Footprints of a Singular 22-Nucleotide RNA Ring at the Origin of Life

(1) Background: Previous experimental observations and theoretical hypotheses have been providing insight into a hypothetical world where an RNA hairpin or ring may have debuted as the primary informational and functional molecule. We propose a model revisiting the architecture of RNA-peptide interactions at the origin of life through the evolutionary dynamics of RNA populations. (2) Methods: By performing a step-by-step computation of the smallest possible hairpin/ring RNA sequences compatible with building up a variety of peptides of the primitive network, we inferred the sequence of a singular docosameric RNA molecule, we call the ALPHA sequence. Then, we searched for any relics of the peptides made from ALPHA in sequences deposited in the different public databases. (3) Results: Sequence matching between ALPHA and sequences from organisms among the earliest forms of life on Earth were found at high statistical relevance. We hypothesize that the frequency of appearance of relics from ALPHA sequence in present genomes has a functional necessity. (4) Conclusions: Given the fitness of ALPHA as a supportive sequence of the framework of all existing theories, and the evolution of Archaea and giant viruses, it is anticipated that the unique properties of this singular archetypal ALPHA sequence should prove useful as a model matrix for future applications, ranging from synthetic biology to DNA computing.

[1]  C. Woese A New Biology for a New Century , 2004, Microbiology and Molecular Biology Reviews.

[2]  E. Bartnik,et al.  A glycine tRNA gene from lupine mitochondria. , 1986, Nucleic acids research.

[3]  Toshimichi Ikemura,et al.  tRNADB-CE: tRNA gene database curated manually by experts , 2008, Nucleic Acids Res..

[4]  A. Gospodinov,et al.  Possible Emergence of Sequence Specific RNA Aminoacylation via Peptide Intermediary to Initiate Darwinian Evolution and Code through Origin of Life , 2018, Life.

[5]  Alain Xayaphoummine,et al.  Kinefold web server for RNA/DNA folding path and structure prediction including pseudoknots and knots , 2005, Nucleic Acids Res..

[6]  Richard Robinson Jump-Starting a Cellular World: Investigating the Origin of Life, from Soup to Networks , 2005, PLoS biology.

[7]  Jacques Demongeot,et al.  A possible circular RNA at the origin of life. , 2007, Journal of theoretical biology.

[8]  K. Kaneko,et al.  The origin of the central dogma through conflicting multilevel selection , 2019, bioRxiv.

[9]  Georges Weil,et al.  The cyclic genetic code as a constraint satisfaction problem , 2004, Theor. Comput. Sci..

[10]  Andrzej Zielezinski,et al.  5SRNAdb: an information resource for 5S ribosomal RNAs , 2015, Nucleic Acids Res..

[11]  P. Schimmel,et al.  Oligonucleotide-directed peptide synthesis in a ribosome- and ribozyme-free system. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Harold S. Bernhardt The RNA world hypothesis: the worst theory of the early evolution of life (except for all the others)a , 2012, Biology Direct.

[13]  A. Barroso-deljesús,et al.  Specificity of the Hairpin Ribozyme , 1999, The Journal of Biological Chemistry.

[14]  Patricia P. Chan,et al.  GtRNAdb 2.0: an expanded database of transfer RNA genes identified in complete and draft genomes , 2015, Nucleic Acids Res..

[15]  H. Garner,et al.  Genomic leftovers: identifying novel microsatellites, over-represented motifs and functional elements in the human genome , 2016, Scientific Reports.

[16]  B. K. Davis Evolution of the genetic code. , 1999, Progress in biophysics and molecular biology.

[17]  J. Demongeot,et al.  Pentamers with Non-redundant Frames: Bias for Natural Circular Code Codons , 2020, Journal of Molecular Evolution.

[18]  V. Shestivska,et al.  Formation of nucleobases in a Miller–Urey reducing atmosphere , 2017, Proceedings of the National Academy of Sciences.

[19]  Paul Schimmel,et al.  Chiral-Selective Aminoacylation of an RNA Minihelix , 2004, Science.

[20]  J. Demongeot,et al.  Why Is AUG the Start Codon? , 2020, BioEssays : news and reviews in molecular, cellular and developmental biology.

[21]  J. M. Buzayan,et al.  Nucleic Acids Research Nucleotide sequence and newly formed phosphodJester bond of spontaneously Ugated satellite tobacco ringspot virus RNA , 2005 .

[22]  J. T. Staley Domain Cell Theory supports the independent evolution of the Eukarya, Bacteria and Archaea and the Nuclear Compartment Commonality hypothesis , 2017, Open Biology.

[23]  P. Schimmel,et al.  Chiral-selective aminoacylation of an RNA minihelix: Mechanistic features and chiral suppression , 2006, Proceedings of the National Academy of Sciences.

[24]  Takashi Ikegami,et al.  Artificial Chemistry: Computational Studies on the Emergence of Self-Reproducing Units , 2001, ECAL.

[25]  J. Demongeot,et al.  The Poitiers School of Mathematical and Theoretical Biology: Besson–Gavaudan–Schützenberger’s Conjectures on Genetic Code and RNA Structures , 2016, Acta biotheoretica.

[26]  Susanna Manrubia,et al.  On the networked architecture of genotype spaces and its critical effects on molecular evolution , 2018, Open Biology.

[27]  R. Pasini,et al.  Response to selection for seed yield and nitrogen (N2) fixation in common bean (Phaseolus vulgaris L.) , 1999 .

[28]  K. Opron,et al.  A tRNA- and Anticodon-Centric View of the Evolution of Aminoacyl-tRNA Synthetases, tRNAomes, and the Genetic Code , 2019, Life.

[29]  U. F. Müller Design and Experimental Evolution of trans-Splicing Group I Intron Ribozymes , 2017, Molecules.

[30]  Eugene V Koonin,et al.  Origin and evolution of the genetic code: The universal enigma , 2008, IUBMB life.

[31]  R. Breaker,et al.  Biochemical analysis of pistol self-cleaving ribozymes , 2015, RNA.

[32]  B. Damer,et al.  The Hot Spring Hypothesis for an Origin of Life , 2019, Astrobiology.

[33]  I. Agmon Could a Proto-Ribosome Emerge Spontaneously in the Prebiotic World? , 2016, Molecules.

[34]  E N Trifonov,et al.  Consensus temporal order of amino acids and evolution of the triplet code. , 2000, Gene.

[35]  G. F. Joyce,et al.  A self-replicating ligase ribozyme , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[36]  J. Demongeot,et al.  Emergence of a “Cyclosome” in a Primitive Network Capable of Building “Infinite” Proteins † , 2019, Life.

[37]  M. Di Giulio A comparison among the models proposed to explain the origin of the tRNA molecule: A synthesis. , 2009, Journal of molecular evolution.

[38]  D. Lancet,et al.  Protobiotic Systems Chemistry Analyzed by Molecular Dynamics , 2019, Life.

[39]  Taobo Hu,et al.  Coevolution Theory of the Genetic Code at Age Forty: Pathway to Translation and Synthetic Life , 2016, Life.

[40]  M. Yarus,et al.  Genetic code origins , 1989, Nature.

[41]  I. Potrykus,et al.  “Horizontal” Gene Transfer from a Transgenic Potato Line to a Bacterial Pathogen (Erwinia chrysanthemi) Occurs—if at All—at an Extremely Low Frequency , 1995, Bio/Technology.

[42]  Hervé Seligmann,et al.  Deamination gradients within codons after 12 position swap predict amino acid hydrophobicity and parallel β-sheet conformational preference , 2020, Biosyst..

[43]  M. Yarus The Genetic Code and RNA-Amino Acid Affinities , 2017, Life.

[44]  T. Ikegami,et al.  Self-maintenance and self-reproduction in an abstract cell model. , 2000, Journal of theoretical biology.

[45]  H. Seligmann Protein Sequences Recapitulate Genetic Code Evolution , 2018, Computational and structural biotechnology journal.

[46]  Zasha Weinberg,et al.  Identification of Hammerhead Ribozymes in All Domains of Life Reveals Novel Structural Variations , 2011, PLoS Comput. Biol..

[47]  Jonathan Perreault,et al.  The ubiquitous hammerhead ribozyme. , 2012, RNA.

[48]  D. Raoult,et al.  Unifying view of stem-loop hairpin RNA as origin of current and ancient parasitic and non-parasitic RNAs, including in giant viruses. , 2016, Current opinion in microbiology.

[49]  Huang Gao,et al.  Database resources of the National Center for Biotechnology Information , 2015, Nucleic Acids Res..

[50]  C J Michel,et al.  A complementary circular code in the protein coding genes. , 1996, Journal of theoretical biology.

[51]  J. Oró,et al.  Synthesis of purines under possible primitive earth conditions. I. Adenine from hydrogen cyanide. , 1961, Archives of biochemistry and biophysics.

[52]  J. Demongeot,et al.  Spontaneous evolution of circular codes in theoretical minimal RNA rings. , 2019, Gene.

[53]  Thijs J. G. Ettema,et al.  Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life , 2017, Science.

[54]  J. Demongeot,et al.  Theoretical minimal RNA rings recapitulate the order of the genetic code's codon-amino acid assignments. , 2019, Journal of theoretical biology.

[55]  J. Claverie,et al.  Diversity and evolution of the emerging Pandoraviridae family , 2017, Nature Communications.

[56]  M. Yarus Eighty routes to a ribonucleotide world; dispersion and stringency in the decisive selection , 2018, RNA.

[57]  Jacques Demongeot,et al.  Bias for 3′-Dominant Codon Directional Asymmetry in Theoretical Minimal RNA Rings , 2019, J. Comput. Biol..

[58]  V. Cognat,et al.  A global picture of tRNA genes in plant genomes. , 2011, The Plant journal : for cell and molecular biology.

[59]  E. Trifonov,et al.  Sequence fossils, triplet expansion, and reconstruction of earliest codons. , 1997, Gene.

[60]  J. Fontecilla-Camps Geochemical Continuity and Catalyst/Cofactor Replacement in the Emergence and Evolution of Life. , 2018, Angewandte Chemie.

[61]  H. Santana,et al.  Which Amino Acids Should Be Used in Prebiotic Chemistry Studies? , 2008, Origins of Life and Evolution of Biospheres.

[62]  A. Driessen,et al.  Archaeal phospholipids: Structural properties and biosynthesis. , 2017, Biochimica et biophysica acta. Molecular and cell biology of lipids.

[63]  Patricia P. Chan,et al.  tRNAscan-SE: Searching for tRNA Genes in Genomic Sequences. , 2019, Methods in molecular biology.

[64]  M J Dufton,et al.  Genetic code synonym quotas and amino acid complexity: cutting the cost of proteins? , 1997, Journal of theoretical biology.

[65]  J. Demongeot,et al.  The primordial tRNA acceptor stem code from theoretical minimal RNA ring clusters , 2020, BMC Genetics.

[66]  M. Eigen Selforganization of matter and the evolution of biological macromolecules , 1971, Naturwissenschaften.

[67]  Valérie Cognat,et al.  PlantRNA, a database for tRNAs of photosynthetic eukaryotes , 2012, Nucleic Acids Res..

[68]  M. Eigen,et al.  Transfer-RNA: The early adaptor , 1981, Naturwissenschaften.

[69]  D. Raine,et al.  A Fission-Fusion Origin for Life , 1998, Origins of life and evolution of the biosphere.

[70]  Pelin Yilmaz,et al.  The SILVA ribosomal RNA gene database project: improved data processing and web-based tools , 2012, Nucleic Acids Res..

[71]  M. Paecht-Horowitz The origin of life. , 1973, Angewandte Chemie.

[72]  J. Demongeot,et al.  Accretion history of large ribosomal subunits deduced from theoretical minimal RNA rings is congruent with histories derived from phylogenetic and structural methods. , 2020, Gene.

[73]  Yan Boucher,et al.  Use of 16S rRNA and rpoB Genes as Molecular Markers for Microbial Ecology Studies , 2006, Applied and Environmental Microbiology.

[74]  Paul Bourgine,et al.  Autopoiesis and Cognition , 2004, Artificial Life.

[75]  M. K. Hobish,et al.  Direct interaction between amino acids and nucleotides as a possible physicochemical basis for the origin of the genetic code. , 1995, Advances in space research : the official journal of the Committee on Space Research.

[76]  J. Demongeot,et al.  Theoretical minimal RNA rings designed according to coding constraints mimic deamination gradients , 2019, The Science of Nature.

[77]  S. Miller A production of amino acids under possible primitive earth conditions. , 1953, Science.

[78]  J. Thompson,et al.  Circular code motifs in the ribosome: a missing link in the evolution of translation? , 2019, RNA.

[79]  M. Rodnina,et al.  Importance of tRNA interactions with 23S rRNA for peptide bond formation on the ribosome: studies with substrate analogs , 2007, Biological chemistry.

[80]  D. Raoult,et al.  Stem-Loop RNA Hairpins in Giant Viruses: Invading rRNA-Like Repeats and a Template Free RNA , 2018, Front. Microbiol..

[81]  E. Szathmáry,et al.  On origin of genetic code and tRNA before translation , 2011, Biology Direct.

[82]  J. Wong,et al.  Coevolution theory of the genetic code at age thirty. , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[83]  Erin A. Becker,et al.  Phylogenetically Driven Sequencing of Extremely Halophilic Archaea Reveals Strategies for Static and Dynamic Osmo-response , 2014, PLoS genetics.

[84]  How did Metabolism and Genetic Replication Get Married? , 2012, Origins of Life and Evolution of Biospheres.

[85]  P. Forterre,et al.  Phylogeny and evolution of the Archaea: one hundred genomes later. , 2011, Current opinion in microbiology.

[86]  E. Koonin Frozen Accident Pushing 50: Stereochemistry, Expansion, and Chance in the Evolution of the Genetic Code , 2017, Life.

[87]  P. Forterre The Common Ancestor of Archaea and Eukarya Was Not an Archaeon , 2013, Archaea.

[88]  R. Knight,et al.  RNA–Amino Acid Binding: A Stereochemical Era for the Genetic Code , 2009, Journal of Molecular Evolution.

[89]  S. Giannerini,et al.  On the origin of degeneracy in the genetic code , 2019, Interface Focus.

[90]  G. Kroemer,et al.  Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere , 2018, Nature Communications.

[91]  C. Sagan,et al.  Synthesis of Adenosine Triphosphate Under Possible Primitive Earth Conditions , 1963, Nature.

[92]  Antonio Lazcano,et al.  Primordial synthesis of amines and amino acids in a 1958 Miller H2S-rich spark discharge experiment , 2011, Proceedings of the National Academy of Sciences.

[93]  D. Raine,et al.  Lipid domain boundaries as prebiotic catalysts of peptide bond formation. , 2007, Journal of theoretical biology.

[94]  J. Demongeot,et al.  More Pieces of Ancient than Recent Theoretical Minimal Proto-tRNA-Like RNA Rings in Genes Coding for tRNA Synthetases , 2019, Journal of Molecular Evolution.

[95]  P. Schimmel,et al.  Peptide synthesis with a template-like RNA guide and aminoacyl phosphate adaptors , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[96]  Peter F. Stadler,et al.  tRNAdb 2009: compilation of tRNA sequences and tRNA genes , 2008, Nucleic Acids Res..

[97]  M. Giulio On the Origin of Protein Synthesis: A Speculative Model Based on Hairpin RNA Structures , 1994 .

[98]  M. Tomita,et al.  Sequence Evidence in the Archaeal Genomes that tRNAs Emerged Through the Combination of Ancestral Genes as 5′ and 3′ tRNA Halves , 2008, PloS one.

[99]  Robert D. Finn,et al.  Rfam 13.0: shifting to a genome-centric resource for non-coding RNA families , 2017, Nucleic Acids Res..

[100]  R. Shapiro Small Molecule Interactions were Central to the Origin of Life , 2006, The Quarterly Review of Biology.

[101]  Doron Lancet,et al.  Systems protobiology: origin of life in lipid catalytic networks , 2018, Journal of The Royal Society Interface.

[102]  Laura Eme,et al.  Archaea and the origin of eukaryotes , 2017, Nature Reviews Microbiology.

[103]  J. Wedekind,et al.  Water in the active site of an all-RNA hairpin ribozyme and effects of Gua8 base variants on the geometry of phosphoryl transfer. , 2006, Biochemistry.