Coupled Catabolism and Anabolism in Autocatalytic RNA Sets

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2018 Jul 9

PMID 29982824

Citations 20

Authors

Simon Arsene

Sandeep Ameta

Niles Lehman

Andrew D Griffiths

Philippe Nghe

Affiliations

Soon will be listed here.

Abstract

The ability to process molecules available in the environment into useable building blocks characterizes catabolism in contemporary cells and was probably critical for the initiation of life. Here we show that a catabolic process in collectively autocatalytic sets of RNAs allows diversified substrates to be assimilated. We modify fragments of the Azoarcus group I intron and find that the system is able to restore the original native fragments by a multi-step reaction pathway. This allows in turn the formation of catalysts by an anabolic process, eventually leading to the accumulation of ribozymes. These results demonstrate that rudimentary self-reproducing RNA systems based on recombination possess an inherent capacity to assimilate an expanded repertoire of chemical resources and suggest that coupled catabolism and anabolism could have arisen at a very early stage in primordial living systems.

Citing Articles

Competitive exclusion among self-replicating molecules curtails the tendency of chemistry to diversify.

Eleveld M, Geiger Y, Wu J, Kiani A, Schaeffer G, Otto S Nat Chem. 2024; 17(1):132-140.

PMID: 39613869 DOI: 10.1038/s41557-024-01664-0.

Origin & influence of autocatalytic reaction networks at the advent of the RNA world.

Zorc S, Roy R RNA Biol. 2024; 21(1):78-92.

PMID: 39358873 PMC: 11451275. DOI: 10.1080/15476286.2024.2405757.

The protometabolic nature of prebiotic chemistry.

Nogal N, Sanz-Sanchez M, Vela-Gallego S, Ruiz-Mirazo K, de la Escosura A Chem Soc Rev. 2023; 52(21):7359-7388.

PMID: 37855729 PMC: 10614573. DOI: 10.1039/d3cs00594a.

Light-driven eco-evolutionary dynamics in a synthetic replicator system.

Liu K, Blokhuis A, van Ewijk C, Kiani A, Wu J, Roos W Nat Chem. 2023; 16(1):79-88.

PMID: 37653230 DOI: 10.1038/s41557-023-01301-2.

Multispecies autocatalytic RNA reaction networks in coacervates.

Ameta S, Kumar M, Chakraborty N, Matsubara Y, Prashanth S , Gandavadi D Commun Chem. 2023; 6(1):91.

PMID: 37156998 PMC: 10167250. DOI: 10.1038/s42004-023-00887-5.

References

Eigen M, Schuster P . The hypercycle. A principle of natural self-organization. Part A: Emergence of the hypercycle. Naturwissenschaften. 1977; 64(11):541-65. DOI: 10.1007/BF00450633. View

Kivioja T, Vaharautio A, Karlsson K, Bonke M, Enge M, Linnarsson S . Counting absolute numbers of molecules using unique molecular identifiers. Nat Methods. 2011; 9(1):72-4. DOI: 10.1038/nmeth.1778. View

Jayathilaka T, Lehman N . Spontaneous Covalent Self-Assembly of the Azoarcus Ribozyme from Five Fragments. Chembiochem. 2017; 19(3):217-220. DOI: 10.1002/cbic.201700591. View

Hordijk W, Steel M . Chasing the tail: The emergence of autocatalytic networks. Biosystems. 2016; 152:1-10. DOI: 10.1016/j.biosystems.2016.12.002. View

Kim D, Joyce G . Cross-catalytic replication of an RNA ligase ribozyme. Chem Biol. 2004; 11(11):1505-12. DOI: 10.1016/j.chembiol.2004.08.021. View

Sievers D, von Kiedrowski G . Self-replication of complementary nucleotide-based oligomers. Nature. 1994; 369(6477):221-4. DOI: 10.1038/369221a0. View

Lee D, Severin K, Ghadiri M . Autocatalytic networks: the transition from molecular self-replication to molecular ecosystems. Curr Opin Chem Biol. 1998; 1(4):491-6. DOI: 10.1016/s1367-5931(97)80043-9. View

Huang W, Ferris J . One-step, regioselective synthesis of up to 50-mers of RNA oligomers by montmorillonite catalysis. J Am Chem Soc. 2006; 128(27):8914-9. DOI: 10.1021/ja061782k. View

Orgel L . Prebiotic chemistry and the origin of the RNA world. Crit Rev Biochem Mol Biol. 2004; 39(2):99-123. DOI: 10.1080/10409230490460765. View

10.

Vaidya N, Walker S, Lehman N . Recycling of informational units leads to selection of replicators in a prebiotic soup. Chem Biol. 2013; 20(2):241-52. DOI: 10.1016/j.chembiol.2013.01.007. View

11.

Draper W, Hayden E, Lehman N . Mechanisms of covalent self-assembly of the Azoarcus ribozyme from four fragment oligonucleotides. Nucleic Acids Res. 2007; 36(2):520-31. PMC: 2241849. DOI: 10.1093/nar/gkm1055. View

12.

Copley S, Smith E, Morowitz H . The origin of the RNA world: co-evolution of genes and metabolism. Bioorg Chem. 2007; 35(6):430-43. DOI: 10.1016/j.bioorg.2007.08.001. View

13.

Jain S, Krishna S . A model for the emergence of cooperation, interdependence, and structure in evolving networks. Proc Natl Acad Sci U S A. 2001; 98(2):543-7. PMC: 14623. DOI: 10.1073/pnas.98.2.543. View

14.

Kauffman S . Autocatalytic sets of proteins. J Theor Biol. 1986; 119(1):1-24. DOI: 10.1016/s0022-5193(86)80047-9. View

15.

Chen X, Li N, Ellington A . Ribozyme catalysis of metabolism in the RNA world. Chem Biodivers. 2007; 4(4):633-55. DOI: 10.1002/cbdv.200790055. View

16.

Hayden E, von Kiedrowski G, Lehman N . Systems chemistry on ribozyme self-construction: evidence for anabolic autocatalysis in a recombination network. Angew Chem Int Ed Engl. 2008; 47(44):8424-8. DOI: 10.1002/anie.200802177. View

17.

Higgs P, Lehman N . The RNA World: molecular cooperation at the origins of life. Nat Rev Genet. 2014; 16(1):7-17. DOI: 10.1038/nrg3841. View

18.

Hordijk W, Steel M, Kauffman S . The structure of autocatalytic sets: evolvability, enablement, and emergence. Acta Biotheor. 2012; 60(4):379-92. DOI: 10.1007/s10441-012-9165-1. View

19.

Cech T . Self-splicing of group I introns. Annu Rev Biochem. 1990; 59:543-68. DOI: 10.1146/annurev.bi.59.070190.002551. View

20.

Yeates J, Hilbe C, Zwick M, Nowak M, Lehman N . Dynamics of prebiotic RNA reproduction illuminated by chemical game theory. Proc Natl Acad Sci U S A. 2016; 113(18):5030-5. PMC: 4983821. DOI: 10.1073/pnas.1525273113. View