Early evolution: prokaryotes, the new kids on the block.

Prokaryotes are generally assumed to be the oldest existing form of life on earth. This assumption, however, makes it difficult to understand certain aspects of the transition from earlier stages in the origin of life to more complex ones, and it does not account for many apparently ancient features in the eukaryotes. From a model of the RNA world, based on relic RNA species in modern organisms, one can infer that there was an absolute requirement for a high-accuracy RNA replicase even before proteins evolved. In addition, we argue here that the ribosome (together with the RNAs involved in its assembly) is so large that it must have had a prior function before protein synthesis. A model that connects and equates these two requirements (high-accuracy RNA replicase and prior function of the ribosome) can explain many steps in the origin of life while accounting for the observation that eukaryotes have retained more vestiges of the RNA world. The later derivation of prokaryote RNA metabolism and genome structure can be accounted for by the two complementary mechanisms of r-selection and thermoreduction.

[1]  Radhey S. Gupta,et al.  Phylogenetic analysis of 70 kD heat shock protein sequences suggests a chimeric origin for the eukaryotic cell nucleus , 1994, Current Biology.

[2]  R. Watson,et al.  Early and late helix-coil transitions in closed circular DNA. The number of superhelical turns in polyoma DNA. , 1968, Journal of molecular biology.

[3]  B. Sjöberg,et al.  A glycyl radical site in the crystal structure of a class III ribonucleotide reductase. , 1999, Science.

[4]  P. Forterre,et al.  DNA stability at temperatures typical for hyperthermophiles. , 1994, Nucleic acids research.

[5]  Masasuke Yoshida,et al.  Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[6]  G. B. Golding,et al.  The origin of the eukaryotic cell. , 1996, Trends in biochemical sciences.

[7]  Maurille J. Fournier,et al.  The Pseudouridine Residues of rRNA: Number, Location, Biosynthesis, and Function , 1998 .

[8]  Stanley L. Miller,et al.  The Origin and Early Evolution of Life: Prebiotic Chemistry, the Pre-RNA World, and Time , 1996, Cell.

[9]  S. Osawa,et al.  Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[10]  J A Lake,et al.  Evidence that eukaryotes and eocyte prokaryotes are immediate relatives. , 1992, Science.

[11]  D. Herschlag,et al.  An RNA chaperone activity of non‐specific RNA binding proteins in hammerhead ribozyme catalysis. , 1994, The EMBO journal.

[12]  I. Wool.  Extraribosomal functions of ribosomal proteins. , 1996, Trends in biochemical sciences.

[13]  H. Philippe,et al.  Archaea sister group of Bacteria? Indications from tree reconstruction artifacts in ancient phylogenies. , 1999, Molecular biology and evolution.

[14]  C. M. Joyce,et al.  A single side chain prevents Escherichia coli DNA polymerase I (Klenow fragment) from incorporating ribonucleotides. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[15]  W. Doolittle,et al.  Cytoskeletal proteins: The evolution of cell division , 1998, Current Biology.

[16]  Eugene V. Koonin,et al.  Helicases: amino acid sequence comparisons and structure-function relationships , 1993 .

[17]  W. Filipowicz,et al.  Exonucleolytic processing of small nucleolar RNAs from pre-mRNA introns. , 1995, Genes & development.

[18]  D. Penny,et al.  The Path from the RNA World , 1998, Journal of Molecular Evolution.

[19]  I. Bozzoni,et al.  A novel small nucleolar RNA (U16) is encoded inside a ribosomal protein intron and originates by processing of the pre‐mRNA. , 1993, The EMBO journal.

[20]  J. Steitz,et al.  Sno Storm in the Nucleolus: New Roles for Myriad Small RNPs , 1997, Cell.

[21]  P. Forterre.  A Hot Topic: The Origin of Hyperthermophiles , 1996, Cell.

[22]  P. Reichard,et al.  The evolution of ribonucleotide reduction. , 1997, Trends in biochemical sciences.

[23]  K. Gordon,et al.  Were RNA replication and translation directly coupled in the RNA (+protein?) World? , 1995, Journal of theoretical biology.

[24]  R. Sousa,et al.  A mutant T7 RNA polymerase as a DNA polymerase. , 1995, The EMBO journal.

[25]  W. Gilbert.  Origin of life: The RNA world , 1986, Nature.

[26]  A. Weiner,et al.  CCA-adding enzymes and poly(A) polymerases are all members of the same nucleotidyltransferase superfamily: characterization of the CCA-adding enzyme from the archaeal hyperthermophile Sulfolobus shibatae. , 1996, RNA.

[27]  V. Ambros,et al.  The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14 , 1993, Cell.

[28]  MICHAEL A. CHARLESTON,et al.  The Effects of Sequence Length, Tree Topology, and Number of Taxa on the Performance of Phylogenetic Methods , 1994, J. Comput. Biol..

[29]  H. Noller,et al.  A base pair between tRNA and 23S rRNA in the peptidyl transferase centre of the ribosome , 1995, Nature.

[30]  H F Noller,et al.  Identification of bases in 16S rRNA essential for tRNA binding at the 30S ribosomal P site , 1995, Science.

[31]  E. Szathmáry,et al.  Coding coenzyme handles: a hypothesis for the origin of the genetic code. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[32]  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.

[33]  R. Benne,et al.  RNA editing in kinetoplastid parasites: what to do with U. , 1997, Trends in microbiology.

[34]  V. Ramakrishnan,et al.  Ribosomal protein structures: insights into the architecture, machinery and evolution of the ribosome. , 1998, Trends in biochemical sciences.

[35]  M. Eigen,et al.  The Hypercycle: A principle of natural self-organization , 2009 .

[36]  Melting characteristics of highly supercoiled DNA. , 1992, Biophysical chemistry.

[37]  M. Fournier,et al.  The small nucleolar RNAs. , 1995, Annual review of biochemistry.

[38]  H. Noller.  Peptidyl transferase: protein, ribonucleoprotein, or RNA? , 1993, Journal of bacteriology.

[39]  A. Lamond,et al.  Structure and function in the nucleus. , 1998, Science.

[40]  P. Forterre.  Thermoreduction, a hypothesis for the origin of prokaryotes. , 1995, Comptes rendus de l'Academie des sciences. Serie III, Sciences de la vie.

[41]  J. Steitz,et al.  A small nucleolar RNA is processed from an intron of the human gene encoding ribosomal protein S3. , 1993, Genes & Development.

[42]  B. Ganem.  RNA world , 1987, Nature.

[43]  J. Steitz,et al.  A mammalian gene with introns instead of exons generating stable RNA products , 1996, Nature.

[44]  David Penny,et al.  Relics from the RNA World , 1998, Journal of Molecular Evolution.

[45]  M. Carlile.  Prokaryotes and eukaryotes: strategies and successes , 1982 .

[46]  M. Bortolin,et al.  Human U19 intron-encoded snoRNA is processed from a long primary transcript that possesses little potential for protein coding. , 1998, RNA.

[47]  R. Weinberg,et al.  The catalytic subunit of yeast telomerase. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[48]  R. Sousa,et al.  Structural and mechanistic relationships between nucleic acid polymerases. , 1996, Trends in biochemical sciences.

[49]  A. Weiner,et al.  Phylogeny from function: evidence from the molecular fossil record that tRNA originated in replication, not translation. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[50]  M. Belfort,et al.  Escherichia coli proteins, including ribosomal protein S12, facilitate in vitro splicing of phage T4 introns by acting as RNA chaperones. , 1994, Genes & development.

[51]  C. Woese,et al.  Phylogenetic structure of the prokaryotic domain: The primary kingdoms , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[52]  H. Philippe,et al.  How good are deep phylogenetic trees? , 1998, Current opinion in genetics & development.

[53]  O. Kandler,et al.  Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[54]  W A Hendrickson,et al.  Conferring RNA polymerase activity to a DNA polymerase: a single residue in reverse transcriptase controls substrate selection. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[55]  E. Pennisi.  The Nucleus's Revolving Door , 1998, Science.

[56]  J. Bachellerie,et al.  Small Nucleolar RNAs Guide the Ribose Methylations of Eukaryotic rRNAs , 1998 .

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

[58]  W. Gilbert,et al.  On the ancient nature of introns. , 1993, Gene.