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. 2003 Feb;4(1):56–65. doi: 10.1002/cfg.246

Pressures in Archaeal Protein Coding Genes: A Comparative Study

Sujay Chattopadhyay 1,✉, Satyabrata Sahoo 1, William A Kanner 2, Jayprokas Chakrabarti 1
PMCID: PMC2447400  PMID: 18629113

Abstract

Our studies on the bases of codons from 11 completely sequenced archaeal genomes show that, as we move from GC-rich to AT-rich protein-coding gene-containing species, the differences between G and C and between A and T, the purine load (AG content), and also the overall persistence (i.e. the tendency of a base to be followed by the same base) within codons, all increase almost simultaneously, although the extent of increase is different over the three positions within codons. These findings suggest that the deviations from the second parity rule (through the increasing differences between complementary base contents) and the increasing purine load hinder the chance of formation of the intra-strand Watson–Crick base-paired secondary structures in mRNAs (synonymous with the protein-coding genes we dealt with), thereby increasing the translational efficiency. We hypothesize that the ATrich protein-coding gene-containing archaeal species might have better translational efficiency than their GC-rich counterparts.

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Selected References

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  1. Antezana M. A., Kreitman M. The nonrandom location of synonymous codons suggests that reading frame-independent forces have patterned codon preferences. J Mol Evol. 1999 Jul;49(1):36–43. doi: 10.1007/pl00006532. [DOI] [PubMed] [Google Scholar]
  2. Ball L. A. Implications of secondary structure in messenger RNA. J Theor Biol. 1972 Aug;36(2):313–320. doi: 10.1016/0022-5193(72)90100-2. [DOI] [PubMed] [Google Scholar]
  3. Ball L. A. Secondary structure and coding potential of the coat protein gene of bacteriophage MS2. Nat New Biol. 1973 Mar 14;242(115):44–45. doi: 10.1038/newbio242044a0. [DOI] [PubMed] [Google Scholar]
  4. Bell S. J., Forsdyke D. R. Deviations from Chargaff's second parity rule correlate with direction of transcription. J Theor Biol. 1999 Mar 7;197(1):63–76. doi: 10.1006/jtbi.1998.0858. [DOI] [PubMed] [Google Scholar]
  5. Berg O. G., Silva P. J. Codon bias in Escherichia coli: the influence of codon context on mutation and selection. Nucleic Acids Res. 1997 Apr 1;25(7):1397–1404. doi: 10.1093/nar/25.7.1397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bernardi G., Bernardi G. Compositional constraints and genome evolution. J Mol Evol. 1986;24(1-2):1–11. doi: 10.1007/BF02099946. [DOI] [PubMed] [Google Scholar]
  7. Brown J. R., Doolittle W. F. Archaea and the prokaryote-to-eukaryote transition. Microbiol Mol Biol Rev. 1997 Dec;61(4):456–502. doi: 10.1128/mmbr.61.4.456-502.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bult C. J., White O., Olsen G. J., Zhou L., Fleischmann R. D., Sutton G. G., Blake J. A., FitzGerald L. M., Clayton R. A., Gocayne J. D. Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science. 1996 Aug 23;273(5278):1058–1073. doi: 10.1126/science.273.5278.1058. [DOI] [PubMed] [Google Scholar]
  9. Cavalier-Smith T. The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. Int J Syst Evol Microbiol. 2002 Jan;52(Pt 1):7–76. doi: 10.1099/00207713-52-1-7. [DOI] [PubMed] [Google Scholar]
  10. Dang K. D., Dutt P. B., Forsdyke D. R. Chargaff difference analysis of the bithorax complex of Drosophila melanogaster. Biochem Cell Biol. 1998;76(1):129–137. doi: 10.1139/o97-095. [DOI] [PubMed] [Google Scholar]
  11. Fedorov Alexei, Saxonov Serge, Gilbert Walter. Regularities of context-dependent codon bias in eukaryotic genes. Nucleic Acids Res. 2002 Mar 1;30(5):1192–1197. doi: 10.1093/nar/30.5.1192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Friedman S. M., Malik M., Drlica K. DNA supercoiling in a thermotolerant mutant of Escherichia coli. Mol Gen Genet. 1995 Aug 30;248(4):417–422. doi: 10.1007/BF02191641. [DOI] [PubMed] [Google Scholar]
  13. Gaasterland T. Archaeal genomics. Curr Opin Microbiol. 1999 Oct;2(5):542–547. doi: 10.1016/s1369-5274(99)00014-4. [DOI] [PubMed] [Google Scholar]
  14. Galtier N., Lobry J. R. Relationships between genomic G+C content, RNA secondary structures, and optimal growth temperature in prokaryotes. J Mol Evol. 1997 Jun;44(6):632–636. doi: 10.1007/pl00006186. [DOI] [PubMed] [Google Scholar]
  15. Karlin S., Mrázek J. What drives codon choices in human genes? J Mol Biol. 1996 Oct 4;262(4):459–472. doi: 10.1006/jmbi.1996.0528. [DOI] [PubMed] [Google Scholar]
  16. Kawarabayasi Y., Hino Y., Horikawa H., Jin-no K., Takahashi M., Sekine M., Baba S., Ankai A., Kosugi H., Hosoyama A. Complete genome sequence of an aerobic thermoacidophilic crenarchaeon, Sulfolobus tokodaii strain7. DNA Res. 2001 Aug 31;8(4):123–140. doi: 10.1093/dnares/8.4.123. [DOI] [PubMed] [Google Scholar]
  17. Kawarabayasi Y., Hino Y., Horikawa H., Yamazaki S., Haikawa Y., Jin-no K., Takahashi M., Sekine M., Baba S., Ankai A. Complete genome sequence of an aerobic hyper-thermophilic crenarchaeon, Aeropyrum pernix K1. DNA Res. 1999 Apr 30;6(2):83-101, 145-52. doi: 10.1093/dnares/6.2.83. [DOI] [PubMed] [Google Scholar]
  18. Kawarabayasi Y., Sawada M., Horikawa H., Haikawa Y., Hino Y., Yamamoto S., Sekine M., Baba S., Kosugi H., Hosoyama A. Complete sequence and gene organization of the genome of a hyper-thermophilic archaebacterium, Pyrococcus horikoshii OT3 (supplement). DNA Res. 1998 Apr 30;5(2):147–155. doi: 10.1093/dnares/5.2.147. [DOI] [PubMed] [Google Scholar]
  19. Keeling P. J., Doolittle W. F. Archaea: narrowing the gap between prokaryotes and eukaryotes. Proc Natl Acad Sci U S A. 1995 Jun 20;92(13):5761–5764. doi: 10.1073/pnas.92.13.5761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Klenk H. P., Clayton R. A., Tomb J. F., White O., Nelson K. E., Ketchum K. A., Dodson R. J., Gwinn M., Hickey E. K., Peterson J. D. The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature. 1997 Nov 27;390(6658):364–370. doi: 10.1038/37052. [DOI] [PubMed] [Google Scholar]
  21. Lao P. J., Forsdyke D. R. Thermophilic bacteria strictly obey Szybalski's transcription direction rule and politely purine-load RNAs with both adenine and guanine. Genome Res. 2000 Feb;10(2):228–236. doi: 10.1101/gr.10.2.228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. McVean G. A., Hurst G. D. Evolutionary lability of context-dependent codon bias in bacteria. J Mol Evol. 2000 Mar;50(3):264–275. doi: 10.1007/s002399910031. [DOI] [PubMed] [Google Scholar]
  23. Mrázek J., Kypr J. Biased distribution of adenine and thymine in gene nucleotide sequences. J Mol Evol. 1994 Nov;39(5):439–447. doi: 10.1007/BF00173412. [DOI] [PubMed] [Google Scholar]
  24. Myllykallio H., Lopez P., López-García P., Heilig R., Saurin W., Zivanovic Y., Philippe H., Forterre P. Bacterial mode of replication with eukaryotic-like machinery in a hyperthermophilic archaeon. Science. 2000 Jun 23;288(5474):2212–2215. doi: 10.1126/science.288.5474.2212. [DOI] [PubMed] [Google Scholar]
  25. Olsen G. J., Woese C. R. Archaeal genomics: an overview. Cell. 1997 Jun 27;89(7):991–994. doi: 10.1016/s0092-8674(00)80284-6. [DOI] [PubMed] [Google Scholar]
  26. Olsen G. J., Woese C. R., Overbeek R. The winds of (evolutionary) change: breathing new life into microbiology. J Bacteriol. 1994 Jan;176(1):1–6. doi: 10.1128/jb.176.1.1-6.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Olsen G. J., Woese C. R. Ribosomal RNA: a key to phylogeny. FASEB J. 1993 Jan;7(1):113–123. doi: 10.1096/fasebj.7.1.8422957. [DOI] [PubMed] [Google Scholar]
  28. Pühler G., Leffers H., Gropp F., Palm P., Klenk H. P., Lottspeich F., Garrett R. A., Zillig W. Archaebacterial DNA-dependent RNA polymerases testify to the evolution of the eukaryotic nuclear genome. Proc Natl Acad Sci U S A. 1989 Jun;86(12):4569–4573. doi: 10.1073/pnas.86.12.4569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ruepp A., Graml W., Santos-Martinez M. L., Koretke K. K., Volker C., Mewes H. W., Frishman D., Stocker S., Lupas A. N., Baumeister W. The genome sequence of the thermoacidophilic scavenger Thermoplasma acidophilum. Nature. 2000 Sep 28;407(6803):508–513. doi: 10.1038/35035069. [DOI] [PubMed] [Google Scholar]
  30. She Q., Singh R. K., Confalonieri F., Zivanovic Y., Allard G., Awayez M. J., Chan-Weiher C. C., Clausen I. G., Curtis B. A., De Moors A. The complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc Natl Acad Sci U S A. 2001 Jun 26;98(14):7835–7840. doi: 10.1073/pnas.141222098. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Smith D. R., Doucette-Stamm L. A., Deloughery C., Lee H., Dubois J., Aldredge T., Bashirzadeh R., Blakely D., Cook R., Gilbert K. Complete genome sequence of Methanobacterium thermoautotrophicum deltaH: functional analysis and comparative genomics. J Bacteriol. 1997 Nov;179(22):7135–7155. doi: 10.1128/jb.179.22.7135-7155.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sueoka N. Intrastrand parity rules of DNA base composition and usage biases of synonymous codons. J Mol Evol. 1995 Mar;40(3):318–325. doi: 10.1007/BF00163236. [DOI] [PubMed] [Google Scholar]
  33. Sueoka N. Two aspects of DNA base composition: G+C content and translation-coupled deviation from intra-strand rule of A = T and G = C. J Mol Evol. 1999 Jul;49(1):49–62. doi: 10.1007/pl00006534. [DOI] [PubMed] [Google Scholar]
  34. Szybalski W., Kubinski H., Sheldrick P. Pyrimidine clusters on the transcribing strand of DNA and their possible role in the initiation of RNA synthesis. Cold Spring Harb Symp Quant Biol. 1966;31:123–127. doi: 10.1101/sqb.1966.031.01.019. [DOI] [PubMed] [Google Scholar]
  35. Woese C. R. Bacterial evolution. Microbiol Rev. 1987 Jun;51(2):221–271. doi: 10.1128/mr.51.2.221-271.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Woese C. R., Fox G. E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci U S A. 1977 Nov;74(11):5088–5090. doi: 10.1073/pnas.74.11.5088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Woese C. R., Kandler O., Wheelis M. L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4576–4579. doi: 10.1073/pnas.87.12.4576. [DOI] [PMC free article] [PubMed] [Google Scholar]

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