The origin of the RNA world: co-evolution of genes and metabolism.

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.

[1]  H. Noller The driving force for molecular evolution of translation. , 2004, RNA.

[2]  M Yarus,et al.  RNA-Catalyzed CoA, NAD, and FAD synthesis from phosphopantetheine, NMN, and FMN. , 2000, Biochemistry.

[3]  Y. Pilpel,et al.  Graded Autocatalysis Replication Domain (GARD): Kinetic Analysis of Self-Replication in Mutually Catalytic Sets , 1998, Origins of life and evolution of the biosphere.

[4]  D. Bartel,et al.  Processivity of ribozyme-catalyzed RNA polymerization. , 2003, Biochemistry.

[5]  A. Weber The Sugar Model: Catalysis by Amines and Amino Acid Products , 2001, Origins of life and evolution of the biosphere.

[6]  T. Steitz,et al.  The structural basis of ribosome activity in peptide bond synthesis. , 2000, Science.

[7]  H. Cleaves,et al.  The Nicotinamide Biosynthetic Pathway Is a By-Product of the RNA World , 2001, Journal of Molecular Evolution.

[8]  D. Rees Great metalloclusters in enzymology. , 2002, Annual review of biochemistry.

[9]  H. White Coenzymes as fossils of an earlier metabolic state , 1976, Journal of Molecular Evolution.

[10]  S. Strobel,et al.  Structural Evidence for a Two-Metal-Ion Mechanism of Group I Intron Splicing , 2005, Science.

[11]  M Yarus,et al.  A tiny RNA that catalyzes both aminoacyl-RNA and peptidyl-RNA synthesis. , 1999, RNA.

[12]  R. Rosenfeld Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[13]  G. F. Joyce The antiquity of RNA-based evolution , 2002, Nature.

[14]  Eric Smith,et al.  A mechanism for the association of amino acids with their codons and the origin of the genetic code. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[15]  F. Liu,et al.  Dipeptide seryl-histidine and related oligopeptides cleave DNA, protein, and a carboxyl ester. , 2000, Bioorganic & medicinal chemistry.

[16]  D. Kohda,et al.  Thermodynamic study of hybridization properties of heterochiral nucleic acids. , 2003, Biochemical and biophysical research communications.

[17]  M. Famulok,et al.  A novel ribozyme with ester transferase activity. , 1998, Chemistry & biology.

[18]  F. Young Biochemistry , 1955, The Indian Medical Gazette.

[19]  Deborah S. Kelley,et al.  Volcanoes, Fluids, and Life at Mid-Ocean Ridge Spreading Centers , 2002 .

[20]  H. Ohmoto,et al.  Evolution of early earth's atmosphere, hydrosphere, and biosphere : constraints from ore deposits , 2006 .

[21]  J. S. Weinger,et al.  Substrate-assisted catalysis of peptide bond formation by the ribosome , 2004, Nature Structural &Molecular Biology.

[22]  Constructing an RNA world , 1999 .

[23]  D. A. Usher,et al.  Hydrolytic stability of helical RNA: a selective advantage for the natural 3',5'-bond. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[24]  D. Söll,et al.  Aminoacyl-tRNA synthesis. , 2000, Annual review of biochemistry.

[25]  T. Higuchi,et al.  The intramolecular facilitated hydrolytic rates of methyl-substituted succinanilic acids. , 1966, Journal of the American Chemical Society.

[26]  S. Valadkhan snRNAs as the catalysts of pre-mRNA splicing. , 2005, Current opinion in chemical biology.

[27]  David Penny,et al.  An Interpretive Review of the Origin of Life Research , 2005 .

[28]  M. Yarus,et al.  RNA enzymes with two small-molecule substrates. , 1998, Chemistry & biology.

[29]  S. Altman,et al.  A trinucleotide can promote metal ion-dependent specific cleavage of RNA. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[30]  S. Bombard,et al.  Probing the mechanism of an Mn2+-dependent ribozyme by means of platinum complexes. , 1998, European Journal of Biochemistry.

[31]  J W Szostak,et al.  Nonenzymatic, template-directed ligation of oligoribonucleotides is highly regioselective for the formation of 3'-5' phosphodiester bonds. , 1996, Journal of the American Chemical Society.

[32]  太垣 和一郎,et al.  Bioorganic Chemistry , 2000 .

[33]  A. Jäschke,et al.  A small catalytic RNA motif with Diels-Alderase activity. , 1999, Chemistry & biology.

[34]  T. Dieckmann,et al.  Aptamer to Ribozyme: The Intrinsic Catalytic Potential of a Small RNA , 2006, Chembiochem : a European journal of chemical biology.

[35]  G. Cody,et al.  Primordial carbonylated iron-sulfur compounds and the synthesis of pyruvate. , 2000, Science.

[36]  R R Breaker,et al.  An amino acid as a cofactor for a catalytic polynucleotide. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[37]  M. Yarus,et al.  RNA-catalyzed amino acid activation. , 2001, Biochemistry.

[38]  A. Ellington,et al.  In vitro selection of ribozymes dependent on peptides for activity. , 2004, RNA.

[39]  M. Yarus,et al.  Acyl-CoAs from coenzyme ribozymes. , 2002, Biochemistry.

[40]  H. Urata,et al.  Kinetic analysis of hydrolytic reaction of homo- and heterochiral adenylyl(3'-5')adenosine isomers: breaking homochirality reduces hydrolytic stability of RNA. , 2005, Chemical communications.

[41]  W. Martin,et al.  On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[42]  B. List Proline-catalyzed asymmetric reactions , 2002 .

[43]  Elchanan Mossel,et al.  Random biochemical networks: the probability of self-sustaining autocatalysis. , 2005, Journal of theoretical biology.