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 inPLoS computational biology Vol. 17; no. 1; p. e1008634
Main Authors Vörös, Dániel, Könnyű, Balázs, Czárán, Tamás
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 26.01.2021
Public Library of Science (PLoS)
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ISSN1553-7358
1553-734X
1553-7358
DOI10.1371/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.
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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– name: 3 ELKH-ELTE Theoretical Biology and Evolutionary Research Group, Eötvös Loránd University, Budapest, Hungary
– name: 1 Department of Plant Systematics, Ecology and Theoretical Biology, Institute of Biology, Eötvös Loránd University, Budapest, Hungary
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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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