Catalytic promiscuity in the RNA World may have aided the evolution of prebiotic metabolism
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 replicato...
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Published in | PLoS computational biology Vol. 17; no. 1; p. e1008634 |
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Main Authors | , , |
Format | Journal Article |
Language | English |
Published |
United States
Public Library of Science
26.01.2021
Public Library of Science (PLoS) |
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Online Access | Get full text |
ISSN | 1553-7358 1553-734X 1553-7358 |
DOI | 10.1371/journal.pcbi.1008634 |
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Abstract | 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. |
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AbstractList | 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.
Complex biochemical machineries responsible for maintaining the correct ratio of enzymes and genes were highly unlikely to exist at the wake of life. Individual genes must have been subject to competition for resources of replication leading to the competitive exclusion between them, and thus to the loss of genetic information. A feasible scenario that avoids competitive exclusion requires the assumption of mandatory cooperation between the enzymes.
A potentially dynamically important but mostly neglected feature of RNA enzymes (ribozymes) is their capacity to catalyse more than a single reaction. Here, we analyse the possibility that this “promiscous” nature of prebiotic ribozymes could have helped the maintenance of early replicator communities cooperating in running a simple metabolism. To do so, we have implemented a spatially explicit computer model simulating the dynamics of replicating entities on a mineral surface–an extension of the Metabolically Coupled Replicator System including the possibility of multiple catalytic activities within the same replicator. Our results suggest that under realistic assumptions of replicator and metabolite mobility and feasible trade-off relations between different catalytic activities of the same RNA replicator molecule, catalytic promiscuity may have indeed helped booting up life through supporting the assembly of minimal metabolisms. Introduction Based on our current knowledge about life it is safe to say that every recent living creature consists of one or more cells, each cell featuring three functional units/“subsystems” [1,2]: one storing the genetic know-how of self-maintenance and reproduction and passing it down the generations (genetic machinery), another one supporting the other two subsystems with material and energy (metabolism) [1], and a boundary subsystem (e.g. membrane) connecting the previous two to the external world while providing them with individual existence. Apart from the many difficult problems related to the prebiotic supply of RNA building blocks [3,6–8] and template replication in the absence of specialized replicase enzymes [9–14], the RNA world hypothesis has to answer questions related to the stable maintenance of genetic information in RNA sequences that are sufficient to encode a working metabolism providing building blocks (nucleotides) for RNA replication, and a working replication machinery. Eigen himself looked for a solution to the competitive exclusion problem by proposing the hypercycle model, but it has been proven to be evolutionarily unstable in all its implementations except when wrapped in growing and dividing membrane vesicles, which amounts to invoking the–unlikely–emergence of the gene/membrane infrabiological system from the very beginning without a functional coupling of the two subsystems and leaving metabolism out altogether [33]. The obvious solution to this problem would be chromosomatization (the containment of more than a single gene in one RNA sequence), but this implies yet another potentially complicated mechanism: the selective and restricted splicing of long RNA strands, which requires at least another ribozyme species, besides an accurate replicase capable of copying long chromosomes without too many errors. 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.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. 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. Introduction Based on our current knowledge about life it is safe to say that every recent living creature consists of one or more cells, each cell featuring three functional units/“subsystems” [1,2]: one storing the genetic know-how of self-maintenance and reproduction and passing it down the generations (genetic machinery), another one supporting the other two subsystems with material and energy (metabolism) [1], and a boundary subsystem (e.g. membrane) connecting the previous two to the external world while providing them with individual existence. Apart from the many difficult problems related to the prebiotic supply of RNA building blocks [3,6–8] and template replication in the absence of specialized replicase enzymes [9–14], the RNA world hypothesis has to answer questions related to the stable maintenance of genetic information in RNA sequences that are sufficient to encode a working metabolism providing building blocks (nucleotides) for RNA replication, and a working replication machinery. Eigen himself looked for a solution to the competitive exclusion problem by proposing the hypercycle model, but it has been proven to be evolutionarily unstable in all its implementations except when wrapped in growing and dividing membrane vesicles, which amounts to invoking the–unlikely–emergence of the gene/membrane infrabiological system from the very beginning without a functional coupling of the two subsystems and leaving metabolism out altogether [33]. The obvious solution to this problem would be chromosomatization (the containment of more than a single gene in one RNA sequence), but this implies yet another potentially complicated mechanism: the selective and restricted splicing of long RNA strands, which requires at least another ribozyme species, besides an accurate replicase capable of copying long chromosomes without too many errors. |
Audience | Academic |
Author | Könnyű, Balázs Vörös, Dániel Czárán, Tamás |
AuthorAffiliation | Christian Albrechts Universitat zu Kiel, GERMANY 1 Department of Plant Systematics, Ecology and Theoretical Biology, Institute of Biology, Eötvös Loránd University, Budapest, Hungary 3 ELKH-ELTE Theoretical Biology and Evolutionary Research Group, Eötvös Loránd University, Budapest, Hungary 4 Institute of Evolution, ELKH Centre for Ecological Research, Budapest, Hungary 2 Evolutionary Systems Research Group, ELKH Centre for Ecological Research, Tihany, Hungary |
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BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33497378$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_1016_j_pbiomolbio_2024_07_002 crossref_primary_10_1038_s42003_025_07841_2 crossref_primary_10_1038_s41467_022_31387_0 |
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Snippet | The Metabolically Coupled Replicator System (MCRS) model of early chemical evolution offers a plausible and efficient mechanism for the self-assembly and the... Introduction Based on our current knowledge about life it is safe to say that every recent living creature consists of one or more cells, each cell featuring... |
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SubjectTerms | Analysis Biology and Life Sciences Catalytic RNA Chemical evolution (Origin of life) Chromosomes Computer and Information Sciences Containment Copying Efficiency Energy metabolism Engineering and Technology Enzyme activation Enzymes Evolution Gene sequencing Genes Genetic aspects Hypotheses Maintenance Membrane vesicles Membranes Metabolism Mutation Nucleotide sequence Nucleotides Parasites Physical Sciences Physiological aspects Prebiotics Replicase Replication Ribonucleic acid RNA Splicing Subsystems |
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Title | Catalytic promiscuity in the RNA World may have aided the evolution of prebiotic metabolism |
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