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What RNA World? Why a Peptide/RNA Partnership Merits Renewed Experimental Attention.

Carter CW - Life (Basel) (2015)

Bottom Line: We review arguments that biology emerged from a reciprocal partnership in which small ancestral oligopeptides and oligonucleotides initially both contributed rudimentary information coding and catalytic rate accelerations, and that the superior information-bearing qualities of RNA and the superior catalytic potential of proteins emerged from such complexes only with the gradual invention of the genetic code.Parallel hierarchical catalytic repertoires for increasingly highly conserved sequences from the two synthetase classes now increase the likelihood that they arose as translation products from opposite strands of a single gene.Sense/antisense coding affords a new bioinformatic metric for phylogenetic relationships much more distant than can be reconstructed from multiple sequence alignments of a single superfamily.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599-7260, USA. carter@med.unc.edu.

ABSTRACT
We review arguments that biology emerged from a reciprocal partnership in which small ancestral oligopeptides and oligonucleotides initially both contributed rudimentary information coding and catalytic rate accelerations, and that the superior information-bearing qualities of RNA and the superior catalytic potential of proteins emerged from such complexes only with the gradual invention of the genetic code. A coherent structural basis for that scenario was articulated nearly a decade before the demonstration of catalytic RNA. Parallel hierarchical catalytic repertoires for increasingly highly conserved sequences from the two synthetase classes now increase the likelihood that they arose as translation products from opposite strands of a single gene. Sense/antisense coding affords a new bioinformatic metric for phylogenetic relationships much more distant than can be reconstructed from multiple sequence alignments of a single superfamily. Evidence for distinct coding properties in tRNA acceptor stems and anticodons, and experimental demonstration that the two synthetase family ATP binding sites can indeed be coded by opposite strands of the same gene supplement these biochemical and bioinformatic data, establishing a solid basis for key intermediates on a path from simple, stereochemically coded, reciprocally catalytic peptide/RNA complexes through the earliest peptide catalysts to contemporary aminoacyl-tRNA synthetases. That scenario documents a path to increasing complexity that obviates the need for a single polymer to act both catalytically and as an informational molecule.

No MeSH data available.


Detailed scenario for the emergence of peptide and RNA polymers and steps toward the creation of the genetic code. Approximate time intervals run from the formation of liquid water on the earth to the appearance of the last universal common ancestor (LUCA) and specifically plot stages in the evolution of the aaRS that we have documented either by model building (Figure 1 and Figure 2) or experiments (Figure 5), and which therefore are arguable intermediates that do not require prior evolution of human technology. Major biochemical events are in italicized bold face. Sense/antisense coding appeared with the first reciprocally autocatalytic peptide–RNA complex and persisted until the evolution of aminoacyl-tRNA synthetases, tRNAs, and ribosomes enabled higher-specificity genetic coding.
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life-05-00294-f010: Detailed scenario for the emergence of peptide and RNA polymers and steps toward the creation of the genetic code. Approximate time intervals run from the formation of liquid water on the earth to the appearance of the last universal common ancestor (LUCA) and specifically plot stages in the evolution of the aaRS that we have documented either by model building (Figure 1 and Figure 2) or experiments (Figure 5), and which therefore are arguable intermediates that do not require prior evolution of human technology. Major biochemical events are in italicized bold face. Sense/antisense coding appeared with the first reciprocally autocatalytic peptide–RNA complex and persisted until the evolution of aminoacyl-tRNA synthetases, tRNAs, and ribosomes enabled higher-specificity genetic coding.

Mentions: Figure 10 summarizes a scenario for the origins of translation and the contemporary genetic code from an ensemble of peptide–RNA complexes (Figure 1 and Figure 2). This scenario makes several assumptions. Because reciprocal autocatalysis enables the transition from simplicity to complexity, these assumptions are far more limited than those necessary to produce a population of functional polymers of only one type. The most significant assumption is that a source of chemical free energy, perhaps polyphosphate [65,66], could drive the earliest dehydration reactions necessary for monomers to oligomerize and eventually, in the same time frame, for synthesis of nucleotide triphosphates (NTPs). Among the virtues of this scenario are that it is built from pieces that have been demonstrated, often by both model building and experimental construction and assays, and that all but the earliest of the postulated molecular species have strong phylogenetic support because they derive successively from the most highly conserved amino acid sequences in contemporary aaRS.


What RNA World? Why a Peptide/RNA Partnership Merits Renewed Experimental Attention.

Carter CW - Life (Basel) (2015)

Detailed scenario for the emergence of peptide and RNA polymers and steps toward the creation of the genetic code. Approximate time intervals run from the formation of liquid water on the earth to the appearance of the last universal common ancestor (LUCA) and specifically plot stages in the evolution of the aaRS that we have documented either by model building (Figure 1 and Figure 2) or experiments (Figure 5), and which therefore are arguable intermediates that do not require prior evolution of human technology. Major biochemical events are in italicized bold face. Sense/antisense coding appeared with the first reciprocally autocatalytic peptide–RNA complex and persisted until the evolution of aminoacyl-tRNA synthetases, tRNAs, and ribosomes enabled higher-specificity genetic coding.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4390853&req=5

life-05-00294-f010: Detailed scenario for the emergence of peptide and RNA polymers and steps toward the creation of the genetic code. Approximate time intervals run from the formation of liquid water on the earth to the appearance of the last universal common ancestor (LUCA) and specifically plot stages in the evolution of the aaRS that we have documented either by model building (Figure 1 and Figure 2) or experiments (Figure 5), and which therefore are arguable intermediates that do not require prior evolution of human technology. Major biochemical events are in italicized bold face. Sense/antisense coding appeared with the first reciprocally autocatalytic peptide–RNA complex and persisted until the evolution of aminoacyl-tRNA synthetases, tRNAs, and ribosomes enabled higher-specificity genetic coding.
Mentions: Figure 10 summarizes a scenario for the origins of translation and the contemporary genetic code from an ensemble of peptide–RNA complexes (Figure 1 and Figure 2). This scenario makes several assumptions. Because reciprocal autocatalysis enables the transition from simplicity to complexity, these assumptions are far more limited than those necessary to produce a population of functional polymers of only one type. The most significant assumption is that a source of chemical free energy, perhaps polyphosphate [65,66], could drive the earliest dehydration reactions necessary for monomers to oligomerize and eventually, in the same time frame, for synthesis of nucleotide triphosphates (NTPs). Among the virtues of this scenario are that it is built from pieces that have been demonstrated, often by both model building and experimental construction and assays, and that all but the earliest of the postulated molecular species have strong phylogenetic support because they derive successively from the most highly conserved amino acid sequences in contemporary aaRS.

Bottom Line: We review arguments that biology emerged from a reciprocal partnership in which small ancestral oligopeptides and oligonucleotides initially both contributed rudimentary information coding and catalytic rate accelerations, and that the superior information-bearing qualities of RNA and the superior catalytic potential of proteins emerged from such complexes only with the gradual invention of the genetic code.Parallel hierarchical catalytic repertoires for increasingly highly conserved sequences from the two synthetase classes now increase the likelihood that they arose as translation products from opposite strands of a single gene.Sense/antisense coding affords a new bioinformatic metric for phylogenetic relationships much more distant than can be reconstructed from multiple sequence alignments of a single superfamily.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599-7260, USA. carter@med.unc.edu.

ABSTRACT
We review arguments that biology emerged from a reciprocal partnership in which small ancestral oligopeptides and oligonucleotides initially both contributed rudimentary information coding and catalytic rate accelerations, and that the superior information-bearing qualities of RNA and the superior catalytic potential of proteins emerged from such complexes only with the gradual invention of the genetic code. A coherent structural basis for that scenario was articulated nearly a decade before the demonstration of catalytic RNA. Parallel hierarchical catalytic repertoires for increasingly highly conserved sequences from the two synthetase classes now increase the likelihood that they arose as translation products from opposite strands of a single gene. Sense/antisense coding affords a new bioinformatic metric for phylogenetic relationships much more distant than can be reconstructed from multiple sequence alignments of a single superfamily. Evidence for distinct coding properties in tRNA acceptor stems and anticodons, and experimental demonstration that the two synthetase family ATP binding sites can indeed be coded by opposite strands of the same gene supplement these biochemical and bioinformatic data, establishing a solid basis for key intermediates on a path from simple, stereochemically coded, reciprocally catalytic peptide/RNA complexes through the earliest peptide catalysts to contemporary aminoacyl-tRNA synthetases. That scenario documents a path to increasing complexity that obviates the need for a single polymer to act both catalytically and as an informational molecule.

No MeSH data available.