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Cited by 96RNA and protein synthesis mechanismsOrigins and Evolution of LifeEvolution and Genetic Dynamics

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

Open access
Carter, Charles·2015·Life
DOI 10.3390/life5010294PMC PMC4390853
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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.

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  • The RNA world paradigm is shifting to a peptide/RNA world paradigm.

    “In recent times, the RNA world paradigm is shifting to a peptide/RNA world paradigm [9,17,18,19,20,21,22,23,24,25,26].”

    From The Origin of Prebiotic Information System in the Peptide/RNA World: A Simulation Model of the Evolution of Translation and the Genetic Code (2019) · cites this paper as [17]

    The Conclusions (page unavailable) present a peptide/RNA world as a more credible alternative to the RNA World hypothesis. They also call the RNA World view the prevailing idea; the paper advocates an alternative but does not establish that the field’s paradigm is shifting toward it. (LLM, conf=0.87)

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  • Monomers such as nucleotides and amino acids were selected from random assemblies of molecular pools and polymerized on mineral substrate to create RNAs and peptides, heralding the peptide/RNA world.

    “Monomers, such as nucleotides and amino acids, were selected from random assemblies of molecular pools and then polymerized on the pores and pockets of the mineral substrate to create RNAs and peptides, heralding the peptide/RNA world [9,17,18,19,20,21,22,23,24,25,26].”

    From The Origin of Prebiotic Information System in the Peptide/RNA World: A Simulation Model of the Evolution of Translation and the Genetic Code (2019) · cites this paper as [17]

    Section 3.7 describes a proposed scenario in which amino acid and nucleic acid monomers assemble into peptide–RNA complexes, with peptide and oligonucleotide synthesis. The paper does not say that monomers were selected from random molecular pools or polymerized in pores and pockets of a mineral substrate. The pockets described in the Introduction’s Figure 2 belong to peptide–RNA structures, not minerals. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • The assembly of large and small subunits is dependent upon ribosomal proteins.

    “The assembly of large and small subunits that are dependent upon ribosomal proteins [17,92].”

    From The Origin of Prebiotic Information System in the Peptide/RNA World: A Simulation Model of the Evolution of Translation and the Genetic Code (2019) · cites this paper as [17]

    Section 3.3 of Results and Discussion (page unavailable) suggests that the simplest functional peptidyl-transferase center requires ribosomal proteins L2 and L3. It does not say that assembly of both the large and small ribosomal subunits depends on ribosomal proteins; its narrower, tentative point supports only part of the claim. (LLM, conf=0.81)

    Experimental — accuracy not yet measured

  • RNAs and proteins developed a symbiotic relationship to create ribosomes in the peptide/RNA world.

    “RNAs and proteins developed a symbiotic relationship to create ribosomes in the peptide/RNA world [17,18,19].”

    From The Origin of Prebiotic Information System in the Peptide/RNA World: A Simulation Model of the Evolution of Translation and the Genetic Code (2019) · cites this paper as [17]

    The Introduction proposes a reciprocal peptide–RNA partnership that could have formed a prototypic ancestral ribosome. Section 3.7 describes a putative path by which double-stranded RNA became the large ribosomal subunit. The paper presents this as an unproven evolutionary scenario, not an established account of how ribosomes arose. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • The ribosome may have first originated in a peptide/RNA world, where both amino acids and a variety of enzymes were available.

    “In recent times, the role of proteins in the origin of ribosomes is gaining currency, implying that the ribosome may have first originated in a peptide/RNA world, where both amino acids and a variety of enzymes were available [9,13,14,15,16,17,18,19,20,21,22,92].”

    From The Origin of Prebiotic Information System in the Peptide/RNA World: A Simulation Model of the Evolution of Translation and the Genetic Code (2019) · cites this paper as [17]

    The Introduction proposes a peptide–RNA complex as a possible prototypic ancestral ribosome, and Results and Discussion links early peptide catalysts to the origin of translation. But the paper does not establish that a variety of enzymes were available at that stage; Results and Discussion instead identifies the unavailability of activated amino acids as a critical barrier. The indexed passages have no page numbers. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

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Authors
Carter, C.
Affiliations
University of North Carolina at Chapel Hill (US)
Corresponding author
Carter, Charles
ORCID
Carter, Charles
Venue
Life
Publisher
MDPI AG
Published
2015-01-23
Volume
5
Issue
1
Pages
294-320
ISSN
2075-1729 (ISSN-L)
DOI
10.3390/life5010294
PMC
PMC4390853
OpenAlex
W2085949071
Cited by
95
References
108
Citations by year
2026: 4 · 2025: 8 · 2024: 9 · 2023: 8 · 2022: 13 · 2021: 6 · 2020: 13 · 2019: 12 · 2018: 6 · 2017: 4 · 2016: 4 · 2015: 8
FWCI
0.71
Type
journal article
Language
en
Open access
Licence
Locations
  • Life (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • NIGMS (78227)
  • NIH (40906)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
  • Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Keywords
RNA world, origin of life, oligopeptides, oligonucleotides, origin of the genetic code, aminoacyl-tRNA synthetase, tRNA anticodon, tRNA acceptor stem, ATP binding site, phylogenetic relationships, ribozymes, origin of translation

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