Analysis of Free Energy Signals Arising from Nucleotide Hybridization Between rRNA and mRNA Sequences during Translation in Eubacteria

Abstract

A decoding algorithm is tested that mechanistically models the progressive alignments that arise as the mRNA moves past the rRNA tail during translation elongation. Each of these alignments provides an opportunity for hybridization between the single-stranded, -terminal nucleotides of the 16S rRNA and the spatially accessible window of mRNA sequence, from which a free energy value can be calculated. Using this algorithm we show that a periodic, energetic pattern of frequency 1/3 is revealed. This periodic signal exists in the majority of coding regions of eubacterial genes, but not in the non-coding regions encoding the 16S and 23S rRNAs. Signal analysis reveals that the population of coding regions of each bacterial species has a mean phase that is correlated in a statistically significant way with species () content. These results suggest that the periodic signal could function as a synchronization signal for the maintenance of reading frame and that codon usage provides a mechanism for manipulation of signal phase.

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References

  1. 1.

    Frick DN, Richardson CC: DNA primases. Annual Review of Biochemistry 2001, 70: 39-80. 10.1146/annurev.biochem.70.1.39

    Article  Google Scholar 

  2. 2.

    Rymond BC, Rosbash M: Yeast pre-mRNA splicing. In The Molecular and Cellular Biology of the Yeast Saccharomyces: Vol. II. Gene Expression. Volume 2. Edited by: Jones E, Pringle J, Broach J. New York, NY, USA; 1992:143-192.

    Google Scholar 

  3. 3.

    Doench JG, Petersen CP, Sharp PA: siRNAs can function as miRNAs. Genes and Development 2003,17(4):438-442. 10.1101/gad.1064703

    Article  Google Scholar 

  4. 4.

    Shine J, Dalgarno L:The -terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proceedings of the National Academy of Sciences of the United States of America 1974,71(4):1342-1346. 10.1073/pnas.71.4.1342

    Article  Google Scholar 

  5. 5.

    Steitz JA, Jakes K:How ribosomes select initiator regions in mRNA: base pair formation between the terminus of 16S rRNA and the mRNA during initiation of protein synthesis in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 1975,72(12):4734-4738. 10.1073/pnas.72.12.4734

    Article  Google Scholar 

  6. 6.

    Hui A, de Boer HA: Specialized ribosome system: preferential translation of a single mRNA species by a subpopulation of mutated ribosomes in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 1987,84(14):4762-4766. 10.1073/pnas.84.14.4762

    Article  Google Scholar 

  7. 7.

    Weiss RB, Dunn DM, Atkins JF, Gesteland RF:Slippery runs, shifty stops, backward steps, and forward hops: , , , , , and ribosomal frameshifting Cold Spring Harbor Symposia on Quantitative Biology 1987, 52: 687-693.

    Article  Google Scholar 

  8. 8.

    Weiss RB, Dunn DM, Dahlberg AE, Atkins JF, Gesteland RF:Reading frame switch caused by base-pair formation between the end of 16S rRNA and the mRNA during elongation of protein synthesis in Escherichia coli. EMBO Journal 1988,7(5):1503-1507.

    Google Scholar 

  9. 9.

    Starmer JD: Free2Bind: tools for computing minimum free energy binding between two separate RNA molecules. http://sourceforge.net/projects/free2bind/

  10. 10.

    Starmer J, Stomp A-M, Vouk MA, Bitzer DL: Predicting Shine-Dalgarno sequence locations exposes genome annotation errors. PLoS Computational Biology 2006,2(5):454-466.

    Article  Google Scholar 

  11. 11.

    Xia T, SantaLucia J Jr., Burkard ME, et al.: Thermodynamic parameters for an expanded nearest-neighbor model for formation of RNA duplexes with Watson-Crick base pairs. Biochemistry 1998,37(42):14719-14735. 10.1021/bi9809425

    Article  Google Scholar 

  12. 12.

    Jaeger JA, Turner DH, Zuker M: Improved predictions of secondary structures for RNA. Proceedings of the National Academy of Sciences of the United States of America 1989,86(20):7706-7710. 10.1073/pnas.86.20.7706

    Article  Google Scholar 

  13. 13.

    Mathews DH, Sabina J, Zuker M, Turner DH: Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. Journal of Molecular Biology 1999,288(5):911-940. 10.1006/jmbi.1999.2700

    Article  Google Scholar 

  14. 14.

    Schluenzen F, Tocilj A, Zarivach R, et al.: Structure of functionally activated small ribosomal subunit at 3.3 angstroms resolution. Cell 2000,102(5):615-623. 10.1016/S0092-8674(00)00084-2

    Article  Google Scholar 

  15. 15.

    Yusupova GZ, Yusupov MM, Cate JHD, Noller HF: The path of messenger RNA through the ribosome. Cell 2001,106(2):233-241. 10.1016/S0092-8674(01)00435-4

    Article  Google Scholar 

  16. 16.

    Schurr T, Nadir E, Margalit H: Identification and characterization of E.coli ribosomal binding sites by free energy computation. Nucleic Acids Research 1993,21(17):4019-4023. 10.1093/nar/21.17.4019

    Article  Google Scholar 

  17. 17.

    Osada Y, Saito R, Tomita M:Analysis of base-pairing potentials between 16S rRNA and UTR for translation initiation in various prokaryotes. Bioinformatics 1999,15(7-8):578-581.

    Article  Google Scholar 

  18. 18.

    Thanaraj TA, Pandit MW: An additional ribosome-binding site on mRNA of highly expressed genes and a bifunctional site on the colicin fragment of 16S rRNA from Escherichia coli: important determinants of the efficiency of translation-initiation. Nucleic Acids Research 1989,17(8):2973-2985. 10.1093/nar/17.8.2973

    Article  Google Scholar 

  19. 19.

    Lithwick G, Margalit H: Hierarchy of sequence-dependent features associated with prokaryotic translation. Genome Research 2003,13(12):2665-2673. 10.1101/gr.1485203

    Article  Google Scholar 

  20. 20.

    Lee K, Holland-Staley CA, Cunningham PR: Genetic analysis of the Shine-Dalgarno interaction: selection of alternative functional mRNA-rRNA combinations. RNA 1996,2(12):1270-1285.

    Google Scholar 

  21. 21.

    Komarova AV, Tchufistova LS, Supina EV, Boni IV:Extensive complementarity of the Shine-Dalgarno region and -end of 16S rRNA is inefficient for translation in vivo. Russian Journal of Bioorganic Chemistry 2001,27(4):248-255. 10.1023/A:1011356520576

    Article  Google Scholar 

  22. 22.

    Ma J, Campbell A, Karlin S: Correlations between Shine-Dalgarno sequences and gene features such as predicted expression levels and operon structures. Journal of Bacteriology 2002,184(20):5733-5745. 10.1128/JB.184.20.5733-5745.2002

    Article  Google Scholar 

  23. 23.

    Oppenheim AV, Schafer RW: Digital Signal Processing. 1st edition. Prentice-Hall, Englewood Cliffs, NJ, USA; 1975.

    Google Scholar 

  24. 24.

    Brockwell PJ, Davis RA: Time Series: Theory and Methods. 2nd edition. Springer, New York, NY, USA; 1991.

    Google Scholar 

  25. 25.

    Kay SM: Fundamentals of Statistical Signal Processing, Vol. I: Estimation Theory. Prentice-Hall, Englewood Cliffs, NJ, USA; 1993.

    Google Scholar 

  26. 26.

    Brocklebank JC, Dickey DA: SAS for Forecasting Time Series. 2nd edition. John Wiley & Sons, New York, NY, USA; 2003.

    Google Scholar 

  27. 27.

    Lio P, Ruffo S, Buiatti M:Third codon periodicity as a possible signal for an "Internal" selective constraint. Journal of Theoretical Biology 1994,171(2):215-223. 10.1006/jtbi.1994.1225

    Article  Google Scholar 

  28. 28.

    D'Onofrio G, Bernardi G: A universal compositional correlation among codon positions. Gene 1992,110(1):81-88. 10.1016/0378-1119(92)90447-W

    Article  Google Scholar 

  29. 29.

    Cocho G, Rius JL: Structural constraints and gene dynamics. Rivista di Biologia - Biology Forum 1989,82(3-4):344-345, 416–417.

    Google Scholar 

  30. 30.

    Gouy M, Gautier C: Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Research 1982,10(22):7055-7074. 10.1093/nar/10.22.7055

    Article  Google Scholar 

  31. 31.

    Trifonov EN: Translation framing code and frame-monitoring mechanism as suggested by the analysis of mRNA and 16S rRNA nucleotide sequences. Journal of Molecular Biology 1987,194(4):643-652. 10.1016/0022-2836(87)90241-5

    Article  Google Scholar 

  32. 32.

    Ponnala L, Barnes T, Bitzer DL, Vouk MA, Stomp A-M: A signal processing-based model for analyzing programmed frameshifts. Proceedings of IEEE International Workshop on Genomic Signal Processing and Statistics (GENSIPS '05), Newport, RI, USA, May 2005

    Google Scholar 

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Correspondence to Lalit Ponnala.

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Ponnala, L., Stomp, AM., Bitzer, D.L. et al. Analysis of Free Energy Signals Arising from Nucleotide Hybridization Between rRNA and mRNA Sequences during Translation in Eubacteria. J Bioinform Sys Biology 2006, 23613 (2006). https://doi.org/10.1155/BSB/2006/23613

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Keywords

  • Nucleotide
  • Codon
  • Free Energy
  • Bacterial Species
  • Signal Analysis