{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,31]],"date-time":"2025-12-31T11:19:07Z","timestamp":1767179947441,"version":"build-2238731810"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1008634","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,2,5]],"date-time":"2021-02-05T00:00:00Z","timestamp":1612483200000}}],"reference-count":50,"publisher":"Public Library of Science (PLoS)","issue":"1","license":[{"start":{"date-parts":[[2021,1,26]],"date-time":"2021-01-26T00:00:00Z","timestamp":1611619200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100012550","name":"Nemzeti Kutat\u00e1si, Fejleszt\u00e9si \u00e9s Innovaci\u00f3s Alap","doi-asserted-by":"publisher","award":["K124438"],"award-info":[{"award-number":["K124438"]}],"id":[{"id":"10.13039\/501100012550","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012550","name":"Nemzeti Kutat\u00e1si, Fejleszt\u00e9si \u00e9s Innovaci\u00f3s Alap","doi-asserted-by":"publisher","award":["K124438"],"award-info":[{"award-number":["K124438"]}],"id":[{"id":"10.13039\/501100012550","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012550","name":"Nemzeti Kutat\u00e1si, Fejleszt\u00e9si \u00e9s Innovaci\u00f3s Alap","doi-asserted-by":"publisher","award":["K119347"],"award-info":[{"award-number":["K119347"]}],"id":[{"id":"10.13039\/501100012550","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012550","name":"Nemzeti Kutat\u00e1si, Fejleszt\u00e9si \u00e9s Innovaci\u00f3s Alap","doi-asserted-by":"publisher","award":["K119347"],"award-info":[{"award-number":["K119347"]}],"id":[{"id":"10.13039\/501100012550","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012550","name":"Nemzeti Kutat\u00e1si, Fejleszt\u00e9si \u00e9s Innovaci\u00f3s Alap","doi-asserted-by":"publisher","award":["PD120799"],"award-info":[{"award-number":["PD120799"]}],"id":[{"id":"10.13039\/501100012550","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012550","name":"Nemzeti Kutat\u00e1si, Fejleszt\u00e9si \u00e9s Innovaci\u00f3s Alap","doi-asserted-by":"publisher","award":["GINOP 2.3.2-15-2016-00057"],"award-info":[{"award-number":["GINOP 2.3.2-15-2016-00057"]}],"id":[{"id":"10.13039\/501100012550","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>The Metabolically Coupled Replicator System (MCRS) model of early chemical evolution offers a plausible and efficient mechanism for the self-assembly and the maintenance of prebiotic RNA replicator communities, the likely predecessors of all life forms on Earth. The MCRS can keep different replicator species together due to their mandatory metabolic cooperation and limited mobility on mineral surfaces, catalysing reaction steps of a coherent reaction network that produces their own monomers from externally supplied compounds. The complexity of the MCRS chemical engine can be increased by assuming that each replicator species may catalyse more than a single reaction of metabolism, with different catalytic activities of the same RNA sequence being in a trade-off relation: one catalytic activity of a promiscuous ribozyme can increase only at the expense of the others on the same RNA strand. Using extensive spatially explicit computer simulations we have studied the possibility and the conditions of evolving ribozyme promiscuity in an initial community of single-activity replicators attached to a 2D surface, assuming an additional trade-off between replicability and catalytic activity. We conclude that our promiscuous replicators evolve under weak catalytic trade-off, relatively strong activity\/replicability trade-off and low surface mobility of the replicators and the metabolites they produce, whereas catalytic specialists benefit from very strong catalytic trade-off, weak activity\/replicability trade-off and high mobility. We argue that the combination of conditions for evolving promiscuity are more probable to occur for surface-bound RNA replicators, suggesting that catalytic promiscuity may have been a significant factor in the diversification of prebiotic metabolic reaction networks.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1008634","type":"journal-article","created":{"date-parts":[[2021,1,26]],"date-time":"2021-01-26T13:48:32Z","timestamp":1611668912000},"page":"e1008634","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":4,"title":["Catalytic promiscuity in the RNA World may have aided the evolution of prebiotic metabolism"],"prefix":"10.1371","volume":"17","author":[{"given":"D\u00e1niel","family":"V\u00f6r\u00f6s","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9729-1224","authenticated-orcid":true,"given":"Bal\u00e1zs","family":"K\u00f6nny\u0171","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tam\u00e1s","family":"Cz\u00e1r\u00e1n","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2021,1,26]]},"reference":[{"key":"pcbi.1008634.ref001","doi-asserted-by":"crossref","first-page":"729","DOI":"10.1006\/cbir.2000.0668","article-title":"on the Early Evolutionary Origin of Biological Periodicity","volume":"26","author":"T G\u00e1nti","year":"2002","journal-title":"Cell Biol Int"},{"key":"pcbi.1008634.ref002","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1016\/0303-2647(74)90031-8","article-title":"Autopoiesis: The organization of living systems, its characterization and a model","volume":"5","author":"FG Varela","year":"1974","journal-title":"Biosystems"},{"key":"pcbi.1008634.ref003","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1038\/nchem.2202","article-title":"Common origins of RNA, protein and lipid precursors in a cyanosulfidic protometabolism","volume":"7","author":"BH Patel","year":"2015","journal-title":"Nat Chem"},{"key":"pcbi.1008634.ref004","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1038\/433469a","article-title":"In search of the simplest cell","volume":"433","author":"E Szathm\u00e1ry","year":"2005","journal-title":"Nature"},{"key":"pcbi.1008634.ref005","first-page":"618","author":"W Gilbert","year":"1986","journal-title":"The RNA world. Nature"},{"key":"pcbi.1008634.ref006","doi-asserted-by":"crossref","first-page":"2025","DOI":"10.1021\/ar200332w","article-title":"Asphalt, Water, and the Prebiotic Synthesis of Ribose, Ribonucleosides, and RNA","volume":"45","author":"SA Benner","year":"2012","journal-title":"Acc Chem Res"},{"key":"pcbi.1008634.ref007","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1007\/BF01733839","article-title":"HCN: A plausible source of purines, pyrimidines and amino acids on the primitive earth","volume":"11","author":"JP Ferris","year":"1978","journal-title":"J Mol Evol"},{"key":"pcbi.1008634.ref008","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1038\/26193","article-title":"RNA-catalysed nucleotide synthesis","volume":"395","author":"PJ Unrau","year":"1998","journal-title":"Nature"},{"key":"pcbi.1008634.ref009","doi-asserted-by":"crossref","first-page":"1011","DOI":"10.1038\/nchem.1781","article-title":"In-ice evolution of RNA polymerase ribozyme activity","volume":"5","author":"J Attwater","year":"2013","journal-title":"Nat Chem"},{"key":"pcbi.1008634.ref010","doi-asserted-by":"crossref","first-page":"1777","DOI":"10.1098\/rstb.2006.1903","article-title":"Montmorillonite-catalysed formation of RNA oligomers: the possible role of catalysis in the origins of life","volume":"361","author":"JP Ferris","year":"2006","journal-title":"Philos Trans R Soc Lond B Biol Sci"},{"key":"pcbi.1008634.ref011","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1038\/381059a0","article-title":"Synthesis of long Prebiotic Oligomers on Mineral Surfaces","volume":"381","author":"JP Ferris","year":"1996","journal-title":"Nature"},{"key":"pcbi.1008634.ref012","doi-asserted-by":"crossref","first-page":"9786","DOI":"10.1073\/pnas.1610103113","article-title":"Amplification of RNA by an RNA polymerase ribozyme","volume":"113","author":"DP Horning","year":"2016","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1008634.ref013","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1016\/S1074-5521(03)00003-6","article-title":"In search of an RNA replicase ribozyme","volume":"10","author":"KE McGinness","year":"2003","journal-title":"Chem Biol"},{"key":"pcbi.1008634.ref014","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1126\/science.1200752","article-title":"Ribozyme-Catalyzed Transcription of an Active Ribozyme","volume":"332","author":"A Wochner","year":"2011","journal-title":"Science (80-)"},{"key":"pcbi.1008634.ref015","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1007\/BF00623322","article-title":"Selforganization of matter and the evolution of biological macromolecules","volume":"58","author":"M Eigen","year":"1971","journal-title":"Naturwissenschaften"},{"key":"pcbi.1008634.ref016","doi-asserted-by":"crossref","first-page":"1751","DOI":"10.1098\/rstb.2007.2067","article-title":"Structural analyses of a hypothetical minimal metabolism","volume":"362","author":"T Gabald\u00f3n","year":"2007","journal-title":"Philos Trans R Soc B Biol Sci"},{"key":"pcbi.1008634.ref017","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1128\/MMBR.68.3.518-537.2004","article-title":"Determination of the Core of a Minimal Bacterial Gene Set","volume":"68","author":"R Gil","year":"2004","journal-title":"Microbiol Mol Biol Rev"},{"key":"pcbi.1008634.ref018","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1111\/nyas.12700","article-title":"The dynamics of the RNA world: insights and challenges","volume":"1341","author":"\u00c1 Kun","year":"2015","journal-title":"Ann N Y Acad Sci"},{"key":"pcbi.1008634.ref019","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/0167-2789(91)90049-F","article-title":"Spiral wave structure in pre-biotic evolution: Hypercycles stable against parasites","volume":"48","author":"MC Boerlijst","year":"1991","journal-title":"Phys D Nonlinear Phenom"},{"key":"pcbi.1008634.ref020","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1017\/CBO9780511525537.009","volume-title":"The geometry of ecological interactions: simplifying spatial complexity","author":"T Cz\u00e1r\u00e1n","year":"2000"},{"key":"pcbi.1008634.ref021","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1016\/S0022-5193(87)80191-1","article-title":"Group selection of early replicators and the origin of life","volume":"128","author":"E Szathm\u00e1ry","year":"1987","journal-title":"J Theor Biol"},{"key":"pcbi.1008634.ref022","first-page":"1669","article-title":"The evolution of replicators. Charlesworth B, Harvey PH, editors","volume":"355","author":"E Szathm\u00e1ry","year":"2000","journal-title":"Philos Trans R Soc London Ser B Biol Sci"},{"key":"pcbi.1008634.ref023","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1556\/Select.1.2000.1-3.13","article-title":"Avoiding Catch-22 of Early Evolution by Stepwise Increase in Copying Fidelity","volume":"1","author":"I Scheuring","year":"2000","journal-title":"Selection"},{"key":"pcbi.1008634.ref024","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1146\/annurev-biochem-030409-143718","article-title":"Enzyme Promiscuity: A Mechanistic and Evolutionary Perspective","volume":"79","author":"O Khersonsky","year":"2010","journal-title":"Annu Rev Biochem"},{"key":"pcbi.1008634.ref025","doi-asserted-by":"crossref","first-page":"448","DOI":"10.1126\/science.289.5478.448","article-title":"One Sequence, Two Ribozymes: Implications for the Emergence of New Ribozyme Folds","volume":"289","author":"EA Schultes","year":"2000","journal-title":"Science (80-)"},{"key":"pcbi.1008634.ref026","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-019-56986-8","article-title":"Dynamics and stability in prebiotic information integration: an RNA World model from first principles","volume":"10","author":"A Szil\u00e1gyi","year":"2020","journal-title":"Sci Rep"},{"key":"pcbi.1008634.ref027","doi-asserted-by":"crossref","first-page":"e20931","DOI":"10.1371\/journal.pone.0020931","article-title":"The evolution of enzyme specificity in the metabolic replicator model of prebiotic evolution","volume":"6","author":"B K\u00f6nny\u0171","year":"2011","journal-title":"PLoS One"},{"key":"pcbi.1008634.ref028","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1073\/pnas.58.1.217","article-title":"An extracellular Darwinian experiment with a self-duplicating nucleic acid molecule","volume":"58","author":"DR Mills","year":"1967","journal-title":"Proc Natl Acad Sci"},{"key":"pcbi.1008634.ref029","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1038\/280445a0","article-title":"Hypercycles and the origin of life","volume":"280","author":"J Maynard-Smith","year":"1979","journal-title":"Nature"},{"key":"pcbi.1008634.ref030","first-page":"9","article-title":"Gause\u2019s Principle and the Effect of Resource Partitioning on the Dynamical Coexistence of Replicating Templates","author":"A Szil\u00e1gyi","year":"2013","journal-title":"PLoS Comput Biol"},{"key":"pcbi.1008634.ref031","volume-title":"The Struggle for Existence","author":"GF Gause","year":"1934"},{"key":"pcbi.1008634.ref032","doi-asserted-by":"crossref","first-page":"1292","DOI":"10.1126\/science.131.3409.1292","article-title":"The Competitive Exclusion Principle","author":"G Hardin","year":"1960","journal-title":"Science. American Association for the Advancement of Science"},{"key":"pcbi.1008634.ref033","doi-asserted-by":"crossref","first-page":"48","DOI":"10.3390\/life7040048","article-title":"Ecology and Evolution in the RNA World Dynamics and Stability of Prebiotic Replicator Systems","volume":"7","author":"A Szil\u00e1gyi","year":"2017","journal-title":"Life"},{"key":"pcbi.1008634.ref034","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/j.jtbi.2015.06.002","article-title":"Metabolically Coupled Replicator Systems: Overview of an RNA-world model concept of prebiotic evolution on mineral surfaces","volume":"381","author":"T Cz\u00e1r\u00e1n","year":"2015","journal-title":"J Theor Biol"},{"key":"pcbi.1008634.ref035","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1186\/s12862-014-0234-8","article-title":"Phenotype\/genotype sequence complementarity and prebiotic replicator coexistence in the metabolically coupled replicator system","volume":"14","author":"B K\u00f6nny\u0171","year":"2014","journal-title":"BMC Evol Biol"},{"key":"pcbi.1008634.ref036","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1186\/s13062-015-0049-6","article-title":"In silico ribozyme evolution in a metabolically coupled RNA population","volume":"10","author":"B K\u00f6nny\u0171","year":"2015","journal-title":"Biol Direct"},{"key":"pcbi.1008634.ref037","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1007\/s00239-009-9278-6","article-title":"The origin of life: Chemical evolution of a metabolic system in a mineral honeycomb?","volume":"69","author":"S Branciamore","year":"2009","journal-title":"J Mol Evol"},{"key":"pcbi.1008634.ref038","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1128\/MR.52.4.452-484.1988","article-title":"Before enzymes and templates: theory of surface metabolism","volume":"52","author":"G W\u00e4chtersh\u00e4user","year":"1988","journal-title":"Microbiol Rev"},{"key":"pcbi.1008634.ref039","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1023\/A:1023982008714","article-title":"Cations as Mediators of the Adsorption of Nucleic Acids on Clay Surfaces in Prebiotic Environments","volume":"33","author":"M Franchi","year":"2003","journal-title":"Orig Life Evol Biosph"},{"key":"pcbi.1008634.ref040","doi-asserted-by":"crossref","first-page":"13750","DOI":"10.1021\/ja104106y","article-title":"Clay minerals mediate folding and regioselective interactions of RNA: A large-scale atomistic simulation study","volume":"132","author":"JB Swadling","year":"2010","journal-title":"J Am Chem Soc"},{"key":"pcbi.1008634.ref041","doi-asserted-by":"crossref","first-page":"909","DOI":"10.1016\/j.chembiol.2006.06.014","article-title":"Self-Assembly of a Group I Intron from Inactive Oligonucleotide Fragments","volume":"13","author":"EJ Hayden","year":"2006","journal-title":"Chem Biol"},{"key":"pcbi.1008634.ref042","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1186\/1471-2148-13-204","article-title":"Spatial aspects of prebiotic replicator coexistence and community stability in a surface-bound RNA world model","volume":"13","author":"B K\u00f6nny\u0171","year":"2013","journal-title":"BMC Evol Biol"},{"key":"pcbi.1008634.ref043","doi-asserted-by":"crossref","first-page":"498","DOI":"10.1016\/j.cbpa.2006.08.011","article-title":"Enzyme promiscuity: evolutionary and mechanistic aspects","volume":"10","author":"O Khersonsky","year":"2006","journal-title":"Curr Opin Chem Biol"},{"key":"pcbi.1008634.ref044","doi-asserted-by":"crossref","first-page":"1161","DOI":"10.1126\/science.860134","article-title":"Evolution and Tinkering","volume":"196","author":"F Jacob","year":"1977","journal-title":"Science (80-)"},{"key":"pcbi.1008634.ref045","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1146\/annurev.mi.30.100176.002205","article-title":"Enzyme Recruitment in Evolution of New Function","volume":"30","author":"RA Jensen","year":"1976","journal-title":"Annu Rev Microbiol"},{"key":"pcbi.1008634.ref046","doi-asserted-by":"crossref","first-page":"R91","DOI":"10.1016\/S1074-5521(99)80033-7","article-title":"Catalytic promiscuity and the evolution of new enzymatic activities","volume":"6","author":"PJ O\u2019Brien","year":"1999","journal-title":"Chem Biol"},{"key":"pcbi.1008634.ref047","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1038\/ng1482","article-title":"The \u201cevolvability\u201d of promiscuous protein functions","volume":"37","author":"A Aharoni","year":"2005","journal-title":"Nat Genet"},{"key":"pcbi.1008634.ref048","doi-asserted-by":"crossref","DOI":"10.7551\/mitpress\/1763.001.0001","volume-title":"Cellular automata machines: a new environment for modeling","author":"T Toffoli","year":"1987"},{"key":"pcbi.1008634.ref049","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/j.gene.2004.11.002","article-title":"A surface-mediated origin of the RNA world: Biogenic activities of clay-adsorbed RNA molecules","volume":"346","author":"M Franchi","year":"2005","journal-title":"Gene"},{"key":"pcbi.1008634.ref050","doi-asserted-by":"crossref","first-page":"318","DOI":"10.3390\/life4030318","article-title":"Prebiotic RNA Synthesis by Montmorillonite Catalysis","volume":"4","author":"S Jheeta","year":"2014","journal-title":"Life"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1008634","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,2,5]],"date-time":"2021-02-05T00:00:00Z","timestamp":1612483200000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1008634","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,2,8]],"date-time":"2021-02-08T01:45:47Z","timestamp":1612748747000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1008634"}},"subtitle":[],"editor":[{"given":"Christoph","family":"Kaleta","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2021,1,26]]},"references-count":50,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,1,26]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1008634","relation":{},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,1,26]]}}}