M. (1998) · Chemistry & Biology · doi:10.1016/s1074-5521(98)90084-9 · Cited by 97 · see citing works
The driving force for molecular evolution of translation
NOLLER, H. F. (2004) · RNA · doi:10.1261/rna.7142404 · Cited by 96 · see citing works
An Interpretive Review of the Origin of Life Research
Penny, D. (2005) · Biology & Philosophy · doi:10.1007/s10539-004-7342-6 · Cited by 76 · see citing works
Processivity of Ribozyme-Catalyzed RNA Polymerization
Lawrence, M. S., & Bartel, D. P. (2003) · Biochemistry · doi:10.1021/bi034228l · Cited by 62 · see citing works
A trinucleotide can promote metal ion-dependent specific cleavage of RNA.
Kazakov, S. A., & 幹, 直. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.17.7939 · Cited by 60 · see citing works
In vitro selection of ribozymes dependent on peptides for activity
Robertson, M. P., Knudsen, S. M., & Ellington, A. D. (2003) · RNA · doi:10.1261/rna.5900204 · Cited by 52 · see citing works
The Nicotinamide Biosynthetic Pathway Is a By-Product of the RNA World
Cleaves, H. J., & Miller, S. L. (2001) · Journal of Molecular Evolution · doi:10.1007/s002390010135 · Cited by 52 · see citing works
Acyl-CoAs from Coenzyme Ribozymes
Jadhav, V., & Yarus, M. (2001) · Biochemistry · doi:10.1021/bi011803h · Cited by 48 · see citing works
RNA enzymes with two small-molecule substrates
Huang, F., Yang, Z., & Yarus, M. (1998) · Chemistry & Biology · doi:10.1016/s1074-5521(98)90294-0 · Cited by 33 · see citing works
The Intramolecular Facilitated Hydrolytic Rates of Methyl-Substituted Succinanilic Acids1
Higuchi, T., EBERSON, L. E., & Herd, A. K. (1966) · Journal of the American Chemical Society · doi:10.1021/ja00968a023 · Cited by 28 · see citing works
Aptamer to Ribozyme: The Intrinsic Catalytic Potential of a Small RNA
Brackett, D. M., & Dieckmann, T. (2006) · ChemBioChem · doi:10.1002/cbic.200500538 · Cited by 23 · see citing works
Thermodynamic study of hybridization properties of heterochiral nucleic acids
Urata, H., Shimizu, H., Hiroaki, H., Kohda, D., & Akagi, M. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(03)01531-6 · Cited by 20 · see citing works
Probing the mechanism of an Mn2+‐dependent ribozyme by means of platinum complexes
Bombard, S., Kozelka, J., Favre, A., & Chottard, J. (1998) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.1998.2520025.x · Cited by 19 · see citing works
Bartel, D. P., & Unrau, P. J. (1999) · Trends in Genetics · doi:10.1016/s0168-9525(99)01898-3 · Cited by 11 · see citing works
Urata, H., Sasaki, R., Morita, H., Kusumoto, M., Ogawa, Y., Mitsuda, K., & Akagi, M. (2005) · Chemical Communications · doi:10.1039/b500673b · Cited by 6 · see citing works
Riboswitches: Regulators of modern and ancient metabolism
Kim, J. C., & Breaker, R. R. (2006) · The Biochemist · doi:10.1042/bio02802011 · Cited by 1 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
How did LUCA make a living? Chemiosmosis in the origin of life
Lane, N., Allen, J. F., & Martin, W. (2010) · BioEssays · doi:10.1002/bies.200900131 · Cited by 377 · see citing works
Resynthesizing behavior through phylogenetic refinement
Cisek, P. (2019) · Attention Perception & Psychophysics · doi:10.3758/s13414-019-01760-1 · Cited by 294 · see citing works
Synthesis of Carbohydrates in Mineral-Guided Prebiotic Cycles
Kim, H.-J., Ricardo, A., Illangkoon, H. I., Kim, M. J., Carrigan, M. A., Frye, F., & Benner, S. A. (2011) · Journal of the American Chemical Society · doi:10.1021/ja201769f · Cited by 268 · see citing works
The “Strong” RNA World Hypothesis: Fifty Years Old
Neveu, M. F., Kim, H., & Benner, S. A. (2013) · Astrobiology · doi:10.1089/ast.2012.0868 · Cited by 229 · see citing works
The Origin and Nature of Life on Earth: The Emergence of the Fourth Geosphere
Smith, E., & Morowitz, H. J. (2016) · doi:10.1017/cbo9781316348772 · Cited by 215 · see citing works
Self-citationGenetics first or metabolism first? The formamide clue
Saladino, R., Botta, G., Pino, S., Costanzo, G., & Di Mauro, E. (2012) · Chemical Society Reviews · doi:10.1039/c2cs35066a · Cited by 215 · see citing works
A Hydrothermal-Sedimentary Context for the Origin of Life
Westall, F., Hickman-Lewis, K., Hinman, N., Gautret, P., Campbell, K. A., Bréhéret, J. G., Foucher, F., Hubert, A., Sorieul, S., Dass, A. V., et al. (2018) · Astrobiology · doi:10.1089/ast.2017.1680 · Cited by 189 · see citing works
The Role of Meteorite Impacts in the Origin of Life
Osinski, G. R., Cockell, C., Pontefract, A., & Sapers, H. (2020) · Astrobiology · doi:10.1089/ast.2019.2203 · Cited by 179 · see citing works
Gissot, A., Camplo, M., Grinstaff, M. W., & Barthélémy, P. (2008) · Organic & Biomolecular Chemistry · doi:10.1039/b719280k · Cited by 171 · see citing works
Iron catalysis at the origin of life
Camprubi, E., Jordan, S. F., Vasiliadou, R., & Lane, N. (2017) · IUBMB Life · doi:10.1002/iub.1632 · Cited by 144 · see citing works
Spitzer, J. J., & Poolman, B. (2009) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00010-09 · Cited by 153 · see citing works
Influence of the UV Environment on the Synthesis of Prebiotic Molecules
Ranjan, S., & Sasselov, D. D. (2016) · Astrobiology · doi:10.1089/ast.2015.1359 · Cited by 159 · see citing works
The Compositional and Evolutionary Logic of Metabolism
Braakman, R., & Smith, E. (2012) · Physical Biology · doi:10.1088/1478-3975/10/1/011001 · Cited by 158 · see citing works
Self-citationDomagal-Goldman, S. D., Wright, K. E., Domagal-Goldman, S. D., Wright, K. E., Adamala, K., Arina de la Rubia, L., Bond, J., Dartnell, L. R., Goldman, A. D., Lynch, K., et al. (2016) · Astrobiology · doi:10.1089/ast.2015.1460 · Cited by 136 · see citing works
“In this view, present-day metabolism is a direct consequence of prebiotic chemistry, rather than an accidental by-product, and the origin of RNA and DNA is intimately linked with these proto-metabolic reactions (Copley et al., 2007).”
Did life originate from a global chemical reactor?
Stüeken, E. E., Anderson, R. E., Bowman, J. S., Brazelton, W. J., Colangelo-Lillis, J. R., Goldman, A. D., Som, S. M., & Baross, J. A. (2013) · Geobiology · doi:10.1111/gbi.12025 · Cited by 130 · see citing works
Mulkidjanian, A. Y., & Galperin, M. Y. (2009) · Biology Direct · doi:10.1186/1745-6150-4-27 · Cited by 130 · see citing works
Membrane Transport in Primitive CellsPreprint
Mansy, S. S. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a002188 · Cited by 127 · see citing works
Maury, C. P. J. (2009) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-009-9165-6 · Cited by 118 · see citing works
Mulkidjanian, A. Y. (2009) · Biology Direct · doi:10.1186/1745-6150-4-26 · Cited by 117 · see citing works
Proton gradients at the origin of life
Lane, N. (2017) · BioEssays · doi:10.1002/bies.201600217 · Cited by 115 · see citing works
Toward a theory of evolution as multilevel learning
Vanchurin, V., Wolf, Y. I., Katsnelson, M. I., & Koonin, E. V. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2120037119 · Cited by 121 · see citing works
Bonfio, C., Godino, E., Corsini, M., Biani, F. F. D., Guella, G., & Mansy, S. S. (2018) · Nature Catalysis · doi:10.1038/s41929-018-0116-3 · Cited by 107 · see citing works
A prebiotic basis for ATP as the universal energy currency
Pinna, S., Kunz, C., Halpern, A., Harrison, S. A., Jordan, S. F., Ward, J., Werner, F., & Lane, N. (2022) · PLOS Biology · doi:10.1371/journal.pbio.3001437 · Cited by 103 · see citing works
Getting Past the RNA World: The Initial Darwinian AncestorPreprint
Yarus, M. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a003590 · Cited by 100 · see citing works
Acetyl Phosphate as a Primordial Energy Currency at the Origin of Life
Whicher, A., Camprubi, E., Pinna, S., Herschy, B., & Lane, N. (2018) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-018-9555-8 · Cited by 81 · see citing works
Constraints on the Early Terrestrial Surface UV Environment Relevant to Prebiotic Chemistry
Ranjan, S., & Sasselov, D. D. (2017) · Astrobiology · doi:10.1089/ast.2016.1519 · Cited by 86 · see citing works
Mechanistic Insight into Metal Ion-Catalyzed Transamination
Mayer, R. J., Kaur, H., Rauscher, S. A., & Moran, J. (2021) · Journal of the American Chemical Society · doi:10.1021/jacs.1c08535 · Cited by 68 · see citing works
Evolution of replication machines
Yao, N. Y., & O’Donnell, M. E. (2015) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2015.1125845 · Cited by 68 · see citing works
Thermodynamics of natural selection I: Energy flow and the limits on organization
Smith, E. (2008) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2008.02.010 · Cited by 65 · see citing works
Self-citationThe dynamics of the RNA world: insights and challenges
Kun, Á., Szilágyi, A., Könnyű, B., Boza, G., Zachar, I., & Szathmáry, E. (2015) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12700 · Cited by 65 · see citing works
Coupled catabolism and anabolism in autocatalytic RNA sets
Arsène, S., Ameta, S., Lehman, N., Griffiths, A. D., & Nghe, P. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky598 · Cited by 57 · see citing works
Metal Catalysts and the Origin of Life
Belmonte, L., & Mansy, S. S. (2016) · Elements · doi:10.2113/gselements.12.6.413 · Cited by 53 · see citing works
Metal Binding Motif in the Active Site of the HDV Ribozyme Binds Divalent and Monovalent Ions
Veeraraghavan, N., Ganguly, A., Chen, J.-H., Bevilacqua, P. C., Hammes‐Schiffer, S., & Golden, B. L. (2011) · Biochemistry · doi:10.1021/bi2000164 · Cited by 51 · see citing works
Model genotype–phenotype mappings and the algorithmic structure of evolution
Nichol, D., Robertson‐Tessi, M., Anderson, A. R. A., & Jeavons, P. (2019) · Journal of The Royal Society Interface · doi:10.1098/rsif.2019.0332 · Cited by 62 · see citing works
From Prelife to Life: How Chemical Kinetics Become Evolutionary Dynamics
Chen, I. A., & Nowak, M. A. (2012) · Accounts of Chemical Research · doi:10.1021/ar2002683 · Cited by 50 · see citing works
The evolution and functional repertoire of translation proteins following the origin of life
Goldman, A. D., Samudrala, R., & Baross, J. A. (2010) · Biology Direct · doi:10.1186/1745-6150-5-15 · Cited by 47 · see citing works
A Nonenzymatic Analog of Pyrimidine Nucleobase Biosynthesis
Yi, J., Kaur, H., Kazöne, W., Rauscher, S. A., Gravillier, L., Muchowska, K. B., & Moran, J. (2022) · Angewandte Chemie International Edition · doi:10.1002/anie.202117211 · Cited by 47 · see citing works
Catalysts, autocatalysis and the origin of metabolism
Preiner, M., Xavier, J. C., Vieira, A. D. N., Kleinermanns, K., Allen, J. F., & Martin, W. F. (2019) · Interface Focus · doi:10.1098/rsfs.2019.0072 · Cited by 43 · see citing works
Non-viral vectors for the mediation of RNAi
Zhang, S., Zhao, Y., Zhi, D., & Zhang, S. (2011) · Bioorganic Chemistry · doi:10.1016/j.bioorg.2011.07.005 · Cited by 40 · see citing works
The Quest for a Universal Theory of Life
Cleland, C. E. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139046893 · Cited by 122 · see citing works
Czárán, T., Könnyű, B., & Szathmáry, E. (2015) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2015.06.002 · Cited by 37 · see citing works
Coenzyme Autocatalytic Network on the Surface of Oil Microspheres as a Model for the Origin of Life
Sharov, A. A. (2009) · International Journal of Molecular Sciences · doi:10.3390/ijms10041838 · Cited by 37 · see citing works
Hydrogen Drives Part of the Reverse Krebs Cycle under Metal or Meteorite Catalysis
Rauscher, S. A., & Moran, J. (2022) · Angewandte Chemie International Edition · doi:10.1002/anie.202212932 · Cited by 39 · see citing works
Diagnostik und Begutachtung asbestbedingter Berufskrankheiten
Baur, X., Clasen, M., Fisseler-Eckhoff, A., Heger, M., Hering, K. G., Hofmann-Preiß, K., Köhler, D., Kranig, A., Kraus, T., Letzel, S., et al. (2011) · Pneumologie · doi:10.1055/s-0030-1255992 · Cited by 36 · see citing works
Sharov, A. A., & Gordon, R. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-811940-2.00011-3 · Cited by 37 · see citing works
Piece by piece: Building a ribozyme
Gray, M. W., & Gopalan, V. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.rev119.009929 · Cited by 33 · see citing works
In the Beginning was a Mutualism - On the Origin of Translation
Vitas, M., & Dobovišek, A. (2018) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-018-9557-6 · Cited by 34 · see citing works
Viroids and Viroid-like Circular RNAs: Do They Descend from Primordial Replicators?
Lee, B. D., & Koonin, E. V. (2022) · Life · doi:10.3390/life12010103 · Cited by 30 · see citing works
Metal/ADP Complexes Promote Phosphorylation of Ribonucleotides
Werner, E., Pinna, S., Mayer, R. J., & Moran, J. (2023) · Journal of the American Chemical Society · doi:10.1021/jacs.3c08047 · Cited by 29 · see citing works
A biophysical basis for the emergence of the genetic code in protocells
Harrison, S. A., Palmeira, R. N., Halpern, A., & Lane, N. J. (2022) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2022.148597 · Cited by 28 · see citing works
On the importance of studying asteroids: A comprehensive review
Azadmanesh, M., Roshanian, J., & Hassanalian, M. (2023) · Progress in Aerospace Sciences · doi:10.1016/j.paerosci.2023.100957 · Cited by 23 · see citing works
Adsorption of nucleic acid bases on magnesium oxide (MgO)
Fornaro, T., Brucato, J. R., Branciamore, S., & Pucci, A. (2012) · International Journal of Astrobiology · doi:10.1017/s1473550412000444 · Cited by 26 · see citing works
Technological Approaches in the Analysis of Extracellular Vesicle Nucleotide Sequences
Tesovnik, T., Bizjan, B. J., Šket, R., Debeljak, M., Battelino, T., & Kovač, J. (2021) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2021.787551 · Cited by 25 · see citing works
Origin of Chirality in the Molecules of Life
Cowan, J. A., & Furnstahl, R. J. (2022) · ACS Earth and Space Chemistry · doi:10.1021/acsearthspacechem.2c00032 · Cited by 24 · see citing works
Babajanyan, S. G., Wolf, Y. I., Khachatryan, A., ALLAHVERDYAN, A. E., López‐García, P., & Koonin, E. V. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2301522120 · Cited by 24 · see citing works
The limits of metabolic heredity in protocells
Nunes Palmeira, R., Colnaghi, M., Harrison, S. A., Pomiankowski, A., & Lane, N. (2022) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2022.1469 · Cited by 23 · see citing works
Nicotinamide Coenzyme Synthesis: A Case of Ribonucleotide Emergence or a Byproduct of the RNA World?
Raffaelli, N. (2011) · Springer eBooks · doi:10.1007/978-3-642-21625-1_9 · Cited by 22 · see citing works
On the formation of niacin (vitamin B3) and pyridine carboxylic acids in interstellar model ices
McMurtry, B. M., Turner, A. M., Saito, S. E. J., & Kaiser, R. I. (2016) · Chemical Physics · doi:10.1016/j.chemphys.2016.03.010 · Cited by 22 · see citing works
Hedwig, G. R., gseth, E. H., & Høiland, H. (2013) · The Journal of Chemical Thermodynamics · doi:10.1016/j.jct.2012.12.028 · Cited by 21 · see citing works
The Origin of Large Molecules in Primordial Autocatalytic Reaction Networks
Giri, V., & Jain, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029546 · Cited by 20 · see citing works
Clay, A. P., Cooke, R. E., Kumar, R., Yadav, M., Krishnamurthy, R., & Springsteen, G. (2022) · Angewandte Chemie International Edition · doi:10.1002/anie.202112572 · Cited by 18 · see citing works
Informed Generation: Physical origin and biological evolution of genetic codescript interpreters
Wills, P. R. (2009) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2008.12.030 · Cited by 18 · see citing works
On Causality in Nonlinear Complex Systems
Coffman, J. A. (2011) · Elsevier eBooks · doi:10.1016/b978-0-444-52076-0.50010-9 · Cited by 17 · see citing works
Gorrell, I. B., Henderson, T., Albdeery, K. G. S., Savage, P., & Kee, T. P. (2017) · Life · doi:10.3390/life7040045 · Cited by 16 · see citing works
Viroids-First—A Model for Life on Earth, Mars and Exoplanets
Moelling, K., & Broecker, F. (2019) · Geosciences · doi:10.3390/geosciences9050241 · Cited by 15 · see citing works
Bianco, C. D., & Mansy, S. S. (2012) · Accounts of Chemical Research · doi:10.1021/ar300097w · Cited by 14 · see citing works
Toward the Relational Formulation of Biological Thermodynamics
Igamberdiev, A. U. (2023) · Entropy · doi:10.3390/e26010043 · Cited by 14 · see citing works
Evolution at the Origins of Life?
Schoenmakers, L. L. J., Reydon, T. A. C., & Kirschning, A. (2024) · Life · doi:10.3390/life14020175 · Cited by 14 · see citing works
Giulio, M. D. (2021) · Biosystems · doi:10.1016/j.biosystems.2021.104449 · Cited by 13 · see citing works
A single phosphorylation mechanism in early metabolism – the case of phosphoenolpyruvate
Zimmermann, J., Mayer, R. J., & Moran, J. (2023) · Chemical Science · doi:10.1039/d3sc04116f · Cited by 13 · see citing works
Armstrong, D. L., Lancet, D., & Zidovetzki, R. (2018) · Astrobiology · doi:10.1089/ast.2016.1615 · Cited by 13 · see citing works
Protometabolism as out-of-equilibrium chemistry
Nader, S., Sebastianelli, L., & Mansy, S. S. (2022) · Philosophical Transactions of the Royal Society A Mathematical Physical and Engineering Sciences · doi:10.1098/rsta.2020.0423 · Cited by 13 · see citing works
Primitive templated catalysis of a peptide ligation by self-folding RNAs
Kashiwagi, N., Furuta, H., & Ikawa, Y. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp111 · Cited by 12 · see citing works
Protocells and LUCA: Transport of substances from first physicochemical principles
Melkikh, A. V., & Sutormina, M. (2019) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2018.12.011 · Cited by 12 · see citing works
From genome to evolution: investigating type II methylotrophs using a pangenomic analysis
Samanta, D., Rauniyar, S., Saxena, P., & Sani, R. K. (2024) · mSystems · doi:10.1128/msystems.00248-24 · Cited by 11 · see citing works
On a quest of reverse translation
Vitas, M., & Dobovišek, A. (2016) · Foundations of Chemistry · doi:10.1007/s10698-016-9260-5 · Cited by 13 · see citing works
Cleland, C. E. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139046893.004 · Cited by 11 · see citing works
Modeling the complex dynamics of enzyme-pathway coevolution
Schütte, M., Skupin, A., Segrè, D., & Ebenhöh, O. (2010) · Chaos An Interdisciplinary Journal of Nonlinear Science · doi:10.1063/1.3530440 · Cited by 9 · see citing works
The Archean–Hadean Earth: Modern paradigms and ancient processes
Mueller, P. A., & Nutman, A. P. (2017) · Geological Society of America eBooks · doi:10.1130/2017.2523(03 · Cited by 10 · see citing works
An Evolutionary Perspective on Embodiment
Cisek, P. (2021) · Springer eBooks · doi:10.1007/978-3-030-78471-3_24 · Cited by 8 · see citing works
Armstrong, D. L., Markovitch, O., Zidovetzki, R., & Lancet, D. (2011) · Physical Biology · doi:10.1088/1478-3975/8/6/066001 · Cited by 9 · see citing works
Origin of the Directed Movement of Protocells in the Early Stages of the Evolution of Life
Melkikh, A. V., & Chesnokova, O. I. (2012) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-012-9291-4 · Cited by 9 · see citing works
A Unifying Scenario on the Origin and Evolution of Cellular and Viral DomainsPreprint
BANDEA, C. I. (2009) · Nature Precedings · doi:10.1038/npre.2009.3888.1 · Cited by 9 · see citing works
Transformers in RNA structure prediction: A review
Chaturvedi, M., Rashid, M. A., & Paliwal, K. K. (2025) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2025.03.021 · Cited by 8 · see citing works
A Nonenzymatic Analog of Pyrimidine Nucleobase Biosynthesis
Yi, J., Kaur, H., Kazöne, W., Rauscher, S. A., Gravillier, L., Muchowska, K. B., & Moran, J. (2022) · Angewandte Chemie · doi:10.1002/ange.202117211 · Cited by 8 · see citing works
On the Meaning of Chance in Biology
Coffman, J. A. (2014) · Biosemiotics · doi:10.1007/s12304-014-9206-z · Cited by 8 · see citing works
Coenzymes, viruses and the RNA world
Reyes-Prieto, F., Hernández-Morales, R., Jácome, R., Becerra, A., & Lazcano, A. (2012) · Biochimie · doi:10.1016/j.biochi.2012.01.004 · Cited by 9 · see citing works
Integrative Perspectives: In Quest of a Coherent Framework for Origins of Life on Earth
Egel, R. (2011) · Springer eBooks · doi:10.1007/978-3-642-21625-1_12 · Cited by 8 · see citing works
Polymer phosphorylases: clues to the emergence of non-replicative and replicative polymers
Freire, M. Á. (2011) · Theory in Biosciences · doi:10.1007/s12064-011-0131-2 · Cited by 8 · see citing works
Active centrum hypothesis: The origin of chiral homogeneity and the RNA-world
Garay, J. (2010) · Biosystems · doi:10.1016/j.biosystems.2010.09.004 · Cited by 8 · see citing works
Non‐enzymatic Ribonucleotide Reduction in the Prebiotic Context
Dragičević, I., Barić, D., Kovačević, B., Golding, B. T., & Smith, D. M. (2015) · Chemistry - A European Journal · doi:10.1002/chem.201405741 · Cited by 9 · see citing works
Directionality theory and the origin of life
Demetrius, L. (2024) · Royal Society Open Science · doi:10.1098/rsos.230623 · Cited by 7 · see citing works
Essential Logic and Facts Behind the Expansion of the Genetic Code: A Critical Assessment
Luu, H. T. L., Karbalaei‐Heidari, H. R., & Budiša, N. (2025) · ChemCatChem · doi:10.1002/cctc.202500809 · Cited by 8 · see citing works
Bifurcations and phase transitions in the origins of life
Solé, R. V., & Domenico, M. D. (2025) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2024.0295 · Cited by 7 · see citing works
Pereira, D. P. H., Xie, X., Stewart, S., Subrati, Z., Beyazay, T., Paczia, N., Belz, J., Volz, K., Erastova, V., Tüysüz, H., et al. (2025) · Communications Chemistry · doi:10.1038/s42004-025-01752-3 · Cited by 8 · see citing works
Gonzalez-Ramirez, L. A., Moreno, A., Ng, J. D., & Garcı́a-Ruiz, J. M. (2022) · Astrobiology · doi:10.1089/ast.2022.0004 · Cited by 7 · see citing works
Hypothesis for Molecular Evolution in the Pre‐Cellular Stage of the Origin of Life
Wang, Y., & Du, Y. (2025) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.70001 · Cited by 6 · see citing works
Könnyű, B., & Czárán, T. (2014) · BMC Evolutionary Biology · doi:10.1186/s12862-014-0234-8 · Cited by 7 · see citing works
Towards a Theory of Evolution as Multilevel LearningPreprint
Vanchurin, V., Wolf, Y. I., Katsnelson, M. I., & Koonin, E. V. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.11.03.466494 · Cited by 7 · see citing works
- Authors
- Copley, S. D., Smith, E., & Morowitz, H. J.
- Affiliations
- Cooperative Institute for Research in Environmental Sciences (US)
- Santa Fe Institute (US)
- George Mason University (US)
- Corresponding author
- Copley, Shelley D.
- Venue
- Bioorganic Chemistry
- Publisher
- Elsevier BV
- Published
- 2007-12
- Volume
- 35
- Issue
- 6
- Pages
- 430-443
- ISSN
- 0045-2068 (ISSN-L)
- OpenAlex
- W2091007915
- Cited by
- 184
- References
- 41
- Citations by year
- 2026: 5 · 2025: 12 · 2024: 9 · 2023: 9 · 2022: 18 · 2021: 8 · 2020: 7 · 2019: 25 · 2018: 10 · 2017: 9 · 2016: 10 · 2015: 9 · 2014: 4 · 2013: 8 · 2012: 13
- FWCI
- 3.39
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Bioorganic Chemistry (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- RNA world, origin of life, RNA catalysis, homochirality, metal cofactors, biosynthetic pathway, early Earth chemistry
- MeSH terms
- Origin of Life, Catalysis, Models, Theoretical, RNA, Thermodynamics, Evolution, Molecular
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
