The "strong" RNA world hypothesis: fifty years old.

This year marks the 50(th) anniversary of a proposal by Alex Rich that RNA, as a single biopolymer acting in two capacities, might have supported both genetics and catalysis at the origin of life. We review here both published and previously unreported experimental data that provide new perspectives on this old proposal. The new data include evidence that, in the presence of borate, small amounts of carbohydrates can fix large amounts of formaldehyde that are expected in an environment rich in carbon dioxide. Further, we consider other species, including arsenate, arsenite, phosphite, and germanate, that might replace phosphate as linkers in genetic biopolymers. While linkages involving these oxyanions are judged to be too unstable to support genetics on Earth, we consider the possibility that they might do so in colder semi-aqueous environments more exotic than those found on Earth, where cosolvents such as ammonia might prevent freezing at temperatures well below 273 K. These include the ammonia-water environments that are possibly present at low temperatures beneath the surface of Titan, Saturn's largest moon.

[1]  M. Frank-Kamenetskii Are there any laws in biology?: comment on "How life changes itself: the Read-Write (RW) genome" by James Shapiro. , 2013, Physics of life reviews.

[2]  Steven A Benner,et al.  Amplification, mutation, and sequencing of a six-letter synthetic genetic system. , 2011, Journal of the American Chemical Society.

[3]  Steven A Benner,et al.  Phosphates, DNA, and the search for nonterrean life: a second generation model for genetic molecules. , 2002, Bioorganic chemistry.

[4]  R. Hazen,et al.  Mineral-organic interfacial processes: potential roles in the origins of life. , 2012, Chemical Society reviews.

[5]  M. Ebert,et al.  The structure of a TNA-TNA complex in solution: NMR study of the octamer duplex derived from alpha-(L)-threofuranosyl-(3'-2')-CGAATTCG. , 2008, Journal of the American Chemical Society.

[6]  A. Schoffstall Prebiotic phosphorylation of nucleosides in formamide , 1976, Origins of life.

[7]  Ronald Breslow,et al.  On the mechanism of the formose reaction , 1959 .

[8]  M. Chaussidon,et al.  Boron isotopic composition of tourmalines from the 3.8-Ga-old Isua supracrustals, West Greenland: implications on the δ11B value of early Archean seawater , 1997 .

[9]  Chiaolong Hsiao,et al.  RNA Folding and Catalysis Mediated by Iron (II) , 2012, PloS one.

[10]  J. Ferris,et al.  One-step, regioselective synthesis of up to 50-mers of RNA oligomers by montmorillonite catalysis. , 2006, Journal of the American Chemical Society.

[11]  H. Saimoto,et al.  Formose reactions. XXVIII. Selective formation of 2,4-bis(hydroxymethyl)-3-pentulose in N, N-dimethylformamide-water mixed solvent. , 1990 .

[12]  Gerald F. Joyce,et al.  1 Prospects for Understanding the Origin of the RNA World , 1993 .

[13]  S. Freier,et al.  The ups and downs of nucleic acid duplex stability: structure-stability studies on chemically-modified DNA:RNA duplexes. , 1997, Nucleic acids research.

[14]  C. Switzer,et al.  A pre-RNA candidate revisited: both enantiomers of flexible nucleoside triphosphates are DNA polymerase substrates. , 2008, Journal of the American Chemical Society.

[15]  Steven A Benner,et al.  2-Hydroxymethylboronate as a reagent to detect carbohydrates: application to the analysis of the formose reaction. , 2006, The Journal of organic chemistry.

[16]  S. Benner Water: Constraining Biological Chemistry and the Origin of Life , 2010 .

[17]  J. Pinto,et al.  Photochemical Production of Formaldehyde in Earth's Primitive Atmosphere , 1980, Science.

[18]  Steven A Benner,et al.  Synthetic Biology, Tinkering Biology, and Artificial Biology. What are We Learning? , 2011, Comptes rendus. Chimie.

[19]  W. Löb Über das Verhalten des Formamids unter der Wirkung der stillen Entladung Ein Beitrag zur Frage der Stickstoff-Assimilation , 1913 .

[20]  S A Benner,et al.  Modern metabolism as a palimpsest of the RNA world. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Samanta Pino,et al.  Generation of Long RNA Chains in Water* , 2009, The Journal of Biological Chemistry.

[22]  D. Deamer,et al.  Lipid-assisted Synthesis of RNA-like Polymers from Mononucleotides , 2008, Origins of Life and Evolution of Biospheres.

[23]  A W Schwartz,et al.  The case for an ancestral genetic system involving simple analogues of the nucleotides. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[24]  R. Curnow,et al.  The evolution of the genetic code. , 1976, Biochimie.

[25]  E. Szathmáry,et al.  What is the optimum size for the genetic alphabet? , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Thomas A Steitz,et al.  The structural basis of large ribosomal subunit function. , 2002, Annual review of biochemistry.

[27]  Gerald F. Joyce,et al.  2 Prospects for Understanding the Origin of the RNA World , 1999 .

[28]  Raffaele Saladino,et al.  Advances in the Prebiotic Synthesis of Nucleic Acids Bases: Implications for the Origin of Life , 2004 .

[29]  R V Williams,et al.  Genetic Takeover and the Mineral Origins of Life , 1983 .

[30]  J. Lunine,et al.  Modeling ammonia–ammonium aqueous chemistries in the Solar System’s icy bodies , 2012 .

[31]  H. Cleaves,et al.  The prebiotic geochemistry of formaldehyde , 2008 .

[32]  P. Holliger,et al.  Ribozyme-Catalyzed Transcription of an Active Ribozyme , 2011, Science.

[33]  J. B. Lambert,et al.  The Silicate-Mediated Formose Reaction: Bottom-Up Synthesis of Sugar Silicates , 2010, Science.

[34]  J. Szostak,et al.  Kinetic Analysis of an Efficient DNA-Dependent TNA Polymerase , 2005, Journal of the American Chemical Society.

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

[36]  P. Georghiou,et al.  The chemistry of the chromotropic acid method for the analysis of formaldehyde , 1989 .

[37]  M. Famulok,et al.  Generation and enzymatic amplification of high-density functionalized DNA double strands. , 2004, Angewandte Chemie.

[38]  S A Benner,et al.  Borate Minerals Stabilize Ribose , 2004, Science.

[39]  N. Sleep,et al.  Serpentinite and the dawn of life , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[40]  A. Jambon,et al.  Boron content and isotopic composition of oceanic basalts: Geochemical and cosmochemical implications , 1994 .

[41]  P. Coveney,et al.  Clay minerals mediate folding and regioselective interactions of RNA: a large-scale atomistic simulation study. , 2010, Journal of the American Chemical Society.

[42]  S. Benner,et al.  Synthesis of carbohydrates in mineral-guided prebiotic cycles. , 2011, Journal of the American Chemical Society.

[43]  C. Switzer,et al.  Nonenzymatic oligomerization of RNA by TNA templates. , 2006, Organic letters.

[44]  John S. Lewis,et al.  Book Review: The chemical evolution of the atmosphere and oceans. By Heinrich D. Holland. Princeton Univ. Press, Princeton, N.J., 1984. pp., pb 24.50, hb 75.00 , 1985 .

[45]  Eric Smith,et al.  The origin of the RNA world: co-evolution of genes and metabolism. , 2007, Bioorganic chemistry.

[46]  S. Benner,et al.  Oligonucleotides containing flexible nucleoside analogs , 1990 .

[47]  C. Woese,et al.  Evolution of the genetic code , 2004, The Science of Nature.

[48]  Weihong Tan,et al.  Locked nucleic acid molecular beacons. , 2005, Journal of the American Chemical Society.

[49]  R. Kellogg,et al.  Biotin. Its place in evolution , 1978, Journal of Molecular Evolution.

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

[51]  G. Fox,et al.  An exit cavity was crucial to the polymerase activity of the early ribosome. , 2012, Astrobiology.

[52]  SPATIAL, CHIRAL, AND TEMPORAL SELF‐ORGANIZATION THROUGH BIFURCATION IN “BIOIDS,” OPEN SYSTEMS CAPABLE OF A GENERALIZED DARWINIAN EVOLUTION , 1979 .

[53]  L. Orgel,et al.  Studies in prebiotic synthesis. VI. Synthesis of purine nucleosides. , 1968, Journal of molecular biology.

[54]  H. Beinert Iron-sulfur proteins: ancient structures, still full of surprises , 2000, JBIC Journal of Biological Inorganic Chemistry.

[55]  S. Benner,et al.  Comment on “The Silicate-Mediated Formose Reaction: Bottom-Up Synthesis of Sugar Silicates” , 2010, Science.

[56]  Michael Famulok,et al.  A versatile toolbox for variable DNA functionalization at high density. , 2005, Journal of the American Chemical Society.

[57]  Dan Schneider,et al.  Expanding the chemistry of DNA for in vitro selection. , 2010, Journal of the American Chemical Society.

[58]  B. Burgess The Iron-Molybdenum Cofactor of Nitrogenase , 1990 .

[59]  J. Bada,et al.  Borate Minerals and Origin of the RNA World , 2011, Origins of Life and Evolution of Biospheres.

[60]  F. Crick Origin of the Genetic Code , 1967, Nature.

[61]  Alexander Rich,et al.  On the problems of evolution and biochemical information transfer , 1962 .

[62]  N. Hud,et al.  Formation of a beta-pyrimidine nucleoside by a free pyrimidine base and ribose in a plausible prebiotic reaction. , 2007, Journal of the American Chemical Society.

[63]  R. J. Barto,et al.  Nucleoside and deoxynucleoside phosphorylation in formamide solutions , 1982, Origins of life.

[64]  L. Orgel,et al.  Studies in prebiotic synthesis. VII , 1972, Journal of Molecular Evolution.

[65]  M. Hollenstein,et al.  A DNAzyme with Three Protein‐Like Functional Groups: Enhancing Catalytic Efficiency of M2+‐Independent RNA Cleavage , 2009, Chembiochem : a European journal of chemical biology.

[66]  M. Robertson,et al.  Rates of decomposition of ribose and other sugars: implications for chemical evolution. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[67]  G. F. Joyce,et al.  Self-Sustained Replication of an RNA Enzyme , 2009, Science.

[68]  S. Benner,et al.  Inferring the palaeoenvironment of ancient bacteria on the basis of resurrected proteins , 2003, Nature.

[69]  A. Schoffstall,et al.  Phosphorylation mechanisms in chemical evolution , 1985, Origins of life and evolution of the biosphere.

[70]  L. Petruš,et al.  The Bílik Reaction , 2001 .

[71]  Peter Decker,et al.  Bioids : X. Identification of formose sugars, presumable prebiotic metabolites, using capillary gas chromatography/gas chromatography—mas spectrometry of n-butoxime trifluoroacetates on OV-225 , 1982 .