Nucleotide tetramers TCGA and CTAG: viral DNA and the genetic code (hypothesis)



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Abstract

Introduction. The published and our own data show that CTAG and, to a lesser extent, TCGA tetra-nucleotides have significantly lower concentrations in frequency profiles (FPs) of herpesvirus DNAs compared to other complete, bilaterally symmetrical tetra-nucleotides.

The aim of the study is to present a comparative analysis of CTAG and TCGA tetra-nucleotide FPs in viral DNAs.

Materials and methods. We have analyzed FPs and other characteristics of the two above tetramers in DNAs of at least one species of viruses of each genus (or each subfamily, if the classification into genera was not available), complying with the size limit requirements (minimum 100,000 base pairs) — a total of more than 200 species of viruses. The analysis was performed using the GenBank database.

Results. Two groups of characteristics of TCGA and CTAG tetramers have been described. One of them covers the results of the FP analysis for these tetranucleotides in viral DNAs and shows that DNAs with GC:AT > 2 are characterized by nCGn FP symmetries while these symmetries are frequently distorted in nTAn FP due to CTAG underrepresentation. The other group of tetramer characteristics demonstrates differences in their FPs in complete viral DNAs and in their genomes (a coding part, which can reach 80% in some studied viruses, thus making the analysis of their DNAs more significant than the analysis of DNAs of cellular live forms) and suggests that these tetramers may have participated in the origin of the universal genetic code.

Discussion. Assumedly, the genetic code started evolving amid C+G prevailing in "pre-code" DNA polymers; then the initial code forms evolved further to their final structure where TCGA and CTAG tetramers hold a central position, encapsulating the previous stages of this evolution. The nCGn FP symmetries typical of the "complete" DNA of Herpes simplex viruses disappear in the sequence of the second codon letters of the genome of these viruses, implying that their functions differ from functions of other letters and emphasizing the reasonableness of presenting the genetic code as a calligram where the second line is not symmetrical.

About the authors

F. P. Filatov

I. Mechnikov Research Institute of Vaccines and Sera; National Research Center for Epidemiology and Microbiology named after Honorary Academician N.F. Gamaleya

Author for correspondence.
Email: felix001@gmail.com
ORCID iD: 0000-0001-6182-2241

Felix P. Filatov — D. Sci. (Biol.), leading researcher, Laboratory of molecular biotechnology, Department of virology, I. Mechnikov Research Institute of Vaccines and Sera; leading researcher, Department of epidemiology, National Research Center for Epidemiology and Microbiology named after Honorary Academician N.F. Gamaleya

Moscow

Russian Federation

References

  1. Филатов Ф.П., Шаргунов А.В. Тетрануклеотидный профиль герпесвирусных ДНК. Журнал микробиологии, эпидемиологии и иммунобиологии. 2020; 97(3): 216–26. https://doi.org/10.36233/0372-9311-2020-97-3-3
  2. Tang L., Zhu S., Mastriani E., Fang X., Zhou Y.J., Li Y.G., et al. Conserved intergenic sequences revealed by CTAG-profiling in Salmonella: thermodynamic modeling for function prediction. Sci. Rep. 2017; 7: 43565. https://doi.org/10.1038/srep43565
  3. Lundberg P., Welander P., Han X., Cantin E. Herpes simplex virus type 1 DNA is immunostimulatory in vitro and in vivo. J. Virol. Oct. 2003; 77(20): 11158–69. https://doi.org/10.1128/JVI.77.20.11158-11169.2003
  4. Sharawy M., Louyakis A., Gogarten J.P., May E.R. CTAG vs. GATC: structural basis for representational differences in reverse palindromic DNA tetranucleotide sequences. Biophys. J. 2021; 120(3): 222a.
  5. Albrecht-Buehler G. Asymptotically increasing compliance of genomes with Chargaff's second parity rules through inversions and inverted transpositions. Proc. Natl Acad. Sci. USA. 2006; 103(47): 17828–33. https://doi.org/10.1073/pnas.0605553103
  6. Albrecht-Buehler G. The three classes of triplet profiles of natural genomes. Genomics. 2007; 89(5): 596–601. https://doi.org/10.1016/j.ygeno.2006.12.009
  7. Zhang S.H., Wang L. A novel common triplet profile for GC-rich prokaryotic genomes. Genomics. 2011; 97(5): 330–1. https://doi.org/10.1016/j.ygeno.2011.02.005
  8. Stevens M., Cheng J., Li D., Xi M., Hong C., Maire C., et al. Estimating absolute methylation levels at single-CpG resolution from methylation enrichment and restriction enzyme sequencing methods. Genome Res. 2013; 23(9): 1541–53. https://doi.org/10.1101/gr.152231.112
  9. Krieg A.M, Yi A.K., Matson S., Waldschmidt T.J., Bishop G.A., Teasdale R., et al. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature. 1995; 374(6522): 546–9. https://doi.org/10.1038/374546a0
  10. Fatemi M., Pao M.M., Jeong S., Gal-Yam E.N., Egger G., Weisenberger D.J., et al. Footprinting of mammalian promoters: use of a CpG DNA methyltransferase revealing nucleosome positions at a single molecule level. Nucleic. Acids Res. 2005; 33(20): e176. https://doi.org/10.1093/nar/gni180
  11. Woellmer A., Hammerschmidt W. Epstein–Barr virus and host cell methylation: regulation of latency, replication and virus reactivation. Curr. Opin. Virol. 2013; 3(3): 260–5. https://doi.org/10.1016/j.coviro.2013.03.005
  12. Burge C., Campbell A.M., Karlin S. Overand under-representation of short oligonucleotides in DNA sequences. PNAS. 1992; 89(4) 1358–62. https://doi.org/10.1073/pnas.89.4.1358
  13. Duret L., Galtier N. The covariation between TpA deficiency, CpG deficiency, and G+C content of human isochores is due to a mathematical artifact. Mol. Biol. Evol. 2000; 17(11): 1620–5. https://doi.org/10.1093/oxfordjournals.molbev.a02621.
  14. Gori F., Mavroeidis D., Jetten M.S.M., Marchiori E. The importance of Chargaff’s second parity rule for genomic signatures in metagenomics. bioRxiv. Preprint. https://doi.org/10.1101/146001
  15. Rudner R., Karkas J.D., Chargaff E. Separation of B. subtilis DNA into complementary strands, 3 Direct Analysis. Proc. Natl Acad. Sci. USA. 1968; 60(3): 921–2. https://doi.org/10.1073/pnas.60.3.921
  16. Makukov M.A., Shcherbak V.I. The “Wow! signal” of the terrestrial genetic code. Icarus. 2013; 224(1): 228–42. https://doi.org/10.1016/j.icarus.2013.02.017
  17. Filatov F. A molecular mass gradient is the key parameter of the genetic code organization. In: Blaho J., Baines J., eds. From the Hallowed Halls of Herpesvirology: A Tribute to Bernard Roizman. World Scientific Publishing Co.; 2012: 155–68. https://doi.org/10.1142/9789814338998_0006
  18. Pellett P., Roizman B. Herpesviridae. In: Knipe D.M., Howley P.M., eds. Fields Virology. Philadelphia: Lippincott Williams & Wilkins; 2013: 1802–2
  19. Prabhu V.V. Symmetry observations in long nucleotide sequences. Nucleic Acids Res. 1993; 21(12): 2797–800. https://doi.org/10.1093/nar/21.12.2797
  20. Forsdyke D.R. Symmetry observations in long nucleotide sequences: a commentary on the discovery note of Qi and Cuticchia. Bioinformatics. 2002; 18(1): 215–7. https://doi.org/10.1093/bioinformatics/18.1.215
  21. Baisnee P.F., Hampson S., Baldi P. Why are complementary strands symmetric? Bioinformatics. 2002; 18(8): 1021–33. https://doi.org/10.1093/bioinformatics/18.8.1021
  22. Румер Ю.Б. О систематизации кодонов в генетическом коде. Доклады Академии наук СССР. 1966; 167(6): 1393–4.
  23. Волькенштейн М.В., Румер Ю.Б. О систематике кодонов. Биофизика. 1967; 12(1): 10–3.
  24. Kim H.Y., Cheon J.H., Lee S.H., Min J.Y., Back S.Y., Song J.G., et al. Ternary nanocomposite carriers based on organic claylipid vesicles as an effective colon-targeted drug delivery system: preparation and in vitro/in vivo characterization. J. Nanobiotechnology. 2020; 18(1): 17. https://doi.org/10.1186/s12951-020-0579-7
  25. Koonin E.V., Novozhilov A.S. Origin and evolution of the genetic code: the universal enigma. IUBMB Life. 2009; 61(2): 99–111. https://doi.org/10.1002/iub.146
  26. Marlaire R., ed. Ames Research Center. NASA Ames Reproduces the Building Blocks of Life in Laboratory. Moffett Field, CA: NASA; 2015.
  27. Herbert K.M., Nag A. A tale of two RNAs during viral infection: how viruses antagonize mRNAs and small non-coding RNAs in the host cell. Viruses. 2016; 8(6): 154. https://doi.org/10.3390/v8060154
  28. Tjhung K.F., Shokhirev M.N., Horning D.P., Joyce G.F. An RNA polymerase ribozyme that synthesizes its own ancestor. Proc. Natl Acad. Sci. USA. 2020; 117(6) 2906–13. https://doi.org/10.1073/pnas.1914282117
  29. Kim J.D., Senn S., Harel A., Jelen B.I., Falkowski P.G. Discovering the electronic circuit diagram of life: structural relationships among transition metal binding sites in oxidoreductases. Philis. Trans. R Soc. Lond. B. Biol. Si. 2013; 368(1622): 20120257. https://doi.org/10.1098/rstb.2012.0257
  30. Yakovchuk P., Protozanova E., Frank-Kamenetskii M.D. Basestacking and base-pairing contributions into thermal stability of the DNA double helix. Nucleic Acids Res. 2006; 34(2): 564–74. https://doi.org/10.1093/nar/gkj454
  31. Forterre P. The origin of viruses and their possible roles in major evolutionary transitionsa. Review. Virus Res. 2006; 117: 5–16.
  32. Mughal F., Nasir A., Caetano-Anolles G. The origin and evolution of viruses inferred from fold family structure. Arch. Virol. 2020; 165(10): 2177–91. https://doi.org/10.1007/s00705-020-04724-1
  33. Brussow H., Kutter E. Genomics and evolution of tailed phages. In: Kutter E., Sulakvelidze A. eds. Bacteriophages: Biology and Applications. Boca Raton, London, New York, Washington: CRC press; 2005: 129–64.
  34. Abedon S.T. Phage evolution and ecology. Adv. Appl. Microbiol. 2009; 67: 1–45. https://doi.org/10.1016/s0065-2164(08)01001-0
  35. Altstein A.D. The progene hypothesis: the nucleoprotein world and how life began. Biol. Direct. 2015; 10: 67. https://doi.org/10.1186/s13062-015-0096-z
  36. Di Giulio M. The origin of the genetic code: theories and their relationships, a review. Biosystems. 2005; 80(2): 175–84. https://doi.org/10.1016/j.biosystems.2004.11.005
  37. Gilis D., Massar S., Cerf N.J., Rooman M. Optimality of the genetic code with respect to protein stability and amino-acid frequencies. Genome Biol. 2001; 2(11): RESEARCH0049. https://doi.org/10.1186/gb-2001-2-11-research0049
  38. Wetzel R. Evolution of the aminoacyl-tRNA synthetases and the origin of the genetic code. J. Mol. Evol. 1995; 40(5): 545–50. https://doi.org/10.1007/bf00166624
  39. McGeoch J., Rixon F.J., Davison A.J. Topics in herpesvirus genomics and evolution. Virus Res. 2006; 117(1): 90–104. https://doi.org/10.1016/j.virusres.2006.01.002
  40. Wang N., Baldi P.F., Gaut B.S. Phylogenetic analysis, genome evolution and the rate of gene gain in the Herpesviridae. Mol. Phylogenet. Evol. 2007; 43(3): 1066–75. https://doi.org/10.1016/j.ympev.2006.11.019
  41. Wertheim J.O., Smith M.D., Smith D.M., Scheffler K., Kosakovsky Pond S.L. Evolutionary origins of human herpes simplex viruses 1 and 2. Mol. Biol. Evol. 2014; 31(9): 2356–64. https://doi.org/10.1093/molbev/msu185
  42. Baker M.L., Jiang W., Rixon F.J., Chiu W. Common ancestry of herpesviruses and tailed DNA bacteriophages. J. Virol. 2005; 79(23): 14967–70. https://doi.org/10.1128/JVI.79.23.14967-14970.2005
  43. Гупал А.М., Гупал Н.А., Островский А.В. Симметрия и свойства записи генетической информации в ДНК. Проблемы управления и информатики. 2011; 5(3): 120–7.
  44. Сергиенко И.В., Гупал А.М., Вагис А.А. Симметричный код и генетические мутации. Кибернетика и системный анализ. 2016; (2): 73–80.

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