Skip to main content
SpringerLink
Log in

Pentamers with Non-redundant Frames: Bias for Natural Circular Code Codons

  • Original Article
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

The natural circular code consists of 20 codons (X0) overrepresented in the coding frame of protein-coding genes as compared to remaining noncoding frames, and X1 and X2 (N1N2N3 → N3N1N2 and N1N2N3 → N2N3N1 permutations of X0, overrepresented in + 1 and − 1 frames of protein-coding genes, not self-complementary). X0, X1 and X2 detect ribosomal, + 1 and − 1 frames. X0 spontaneously emerges in the 25 theoretical minimal RNA rings, 22-nucleotide-long circular RNAs designed to code once for each of the genetic code’s coding signals (a start, a stop and each of the 20 amino acids) by three overlapping frames. RNA rings presumed ancient are biased for X1, and bias for X0 increases in presumed recent RNA rings, indicating an evolutionary X1-to-X0 switch. Here, analyses explore biases for X0, X1 and X2 in non-redundant nucleotide tetra- and pentamers, for different genetic codes. Biases for X0 occur in non-redundant nucleotide pentamers and seem stronger in nuclear than mitochondrial genetic codes; tendencies are opposite for X1. Strand-asymmetric replication presumably causes mitogenomes to escape Chargaff’s rule which expects ratios A/T = G/C = 1 in single-stranded sequences. Hence, presumably X1 emerged in ancient genetic codes used in single-stranded protogenomes/coding RNAs; the self-complementary X0 presumably evolved secondarily with double-stranded genomes and strand-symmetric replication. Results indicate that selection for non-redundant overlap coding in short nucleotide sequences produced the natural circular code.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Abrahams L, Hurst LD (2018) Refining the Ambush hypothesis: evidence that GC- and AT-rich bacteria employ different frameshift defence strategies. Genome Biol Evol 10:1153–1173

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ahmed A, Frey G, Michel CJ (2010) Essential molecular functions associated with the circular code evolution. J Theor Biol 264:613–622

    CAS  PubMed  Google Scholar 

  • Arquès DG, Michel CJ (1996) A complementary circular code in the protein coding genes. J Theor Biol 182:45–58

    PubMed  Google Scholar 

  • Arquès DG, Michel CJ (1997) A circular code in the protein coding genes of mitochondria. J Theor Biol 189:273–290

    PubMed  Google Scholar 

  • Bartonek L, Braun D, Zagrovic B (2019) Invariants of frameshifted variants. bioRxiv, 27 June 2019. https://doi.org/10.1101/684076.

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300

    Google Scholar 

  • Colson P, Ravaux I, Tamalet C, Glazunova O, Baptiste E, Chabriere E, Wiedemann A, Lacabaratz C, Chefrour M, Picard C, Stein A, Levy Y, Raoult D (2014) HIV infection en route to endogenization: two cases. Clim Microbiol Infect 20:1280–1288

    CAS  Google Scholar 

  • Crick FH, Griffith JS, Orgel LE (1957) Codes without commas. Proc Natl Acad Sci USA 43:416–421

    CAS  PubMed  Google Scholar 

  • Demongeot J (1978) Sur la possibilité de considérer le code génétique comme un code à enchaînement. Rev Biomath 62:61–66

    CAS  Google Scholar 

  • Demongeot J, Besson J (1983) Genetic-code and cyclic codes. Comptes R Acad Sci III Life Sci 296:807–810

    CAS  Google Scholar 

  • Demongeot J, Moreira A (2007) A possible circular RNA at the origin of life. J Theor Biol 249:314–324

    CAS  PubMed  Google Scholar 

  • Demongeot J, Norris V (2019) Emergence of a “cyclosome” in a primitive network capable of building “infinite” proteins. Life 9:51

    PubMed Central  Google Scholar 

  • Demongeot J, Seligmann H (2019a) Spontaneous evolution of circular codes in theoretical minimal RNA rings. Gene 705:95–102

    CAS  PubMed  Google Scholar 

  • Demongeot J, Seligmann H (2019b) Theoretical minimal RNA rings recapitulate the order of the genetic code's codon-amino acid assignments. J Theor Biol 471:108–116

    CAS  PubMed  Google Scholar 

  • Demongeot J, Seligmann H (2019c) Bias for 3'-dominant codon directional asymmetry in theoretical minimal RNA rings. J Comput Biol. https://doi.org/10.1089/cmb.2018.0256

    Article  PubMed  Google Scholar 

  • Demongeot J, Seligmann H (2019d) More pieces of ancient than recent theoretical minimal proto-tRNA-like RNA rings in genes coding for tRNA synthetases. J Mol Evol 87(4–6):152–174

    CAS  Google Scholar 

  • Demongeot J, Seligmann H (2019e) Theoretical minimal RNA rings designed according to coding constraints mimic deamination gradients. The Science of Life / Die Naturwissenschaften 106:44

    Google Scholar 

  • Dila G, Michel CJ, Poch O, Ripp R, Thompson J (2018) Evolutionary conservation and functional implications of circular code motifs in eukaryotic genomes. Biosystems 175:57–74

    PubMed  Google Scholar 

  • Eigen M, Winkler-Oswatitsch R (1981) Transfer-RNA, an early gene? Naturwissenschaften 68:282–292

    CAS  PubMed  Google Scholar 

  • El Houmami N, Seligmann H (2017) Evolution of nucleotide punctuation marks: from structural to linear signals. Font Genet 8:36

    Google Scholar 

  • El Soufi K, Michel CJ (2014) Circular code motifs in the ribosome decoding center. Comput Biol Chem 52:9–17

    PubMed  Google Scholar 

  • El Soufi K, Michel CJ (2015) Circular code motifs near the ribosome decoding center. Comput Biol Chem 59A:158–176

    Google Scholar 

  • Elzanowski A, Ostell J (2019) The genetic codes. https://www.ncbi.nlm.nih.gov/Taxonomy/Utils/wprintgc.cgi

  • Ferreira R, Coutinho KR (1993) Simulation studies of self-replicating oligoribotides, with a proposal for the transition to a peptide-assisted stage. J Theor Biol 164:291–305

    CAS  PubMed  Google Scholar 

  • Fimmel E, Strüngmann L (2016) Codon distribution in error-detecting circular codes. Life 6:e14

    PubMed  Google Scholar 

  • Fimmel E, Strüngmann L (2018) Mathematical fundamentals for the noise immunity of the genetic code. Biosystems 164:186–198

    CAS  PubMed  Google Scholar 

  • Fimmel E, Giannerini S, Gonzalez DL, Strüngmann L (2015) Circular codes, symmetries and transformations. J Math Biol 70:1623–1644

    PubMed  Google Scholar 

  • Fimmel E, Michel CJ, Strüngmann L (2017) Strong comma-free codes in genetic information. Bull Math Biol 79:176–1819

    Google Scholar 

  • Fimmel E, Michel CJ, Starman M, Strüngmann L (2018) Self-complementary circular codes in coding theory. Theory Biosci 137:51–65

    CAS  PubMed  Google Scholar 

  • Fimmel E, Gumbel M, Karpuzoglu A, Petoukhov S (2019) On comparing composition principles of long DNA sequences with those of random ones. Biosystems 180:101–108

    CAS  PubMed  Google Scholar 

  • Geyer R, Mamlouk AM (2018) On the efficiency of the genetic code after frameshift mutations. PeerJ 6:e4825. https://doi.org/10.7717/peerj.4825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gonzalez DL, Giannerini S, Rosa R (2011) Circular codes revisited: a statistical approach. J Theor Biol 275:21–28

    CAS  PubMed  Google Scholar 

  • Gonzalez DL, Giannerini S, Rosa R (2017) The non-power model of the genetic code: a paradigm for interpreting genomic information. Philos Trans A. https://doi.org/10.1098/rsta.2015.0062

    Article  Google Scholar 

  • Guimarães RC (2017) Self-referential encoding on modules of anticodon pairs-root of the biological flow system. Life (Basel) 7:16

    Google Scholar 

  • Guimarães RC, Moreira CH, de Farias ST (2008) A self-referential model for the formation of the genetic code. Theory Biosci 127:249–270

    PubMed  Google Scholar 

  • Han DX, Wang HY, Ji ZL, Hu AF, Zhao YF (2010) Amino acid chirality may be linked to the origin of phosphate-based life. J Mol Evol 70:572–582

    CAS  Google Scholar 

  • Ilardo M, Meringer M, Freeland S, Rasulev B, Cleaves HJ II (2015) Extraordinarily adaptive properties of the genetically encoded amino acids. Sci Rep 5:9414

    CAS  PubMed  PubMed Central  Google Scholar 

  • Itzkovitz S, Alon U (2007) The genetic code is nearly optimal for allowing additional information within protein-coding sequences. Genome Res 17:405–412

    CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson DB, Wang L (2010) Imprints of the genetic code in the ribosome. Proc Natl Acad Sci USA 107:8298–8303

    CAS  PubMed  Google Scholar 

  • Křížek M, Křížek P (2012) Why has nature invented three stop codons of DNA and only one start codon? J Theor Biol 304:183–187

    PubMed  Google Scholar 

  • Michel CJ (2012) Circular code motifs in transfer and 16S ribosomal RNAs: a possible translation code in genes. Comput Biol Chem 37:24–37

    CAS  PubMed  Google Scholar 

  • Michel CJ (2013) Circular code motifs in transfer RNAs. Comput Biol Chem 45:17–29

    CAS  PubMed  Google Scholar 

  • Michel CJ (2015) The maximal C(3) self-complementary trinucleotide circular code X in genes of bacteria, eukaryotes, plasmids and viruses. J Theor Biol 380:156–177

    CAS  PubMed  Google Scholar 

  • Michel CJ (2017) The maximal C3 self-complementary trinucleotide circular code x in genes of bacteria, archaea, eukaryotes. Plasmids and Viruses. Life (Basel) 7:e20

    Google Scholar 

  • Michel CJ (2019) Single-frame, multiple frame and framing motifs in genes. Life 9:18

    CAS  PubMed Central  Google Scholar 

  • Michel CJ, Pirillo G (2010) Identification of all trinucleotide circular codes. Comput Biol Chem 34:122–125

    CAS  PubMed  Google Scholar 

  • Michel CJ, Seligmann H (2014) Bijective transformation circular codes and nucleotide exchanging RNA transcription. Biosystems 118:39–50

    CAS  PubMed  Google Scholar 

  • Michel CJ, Pellegrini M, Pirillo G (2016) Maximal dinucleotide and trinucleotide circular codes. J Theor Biol 389:40–46

    CAS  PubMed  Google Scholar 

  • Nikolaou C, Almirantis Y (2006) Deviations from Chargaff's second parity rule in organellar DNA. Insights into the evolution of organellar genomes. Gene 381:34–41

    CAS  PubMed  Google Scholar 

  • Opuu V, Silvert M, Simonson T (2017) Computational design of fully overlapping coding schemes for protein pairs and triplets. Sci Rep 7:15873

    PubMed  PubMed Central  Google Scholar 

  • Philip GK, Freeland SJ (2011) Did evolution select a nonrandom “alphabet” of amino acids? Astrobiology 11:235–240

    CAS  PubMed  Google Scholar 

  • Rogers SO (2019) Evolution of the genetic code based on conservative changes of codons, amino acids, and aminoacyl tRNA synthetases. J Theor Biol 466:1–10

    CAS  PubMed  Google Scholar 

  • Seligmann H (2007) Cost minimization of ribosomal frameshifts. J Theor Biol 249:162–167

    PubMed  Google Scholar 

  • Seligmann H (2010) The ambush hypothesis at the whole-organism level: off frame, 'hidden' stops in vertebrate mitochondrial genes increase developmental stability. Comput Biol Chem 34:80–85

    CAS  PubMed  Google Scholar 

  • Seligmann H (2012a) Overlapping genetic codes for overlapping frameshifted genes in Testudines, and Lepidochelys olivacea as special case. Comput Biol Chem 41:18–34

    CAS  PubMed  Google Scholar 

  • Seligmann H (2012b) Coding constraints modulate chemically spontaneous mutational replication gradients in mitochondrial genomes. Curr genomics 13:37–54

    CAS  PubMed  PubMed Central  Google Scholar 

  • Seligmann H (2015) Phylogeny of genetic codes and punctuation codes within genetic codes. Biosystems 129:36–43

    CAS  PubMed  Google Scholar 

  • Seligmann H (2018a) Directed mutations recode mitochondrial genes: from regular to stopless genetic codes. In: Seligmann H and Warthi G eds, Mitochondrial DNA: New Insights. Intechopen, London. https://doi.org/10.5772/intechopen.80871

    Google Scholar 

  • Seligmann H (2018b) Alignment-based and alignment-free methods converge with experimental data on amino acids coded by stop codons at split between nuclear and mitochondrial genetic codes. Biosystems 167:33–46

    CAS  PubMed  Google Scholar 

  • Seligmann H (2018c) Protein sequences recapitulate genetic code evolution. Comput Struct Biotechnol J 16:177–189

    CAS  PubMed  PubMed Central  Google Scholar 

  • Seligmann H (2019) Localized context-dependent effects of the "ambush" hypothesis: more off frame stop codons downstream of shifty codons. DNA Cell Biol 38(8):786–795

    CAS  PubMed  Google Scholar 

  • Seligmann H, Pollock DD (2004) The ambush hypothesis: hidden stop codons prevent off frame gene reading. DNA Cell Biol 23:701–705

    CAS  PubMed  Google Scholar 

  • Seligmann H, Warthi G (2017) Genetic code optimization for cotranslational protein folding: codon directional asymmetry correlates with antiparallel betasheets, tRNA synthetase classes. Comput Struct Biotechnol 15:412–424

    CAS  Google Scholar 

  • Seligmann H, Warthi G (2019) Transcripts with systematic nucleotide deletion of 1–12 nucleotide in human mitochondrion suggest potential non-canonical transcription. PLoS ONE 14:e0217356

    PubMed  PubMed Central  Google Scholar 

  • Trifonov EN (2000) Consensus temporal order of amino acids and evolution of the triplet code. Gene 261:139–151

    CAS  PubMed  Google Scholar 

  • Tse H, Cai JJ, Tsoi HW, Lam EP, Yuen KY (2010) Natural selection retains overrepresented out-of-frame stop codons against frameshift peptides in prokaryotes. BMC Genom 11:491

    Google Scholar 

  • Wang X, Wang X, Chen G, Zhang J, Liu Y, Yang C (2015) The shiftability of protein coding genes: the genetic code was optimized for frameshift tolerating. PeerJ. https://doi.org/10.7287/peerj.preprints.806v1

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang X, Dong Q, Chen G, Zhang J, Liu Y, Zhao J, Peng H, Wang Y, Cai Y, Wang X, Yang C (2018) The universal genetic code, protein coding genes and genomes of all species were optimized for frameshift tolerance. bioRxiv:067736

  • Xia X (2012) DNA replication and strand asymmetry in prokaryotic and mitochondrial genomes. Curr Genom 13:16–27

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory AGEIS EA 7407, Team Tools for E-Gnosis Medical & Labcom CNRS/UGA/OrangeLabs Telecoms4Health, Faculty of Medicine, Université Grenoble Alpes, 38700, La Tronche, France

    Jacques Demongeot & Hervé Seligmann

  2. The National Natural History Collections, The Hebrew University of Jerusalem, 91904, Jerusalem, Israel

    Hervé Seligmann

Authors
  1. Jacques Demongeot
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hervé Seligmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hervé Seligmann.

Additional information

Handling Editor: Michelle Meyer.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Authors order alphabetical.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Demongeot, J., Seligmann, H. Pentamers with Non-redundant Frames: Bias for Natural Circular Code Codons. J Mol Evol 88, 194–201 (2020). https://doi.org/10.1007/s00239-019-09925-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-019-09925-0

Keywords

Search

Navigation