Skip to main content
Log in

Structure-dependent relationships between growth temperature of prokaryotes and the amino acid frequency in their proteins

  • Original Paper
  • Published:
Extremophiles Aims and scope Submit manuscript

Abstract

We studied the amino acid frequency and substitution patterns between homologues of prokaryotic species adapted to temperatures in the range 0–102°C, and found a significant temperature-dependent difference in frequency for many of the amino acids. This was particularly clear when we analysed the surface and core residues separately. The difference between the surface and the core is getting more pronounced in proteins adapted to warmer environments, with a more hydrophobic core, and more charged and long-chained amino acids on the surface of the proteins. We also see that mesophiles have a more similar amino acid composition to psychrophiles than to thermophiles, and that archea appears to have a slightly different pattern of substitutions than bacteria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

OGT:

Optimal growth temperature

SASA:

Solvent accessible surface area

References

  • Apweiler R, Bairoch A, Wu CH, Barker WC, Boeckmann B, Ferro S, Gasteiger E, Huang H, Lopez R, Magrane M, Martin MJ, Natale DA, O’Donovan C, Redaschi N, Yeh LS (2004) UniProt: the universal protein knowledgebase. Nucleic Acids Res 32(Database issue):D115–D119

    Google Scholar 

  • Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, Khanna A, Marshall M, Moxon S, Sonnhammer EL, Studholme DJ, Yeats C, Eddy SR (2004) The Pfam protein families database. Nucleic Acids Res 32(Database issue):D138–D141

    Google Scholar 

  • Berezovsky IN, Shakhnovich EI (2005) Physics and evolution of thermophilic adaptation. Proc Natl Acad Sci USA 102(36):12742–12747

    Article  PubMed  CAS  Google Scholar 

  • Berezovsky IN, Zeldovich KB, Shakhnovich EI (2007) Positive and negative design in stability and thermal adaptation of natural proteins. PLOS Comput Biol doi:10.1371/journal.pcbi.0030052.eor

  • Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The protein data bank. Nucleic Acids Res 28(1):235–242

    Article  PubMed  CAS  Google Scholar 

  • Bogin O, Peretz M, Burstein Y (1997) Thermoanaerobacter brockii alcohol dehydrogenase: characterization of the active site metal and its ligand amino acids. Protein Sci 6(2):450–458

    Article  PubMed  CAS  Google Scholar 

  • Brinda KV, Vishveshwara S (2005) Oligomeric protein structure networks: insights into protein-protein interactions. BMC Bioinformatics (6):296

  • D’Aquino JA, Gomez J, Hilser VJ, Lee KH, Amzel LM, Freire E (1996) The magnitude of the backbone conformational entropy change in protein folding. Proteins 25(2):143–156

    PubMed  CAS  Google Scholar 

  • Dayhoff SA (1978) Atlas of protein sequence and structure. National Biomedicine Research Foundation, Washington, DC, USA

    Google Scholar 

  • Deming JW (2002) Psychrophiles and polar regions. Curr Opin Microbiol 5(3):301–309

    Article  PubMed  CAS  Google Scholar 

  • Farias ST, Bonato MC (2003) Preferred amino acids and thermostability. Genet Mol Res 2(4):383–393

    PubMed  CAS  Google Scholar 

  • Feller G, d’Amico D, Gerday C (1999) Thermodynamic stability of a cold-active alpha-amylase from the Antarctic bacterium Alteromonas haloplanctis. Biochemistry 38(14):4613–4619

    Article  PubMed  CAS  Google Scholar 

  • Feller G, Gerday C (2003) Psychrophilic enzymes: hot topics in cold adaptation. Nat Rev Microbiol 1(3):200–208

    Article  PubMed  CAS  Google Scholar 

  • Galtier N, Lobry JR (1997) Relationships between genomic G+C content, RNA secondary structures, and optimal growth temperature in prokaryotes. J Mol Evol 44(6):632–636

    Article  PubMed  CAS  Google Scholar 

  • Georlette D, Blaise V, Collins T, D’Amico S, Gratia E, Hoyoux A, Marx JC, Sonan G, Feller G, Gerday C (2004) Some like it cold: biocatalysis at low temperatures. Fems Microbiol Rev 28(1):25–42

    Article  PubMed  CAS  Google Scholar 

  • Gianese G, Argos P, Pascarella S (2001) Structural adaptation of enzymes to low temperatures. Protein Eng 14(3):141–148

    Article  PubMed  CAS  Google Scholar 

  • Gromiha MM, Thomas S, Santhosh C (2002) Role of cation-pi interactions to the stability of thermophilic proteins. Prep Biochem Biotechnol 32(4):355–362

    Article  PubMed  CAS  Google Scholar 

  • Haney P, Konisky J, Koretke KK, Luthey-Schulten Z, Wolynes PG (1997) Structural basis for thermostability and identification of potential active site residues for adenylate kinases from the archaeal genus Methanococcus. Proteins 28(1):117–130

    Article  PubMed  CAS  Google Scholar 

  • Huang SL, Wu LC, Liang HK, Pan KT, Horng JT, Ko MT (2004) PGTdb: a database providing growth temperatures of prokaryotes. Bioinformatics 20(2):276–278

    Article  PubMed  CAS  Google Scholar 

  • Hurst LD, Merchant AR (2001) High guanine-cytosine content is not an adaptation to high temperature: a comparative analysis amongst prokaryotes. Proc Biol Sci 268(1466):493–497

    Article  PubMed  CAS  Google Scholar 

  • Jaenicke R, Bohm G (1998) The stability of proteins in extreme environments. Curr Opin Struct Biol 8(6):738–748

    Article  PubMed  CAS  Google Scholar 

  • Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22(12):2577–2637

    Article  PubMed  CAS  Google Scholar 

  • Kannan N, Vishveshwara S (2000) Aromatic clusters: a determinant of thermal stability of thermophilic proteins. Protein Eng 13(11):753–761

    Article  PubMed  CAS  Google Scholar 

  • Kashefi K, Lovley DR (2003) Extending the upper temperature limit for life. Science 301(5635):934

    Article  PubMed  CAS  Google Scholar 

  • Korkegian A, Black ME, Baker D, Stoddard BL (2005) Computational thermostabilization of an enzyme. Science 308(5723):857–860

    Article  PubMed  CAS  Google Scholar 

  • Kreil DP, Ouzounis CA (2001) Identification of thermophilic species by the amino acid compositions deduced from their genomes. Nucleic Acids Res 29(7):1608–1615

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Nussinov R (2001) How do thermophilic proteins deal with heat. Cell Mol Life Sci 58(9):1216–1233

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tsai CJ, Nussinov R (2001) Thermodynamic differences among homologous thermophilic and mesophilic proteins. Biochemistry 40(47):14152–14165

    Article  PubMed  CAS  Google Scholar 

  • Lee DY, Kim KA, Yu YG, Kim KS (2004) Substitution of aspartic acid with glutamic acid increases the unfolding transition temperature of a protein. Biochem Biophys Res Commun 320(3):900–906

    Article  PubMed  CAS  Google Scholar 

  • Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22(13):1658–1659

    Article  PubMed  CAS  Google Scholar 

  • Li WF, Zhou XX, Lu P (2005) Structural features of thermozymes. Biotechnol Adv 23(4):271–281

    Article  PubMed  CAS  Google Scholar 

  • Marx JC, Blaise V, Collins T, D’Amico S, Delille D, Gratia E, Hoyoux A, Huston AL, Sonan G, Feller G, Gerday C (2004) A perspective on cold enzymes: current knowledge and frequently asked questions. Cell Mol Biol 50(5):643–655

    PubMed  CAS  Google Scholar 

  • Musto H, Naya H, Zavala A, Romero H, Alvarez-Valin F, Bernardi G (2004) Correlations between genomic GC levels and optimal growth temperatures in prokaryotes. FEBS Lett 573(1–3):73–77

    Article  PubMed  CAS  Google Scholar 

  • Musto H, Naya H, Zavala A, Romero H, Alvarez-Valin F, Bernardi G (2006) Genomic GC level, optimal growth temperature, and genome size in prokaryotes. Biochem Biophys Res Commun 347(1):1–3

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Needleman SB, Wunsch CD (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48(3):443–453

    Article  PubMed  CAS  Google Scholar 

  • Olufsen M, Smalas AO, Moe E, Brandsdal BO (2005) Increased flexibility as a strategy for cold adaptation: a comparative molecular dynamics study of cold- and warm-active uracil DNA glycosylase. J Biol Chem 280(18):18042–18048

    Article  PubMed  CAS  Google Scholar 

  • Pack SP, Yoo YJ (2004) Protein thermostability: structure-based difference of amino acid between thermophilic and mesophilic proteins. J Biotechnol 111(3):269–277

    Article  PubMed  CAS  Google Scholar 

  • Pack SP, Yoo YJ (2005) Packing-based difference of structural features between thermophilic and mesophilic proteins. Int J Biol Macromol 35(3–4):169–174

    Article  PubMed  CAS  Google Scholar 

  • R-core-team (2006) R: a language and environment for statistical computing. http://www.r-project.org. Wien, R foundation for statistical computing

  • Sadeghi M, Naderi-Manesh H, Zarrabi M, Ranjbar B (2006) Effective factors in thermostability of thermophilic proteins. Biophys Chem 119(3):256–270

    Article  PubMed  CAS  Google Scholar 

  • Schumann J, Bohm G, Schumacher G, Rudolph R, Jaenicke R (1993) Stabilization of creatinase from Pseudomonas putida by random mutagenesis. Protein Sci 2(10):1612–1620

    Article  PubMed  CAS  Google Scholar 

  • Siddiqui KS, Cavicchioli R (2006) Cold-adapted enzymes. Annu Rev Biochem 75:403–433

    Article  PubMed  CAS  Google Scholar 

  • Siddiqui KS, Poljak A, Guilhaus M, De Francisci D, Curmi PM, Feller G, D’Amico S, Gerday C, Uversky VN, Cavicchioli R (2006) Role of lysine versus arginine in enzyme cold-adaptation: modifying lysine to homo-arginine stabilizes the cold-adapted alpha-amylase from Pseudoalteramonas haloplanktis. Proteins 64(2):486–501

    Article  PubMed  CAS  Google Scholar 

  • Singer GA, Hickey DA (2000) Nucleotide bias causes a genomewide bias in the amino acid composition of proteins. Mol Biol Evol 17(11):1581–1588

    PubMed  CAS  Google Scholar 

  • Singer GAC, Hickey DA (2003) Thermophilic prokaryotes have characteristic patterns of codon usage, amino acid composition and nucleotide content. Gene 317(1–2):39–47

    Article  PubMed  CAS  Google Scholar 

  • Southall NT, Dill KA (2002) Potential of mean force between two hydrophobic solutes in water. Biophys Chem 101–102:295–307

    Article  PubMed  Google Scholar 

  • Taylor WR (1986) The classification of amino acid conservation. J Theor Biol 119(2):205–218

    Article  PubMed  CAS  Google Scholar 

  • Thompson MJ, Eisenberg D (1999) Transproteomic evidence of a loop-deletion mechanism for enhancing protein thermostability. J Mol Biol 290(2):595–604

    Article  PubMed  CAS  Google Scholar 

  • Wang HC, Susko E, Roger AJ (2006) On the correlation between genomic G+C content and optimal growth temperature in prokaryotes: data quality and confounding factors. Biochem Biophys Res Commun 342(3):681–684

    Article  PubMed  CAS  Google Scholar 

  • Watanabe K, Hata Y, Kizaki H, Katsube Y, Suzuki Y (1997) The refined crystal structure of bacillus cereus oligo-1,6-glucosidase at 2.0 A resolution: structural characterization of proline-substitution sites for protein thermostabilization. J Mol Biol 269(1):142–153

    Article  PubMed  CAS  Google Scholar 

  • Xu H, Dill KA (2005) Water’s hydrogen bonds in the hydrophobic effect: a simple model. J Phys Chem B Condens Matter Mater Surf Interfaces Biophys 109(49):23611–23617

    PubMed  CAS  Google Scholar 

  • Zeldovich KB, Berezovsky IN, Shakhnovich EI (2007) Protein and DNA sequence determinants of thermophilic adaptation. PLoS Comput Biol 3(1):e5

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Thanks to William R. Taylor and Trond H. Bø for valuable input. This research was funded by the Norwegian functional genomics program (FUGE) of the Research Council of Norway, through the Envision project and through the technology platform for bioinformatics.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gisle Sælensminde.

Additional information

Communicated by F. Robb.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sælensminde, G., Halskau, Ø., Helland, R. et al. Structure-dependent relationships between growth temperature of prokaryotes and the amino acid frequency in their proteins. Extremophiles 11, 585–596 (2007). https://doi.org/10.1007/s00792-007-0072-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-007-0072-3

Keywords

Navigation