Full Text:   <1694>

CLC number: Q78

On-line Access: 2011-06-07

Received: 2010-09-13

Revision Accepted: 2011-05-05

Crosschecked: 2011-05-09

Cited: 0

Clicked: 3743

Citations:  Bibtex RefMan EndNote GB/T7714

-   Go to

Article info.
1. Reference List
Open peer comments

Journal of Zhejiang University SCIENCE B 2011 Vol.12 No.6 P.419-427


Differences in dinucleotide frequencies of thermophilic genes encoding water soluble and membrane proteins

Author(s):  Hiroshi Nakashima, Yuka Kuroda

Affiliation(s):  Department of Clinical Laboratory Science, Graduate Course of Medical Science and Technology, School of Health Sciences, Kanazawa University, 5-11-80 Kodatsuno, Kanazawa 920-0942, Japan

Corresponding email(s):   naka@kenroku.kanazawa-u.ac.jp

Key Words:  Water soluble and membrane proteins, Purine/pyrimidine dimers, Thermophilic and mesophilic species, Dinucleotide frequencies

Share this article to: More |Next Article >>>

Hiroshi Nakashima, Yuka Kuroda. Differences in dinucleotide frequencies of thermophilic genes encoding water soluble and membrane proteins[J]. Journal of Zhejiang University Science B, 2011, 12(6): 419-427.

@article{title="Differences in dinucleotide frequencies of thermophilic genes encoding water soluble and membrane proteins",
author="Hiroshi Nakashima, Yuka Kuroda",
journal="Journal of Zhejiang University Science B",
publisher="Zhejiang University Press & Springer",

%0 Journal Article
%T Differences in dinucleotide frequencies of thermophilic genes encoding water soluble and membrane proteins
%A Hiroshi Nakashima
%A Yuka Kuroda
%J Journal of Zhejiang University SCIENCE B
%V 12
%N 6
%P 419-427
%@ 1673-1581
%D 2011
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1000331

T1 - Differences in dinucleotide frequencies of thermophilic genes encoding water soluble and membrane proteins
A1 - Hiroshi Nakashima
A1 - Yuka Kuroda
J0 - Journal of Zhejiang University Science B
VL - 12
IS - 6
SP - 419
EP - 427
%@ 1673-1581
Y1 - 2011
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B1000331

The occurrence frequencies of the dinucleotides of genes of three thermophilic and three mesophilic species from both archaea and eubacteria were investigated in this study. The genes encoding water soluble proteins were rich in the dinucleotides of purine dimers, whereas the genes encoding membrane proteins were rich in pyrimidine dimers. The dinucleotides of purine dimers are the counterparts of pyrimidine dimers in a double-stranded DNA. The purine/pyrimidine dimers were favored in the thermophiles but not in the mesophiles, based on comparisons of observed and expected frequencies. This finding is in agreement with our previous study which showed that purine/pyrimidine dimers are positive factors that increase the thermal stability of DNA. The dinucleotides AA, AG, and GA are components of the codons of charged residues of Glu, Asp, Lys, and Arg, and the dinucleotides TT, CT, and TC are components of the codons of hydrophobic residues of Leu, Ile, and Phe. This is consistent with the suitabilities of the different amino acid residues for water soluble and membrane proteins. Our analysis provides a picture of how thermophilic species produce water soluble and membrane proteins with distinctive characters: the genes encoding water soluble proteins use DNA sequences rich in purine dimers, and the genes encoding membrane proteins use DNA sequences rich in pyrimidine dimers on the opposite strand.

Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article


[1]Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J., 1990. Basic local alignment search tool. J. Mol. Biol., 215(3):403-410.

[2]Anderson, I., Ulrich, L.E., Lupa, B., Susanti, D., Porat, I., Hooper, S.D., Lykidis, A., Sieprawska-Lupa, M., Dharmarajan, L., Goltsman, E., et al., 2009. Genomic characterization of methanomicrobiales reveals three classes of methanogens. PLoS One, 4(6):1-9.

[3]Anson, L., 2009. Membrane protein biophysics. Nature, 459(7245):343.

[4]Bao, Q., Tian, Y., Li, W., Xu, Z., Xuan, Z., Hu, S., Dong, W., Yang, J., Chen, Y., Xue, Y., et al., 2002. A complete sequence of the T. tengcongensis genome. Genome Res., 12(5):689-700.

[5]Blattner, F.R., Plunkett, G.III, Bloch, C.A., Perna, N.T., Burland, V., Riley, M., Collado-Vides, J., Glasner, J.D., Rode, C.K., Mayhew, G.F., et al., 1997. The complete genome sequence of Escherichia coli K-12. Science, 277(5331):1453-1462.

[6]Chargaff, E., Lipshitz, R., Green, C., Hodes, M.E., 1951. The composition of the deoxyribonucleic acid of salmon sperm. J. Biol. Chem., 192(1):223-230.

[7]Chargaff, E., Lipshitz, R., Green, C., 1952. Composition of the desoxypentose nucleic acids of four genera of sea-urchin. J. Biol. Chem., 195(1):155-160.

[8]Chou, P.Y., Fasman, G.D., 1978. Empirical predictions of protein conformation. Ann. Rev. Biochem., 47(1):251-276.

[9]Farias, S.T., Bonato, M.C.M., 2003. Preferred amino acids and thermostability. Genet. Mol. Res., 2(4):383-393.

[10]Fleischmann, R.D., Adams, M.D., White, O., Clayton, R.A., Kirkness, E.F., Kerlavage, A.R., Bult, C.J., Tomb, J.F., Dougherty, B.A., Merrick, J.M., et al., 1995. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science, 269(5223):496-512.

[11]Forsdyke, D.R., Mortimer, J.R., 2000. Chargaff’s legacy. Gene, 261(1):127-137.

[12]Fricke, W.F., Seedorf, H., Henne, A., Krüer, M., Liesegang, H., Hedderich, R., Gottschalk, G., Thauer, R.K., 2006. The genome sequence of Methanosphaera stadtmanae reveals why this human intestinal archaeon is restricted to methanol and H2 for methane formation and ATP synthesis. J. Bacteriol., 188(2):642-658.

[13]Hirokawa, T., Boon-Chieng, S., Mitaku, S., 1998. SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics, 14(4):378-379.

[14]Karkas, J.D., Runder, R., Chargaff, E., 1968. Separation of B. subtilis DNA into complementary strands, II. Template functions and composition as determined by transcription with RNA polymerase. PNAS, 60(3):915-920.

[15]Karlin, S., Burge, C., 1995. Dinucleotide relative abundance extremes: a genomic signature. Trends Genet., 11(7):283-290.

[16]Karlin, S., Mrázek, J., Campbell, A.M., 1997. Compositional biases of bacterial genomes and evolutionary implications. J. Bacteriol., 179(12):3899-3913.

[17]Kawabata, T., Fukuchi, S., Homma, K., Ota, M., Araki, J., Ito, T., Ichiyoshi, N., Nishikawa, K., 2002. GTOP: a database of protein structures predicted from genome sequences. Nucleic Acids Res., 30(1):294-298.

[18]Kawarabayasi, Y., Hino, Y., Horikawa, H., Jin-no, K., Takahashi, M., Sekine, M., Baba, S., Ankai, A., Kosugi, H., Hosoyama, A., et al., 2001. Complete genome sequence of an aerobic thermoacidophilic crenarchaeon, Sulfolobus tokodaii strain 7. DNA Res., 8(4):123-140.

[19]Kawashima, T., Amano, N., Koike, H., Makino, S., Higuchi, S., Kawashima-Ohya, Y., Watanabe, K., Yamazaki, M., Kanehori, K., Kawamoto, T., et al., 2000. Archaeal adaptation to higher temperatures revealed by genomic sequence of Thermoplasma volcanium. PNAS, 97(26):14257-14262.

[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., et al., 1997. The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature, 390(6658):364-370.

[21]Kreil, D.P., Ouzounis, C.A., 2001. Identification of thermophilic species by the amino acid compositions deduced from their genomes. Nucleic Acids Res., 29(7):1608-1615.

[22]Kumar, S., Tsai, C.J., Nussinov, R., 2000. Factors enhancing protein thermostability. Protein Eng., 13(3):179-191.

[23]Lambros, R.J., Mortimer, J.R., Forsdyke, D.R., 2003. Optimum growth temperature and the base composition of open reading frames in prokaryotes. Extremophiles, 7(6):443-450.

[24]Lawrence, J.G., Ochman, H., 1997. Amelioration of bacterial genomes: rates of change and exchange. J. Mol. Evol., 44(4):383-397.

[25]Lynn, D.J., Singer, G.A.C., Hickey, D.A., 2002. Synonymous codon usage is subject to selection in thermophilic bacteria. Nucleic Acids Res., 30(19):4272-4277.

[26]Mitchell, D., Bridge, R., 2006. A test of Chargaff’s second rule. Biochem. Biophys. Res. Commun., 340(1):90-94.

[27]Muto, A., Osawa, S., 1987. The guanine and cytosine content of genomic DNA and bacterial evolution. PNAS, 84(1):166-169.

[28]Nakashima, H., Ota, M., Nishikawa, K., Ooi, T., 1998. Gene from nine genomes are separated into their organisms in the dinucleotide composition space. DNA Res., 5(5):251-259.

[29]Nakashima, H., Fukuchi, S., Nishikawa, K., 2003. Compositional changes in RNA, DNA and proteins for bacterial adaptation to higher and lower temperatures. J. Biochem., 133(4):507-513.

[30]Nelson, K.E., Clayton, R.A., Gill, S.R., Gwinn, M.L., Dodson, R.J., Haft, D.H., Hickey, E.K., Peterson, J.D., Nelson, W.C., Ketchum, K.A., et al., 1999. Evidence for lateral gene transfer between Archaea and Bacteria from genome sequence of Thermotoga maritima. Nature, 399(6734):323-329.

[31]Ng, W.V., Kennedy, S.P., Mahairas, G.G., Berquist, B., Pan, M., Shukla, H.D., Lasky, S.R., Baliga, N., Thorsson, V., Sbrogna, J., et al., 2000. Genome sequence of Halobacterium species NRC-1. PNAS, 97(22):12176-12181.

[32]Paz, A., Mester, D., Baca, I., Nevo, E., Korol, A., 2004. Adaptive role of increased frequency of polypurine tracts in mRNA sequences of thermophilic prokaryotes. PNAS, 101(9):2951-2956.

[33]Runder, R., Karkas, J.D., Chargaff, E., 1968. Separation of B. subtilis DNA into complementary strands. III. Direct analysis. PNAS, 60(3):921-922.

[34]Slesarev, A.I., Mezhevaya, K.V., Makarova, K.S., Polushin, N.N., Shcherbinina, O.V., Shakhova, V.V., Belova, G.I., Aravind, L., Natale, D.A., Rogozin, I.B., et al., 2002. The complete genome of hyperthermophile Methanopyrus kandleri AV19 and monophyly of archaeal methanogens. PNAS, 99(7):4644-4649.

[35]Stover, C.K., Pham, X.Q., Erwin, A.L., Mizoguchi, S.D., Warrener, P., Hickey, M.J., Brinkman, F.S.L., Hufnagle, W.O., Kowalik, D.J., Lagrou, M., et al., 2000. Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature, 406(6799):959-964.

[36]Yokota, K., Satou, K., Ohki, S., 2006. Comparative analysis of protein thermostability: differences in amino acid content and substitution at the surfaces and in the core regions of thermophilic and mesophilic proteins. Sci. Technol. Adv. Mater., 7(3):255-262.

[37]Zeldovich, K.B., Berezovsky, I.N., Shakhnovich, E.I., 2007. Protein and DNA sequence determinants of thermophilic adaptation. PLoS Comput. Biol., 3(1):62-72.

[38]Zhou, X.X., Wang, Y.B., Pan, Y.J., Li, W.F., 2008. Differences in amino acids composition and coupling patterns between mesophilic and thermophilic proteins. Amino Acids, 34(1):25-33.

Open peer comments: Debate/Discuss/Question/Opinion


Please provide your name, email address and a comment

Journal of Zhejiang University-SCIENCE, 38 Zheda Road, Hangzhou 310027, China
Tel: +86-571-87952783; E-mail: cjzhang@zju.edu.cn
Copyright © 2000 - 2022 Journal of Zhejiang University-SCIENCE