Chapter 4 : How Nucleic Acids Cope with High Temperature

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This chapter discusses the question of coping up of the nucleic acids with high temperature at the polynucleotide level—RNA, DNA, and their ribonucleoprotein derivatives (RNP/DNP). When nucleic acids are heated in aqueous solution, two types of phenomena take place: denaturation of their architecture and chemical degradation of their building blocks. In vivo, the half-lives of both RNA and DNA of thermophilic organisms are usually longer than that estimated in vitro, attesting to cellular strategies protecting the nucleic acids against the deleterious effects of heat. Despite the susceptibility of certain modified bases and of the ribonucleotide chain to thermal degradation, most naturally occurring tRNAs (especially those from hyperthermophilic organisms) appear fairly resistant to heat denaturation. Despite the intrinsic potentiality of nucleic acids to degrade at elevated temperatures, many hyperthermophiles can survive at very high temperatures approaching or even surpassing the boiling point of water. The majority of stable cellular RNAs, such as tRNA and rRNA molecules, contain a variety of modified nucleosides. Stabilizing strategies of RNAs and DNAs may be classified into three major categories: (i) those which are intrinsic to the chemical structures of the nucleic acids; (ii) those which are dependent on extrinsic interactions with other biomolecules; and (iii) those which are dependent on a battery of enzymes for detecting and repairing the DNA damage or to constantly renew functional RNA molecules. Genetic approach using mutant strains mutated in one or more biomolecules supposedly involved directly or indirectly in stabilization of nucleic acids should be more systematically used.

Citation: Grosjean H, Oshima T. 2007. How Nucleic Acids Cope with High Temperature, p 39-56. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch4
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Image of Figure 1.
Figure 1.

Strategies for thermostabilization of nucleic acids. In boxes are mentioned the various factors that allow a thermophilic organism to protect their nucleic acids against the deleterious effect of heat. A clear distinction between the giant extended macromolecule DNA and the more compact smaller RNA molecules has to be made. For details, see text.

Citation: Grosjean H, Oshima T. 2007. How Nucleic Acids Cope with High Temperature, p 39-56. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch4
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Image of Figure 2.
Figure 2.

Phylogenetic distribution of modified nucleosides in RNA from the three domains of life. Abbreviations of modified nucleosides are the conventional ones. For details, including the chemical structures, see in . Lines point out which ones among the hypermodified nucleosides in correspond to non-ribose methylated counterparts in or .

Citation: Grosjean H, Oshima T. 2007. How Nucleic Acids Cope with High Temperature, p 39-56. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch4
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Image of Figure 3.
Figure 3.

Schematic representation of tertiary interactions in tRNA structure. Numbers indicate conventional tRNA positions. Abbreviations of modified nucleosides are those of Fig. 2 ; see also in . Each nucleotide involved in stacking or base pairing with another nucleotide is represented by a rectangle. The rectangles representing nucleotides of the D-loop are in gray, while those representing nucleotides in the T-loop as well as nucleotides U8 and C48 located in between two stems are in white. Other parts of the tRNA molecule are represented by lines. Inside the dotted circle are elements that contributed to the 3D interaction, allowing an L-shaped spatial conformation to be formed from the 2D cloverleaf structure (see also Fig. 4 ). A wire representation of the 3D conformation is also indicated on the right side.

Citation: Grosjean H, Oshima T. 2007. How Nucleic Acids Cope with High Temperature, p 39-56. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch4
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Image of Figure 4.
Figure 4.

Main factors allowing tRNA molecules to function at high temperatures. On the left part are conventional schematic representations of 2D and 3D structures of tRNA. The remarkable features that are characteristic of a tRNA from a hyperthermophilic organism are indicated on the right side. In the boxes in the central part are indicated the various factors that allow a thermophilic organism to protect their nucleic acids against the deleterious effect of heat. For details, see text. Numbers indicate conventional tRNA positions; letters correspond to bases A, C, G, and U; R for purine, Y for pyrimidine, and N for any base.

Citation: Grosjean H, Oshima T. 2007. How Nucleic Acids Cope with High Temperature, p 39-56. In Gerday C, Glansdorff N (ed), Physiology and Biochemistry of Extremophiles. ASM Press, Washington, DC. doi: 10.1128/9781555815813.ch4
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1. Aas, P. A.,, M. Otterlei,, P. O. Falnes,, C. B. Vagbo,, F. Skorpen,, M. Akbari,, O. Sundheim,, M. Bjoras,, G. Slupphaug,, E. Seeberg, and, H. E. Krokan. 2003. Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA. Nature 421: 859863.
2. Agris, P. F. 1996. The importance of being modified: roles of modified nucleosides and Mg 2+ in RNA structure and function. Prog. Nucleic Acid Res. Mol. Biol. 53: 79129.
3. Agris, P. F.,, H. Koh, and, D. Soll. 1973. The effect of growth temperatures on the in vivo ribose methylation of Bacillus stearothermophilus transfer RNA. Arch. Biochem. Biophys. 154: 277282.
4. Anderson, J. T. 2005. RNA turnover: unexpected consequences of being tailed. Curr. Biol. 15: R635R638.
5. Atomi, H.,, R. Matsumi, and, T. Imanaka. 2004. Reverse gyrase is not a prerequisite for hyperthermophilic life. J. Bacteriol. 186: 48294833.
6. Bass, B. L. 2000. RNA Editing. Oxford University Press, Oxford, United Kingdom.
7. Basu, H. S.,, and L. J. Marton. 1987. The interaction of spermine and pentamines with DNA. Biochem. J. 244: 243246.
8. Becker, H. F.,, Y. Motorin,, M. Sissler,, C. Florentz, and, H. Grosjean. 1997. Major identity determinants for enzymatic formation of ribothymidine and pseudouridine in the T psi-loop of yeast tRNAs. J. Mol. Biol. 274: 505518.
9. Behe, M.,, and G. Felsenfeld. 1981. Effects of methylation on a synthetic polynucleotide: the B–Z transition in poly(dG-m5dC). poly(dG-m5dC). Proc. Natl. Acad. Sci. USA 78: 16191623.
10. Bernander, R.,, and A. Poplawski. 1997. Cell cycle characteristics of thermophilic archaea. J. Bacteriol. 179: 49634969.
11. Bini, E.,, V. Dikshit,, K. Dirksen,, M. Drozda, and, P. Blum. 2002. Stability of mRNA in the hyperthermophilic archaeon Sulfolobus solfataricus. RNA 8: 11291136.
12. Borer, P. N.,, B. Dengler,, I. Tinoco, Jr., and, O. C. Uhlenbeck. 1974. Stability of ribonucleic acid double-stranded helices. J. Mol. Biol. 86: 843853.
13. Bouthier de la Tour, C.,, C. Portemer,, M. Nadal,, K. O. Stetter,, P. Forterre, and, M. Duguet. 1990. Reverse gyrase, a hallmark of the hyperthermophilic archaebacteria. J. Bacteriol. 172: 68036808.
14. Brion, P.,, and E. Westhof. 1997. Hierarchy and dynamics of RNA folding. Annu. Rev. Biophys. Biomol. Struct. 26: 113137.
15. Brown, A. D. 1976. Microbial water stress. Bacteriol. Rev. 40: 803846.
16. Bryson, K.,, and R. J. Greenall. 2000. Binding sites of the polyamines putrescine, cadaverine, spermidine and spermine on A- and B-DNA located by simulated annealing. J. Biomol. Struct. Dyn. 18: 393412.
17. Bubienko, E.,, P. Cruz,, J. F. Thomason, and, P. N. Borer. 1983. Nearest-neighbor effects in the structure and function of nucleic acids. Prog. Nucleic Acid Res. Mol. Biol. 30: 4190.
18. Bujnicki, J. M.,, and M. Radlinska. 1999. Molecular evolution of DNA-(cytosine- N4) methyltransferases: evidence for their polyphyletic origin. Nucleic Acids Res. 27: 45014509.
19. Butzow, J. J.,, and G. L. Eichhorn. 1975. Different susceptibility of DNA and RNA to cleavage by metal ions. Nature 254: 358359.
20. Cammarano, P.,, F. Mazzei,, P. Londei,, A. Teichner,, M. de Rosa, and, A. Gambacorta. 1983. Secondary structure features of ribosomal RNA species within intact ribosomal subunits and efficiency of RNA-protein interactions in thermoacidophilic ( Caldariella acidophila, Bacillus acidocaldarius) and mesophilic ( Escherichia coli) bacteria. Biochim. Biophys. Acta 740: 300312.
21. Cermakian, N.,, and R. Cedergren. 1998. Modified nucleotides always were: an evolutionary model, p. 535–541. In H. Grosjean, and, R. Benne (ed.), Modification and Editing of RNA. ASM Press, Washington, DC.
22. Charlier, D.,, and L. Droogmans. 2005. Microbial life at high temperature, the challenges, the strategies. Cell. Mol. Life Sci. 62: 29742984.
23. Chen, K. Y.,, and H. Martynowicz. 1984. Lack of detectable polyamines in an extremely halophilic bacterium. Biochem. Biophys. Res. Commun. 124: 423429.
24. Cheng, X. 1995. DNA modification by methyltransferases. Curr. Opin. Struct. Biol. 5: 410.
25. Cohen, R. M.,, and R. Wolfenden. 1971. The equilibrium of hydrolytic deamination of cytidine and N4-methylcytidine. J. Biol. Chem. 246: 75667568.
26. Confalonieri, F.,, C. Elie,, M. Nadal,, C. de La Tour,, P. Forterre, and, M. Duguet. 1993. Reverse gyrase: a helicase-like domain and a type I topoisomerase in the same polypeptide. Proc. Natl. Acad. Sci. USA 90: 47534757.
27. Conn, G. L.,, and D. E. Draper. 1998. RNA structure. Curr. Opin. Struct. Biol. 8: 278285.
28. Conn, G. L.,, D. E. Draper,, E. E. Lattman, and, A. G. Gittis. 1999. Crystal structure of a conserved ribosomal protein-RNA complex. Science 284: 11711174.
29. D’Andrea, X.,, Alkema, X.,, Bell, X.,, Coddington, X.,, Haber, X.,, Hughes, X., and, Neilson. 1983. Methylated bases stabilize short RNA duplex. J. Am. Chem. Soc. 105: 636638.
30. Dalluge, J. J.,, T. Hamamoto,, K. Horikoshi,, R. Y. Morita,, K. O. Stetter, and, J. A. McCloskey. 1997. Posttranscriptional modification of tRNA in psychrophilic bacteria. J. Bacteriol. 179: 19181923.
31. Dalluge, J. J.,, T. Hashizume,, A. E. Sopchik,, J. A. McCloskey, and, D. R. Davis. 1996. Conformational flexibility in RNA: the role of dihydrouridine. Nucleic Acids Res. 24: 10731079.
32. Daniel, R. M.,, and D. A. Cowan. 2000. Biomolecular stability and life at high temperatures. Cell. Mol. Life Sci. 57: 250264.
33. Davanloo, P.,, M. Sprinzl,, K. Watanabe,, M. Albani, and, H. Kersten. 1979. Role of ribothymidine in the thermal stability of transfer RNA as monitored by proton magnetic resonance. Nucleic Acids Res. 6: 15711581.
34. Davis, D. R. 1995. Stabilization of RNA stacking by pseudouri-dine. Nucleic Acids Res. 23: 50205026.
35. Dennis, P. P.,, A. Omer, and, T. Lowe. 2001. A guided tour: small RNA function in Archaea. Mol. Microbiol. 40: 509519.
36. DiRuggiero, J.,, N. Santangelo,, Z. Nackerdien,, J. Ravel, and, F. T. Robb. 1997. Repair of extensive ionizing-radiation DNA damage at 95 degrees C in the hyperthermophilic archaeon Pyrococcus furiosus. J. Bacteriol. 179: 46434645.
37. Draper, D. E. 1996. Strategies for RNA folding. Trends Biochem. Sci. 21: 145149.
38. Droogmans, L.,, M. Roovers,, J. M. Bujnicki,, C. Tricot,, T. Hartsch,, V. Stalon, and, H. Grosjean. 2003. Cloning and characterization of tRNA (m 1A58) methyltransferase (TrmI) from Thermus thermophilus HB27, a protein required for cell growth at extreme temperatures. Nucleic Acids Res. 31: 21482156.
39. Edmonds, C. G.,, P. F. Crain,, R. Gupta,, T. Hashizume,, C. H. Hocart,, J. A. Kowalak,, S. C. Pomerantz,, K. O. Stetter, and, J. A. McCloskey. 1991. Posttranscriptional modification of tRNA in thermophilic archaea (Archaebacteria). J. Bacteriol. 173: 31383148.
40. Ehrlich, M.,, M. A. Gama-Sosa,, L. H. Carreira,, L. G. Ljungdahl,, K. C. Kuo, and, C. W. Gehrke. 1985. DNA methylation in thermophilic bacteria: N4-methylcytosine, 5-methylcytosine, and N6-methyladenine. Nucleic Acids Res. 13: 13991412.
41. Ehrlich, M.,, K. F. Norris,, R. Y. Wang,, K. C. Kuo, and, C. W. Gehrke. 1986. DNA cytosine methylation and heat-induced deamination. Biosci. Rep. 6: 387393.
42. Eisen, J. A.,, and P. C. Hanawalt. 1999. A phylogenomic study of DNA repair genes, proteins, and processes. Mutat. Res. 435: 171213.
43. Ellis, R. J. 2001. Macromolecular crowding: an important but neglected aspect of the intracellular environment. Curr. Opin. Struct. Biol. 11: 114119.
44. Engel, J. D.,, and P. H. von Hippel. 1978. Effects of methylation on the stability of nucleic acid conformations. Studies at the polymer level. J. Biol. Chem. 253: 927934.
45. Fang, X. W.,, B. L. Golden,, K. Littrell,, V. Shelton,, P. Thiyagarajan,, T. Pan, and, T. R. Sosnick. 2001. The thermodynamic origin of the stability of a thermophilic ribozyme. Proc. Natl. Acad. Sci. USA 98: 43554360.
46. Farahi, K.,, G. D. Pusch,, R. Overbeek, and, W. B. Whitman. 2004. Detection of lateral gene transfer events in the prokaryotic tRNA synthetases by the ratios of evolutionary distances method. J. Mol. Evol. 58: 615631.
47. Forterre, P. 2002. A hot story from comparative genomics: reverse gyrase is the only hyperthermophile-specific protein. Trends Genet. 18: 236237.
48. Forterre, P. Strategies of hyperthermophiles in adaptation of nucleic acids at high temperatures. In C. Gerday, and, N. Glansdorff (ed.), Extremophiles, Encyclopedia of Life Support Systems, in press. EOLSS Publishers, Oxford, United Kingdom.
49. Forterre, P.,, C. Bouthier De La Tour,, H. Philippe, and, M. Duguet. 2000. Reverse gyrase from hyperthermophiles: probable transfer of a thermoadaptation trait from archaea to bacteria. Trends Genet. 16: 152154.
50. Forterre, P.,, F. Charbonnier,, E. Marguet,, F. Harper, and, G. Henckes. 1992. Chromosome structure and DNA topology in extremely thermophilic archaebacteria. Biochem. Soc. Symp. 58: 99112.
51. Frederico, L. A.,, T. A. Kunkel, and, B. R. Shaw. 1990. A sensitive genetic assay for the detection of cytosine deamination: determination of rate constants and the activation energy. Biochemistry 29: 25322537.
52. Galtier, N.,, and J. R. Lobry. 1997. Relationships between genomic G+C content, RNA secondary structures, and optimal growth temperature in prokaryotes. J. Mol. Evol. 44: 632636.
53. Gong, Q.,, Q. Guo,, K. L. Tong,, G. Zhu,, J. T. Wong, and, H. Xue. 2002. NMR analysis of bovine tRNA Trp: conformation dependence of Mg 2+ binding. J. Biol. Chem. 277: 2069420701.
54. Grayling, R. A.,, K. Sandman, and, J. N. Reeve. 1996. DNA stability and DNA binding proteins. Adv. Protein Chem. 48: 437467.
55. Grogan, D. W. 2003. Cytosine methylation by the SuaI restriction-modification system: implications for genetic fidelity in a hyper-thermophilic archaeon. J. Bacteriol. 185: 46574661.
56. Grogan, D. W. 1996. Exchange of genetic markers at extremely high temperatures in the archaeon Sulfolobus acidocaldarius. J. Bacteriol. 178: 32073211.
57. Grogan, D. W. 2007. Mechanisms of genome stability and evolution, p. 120–138. In R. Cavicchioli (ed.), Archaea: Molecular and Cellular Biology. American Society for Microbiology, Washington, D.C.
58. Grogan, D. W. 2004. Stability and repair of DNA in hyperthermophilic Archaea. Curr. Issues Mol. Biol. 6: 137144.
59. Grogan, D. W.,, G. T. Carver, and, J. W. Drake. 2001. Genetic fidelity under harsh conditions: analysis of spontaneous mutation in the thermoacidophilic archaeon Sulfolobus acidocaldarius. Proc. Natl. Acad. Sci. USA 98: 79287933.
60. Grosjean, H.,, and W. Fiers. 1982. Preferential codon usage in prokaryotic genes: the optimal codon–anticodon interaction energy and the selective codon usage in efficiently expressed genes. Gene 18: 199209.
61. Gruber, T.,, C. Kohrer,, B. Lung,, D. Shcherbakov, and, W. Piendl. 2003. Affinity of ribosomal protein S8 from mesophilic and (hyper)thermophilic archaea and bacteria for 16S rRNA correlates with the growth temperatures of the organisms. FEBS Lett. 549: 123128.
62. Guagliardi, A.,, A. Napoli,, M. Rossi, and, M. Ciaramella. 1997. Annealing of complementary DNA strands above the melting point of the duplex promoted by an archaeal protein. J. Mol. Biol. 267: 841848.
63. Guipaud, O.,, and P. Forterre. 2001. DNA gyrase from Thermotoga maritima. Methods Enzymol. 334: 162171.
64. Guo, F.,, and T. R. Cech. 2002. Evolution of Tetrahymena ribozyme mutants with increased structural stability. Nat. Struct. Biol. 9: 855861.
65. Hamana, K.,, H. Hamana,, M. Niitsu,, K. Samejima,, T. Sakane, and, A. Yokota. 1994. Occurrence of tertiary and quaternary branched polyamines in thermophilic archaebacteria. Microbios 79: 109119.
66. Hamana, K.,, and S. Matsuzaki. 1992. Polyamines as a chemotaxonomic marker in bacterial systematics. Crit. Rev. Microbiol. 18: 261283.
67. Hamana, K.,, M. Niitsu,, S. Matsuzaki,, K. Samejima,, Y. Igarashi, and, T. Kodama. 1992. Novel linear and branched polyamines in the extremely thermophilic eubacteria Thermoleophilum, Bacillus and Hydrogenobacter. Biochem. J. 284(Pt 3) : 741747.
68. Hamana, K.,, M. Niitsu,, K. Samejima, and, S. Matsuzaki. 1991. Polyamine distributions in thermophilic eubacteria belonging to Thermus and Acidothermus. J. Biochem. (Tokyo) 109: 444449.
69. Helm, M. 2006. Post-transcriptional nucleotide modification and alternative folding of RNA. Nucleic Acids Res. 34: 721733.
70. Hennigan, A. N.,, and J. N. Reeve. 1994. mRNAs in the methanogenic archaeon Methanococcus vannielii: number s, half-lives and processing. Mol. Microbiol. 11: 655670.
71. Hensel, R.,, and H. Konig. 1988. Thermoadaptation of methanogenic bacteria by intracellular ion concentration FEMS Microbiol. Lett. 49: 7579.
72. Herschlag, D. 1995. RNA chaperones and the RNA folding problem. J. Biol. Chem. 270: 2087120874.
73. Hethke, C.,, A. Bergerat,, W. Hausner,, P. Forterre, and, M. Thomm. 1999. Cell-free transcription at 95 degrees: thermostability of transcriptional components and DNA topology requirements of Pyrococcus transcription. Genetics 152: 13251333.
74. Hou, M. H.,, S. B. Lin,, J. M. Yuann,, W. C. Lin,, A. H. Wang, and, L. Kan Ls. 2001. Effects of polyamines on the thermal stability and formation kinetics of DNA duplexes with abnormal structure. Nucleic Acids Res. 29: 51215128.
75. House, C. H.,, and S. L. Miller. 1996. Hydrolysis of dihydrouridine and related compounds. Biochemistry 35: 315320.
76. Hurst, L. D.,, and A. R. Merchant. 2001. High guanine-cytosine content is not an adaptation to high temperature: a comparative analysis amongst prokaryotes. Proc. Biol. Sci. 268: 493497.
77. Jain, S.,, G. Zon, and, M. Sundaralingam. 1989. Base only binding of spermine in the deep groove of the A-DNA octamer d(GTGTACAC). Biochemistry 28: 23602364.
78. Jolivet, E.,, F. Matsunaga,, Y. Ishino,, P. Forterre,, D. Prieur, and, H. Myllykallio. 2003. Physiological responses of the hyperthermophilic archaeon Pyrococcus abyssi to DNA damage caused by ionizing radiation. J. Bacteriol. 185: 39583961.
79. Kagawa, Y.,, H. Nojima,, N. Nukiwa,, M. Ishizuka,, T. Nakajima,, T. Yasuhara,, T. Tanaka, and, T. Oshima. 1984. High guanine plus cytosine content in the third letter of codons of an extreme thermophile. DNA sequence of the isopropylmalate dehydrogenase of Thermus thermophilus. J. Biol. Chem. 259: 29562960.
80. Kampmann, M.,, and D. Stock. 2004. Reverse gyrase has heat-protective DNA chaperone activity independent of supercoiling. Nucleic Acids Res. 32: 35373545.
81. Karran, P.,, and T. Lindahl. 1980. Hypoxanthine in deoxyribonucleic acid: generation by heat-induced hydrolysis of adenine residues and release in free form by a deoxyribonucleic acid glycosylase from calf thymus. Biochemistry 19: 60056011.
82. Kawai, G.,, T. Hashizume,, T. Miyazawa,, J. A. McCloskey, and, S. Yokoyama. 1989. Conformational characteristics of 4-acetylcytidine found in tRNA. Nucleic Acids Symp. Ser. : 6162.
83. Kawai, G.,, Y. Yamamoto,, T. Kamimura,, T. Masegi,, M. Sekine,, T. Hata,, T. Iimori,, T. Watanabe,, T. Miyazawa, and, S. Yokoyama. 1992. Conformational rigidity of specific pyrimidine residues in tRNA arises from posttranscriptional modifications that enhance steric interaction between the base and the 2′-hydroxyl group. Biochemistry 31: 10401046.
84. Kawashima, T.,, N. Amano,, H. Koike,, S. Makino,, S. Higuchi,, Y. Kawashima-Ohya,, K. Watanabe,, M. Yamazaki,, K. Kanehori,, T. Kawamoto,, T. Nunoshiba,, Y. Yamamoto,, H. Aramaki,, K. Makino, and, M. Suzuki. 2000. Archaeal adaptation to higher temperatures revealed by genomic sequence of Thermoplasma volcanium. Proc. Natl. Acad. Sci. USA 97: 1425714262.
85. Khachane, A. N.,, K. N. Timmis, and, V. A. dos Santos. 2005. Uracil content of 16S rRNA of thermophilic and psychrophilic prokaryotes correlates inversely with their optimal growth temperatures. Nucleic Acids Res. 33: 40164022.
86. Kikuchi, A.,, and K. Asai. 1984. Reverse gyrase—a topoisomerase which introduces positive superhelical turns into DNA. Nature 309: 677681.
87. Kohrer, C.,, C. Mayer,, O. Neumair,, P. Grobner, and, W. Piendl. 1998. Interaction of ribosomal L1 proteins from mesophilic and thermophilic Archaea and Bacteria with specific L1-binding sites on 23S rRNA and mRNA. Eur. J. Biochem. 256: 97105.
88. Koshlap, K. M.,, R. Guenther,, E. Sochacka,, A. Malkiewicz, and, P. F. Agris. 1999. A distinctive RNA fold: the solution structure of an analogue of the yeast tRNA Phe T-Psi-C domain. Biochemistry 38: 86478656.
89. Kowalak, J. A.,, J. J. Dalluge,, J. A. McCloskey, and, K. O. Stetter. 1994. The role of posttranscriptional modification in stabilization of transfer RNA from hyperthermophiles. Biochemistry 33: 78697876.
90. Kumagai, I.,, K. Watanabe, and, T. Oshima. 1980. Thermally induced biosynthesis of 2′- O-methylguanosine in tRNA from an extreme thermophile, Thermus thermophilus HB27. Proc. Natl. Acad. Sci. USA 77: 19221926.
91. Lambros, R. J.,, J. R. Mortimer, and, D. R. Forsdyke. 2003. Optimum growth temperature and the base composition of open reading frames in prokaryotes. Extremophiles 7: 443450.
92. Lazcano, A.,, R. Guerrero,, L. Margulis, and, J. Oro. 1988. The evolutionary transition from RNA to DNA in early cells. J. Mol. Evol. 27: 283290.
93. Lee, J. C.,, J. J. Cannone, and, R. R. Gutell. 2003. The lonepair triloop: a new motif in RNA structure. J. Mol. Biol. 325: 6583.
94. Levy, M.,, and S. L. Miller. 1999. The prebiotic synthesis of modified purines and their potential role in the RNA world. J. Mol. Evol. 48: 631637.
95. Levy, M.,, and S. L. Miller. 1998. The stability of the RNA bases: implications for the origin of life. Proc. Natl. Acad. Sci. USA 95: 79337938.
96. Limbach, P. A.,, P. F. Crain,, S. C. Pomerantz, and, J. A. McCloskey. 1995. Structures of posttranscriptionally modified nucleosides from RNA. Biochimie 77: 135138.
97. Lindahl, T. 1979. DNA glycosylases, endonucleases for apurinic/apyrimidinic sites, and base excision-repair. Prog. Nucleic Acid Res. Mol. Biol. 22: 135192.
98. Lindahl, T. 1993. Instability and decay of the primary structure of DNA. Nature 362: 709715.
99. Lindahl, T. 1967. Irreversible heat inactivation of transfer ribonucleic acids. J. Biol. Chem. 242: 19701973.
100. Lindahl, T.,, and A. Andersson. 1972. Rate of chain breakage at apurinic sites in double-stranded deoxyribonucleic acid. Biochemistry 11: 36183623.
101. Lindahl, T.,, and O. Karlstrom. 1973. Heat-induced depyrimidination of deoxyribonucleic acid in neutral solution. Biochemistry 12: 51515154.
102. Lindahl, T.,, and B. Nyberg. 1974. Heat-induced deamination of cytosine residues in deoxyribonucleic acid. Biochemistry 13: 34053410.
103. Lindahl, T.,, and B. Nyberg. 1972. Rate of depurination of native deoxyribonucleic acid. Biochemistry 11: 36103618.
104. Londei, P.,, J. Teixido,, M. Acca,, P. Cammarano, and, R. Amils. 1986. Total reconstitution of active large ribosomal subunits of the thermoacidophilic archaebacterium Sulfolobus solfataricus. Nucleic Acids Res. 14: 22692285.
105. Lopez-Garcia, P.,, and P. Forterre. 1999. Control of DNA topology during thermal stress in hyperthermophilic archaea: DNA topoisomerase levels, activities and induced thermotolerance during heat and cold shock in Sulfolobus. Mol. Microbiol. 33: 766777.
106. Lopez-Garcia, P.,, and P. Forterre. 2000. DNA topology and the thermal stress response, a tale from mesophiles and hyperthermophiles. Bioessays 22: 738746.
107. Lurz, R.,, M. Grote,, J. Dijk,, R. Reinhardt, and, B. Dobrinski. 1986. Electron microscopic study of DNA complexes with proteins from the Archaebacterium Sulfolobus acidocaldarius. EMBO J. 5: 37153721.
108. Lutsenko, E.,, and A. S. Bhagwat. 1999. Principal causes of hot spots for cytosine to thymine mutations at sites of cytosine methylation in growing cells. A model, its experimental support and implications. Mutat. Res. 437: 1120.
109. Lynn, D. J.,, G. A. Singer, and, D. A. Hickey. 2002. Synonymous codon usage is subject to selection in thermophilic bacteria. Nucleic Acids Res. 30: 42724277.
110. Makarova, K. S.,, L. Aravind,, N. V. Grishin,, I. B. Rogozin, and, E. V. Koonin. 2002. A DNA repair system specific for thermophilic Archaea and bacteria predicted by genomic context analysis. Nucleic Acids Res. 30: 482496.
111. Makarova, K. S.,, and E. V. Koonin. 2003. Comparative genomics of Archaea: how much have we learned in six years, and what’s next? Genome Biol. 4: 115.
112. Male, R.,, V. M. Fosse, and, K. Kleppe. 1982. Polyamine-induced hydrolysis of apurinic sites in DNA and nucleosomes. Nucleic Acids Res. 10: 63056318.
113. Marck, C.,, and H. Grosjean. 2002. tRNomics: analysis of tRNA genes from 50 genomes of Eukarya, Archaea, and Bacteria reveals anticodon-sparing strategies and domain-specific features. RNA 8: 11891232.
114. Marguet, E.,, and P. Forterre. 1994. DNA stability at temperatures typical for hyperthermophiles. Nucleic Acids Res. 22: 16811686.
115. Marguet, E.,, and P. Forterre. 2001. Stability and manipulation of DNA at extreme temperatures. Methods Enzymol. 334: 205215.
116. Maxam, A. M.,, and W. Gilbert. 1977. A new method for sequencing DNA. Proc. Natl. Acad. Sci. USA 74: 560564.
117. McCloskey, J. A.,, D. E. Graham,, S. Zhou,, P. F. Crain,, M. Ibba,, J. Konisky,, D. Soll, and, G. J. Olsen. 2001. Post-transcriptional modification in archaeal tRNAs: identities and phylogenetic relations of nucleotides from mesophilic and hyperthermophilic Methanococcales. Nucleic Acids Res. 29: 46994706.
118. Minton, A. P. 2001. The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media. J. Biol. Chem. 276: 1057710580.
119. Minyat, E. E.,, V. I. Ivanov,, A. M. Kritzyn,, L. E. Minchenkova, and, A. K. Schyolkina. 1979. Spermine and spermidine-induced B to A transition of DNA in solution. J. Mol. Biol. 128: 397409.
120. Morales, A. J.,, M. A. Swairjo, and, P. Schimmel. 1999. Structure-specific tRNA-binding protein from the extreme thermophile Aquifex aeolicus. EMBO J. 18: 34753483.
121. Nagaswamy, U.,, and G. E. Fox. 2002. Frequent occurrence of the T-loop RNA folding motif in ribosomal RNAs. RNA 8: 11121119.
122. Nakashima, H.,, S. Fukuchi, and, K. Nishikawa. 2003. Compositional changes in RNA, DNA and proteins for bacterial adaptation to higher and lower temperatures. J. Biochem. (Tokyo) 133: 507513.
123. Napoli, A.,, A. Valenti,, V. Salerno,, M. Nadal,, F. Garnier,, M. Rossi, and, M. Ciaramella. 2004. Reverse gyrase recruitment to DNA after UV light irradiation in Sulfolobus solfataricus. J. Biol. Chem. 279: 3319233198.
124. Nobles, K. N.,, C. S. Yarian,, G. Liu,, R. H. Guenther, and, P. F. Agris. 2002. Highly conserved modified nucleosides influence Mg 2+-dependent tRNA folding. Nucleic Acids Res. 30: 47514760.
125. Noon, K. R.,, E. Bruenger, and, J. A. McCloskey. 1998. Posttranscriptional modifications in 16S and 23S rRNAs of the archaeal hyperthermophile Sulfolobus solfataricus. J. Bacteriol. 180: 28832888.
126. Noon, K. R.,, R. Guymon,, P. F. Crain,, J. A. McCloskey,, M. Thomm,, J. Lim, and, R. Cavicchioli. 2003. Influence of temperature on tRNA modification in archaea: Methanococcoides burtonii (optimum growth temperature Topt, 23 degrees C) and Stetteria hydrogenophila ( Topt, 95 degrees C). J. Bacteriol. 185: 54835490.
127. Okada, N.,, S. Noguchi,, H. Kasai,, N. Shindo-Okada,, T. Ohgi,, T. Goto, and, S. Nishimura. 1979. Novel mechanism of post-transcriptional modification of tRNA. Insertion of bases of Q precursors into tRNA by a specific tRNA transglycosylase reaction. J. Biol. Chem. 254: 30673073.
128. Omer, A. D.,, T. M. Lowe,, A. G. Russell,, H. Ebhardt,, S. R. Eddy, and, P. P. Dennis. 2000. Homologs of small nucleolar RNAs in Archaea. Science 288: 517522.
129. Oshima, T. 1989. Polyamines in Thermophiles. The Physiology of Polyamines, p. 35–46, vol. 2. CRC Press, Boca Raton, FL.
130. Oshima, T.,, N. Hamasaki,, M. Senshu,, K. Kakinuma, and, I. Kuwajima. 1987. A new naturally occurring polyamine containing a quaternary ammonium nitrogen. J. Biol. Chem. 262: 1197911981.
131. Oshima, T.,, Y. Sakaki,, N. Wakayama,, K. Watanabe, and, Z. Ohashi. 1976. Biochemical studies on an extreme thermophile Thermus thermophilus: thermal stabilities of cell constituents and a bacteriophage. Experientia Suppl. 26: 317331.
132. Ovadi, J.,, and V. Saks. 2004. On the origin of intracellular compartmentation and organized metabolic systems. Mol. Cell. Biochem. 256-257: 512.
133. Palmer, J. R.,, T. Baltrus,, J. N. Reeve, and, C. J. Daniels. 1992. Transfer RNA genes from the hyperthermophilic Archaeon, Methanopyrus kandleri. Biochim. Biophys. Acta 1132: 315318.
134. Paz, A.,, D. Mester,, I. Baca,, E. Nevo, and, A. Korol. 2004. Adaptive role of increased frequency of polypurine tracts in mRNA sequences of thermophilic prokaryotes. Proc. Natl. Acad. Sci. USA 101: 29512956.
135. Peak, M. J.,, F. T. Robb, and, J. G. Peak. 1995. Extreme resistance to thermally induced DNA backbone breaks in the hyperthermophilic archaeon Pyrococcus furiosus. J. Bacteriol. 177: 63166318.
136. Peattie, D. A. 1979. Direct chemical method for sequencing RNA. Proc. Natl. Acad. Sci. USA 76: 17601764.
137. Pereira, S. L.,, and J. N. Reeve. 1998. Histones and nucleosomes in Archaea and Eukarya: a comparative analysis. Extremophiles 2: 141148.
138. Philippsen, P.,, R. Thiebe,, W. Wintermeyer, and, H. G. Zachau. 1968. Splitting of phenylalanine specific tRNA into half molecules by chemical means. Biochem. Biophys. Res. Commun. 33: 922928.
139. Poole, A.,, D. Penny, and, B. Sjoberg. 2000. Methyl-RNA: an evolutionary bridge between RNA and DNA? Chem. Biol. 7: R207R216.
140. Quigley, G. J.,, M. M. Teeter, and, A. Rich. 1978. Structural analysis of spermine and magnesium ion binding to yeast phenylalanine transfer RNA. Proc. Natl. Acad. Sci USA 75: 6468.
141. Rodriguez, A. C.,, and D. Stock. 2002. Crystal structure of reverse gyrase: insights into the positive supercoiling of DNA. EMBO J. 21: 418426.
142. Romby, P.,, P. Carbon,, E. Westhof,, C. Ehresmann,, J. P. Ebel,, B. Ehresmann, and, R. Giege. 1987. Importance of conserved residues for the conformation of the T-loop in tRNAs. J. Biomol. Struct. Dyn. 5: 669687.
143. Roovers, M.,, J. Wouters,, J. M. Bujnicki,, C. Tricot,, V. Stalon,, H. Grosjean, and, L. Droogmans. 2004. A primordial RNA modification enzyme: the case of tRNA (m 1A) methyltransferase. Nucleic Acids Res. 32: 465476.
144. Sandman, K.,, and Reeve, J. N. 2005. Archaeal chromatin proteins: different structures but common function? Curr. Opin. Microbiol. 8: 656661.
145. Serebrov, V.,, R. J. Clarke,, H. J. Gross, and, L. Kisselev. 2001. Mg 2+-induced tRNA folding. Biochemistry 40: 66886698.
146. Shen, J. C.,, W. M. Rideout III, and, P. A. Jones. 1994. The rate of hydrolytic deamination of 5-methylcytosine in double-stranded DNA. Nucleic Acids Res. 22: 972976.
147. Shigi, N.,, T. Suzuki,, T. Terada,, M. Shirouzu,, S. Yokoyama, and, K. Watanabe. 2006. Temperature-dependent biosynthesis of 2-thioribothymidine of Thermus thermophilus tRNA. J. Biol. Chem. 281: 21042113.
148. Sprinzl, M.,, and K. S. Vassilenko. 2005. Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res. 33: D139D140.
149. Stubbe, J. 2000. Ribonucleotide reductases: the link between an RNA and a DNA world? Curr. Opin. Struct. Biol. 10: 731736.
150. Tehei, M.,, B. Franzetti,, M. C. Maurel,, J. Vergne,, C. Hountondji, and, G. Zaccai. 2002. The search for traces of life: the protective effect of salt on biological macromolecules. Extremophiles 6: 427430.
151. Terui, Y.,, M. Ohnuma,, K. Hiraga,, E. Kawashima, and, T. Oshima. 2005. Stabilization of nucleic acids by unusual polyamines produced by an extreme thermophile, Thermus thermophilus. Biochem. J. 388: 427433.
152. Tong, K. L.,, and J. T. Wong. 2004. Anticodon and wobble evolution. Gene 333: 169177.
153. Urbonavicius, J.,, J. Armengaud, and, H. Grosjean. Identity elements required for enzymatic formation of N( 2), N( 2)-dimethylguanosine from N( 2)-monomethylated derivative and its possible role in avoiding alternative conformations in archaeal tRNA. J. Mol. Biol XXX.
154. Ushida, C.,, T. Muramatsu,, H. Mizushima,, T. Ueda,, K. Watanabe,, K. O. Stetter,, P. F. Crain,, J. A. McCloskey, and, Y. Kuchino. 1996. Structural feature of the initiator tRNA gene from Pyrodictium occultum and the thermal stability of its gene product, tRNA(imet). Biochimie 78: 847855.
155. Vanzo, N. F.,, Y. S. Li,, B. Py,, E. Blum,, C. F. Higgins,, L. C. Raynal,, H. M. Krisch, and, A. J. Carpousis. 1998. Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome. Genes Dev. 12: 27702781.
156. Varani, G. 1995. Exceptionally stable nucleic acid hairpins. Annu. Rev. Biophys. Biomol. Struct. 24: 379404.
157. Varani, G.,, and W. H. McClain. 2000. The G x U wobble base pair. A fundamental building block of RNA structure crucial to RNA function in diverse biological systems. EMBO Rep. 1: 1823.
158. Vergne, J.,, J. A. H. Cognet,, E. Szathmary, and, M.-C. Maurel. In vitro selection of halo-thermophilic RNA reveals two families of resistant RNA. Gene, XXX.
159. Vijayanathan, V.,, T. Thomas,, A. Shirahata, and, T. J. Thomas. 2001. DNA condensation by polyamines: a laser light scattering study of structural effects. Biochemistry 40: 1364413651.
160. Wang, R. Y.,, K. C. Kuo,, C. W. Gehrke,, L. H. Huang, and, M. Ehrlich. 1982. Heat- and alkali-induced deamination of 5-methylcytosine and cytosine residues in DNA. Biochim. Biophys. Acta 697: 371377.
161. Watanabe, K.,, T. Oshima,, K. Iijima,, Z. Yamaizumi, and, S. Nishimura. 1980. Purification and thermal stability of several amino acid-specific tRNAs from an extreme thermophile, Thermus thermophilus HB8. J. Biochem. (Tokyo) 87: 113.
162. Watanabe, K.,, M. Shinma,, T. Oshima, and, S. Nishimura. 1976. Heat-induced stability of tRNA from an extreme thermophil e, Thermus thermophilus. Biochem. Biophys. Res. Commun. 72: 11371144.
163. Watanabe, M.,, M. Matsuo,, S. Tanaka,, H. Akimoto,, S. Asahi,, S. Nishimura,, J. R. Katze,, T. Hashizume,, P. F. Crain,, J. A. McCloskey, and, N. Okada. 1997. Biosynthesis of archaeosine, a novel derivative of 7-deazaguanosine specific to archaeal tRNA, proceeds via a pathway involving base replacement on the tRNA polynucleotide chain. J. Biol. Chem. 272: 2014620151.
164. Weeks, K. M.,, and T. R. Cech. 1996. Assembly of a ribonucleoprotein catalyst by tertiary structure capture. Science 271: 345348.
165. Weinberg, M. V.,, G. J. Schut,, S. Brehm,, S. Datta, and, M. W. Adams. 2005. Cold shock of a hyperthermophilic archaeon: Pyrococcus furiosus exhibits multiple responses to a suboptimal growth temperature with a key role for membrane-bound glyco-proteins. J. Bacteriol. 187: 336348.
166. Westhof, E.,, P. Dumas, and, D. Moras. 1988. Restrained refinement of two crystalline forms of yeast aspartic acid and phenylalanine transfer RNA crystals. Acta Crystallogr. A 44(Pt 2) : 112123.
167. Wildenauer, D.,, H. J. Gross, and, D. Riesner. 1974. Enzymatic methylations: III. Cadaverine-induced conformational changes of E. coli tRNA-fMet as evidenced by the availability of a specific adenosine and a specific cytidine residue for methylation. Nucleic Acids Res. 1: 11651182.
168. Wintermeyer, W.,, and H. G. Zachau. 1970. A specific chemical chain scission of tRNA at 7-methylguanosine. FEBS Lett. 11: 160164.
169. Wright, M. C.,, and G. F. Joyce. 1997. Continuous in vitro evolution of catalytic function. Science 276: 614617.
170. Xaplanteri, M. A.,, A. D. Petropoulos,, G. P. Dinos, and, D. L. Kalpaxis. 2005. Localization of spermine binding sites in 23S rRNA by photoaffinity labeling: parsing the spermine contribution to ribosomal 50S subunit functions. Nucleic Acids Res. 33: 27922805.
171. Xue, H.,, K. L. Tong,, C. Marck,, H. Grosjean, and, J. T. Wong. 2003. Transfer RNA paralogs: evidence for genetic code-amino acid biosynthesis coevolution and an archaeal root of life. Gene 310: 5966.
172. Yokoyama, S.,, K. Watanabe, and, T. Miyazawa. 1987. Dynamic structures and functions of transfer ribonucleic acids from extreme thermophiles. Adv. Biophys. 23: 115147.
173. Yue, D.,, A. Kintanar, and, J. Horowitz. 1994. Nucleoside modifications stabilize Mg 2+ binding in Escherichia coli tRNA-Val: an imino proton NMR investigation. Biochemistry 33: 89058911.
174. Yusupov, M. M.,, G. Z. Yusupova,, A. Baucom,, K. Lieberman,, T. N. Earnest,, J. H. Cate, and, H. F. Noller. 2001. Crystal structure of the ribosome at 5.5 A resolution. Science 292: 883896.
175. Zhang, X.,, and C. K. Mathews. 1994. Effect of DNA cytosine methylation upon deamination-induced mutagenesis in a natural target sequence in duplex DNA. J. Biol. Chem. 269: 70667069.

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