Limits...
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.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.

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.


Related in: MedlinePlus

Stereochemistry of peptide-RNA conformational complementarity [1]. The minor groove in double-stranded RNA (magenta) complements the preferred right-hand twist of antiparallel β hairpin structures (wheat). Adjacent nucleotide and peptide strands are parallel (5'-3'; N-C) and the two sets are antiparallel. Van der Waals distances between peptide and nucleotide components are optimal precisely at a peptide radius for which there are exactly two amino acids per base. (Inset) The double-double helix is also stabilized by recurring hydrogen bonds between peptide carbonyl and the ribose 2'OH groups and between amide nitrogens and water molecules (blue spheres) between the ribose O1 and 2'OH groups. The resulting hydrogen-bonded network stabilizes a ribose orientation such that the 3'OH group is poised to serve as a nucleophile for polymerization.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4390853&req=5

life-05-00294-f001: Stereochemistry of peptide-RNA conformational complementarity [1]. The minor groove in double-stranded RNA (magenta) complements the preferred right-hand twist of antiparallel β hairpin structures (wheat). Adjacent nucleotide and peptide strands are parallel (5'-3'; N-C) and the two sets are antiparallel. Van der Waals distances between peptide and nucleotide components are optimal precisely at a peptide radius for which there are exactly two amino acids per base. (Inset) The double-double helix is also stabilized by recurring hydrogen bonds between peptide carbonyl and the ribose 2'OH groups and between amide nitrogens and water molecules (blue spheres) between the ribose O1 and 2'OH groups. The resulting hydrogen-bonded network stabilizes a ribose orientation such that the 3'OH group is poised to serve as a nucleophile for polymerization.

Mentions: In 1974, Carter and Kraut [1] showed by model building that the range of stable twisted conformations of extended polypeptides included a double-helical configuration that precisely complements the A form RNA double-helix (Figure 1). They proposed that this complementarity, and specifically a repeating hydrogen bond between ribose 2'OH groups and outward-pointing carbonyl oxygen atoms, suggested a basis for reciprocal pre-biotic autocatalysis, in which screw dislocations between the two partners could serve, respectively, as rudimentary active-sites for catalysis of subsequent polymerization of peptides by RNA and RNA by peptides (Figure 2) [1,2]. Thus, they afford simultaneously a stereochemical coding mechanism as well as a prototypic ancestral ribosome and polymerase. This affords an unproven, but logically consistent explanation for the fact that contemporary proteins are assembled by a ribozyme and contemporary nucleic acids are made by a protein polymerase. Although the stereochemistry of this model is compelling, it has not been tested experimentally. Indeed, the odyssey sketched here back again to this model as a possible origin for subsequent biological evolution has been indirect and replete with discovery. It makes a compelling case for pursuing experimental tests of the Carter–Kraut model.


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

Carter CW - Life (Basel) (2015)

Stereochemistry of peptide-RNA conformational complementarity [1]. The minor groove in double-stranded RNA (magenta) complements the preferred right-hand twist of antiparallel β hairpin structures (wheat). Adjacent nucleotide and peptide strands are parallel (5'-3'; N-C) and the two sets are antiparallel. Van der Waals distances between peptide and nucleotide components are optimal precisely at a peptide radius for which there are exactly two amino acids per base. (Inset) The double-double helix is also stabilized by recurring hydrogen bonds between peptide carbonyl and the ribose 2'OH groups and between amide nitrogens and water molecules (blue spheres) between the ribose O1 and 2'OH groups. The resulting hydrogen-bonded network stabilizes a ribose orientation such that the 3'OH group is poised to serve as a nucleophile for polymerization.
© Copyright Policy
Related In: Results  -  Collection

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

life-05-00294-f001: Stereochemistry of peptide-RNA conformational complementarity [1]. The minor groove in double-stranded RNA (magenta) complements the preferred right-hand twist of antiparallel β hairpin structures (wheat). Adjacent nucleotide and peptide strands are parallel (5'-3'; N-C) and the two sets are antiparallel. Van der Waals distances between peptide and nucleotide components are optimal precisely at a peptide radius for which there are exactly two amino acids per base. (Inset) The double-double helix is also stabilized by recurring hydrogen bonds between peptide carbonyl and the ribose 2'OH groups and between amide nitrogens and water molecules (blue spheres) between the ribose O1 and 2'OH groups. The resulting hydrogen-bonded network stabilizes a ribose orientation such that the 3'OH group is poised to serve as a nucleophile for polymerization.
Mentions: In 1974, Carter and Kraut [1] showed by model building that the range of stable twisted conformations of extended polypeptides included a double-helical configuration that precisely complements the A form RNA double-helix (Figure 1). They proposed that this complementarity, and specifically a repeating hydrogen bond between ribose 2'OH groups and outward-pointing carbonyl oxygen atoms, suggested a basis for reciprocal pre-biotic autocatalysis, in which screw dislocations between the two partners could serve, respectively, as rudimentary active-sites for catalysis of subsequent polymerization of peptides by RNA and RNA by peptides (Figure 2) [1,2]. Thus, they afford simultaneously a stereochemical coding mechanism as well as a prototypic ancestral ribosome and polymerase. This affords an unproven, but logically consistent explanation for the fact that contemporary proteins are assembled by a ribozyme and contemporary nucleic acids are made by a protein polymerase. Although the stereochemistry of this model is compelling, it has not been tested experimentally. Indeed, the odyssey sketched here back again to this model as a possible origin for subsequent biological evolution has been indirect and replete with discovery. It makes a compelling case for pursuing experimental tests of the Carter–Kraut model.

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.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.

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.


Related in: MedlinePlus