, Volume 21, Issue 3, pp 419–444 | Cite as

Multifactorial level of extremostability of proteins: can they be exploited for protein engineering?

  • Debamitra Chakravorty
  • Mohd Faheem Khan
  • Sanjukta Patra
Original Paper


Research on extremostable proteins has seen immense growth in the past decade owing to their industrial importance. Basic research of attributes related to extreme-stability requires further exploration. Modern mechanistic approaches to engineer such proteins in vitro will have more impact in industrial biotechnology economy. Developing a priori knowledge about the mechanism behind extreme-stability will nurture better understanding of pathways leading to protein molecular evolution and folding. This review is a vivid compilation about all classes of extremostable proteins and the attributes that lead to myriad of adaptations divulged after an extensive study of 6495 articles belonging to extremostable proteins. Along with detailing on the rationale behind extreme-stability of proteins, emphasis has been put on modern approaches that have been utilized to render proteins extremostable by protein engineering. It was understood that each protein shows different approaches to extreme-stability governed by minute differences in their biophysical properties and the milieu in which they exist. Any general rule has not yet been drawn regarding adaptive mechanisms in extreme environments. This review was further instrumental to understand the drawback of the available 14 stabilizing mutation prediction algorithms. Thus, this review lays the foundation to further explore the biophysical pleiotropy of extreme-stable proteins to deduce a global prediction model for predicting the effect of mutations on protein stability.


Extreme-stability Thermostability pH stability Halostability Barostability Application Engineering Mutation 



Difference in Gibbs free energy of stability


Stability temperature


Change in enthalpy


Change in heat capacity


Melting temperature



Debamitra Chakravorty and Mohd Faheem Khan acknowledge Indian Institute of Technology Guwahati for research fellowship and infrastructure facility for carrying out PhD work. Research funding by Council of Scientific and Industrial Research (CSIR), Government of India is acknowledged.


  1. Abe F, Kato C, Horikoshi K (1999) Pressure-regulated metabolism in microorganisms. Trends Microbiol 7:447–453PubMedCrossRefGoogle Scholar
  2. Ahern TJ, Klibanov AM (1988) Analysis of processes causing thermal inactivation of enzymes. Methods Biochem Anal 33:91–128PubMedCrossRefGoogle Scholar
  3. Allers T, Mevarech M (2005) Archaeal genetics—the third way. Nat Rev Genet 6:58–73PubMedCrossRefGoogle Scholar
  4. Alvarez M et al (1998) Triose-phosphate Isomerase (TIM) of the Psychrophilic Bacterium Vibrio marinus kinetic and structural properties. J Biol Chem 273:2199–2206PubMedCrossRefGoogle Scholar
  5. Alzbutas G, Kaniusaite M, Grybauskas A, Lagunavicius A (2015) Domain organization of DNase from Thioalkali vibrio sp. provides insights into retention of activity in high salt environments. Front Microbiol 6Google Scholar
  6. Anthony LC, Dombkowski AA, Burgess RR (2002) Using disulfide bond engineering to study conformational changes in the β′ 260–309 coiled-coil region of Escherichia coli RNA polymerase during σ70 Binding. J Bacteriol 184:2634–2641PubMedPubMedCentralCrossRefGoogle Scholar
  7. Aparna V, Rambabu G, Panigrahi SK, Sarma J, Desiraju GR (2005) Virtual screening of 4-anilinoquinazoline analogues as EGFR kinase inhibitors: importance of hydrogen bonds in the evaluation of poses and scoring functions. J Chem Inf Model 45:725–738PubMedCrossRefGoogle Scholar
  8. Bagautdinov B et al. (2014) Thermodynamic analysis of unusually thermostable CutA1 protein from human brain and its protease susceptibility. J Biochem mvu062Google Scholar
  9. Baker-Austin C, Dopson M (2007) Life in acid: pH homeostasis in acidophiles. Trends Microbiol 15:165–171PubMedCrossRefGoogle Scholar
  10. Bao Q et al (2002) A complete sequence of the T. tengcongensis genome. Genome Res 12:689–700PubMedPubMedCentralCrossRefGoogle Scholar
  11. Basak S, Banerjee T, Gupta S, Ghosh T (2004) Investigation on the causes of codon and amino acid usages variation between thermophilic Aquifex aeolicus and mesophilic Bacillus subtilis. J Biomol Struct Dyn 22:205–214PubMedCrossRefGoogle Scholar
  12. Benedix A, Becker CM, de Groot BL, Caflisch A, Böckmann RA (2009) Predicting free energy changes using structural ensembles. Nat Methods 6:3–4PubMedCrossRefGoogle Scholar
  13. Berger F, Morellet N, Menu F, Potier P (1996) Cold shock and cold acclimation proteins in the psychrotrophic bacterium Arthrobacter globiformis SI55. J Bacteriol 178:2999–3007PubMedPubMedCentralCrossRefGoogle Scholar
  14. Betz SF (1993) Disulfide bonds and the stability of globular proteins. Protein Sci 2:1551–1558PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bhaskara RM, Srinivasan N (2011) Stability of domain structures in multi-domain proteins. Sci Rep 8(1):40CrossRefGoogle Scholar
  16. Bikadi Z, Demko L, Hazai E (2007) Functional and structural characterization of a protein based on analysis of its hydrogen bonding network by hydrogen bonding plot. Arch Biochem Biophys 461:225–234PubMedCrossRefGoogle Scholar
  17. Braxton S (1996) Protein engineering for stability. Protein engineering. Wiley-Liss, New York, pp 299–316Google Scholar
  18. Britton KL et al (1995) Insights into thermal stability from a comparison of the glutamate dehydrogenases from Pyrococcus furiosus and Thermococcus litoralis. Eur J Biochem 229:688–695PubMedCrossRefGoogle Scholar
  19. Brunk E, Mih N, Monk J, Zhang Z, O’Brien EJ, Bliven SE, Chen K, Chang RL, Bourne PE, Palsson BO (2016) Systems biology of the structural proteome. BMC Syst Biol 10:1CrossRefGoogle Scholar
  20. Bukau B, Horwich AL (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92(3):351–366PubMedCrossRefGoogle Scholar
  21. Bukau B, Weissman J, Horwich A (2006) Molecular chaperones and protein quality control. Cell 125(3):443–451PubMedCrossRefGoogle Scholar
  22. BURG B, Dijkstra BW, Vriend G, VINNE B, Venema G, Eijsink VG (1994) Protein stabilization by hydrophobic interactions at the surface. Eur J Biochem 220:981–985PubMedCrossRefGoogle Scholar
  23. Burley S, Petsko G (1985) Aromatic-aromatic interaction: a mechanism of protein structure stabilization. Science 229:23–28PubMedCrossRefGoogle Scholar
  24. Cacciapuoti G, Porcelli M, Bertoldo C, De Rosa M, Zappia V (1994) Purification and characterization of extremely thermophilic and thermostable 5′-methylthioadenosine phosphorylase from the archaeon Sulfolobus solfataricus. Purine nucleoside phosphorylase activity and evidence for intersubunit disulfide bonds. J Biol Chem 269(40):24762–24769PubMedGoogle Scholar
  25. Cacciapuoti G, Fuccio F, Petraccone L, Del Vecchio P, Porcelli M (2012) Role of disulfide bonds in conformational stability and folding of 5′-deoxy-5′-methylthioadenosine phosphorylase II from the hyperthermophilic archaeon Sulfolobus solfataricus. Biochim Biophys Acta (BBA)-Proteins Proteom 1824(10):1136–1143CrossRefGoogle Scholar
  26. Calderon MI, Vargas C, Rojo F, Iglesias-Guerra F, Csonka LN et al (2004) Complex regulation of the synthesis of the compatible solute ectoine in the halophilic bacterium Chromohalobacter salexigens DSM 3043 T. Microbiology 150:3051–3063PubMedCrossRefGoogle Scholar
  27. Capriotti E, Fariselli P, Casadio R (2005) I-Mutant2. 0: predicting stability changes upon mutation from the protein sequence or structure. Nucleic Acids Res 33:W306–W310PubMedPubMedCentralCrossRefGoogle Scholar
  28. Ceroni A, Passerini A, Vullo A, Frasconi P (2006) DISULFIND: a disulfide bonding state and cysteine connectivity prediction server. Nucleic Acids Res 34:W177–W181PubMedPubMedCentralCrossRefGoogle Scholar
  29. Chakravarty S, Varadarajan R (2000) Elucidation of determinants of protein stability through genome sequence analysis. Febs Lett 470:65–69PubMedCrossRefGoogle Scholar
  30. Chakravarty S, Varadarajan R (2002) Elucidation of factors responsible for enhanced thermal stability of proteins: a structural genomics based study. BioChemistry 41(25):8152–8161PubMedCrossRefGoogle Scholar
  31. Chakravorty D, Patra S (2012) Attaining extremophiles and extremolytes: methodologies and limitations. Extremophiles Sustain Resour Biotechnol Implications 29–74Google Scholar
  32. Chakravorty D, Parameswaran S, Dubey VK, Patra S (2011) In silico characterization of thermostable lipases. Extremophiles 15:89–103PubMedCrossRefGoogle Scholar
  33. Chan C-H, Yu T-H, Wong K-B (2011) Stabilizing salt-bridge enhances protein thermostability by reducing the heat capacity change of unfolding. PLoS One 6:e21624PubMedPubMedCentralCrossRefGoogle Scholar
  34. Chang C, Park BC, Lee D-S, Suh SW (1999) Crystal structures of thermostable xylose isomerases from Thermus caldophilus and Thermus thermophilus: possible structural determinants of thermostability. J Mol Biol 288:623–634PubMedCrossRefGoogle Scholar
  35. Chen C-W, Lin J, Chu Y-W (2013) iStable: off-the-shelf predictor integration for predicting protein stability changes. BMC Bioinform 14:1CrossRefGoogle Scholar
  36. Cheng J, Randall A, Baldi P (2006) Prediction of protein stability changes for single-site mutations using support vector machines. Proteins Struct Funct Bioinform 62:1125–1132CrossRefGoogle Scholar
  37. Costantini S, Colonna G, Facchiano AM (2008) ESBRI: a web server for evaluating salt bridges in proteins. Bioinformation 3:137–138PubMedPubMedCentralCrossRefGoogle Scholar
  38. Creighton TE (1997) Protein structure: a practical approachGoogle Scholar
  39. D’Amico S, Collins T, Marx JC, Feller G, Gerday C (2006) Psychrophilic microorganisms: challenges for life. EMBO Rep 7:385–389PubMedPubMedCentralCrossRefGoogle Scholar
  40. D’Auria S, Rossi M, Lakowicz JR (2001) Glucose-sensing proteins from mesophilic and thermophilic bacteria as new tools in diabetes monitoring. In: BiOS 2001. The International Symposium on Biomedical Optics, 2001. International Society for Optics and Photonics, pp 21–31Google Scholar
  41. Davail S, Feller G, Narinx E, Gerday C (1994) Cold adaptation of proteins. Purification, characterization, and sequence of the heat-labile subtilisin from the antarctic psychrophile Bacillus TA41. J Biol Chem 269:17448–17453PubMedGoogle Scholar
  42. de Vega M, Lázaro JM, Mencía M, Blanco L, Salas M (2010) Improvement of φ29 DNA polymerase amplification performance by fusion of DNA binding motifs. Proc Natl Acad Sci 107(38):16506–16511PubMedPubMedCentralCrossRefGoogle Scholar
  43. Dehouck Y, Grosfils A, Folch B, Gilis D, Bogaerts P, Rooman M (2009) Fast and accurate predictions of protein stability changes upon mutations using statistical potentials and neural networks: PoPMuSiC-2.0. Bioinformatics 25:2537–2543PubMedCrossRefGoogle Scholar
  44. Del Vecchio P, Elias M, Merone L, Graziano G, Dupuy J, Mandrich L, Carullo P, Fournier B, Rochu D, Rossi M, Masson P (2009) Structural determinants of the high thermal stability of SsoPox from the hyperthermophilic archaeon Sulfolobus solfataricus. Extremophiles 13(3):461–470PubMedCrossRefGoogle Scholar
  45. Delboni LF et al (1995) Crystal structure of recombinant triosephosphate isomerase from Bacillus stearothermophilus. An analysis of potential thermostability factors in six isomerases with known three-dimensional structures points to the importance of hydrophobic interactions. Protein Sci 4:2594–2604PubMedPubMedCentralCrossRefGoogle Scholar
  46. Di Giulio M (2005) A comparison of proteins from Pyrococcus furiosus and Pyrococcus abyssi: barophily in the physicochemical properties of amino acids and in the genetic code. Gene 346:1–6PubMedCrossRefGoogle Scholar
  47. Duan X, Cheng S, Ai Y, Wu J (2016) Enhancing the thermostability of Serratia plymuthica sucrose isomerase using B-factor-directed mutagenesis. PLoS One 11:e0149208PubMedPubMedCentralCrossRefGoogle Scholar
  48. Dym O, Mevarech M, Sussman J (1995) Structural features that stabilize halophilic malate dehydrogenase from an archaebacterium. Science 267:1344PubMedCrossRefGoogle Scholar
  49. Edmondson SP, Qiu L, Shriver JW (1995) Solution structure of the DNA-binding protein Sac7d from the hyperthermophile Sulfolobus acidocaldarius. BioChemistry 34:13289–13304PubMedCrossRefGoogle Scholar
  50. Eiberweiser A, Nazet A, Kruchinin SE, Fedotova MV, Buchner R (2015) Hydration and ion binding of the osmolyte ectoine. J Phys Chem B 119:15203–15211PubMedCrossRefGoogle Scholar
  51. Eijsink VG, Bjørk A, Gåseidnes S, Sirevåg R, Synstad B, van den Burg B, Vriend G (2004) Rational engineering of enzyme stability. J Biotechnol 113:105–120PubMedCrossRefGoogle Scholar
  52. Elcock AH (1998) The stability of salt bridges at high temperatures: implications for hyperthermophilic proteins. J Mol Biol 284:489–502PubMedCrossRefGoogle Scholar
  53. Elcock AH, McCammon JA (1998) Electrostatic contributions to the stability of halophilic proteins. J Mol Biol 280:731–748PubMedCrossRefGoogle Scholar
  54. Faria TQ, Knapp S, Ladenstein R, Maçanita AL, Santos H (2003) Protein stabilisation by compatible solutes: effect of mannosylglycerate on unfolding thermodynamics and activity of ribonuclease A. Chembiochem 4:734–741PubMedCrossRefGoogle Scholar
  55. Farias ST, Bonato M (2003) Preferred amino acids and thermostability. Genet Mol Res 2:383–393PubMedGoogle Scholar
  56. Feller G, Gerday C (2003) Psychrophilic enzymes: hot topics in cold adaptation. Nat Rev Microbiol 1:200–208PubMedCrossRefGoogle Scholar
  57. Feller G, Arpigny J, Narinx E, Gerday C (1997) Molecular adaptations of enzymes from psychrophilic organisms. Comparative biochemistry and physiology Part A. Physiology 118:495–499Google Scholar
  58. Ferrè F, Clote P (2006) DiANNA 1.1: an extension of the DiANNA web server for ternary cysteine classification. Nucleic Acids Res 34:W182–W185PubMedPubMedCentralCrossRefGoogle Scholar
  59. Frank A, Lobry J (1999) Asymmetric substitution patterns: a review of possible underlying mutational or selective mechanisms. Gene 238:65–77PubMedCrossRefGoogle Scholar
  60. Frappier V, Najmanovich RJ (2014) A coarse-grained elastic network atom contact model and its use in the simulation of protein dynamics and the prediction of the effect of mutations. PLoS Comput Biol 10:e1003569PubMedPubMedCentralCrossRefGoogle Scholar
  61. Fujinami S, Fujisawa M (2010) Industrial applications of alkaliphiles and their enzymes–past, present and future. Environ Technol 31:845–856PubMedCrossRefGoogle Scholar
  62. Fukuchi S, Yoshimune K, Wakayama M, Moriguchi M, Nishikawa K (2003) Unique amino acid composition of proteins in halophilic bacteria. J Mol Biol 327:347–357PubMedCrossRefGoogle Scholar
  63. Galinski EA, Pfeiffer HP, Trüper HG (1985) 1, 4, 5, 6-Tetrahydro-2-methyl-4-pyrimidinecarboxylic acid. Eur J Biochem 149:135–139PubMedCrossRefGoogle Scholar
  64. Georis J, Esteves FD, Lamotte-Brasseur J, Bougnet V, Devreese B, Giannotta F, Granier B, Frère JM (2000) An additional aromatic interaction improves the thermostability and thermophilicity of a mesophilic family 11 xylanase: structural basis and molecular study. Protein Sci 9:466–475PubMedPubMedCentralCrossRefGoogle Scholar
  65. Gessesse A (1998) Purification and properties of two thermostable Alkaline xylanases from an Alkaliphilic Bacillus sp. Appl Environ Microbiol 64:3533–3535PubMedPubMedCentralGoogle Scholar
  66. Gianese G, Argos P, Pascarella S (2001) Structural adaptation of enzymes to low temperatures. Protein Eng 14:141–148PubMedCrossRefGoogle Scholar
  67. Gibson G, Muse SV (2004) Précis de génomique. De Boeck SupérieurGoogle Scholar
  68. Gilbert HF (1993) Molecular and cellular aspects of thiol-disulfide exchange. Adv Enzymol Relat Areas Mol Biol 63:69–69Google Scholar
  69. Giollo M, Martin AJ, Walsh I, Ferrari C, Tosatto SC (2014) NeEMO: a method using residue interaction networks to improve prediction of protein stability upon mutation. BMC Genom 15:1CrossRefGoogle Scholar
  70. Goldstein RA (2007) Amino-acid interactions in psychrophiles, mesophiles, thermophiles, and hyperthermophiles: Insights from the quasi-chemical approximation. Protein Sci 16:1887–1895PubMedPubMedCentralCrossRefGoogle Scholar
  71. Goodarzi H, Torabi N, Najafabadi HS, Archetti M (2008) Amino acid and codon usage profiles: adaptive changes in the frequency of amino acids and codons. Gene 407:30–41PubMedCrossRefGoogle Scholar
  72. Grocock RJ, Sharp PM (2002) Synonymous codon usage in Pseudomonas aeruginosa PA01. Gene 289:131–139PubMedCrossRefGoogle Scholar
  73. Gromiha MM, Thomas S, Santhosh C (2002) Role of cation-π interactions to the stability of thermophilic proteins. Prep Biochem Biotechnol 32:355–362PubMedCrossRefGoogle Scholar
  74. Gromiha MM, Santhosh C, Ahmad S (2004) Structural analysis of cation–π interactions in DNA binding proteins. Int J Biol Macromol 34:203–211PubMedCrossRefGoogle Scholar
  75. Guerois R, Nielsen JE, Serrano L (2002) Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations. J Mol Biol 320:369–387PubMedCrossRefGoogle Scholar
  76. Gupta RS (1995) Evolution of the chaperonin families (HSP60, HSP 10 and TCP-1) of proteins and the origin of eukaryotic cells. Mol Microbiol 15:1–11PubMedCrossRefGoogle Scholar
  77. Haney PJ, Badger JH, Buldak GL, Reich CI, Woese CR, Olsen GJ (1999) Thermal adaptation analyzed by comparison of protein sequences from mesophilic and extremely thermophilic Methanococcus species. Proc Natl Acad Sci 96:3578–3583PubMedPubMedCentralCrossRefGoogle Scholar
  78. Hoeft SE, Blum JS, Stolz JF, Tabita FR, Witte B, King GM, Santini JM, Oremland RS (2007) Alkalilimnicola ehrlichiisp. nov., a novel, arsenite-oxidizing haloalkaliphilic gammaproteobacterium capable of chemoautotrophic or heterotrophic growth with nitrate or oxygen as the electron acceptor. Int J Syst Evol Microbiol 57:504–512PubMedCrossRefGoogle Scholar
  79. Holden J, Adams MW, Baross JA (2000) Heat-shock response in hyperthermophilic microorganisms microbial biosystems: new frontiers Atlantic Canada Society for Microbial Ecology, Acadia University, Wolfville, Nova Scotia, Canada 663 Google Scholar
  80. Holden JF, Takai K, Summit M, Bolton S, Zyskowski J, Baross JA (2001) Diversity among three novel groups of hyperthermophilic deep-sea Thermococcus species from three sites in the northeastern Pacific Ocean. FEMS Microbiol Ecol 36(:):51–60PubMedCrossRefGoogle Scholar
  81. Horikoshi K (1999) Alkaliphiles: some applications of their products for biotechnology. Microbiol Mol Biol Rev 63:735–750PubMedPubMedCentralGoogle Scholar
  82. Huang L-T, Gromiha MM (2009) Reliable prediction of protein thermostability change upon double mutation from amino acid sequence. Bioinformatics 25:2181–2187PubMedCrossRefGoogle Scholar
  83. Huang L-T, Gromiha MM, Ho S-Y (2007) iPTREE-STAB: interpretable decision tree based method for predicting protein stability changes upon mutations. Bioinformatics 23:1292–1293PubMedCrossRefGoogle Scholar
  84. Hubbard RE, Kamran Haider M (2010) Hydrogen bonds in proteins: role and strength. eLSGoogle Scholar
  85. Hutchinson EG, Thornton JM (1996) PROMOTIF—a program to identify and analyze structural motifs in proteins. Protein Sci 5:212–220PubMedPubMedCentralCrossRefGoogle Scholar
  86. Jaenicke R (1991a) Protein stability and molecular adaptation to extreme conditions. In: EJB Reviews 1991. Springer, Berlin Heidelberg, pp 291–304Google Scholar
  87. Jaenicke R (1991b) Protein folding: local structures, domains, subunits, and assemblies. BioChemistry 30:3147–3161Google Scholar
  88. Jaenicke R (1996) Structure and stability of hyperstable proteins: glycolytic enzymes from hyperthermophilic bacterium Thermotoga maritima. Adv Protein Chem 48:181–269PubMedCrossRefGoogle Scholar
  89. Jaenicke R (2000) Do ultrastable proteins from hyperthermophiles have high or low conformational rigidity? Proc Natl Acad Sci 97:2962–2964PubMedPubMedCentralCrossRefGoogle Scholar
  90. Jaenicke R, Böhm G (1998) The stability of proteins in extreme environments. Curr Opin Struct Biol 8:738–748PubMedCrossRefGoogle Scholar
  91. Johnson CM, Oliveberg M, Clarke J, Fersht AR (1997) Thermodynamics of denaturation of mutants of barnase with disulfide crosslinks. J Mol Biol 268:198–208PubMedCrossRefGoogle Scholar
  92. Jorda J, Yeates TO (2011) Widespread disulfide bonding in proteins from thermophilic archaea. ArchaeaGoogle Scholar
  93. Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577–2637PubMedCrossRefGoogle Scholar
  94. Karplus PA, Schulz GE (1985) Prediction of chain flexibility in proteins. Naturwissenschaften 72:212–213CrossRefGoogle Scholar
  95. Karshikoff A, Ladenstein R (1998) Proteins from thermophilic and mesophilic organisms essentially do not differ in packing. Protein Eng 11:867–872PubMedCrossRefGoogle Scholar
  96. Kataeva IA, Blum DL, Li XL, Ljungdahl LG (2001) Do domain interactions of glycosyl hydrolases from Clostridium thermocellum contribute to protein thermostability? Protein Eng 14(3):167–172PubMedCrossRefGoogle Scholar
  97. Kato C, Bartlett DH (1997) The molecular biology of barophilic bacteria. Extremophiles 1:111–116PubMedCrossRefGoogle Scholar
  98. Kato C, Sato T, Horikoshi K (1995) Isolation and properties of barophilic and barotolerant bacteria from deep-sea mud samples. Biodiversity Conserv 4:1–9Google Scholar
  99. Kato C, Li L, Tamaoka J, Horikoshi K (1997) Molecular analyses of the sediment of the 11000-m deep Mariana Trench. Extremophiles 1:117–123PubMedCrossRefGoogle Scholar
  100. Kaur H, Raghava G (2003) A neural-network based method for prediction of γ-turns in proteins from multiple sequence alignment. Protein Sci 12:923–929PubMedPubMedCentralCrossRefGoogle Scholar
  101. Kaur H, Raghava GPS (2006) Prediction of Cα-H· O and Cα-H· π interactions in proteins using recurrent neural network. In Silico Biol 6:111–125PubMedGoogle Scholar
  102. Khan S, Vihinen M (2010) Performance of protein stability predictors. Hum Mutat 31:675–684PubMedCrossRefGoogle Scholar
  103. Khechinashvili N, Fedorov M, Kabanov A, Monti S, Ghio C, Soda K (2006) Side chain dynamics and alternative hydrogen bonding in the mechanism of protein thermostabilization. J Biomol Struct Dyn 24:255–262PubMedCrossRefGoogle Scholar
  104. Kim S-Y, Hwang KY, Kim S-H, Sung H-C, Han YS, Cho Y (1999) Structural basis for cold adaptation sequence, biochemical properties, and crystal structure of malate dehydrogenase from a psychrophile Aquaspirillium arcticum. J Biol Chem 274:11761–11767PubMedCrossRefGoogle Scholar
  105. Kim SJ, Lee JA, Joo JC, Yoo YJ, Kim YH, Song BK (2010) The development of a thermostable CiP (Coprinus cinereus peroxidase) through in silico design. Biotechnol Prog 26:1038–1046PubMedGoogle Scholar
  106. Klumpp M, Baumeister W (1998) The thermosome: archetype of group II chaperonins. FEBS Lett 430:73–77PubMedCrossRefGoogle Scholar
  107. Knöchel T, Hennig M, Merz A, Darimont B, Kirschner K, Jansonius J (1996) The crystal structure of indole-3-glycerol phosphate synthase from the Hyperthermophilic Archaeon Sulfolobus solfataricusin three different crystal forms: effects of ionic strength. J Mol Biol 262:502–515PubMedCrossRefGoogle Scholar
  108. Kollman PA (1972) Theory of hydrogen bond directionality. J Am Chem Soc 94:1837–1842CrossRefGoogle Scholar
  109. Kreil DP, Ouzounis CA (2001) Identification of thermophilic species by the amino acid compositions deduced from their genomes. Nucleic Acids Res 29:1608–1615PubMedPubMedCentralCrossRefGoogle Scholar
  110. Kuhlmann AU, Bursy J, Gimpel S, Hoffmann T, Bremer E (2008) Synthesis of the compatible solute ectoine in Virgibacillus pantothenticusis triggered by high salinity and low growth temperature. Appl Environ Microbiol 74:4560–4563PubMedPubMedCentralCrossRefGoogle Scholar
  111. Kumar S, Tsai C-J, Nussinov R (2000) Factors enhancing protein thermostability. Protein Eng 13:179–191PubMedCrossRefGoogle Scholar
  112. Küsel K, Dorsch T, Acker G, Stackebrandt E (1999) Microbial reduction of Fe(III) in acidic sediments: isolation of Acidiphilium cryptum JF-5 capable of coupling the reduction of Fe(III) to the oxidation of glucose. Appl Environ Microbiol 65:3633–3640PubMedPubMedCentralGoogle Scholar
  113. Lanyi JK (1974) Salt-dependent properties of proteins from extremely halophilic bacteria. Bacteriol Rev 38:272PubMedPubMedCentralGoogle Scholar
  114. Lee YE, Jain MK, Lee C, Zeikus JG (1993) Taxonomic distinction of saccharolytic thermophilic anaerobes: description of Thermoanaerobacterium xylanolyticum gen. nov., sp. nov., and Thermoanaerobacterium saccharolyticum gen. nov., sp. nov.; reclassification of Thermoanaerobium brockii ,Clostridium thermosulfurogenes, and Clostridium thermohydrosulfuricum E100-69 as Thermoanaerobacter brockii comb. nov., Thermoanaerobacterium thermosulfurigenes comb. nov., and Thermoanaerobacter thermohydrosulfuricus comb. nov., respectively; and transfer of of Clostridium thermohydrosulfuricum 39E to Thermoanaerobacter ethanolicus. Int J Syst Evol Microbiol 43(1):41–51Google Scholar
  115. Lehmann M, Wyss M (2001) Engineering proteins for thermostability: the use of sequence alignments versus rational design and directed evolution. Curr Opin Biotechnol 12:371–375PubMedCrossRefGoogle Scholar
  116. Lentzen G, Schwarz T (2006) Extremolytes: natural compounds from extremophiles for versatile applications. Appl Microbiol Biotechnol 72:623–634PubMedCrossRefGoogle Scholar
  117. Li Y, Fang J (2012) PROTS-RF: a robust model for predicting mutation-induced protein stability changes. PloS one 7:e47247PubMedPubMedCentralCrossRefGoogle Scholar
  118. Liao H et al (2014) A new acidophilic thermostable endo-1, 4-β-mannanase from Penicillium oxalicum GZ-2: cloning, characterization and functional expression in Pichia pastoris. BMC Biotechnol 14:1CrossRefGoogle Scholar
  119. Lin X, Fusek M, Tang J (1991) Thermopsin, a thermostable acid protease from Sulfolobus acidocaldarius. In: Structure and function of the aspartic proteinases. Springer, pp 255–257Google Scholar
  120. Longo LM, Blaber M (2015) Prebiotic protein design supports a halophile origin of foldable proteins. In: The Proceedings from Halophiles 2013, the International Congress on Halophilic Microorganisms, 2015. Frontiers Media, SA, p 237Google Scholar
  121. Lu J-L, Hu X-H, Hu D-G (2012) A new hybrid fractal algorithm for predicting thermophilic nucleotide sequences. J Theor Biol 293:74–81PubMedCrossRefGoogle Scholar
  122. Ma K, Linder D, Stetter K, Thauer R (1991) Purification and properties of N 5, N 10-methylenetetrahydromethanopterin reductase (coenzyme F420-dependent) from the extreme thermophile Methanopyrus kandleri. Arch Microbiol 155:593–600PubMedCrossRefGoogle Scholar
  123. Macario AJ, de Macario EC (2004) The pathology of cellular anti-stress mechanisms: a new frontier. Stress 7:243–249PubMedCrossRefGoogle Scholar
  124. Madern D, Ebel C (2007) Influence of an anion-binding site in the stabilization of halophilic malate dehydrogenase from Haloarcula marismortui. Biochimie 89:981–987PubMedCrossRefGoogle Scholar
  125. Madigan MT (2000) Extremophilic bacteria and microbial diversity. Ann Mo Bot Garden 3–12Google Scholar
  126. Magyar C, Szilágyi A, Závodszky P (1996) Relationship between thermal stability and 3-D structure in a homology model of 3-isopropylmalate dehydrogenase from Escherichia coli. Protein Eng 9(8):663–670PubMedCrossRefGoogle Scholar
  127. Makhatadze GI, Privalov PL (1995) Energetics of protein structure. Adv Protein Chem 47:307–425PubMedCrossRefGoogle Scholar
  128. Mallick P, Boutz DR, Eisenberg D, Yeates TO (2002) Genomic evidence that the intracellular proteins of archaeal microbes contain disulfide bonds. Proc Natl Acad Sci 99:9679–9684PubMedPubMedCentralCrossRefGoogle Scholar
  129. Mally A, Witt SN (2001) GrpE accelerates peptide binding and release from the high affinity state of DnaK. Nat Struct Mol Biol 8(3):254–257CrossRefGoogle Scholar
  130. Manjunath K, Sekar K (2013) Molecular dynamics perspective on the protein thermal stability: a case study using SAICAR synthetase. J Chem Inf Model 53:2448–2461PubMedCrossRefGoogle Scholar
  131. Manukhov IV, Eroshnikov GE, Vyssokikh MY, Zavilgelsky GB (1999) Folding and refolding of thermolabile and thermostable bacterial luciferases: the role of DnaKJ heat-shock proteins. FEBS Lett 448:265–268PubMedCrossRefGoogle Scholar
  132. Marcus Y (2009) Effect of ions on the structure of water: Structure making and breaking. Chem Rev (ACS Publications) 109:1346–1370CrossRefGoogle Scholar
  133. Marshall CJ (1997) Cold-adapted enzymes. Trends Biotechnol 15:359–364PubMedCrossRefGoogle Scholar
  134. Masso M, Vaisman II (2011) A structure-based computational mutagenesis elucidates the spectrum of stability-activity relationships in proteins. In: Engineering in Medicine and Biology Society, EMBC, 2011 Annual International Conference of the IEEE, 2011. IEEE, pp 3225–3228Google Scholar
  135. Matsumura M, Matthews BW (1990) Stabilization of functional proteins by introduction of multiple disulfide bonds. Methods Enzymol 202:336–356CrossRefGoogle Scholar
  136. Matsuura Y, Takehira M, Joti Y, Ogasahara K, Tanaka T, Ono N, Kunishima N, Yutani K (2015) Thermodynamics of protein denaturation at temperatures over 100 °C: CutA1 mutant proteins substituted with hydrophobic and charged residues. Sci Rep 5Google Scholar
  137. Mattos C (2002) Protein–water interactions in a dynamic world. Trends Biochem Sci 27:203–208PubMedCrossRefGoogle Scholar
  138. McDonald IK, Thornton JM (1994) Satisfying hydrogen bonding potential in proteins. J Mol Biol 238:777–793PubMedCrossRefGoogle Scholar
  139. Metpally RPR, Reddy BVB (2009) Comparative proteome analysis of psychrophilic versus mesophilic bacterial species: insights into the molecular basis of cold adaptation of proteins. BMC Genomics 10:1CrossRefGoogle Scholar
  140. Michels PC, Clark DS (1997) Pressure-enhanced activity and stability of a hyperthermophilic protease from a deep-sea methanogen. Appl Environ Microbiol 63:3985–3991PubMedPubMedCentralGoogle Scholar
  141. Miller JF, Shah NN, Nelson CM, Ludlow JM, Clark DS (1988) Pressure and temperature effects on growth and methane production of the extreme thermophile Methanococcus jannaschii. Appl Environ Microbiol 54:3039–3042PubMedPubMedCentralGoogle Scholar
  142. Milner-White EJ, Ross BM, Ismail R, Belhadj-Mostefa K, Poet R (1988) One type of gamma-turn, rather than the other gives rise to chain-reversal in proteins. J Mol Biol 204:777–782PubMedCrossRefGoogle Scholar
  143. Najafabadi HS, Goodarzi H, Torabi N (2005) Optimality of codon usage in Escherichia coli due to load minimization. J Theor Biol 237:203–209PubMedCrossRefGoogle Scholar
  144. Nakamura A, Takumi K, Miki K (2010) Crystal structure of a thermophilic GrpE protein: insight into thermosensing function for the DnaK chaperone system. J Mol Biol 396(4):1000–1011PubMedCrossRefGoogle Scholar
  145. Nayek A, Gupta PSS, Banerjee S, Mondal B, Bandyopadhyay AK (2014) Salt-bridge energetics in halophilic proteins. Plos one 9:e93862PubMedPubMedCentralCrossRefGoogle Scholar
  146. Neira JL, Sevilla P, García-Blanco F (2012) The C-terminal sterile alpha motif (SAM) domain of human p73 is a highly dynamic protein, which acquires high thermal stability through a decrease in backbone flexibility. Phys Chem Chem Phys 14(29):10308–10323PubMedCrossRefGoogle Scholar
  147. Norris PR, Burton NP, Foulis NA (2000) Acidophiles in bioreactor mineral processing. Extremophiles 4:71–76PubMedCrossRefGoogle Scholar
  148. Öberg F, Sjöhamn J, Fischer G, Moberg A, Pedersen A, Neutze R, Hedfalk K (2011) Glycosylation increases the thermostability of human aquaporin 10 protein. J Biol Chem 286:31915–31923PubMedPubMedCentralCrossRefGoogle Scholar
  149. Okada J et al (2010) Evolution and thermodynamics of the slow unfolding of hyperstable monomeric proteins. BMC Evol Biol 10:1CrossRefGoogle Scholar
  150. Olsen O, Thomsen KK (1991) Improvement of bacterial β-glucanase thermostability by glycosylation. Microbiology 137:579–585Google Scholar
  151. Ogawa K, Sonoyama T, Takeda T, Ichiki SI, Nakamura S, Kobayashi Y, Uchiyama S, Nakasone K, Shin-ichi JT, Mita H, Yamamoto Y (2007) Roles of a short connecting disulfide bond in the stability and function of psychrophilic Shewanella violacea cytochrome c5. Extrem 11(6):797–807CrossRefGoogle Scholar
  152. Pace CN (1992) Contribution of the hydrophobic effect to globular protein stability. J Mol Biol 226:29–35PubMedCrossRefGoogle Scholar
  153. Pack SP, Yoo YJ (2004) Protein thermostability: structure-based difference of amino acid between thermophilic and mesophilic proteins. J Biotechnol 111:269–277PubMedCrossRefGoogle Scholar
  154. Packschies L, Theyssen H, Buchberger A, Bukau B, Goody RS, Reinstein J (1997) GrpE accelerates nucleotide exchange of the molecular chaperone DnaK with an associative displacement mechanism. BioChemistry 36(12):3417–3422PubMedCrossRefGoogle Scholar
  155. Palmer B, Angus K, Taylor L, Warwicker J, Derrick JP (2008) Design of stability at extreme alkaline pH in streptococcal protein G. J Biotechnol 134:222–230PubMedCrossRefGoogle Scholar
  156. Panigrahi P, Sule M, Ghanate A, Ramasamy S, Suresh C (2015) Engineering Proteins for Thermostability with iRDP Web Server. PloS one 10:e0139486PubMedPubMedCentralCrossRefGoogle Scholar
  157. Panja AS, Bandopadhyay B, Maiti S (2015) Protein thermostability is owing to their preferences to non-polar smaller volume amino acids, variations in residual physico-chemical properties and more salt-bridges. PloS one 10(7):e0131495PubMedPubMedCentralCrossRefGoogle Scholar
  158. Parthasarathy S, Murthy MR (2000) Protein thermal stability: insights from atomic displacement parameters (B values). Protein Eng 13:9–13PubMedCrossRefGoogle Scholar
  159. Parthiban V (2006) Prediction of factors determining changes in stability in protein mutants. Universität zu, KölnGoogle Scholar
  160. Pastor JM, Salvador M, Argandoña M, Bernal V, Reina-Bueno M, Csonka LN, Iborra JL, Vargas C, Nieto JJ, Cánovas M (2010) Ectoines in cell stress protection: uses and biotechnological production. Biotechnol adv 28(6):782–801PubMedCrossRefGoogle Scholar
  161. Paul S, Bag SK, Das S, Harvill ET, Dutta C (2008) Molecular signature of hypersaline adaptation: insights from genome and proteome composition of halophilic prokaryotes. Genome Biol 9:1CrossRefGoogle Scholar
  162. Paul M, Hazra M, Barman A, Hazra S (2014) Comparative molecular dynamics simulation studies for determining factors contributing to the thermostability of chemotaxis protein “CheY”. J Biomol Struct Dyn 32:928–949PubMedCrossRefGoogle Scholar
  163. Pavlov AR, Belova GI, Kozyavkin SA, Slesarev AI (2002) Helix–hairpin–helix motifs confer salt resistance and processivity on chimeric DNA polymerases. Proc Natl Acad Sci 99(21):13510–13515PubMedPubMedCentralCrossRefGoogle Scholar
  164. Pavlov AR, Pavlova NV, Kozyavkin SA, Slesarev AI (2012) Cooperation between catalytic and DNA binding domains enhances thermostability and supports DNA synthesis at higher temperatures by thermostable DNA polymerases. BioChemistry 51(10):2032–2043PubMedPubMedCentralCrossRefGoogle Scholar
  165. Petsko GA (2001) Structural basis of thermostability in hyperthermophilic proteins, or “ there’s more than one way to skin a cat”. Methods Enzymol 334:469PubMedCrossRefGoogle Scholar
  166. Petsko GA, Ringe D (2004) Protein structure and function. New Science PressGoogle Scholar
  167. Pieper U, Kapadia G, Mevarech M, Herzberg O (1998) Structural features of halophilicity derived from the crystal structure of dihydrofolate reductase from the Dead Sea halophilic archaeon, Haloferax volcanii. Structure 6:75–88PubMedCrossRefGoogle Scholar
  168. Podar M, Reysenbach A-L (2006) New opportunities revealed by biotechnological explorations of extremophiles. Curr Opin Biotechnol 17:250–255PubMedCrossRefGoogle Scholar
  169. Privalov PL, Gill SJ (1988) Stability of protein structure and hydrophobic interaction. Adv Protein Chem 39:191–238PubMedCrossRefGoogle Scholar
  170. Rao JM, Argos P (1981) Structural stability of halophilic proteins. BioChemistry 20:6536–6543PubMedCrossRefGoogle Scholar
  171. Rathi PC, Jaeger K-E, Gohlke H (2015) Structural rigidity and protein thermostability in variants of lipase A from Bacillus subtilis. PloS one 10:e0130289PubMedPubMedCentralCrossRefGoogle Scholar
  172. Reed CJ, Lewis H, Trejo E, Winston V, Evilia C (2013) Protein adaptations in archaeal extremophiles. Archaea 2013Google Scholar
  173. Reetz MT (2013) Biocatalysis in organic chemistry and biotechnology: past, present, and future. J Am Chem Soc 135:12480–12496PubMedCrossRefGoogle Scholar
  174. Reetz MT, Carballeira JD, Vogel A (2006) Iterative saturation mutagenesis on the basis of B factors as a strategy for increasing protein thermostability. Angew Chem Int Ed 45:7745–7751CrossRefGoogle Scholar
  175. Robinson NE (2002) Protein deamidation. Proc Natl Acad Sci 99:5283–5288PubMedPubMedCentralCrossRefGoogle Scholar
  176. Rohl CA, Strauss CE, Misura KM, Baker D (2004) Protein structure prediction using Rosetta. Methods Enzymol 383:66–93PubMedCrossRefGoogle Scholar
  177. Rose GD, Gierasch L, Smith JA (1985) Turns in peptides and proteins. Adv Protein Chem 37:1PubMedCrossRefGoogle Scholar
  178. Rothschild LJ, Mancinelli RL (2001) Life in extreme environments. Nature 409:1092–1101PubMedCrossRefGoogle Scholar
  179. Russell NJ (1998) Molecular adaptations in psychrophilic bacteria: potential for biotechnological applications. In: Biotechnology of extremophiles. Springer, Berlin Heidelberg. pp 1–21CrossRefGoogle Scholar
  180. Russell RJ, Gerike U, Danson MJ, Hough DW, Taylor GL (1998) Structural adaptations of the cold-active citrate synthase from an Antarctic bacterium. Structure 6:351–361PubMedCrossRefGoogle Scholar
  181. Sahlan M, Yohda M (2013a) Molecular chaperones in thermophilic eubacteria and archaea. In: Thermophilic microbes in environmental and industrial biotechnology. Springer, pp 375–394Google Scholar
  182. Sahlan M, Yohda M (2013b) Molecular chaperones in thermophilic eubacteria and archaea. In: Thermophilic microbes in environmental and industrial biotechnology. Springer, Netherlands, pp 375–394Google Scholar
  183. Santos SR, Ochman H (2004) Identification and phylogenetic sorting of bacterial lineages with universally conserved genes and proteins. Environ Microbiol 6:754–759PubMedCrossRefGoogle Scholar
  184. Saunders NF et al. (2003) Mechanisms of thermal adaptation revealed from the genomes of the Antarctic Archaea Methanogenium frigidum and Methanococcoides burtonii. Genome Res 13:1580–1588PubMedPubMedCentralCrossRefGoogle Scholar
  185. Schlessinger A, Yachdav G, Rost B (2006) PROFbval: predict flexible and rigid residues in proteins. Bioinformatics 22:891–893PubMedCrossRefGoogle Scholar
  186. Schumann J, Böhm G, Jaenicke R, Schumacher G, Rudolph R (1993) Stabilization of creatinase from Pseudomonas putida by random mutagenesis. Protein Sci 2:1612–1620PubMedPubMedCentralCrossRefGoogle Scholar
  187. Seeliger D, De Groot BL (2010) Protein thermostability calculations using alchemical free energy simulations. Biophys J 98:2309–2316PubMedPubMedCentralCrossRefGoogle Scholar
  188. Serrano L, Bycroft M, Fersht AR (1991) Aromatic-aromatic interactions and protein stability: investigation by double-mutant cycles. J Mol Biol 218:465–475PubMedCrossRefGoogle Scholar
  189. Setati ME (2010) Diversity and industrial potential of hydrolaseproducing halophilic/halotolerant eubacteria. Afr J Biotechnol 9:1555–1560CrossRefGoogle Scholar
  190. Sharma A, Kawarabayasi Y, Satyanarayana T (2012) Acidophilic bacteria and archaea: acid stable biocatalysts and their potential applications. Extremophiles 16:1–19PubMedCrossRefGoogle Scholar
  191. Shental-Bechor D, Levy Y (2008) Effect of glycosylation on protein folding: a close look at thermodynamic stabilization. Proc Natl Acad Sci 105:8256–8261PubMedPubMedCentralCrossRefGoogle Scholar
  192. Shirley BA (1995) Protein stability and folding: theory and practice. Humana Press, pp 387Google Scholar
  193. Siddiqui KS, Thomas T (2008) Protein adaptation in extremophiles. Nova PublishersGoogle Scholar
  194. Siglioccolo A, Paiardini A, Piscitelli M, Pascarella S (2011) Structural adaptation of extreme halophilic proteins through decrease of conserved hydrophobic contact surface. BMC Struct Biol 11:1CrossRefGoogle Scholar
  195. Singer GA, Hickey DA (2003) Thermophilic prokaryotes have characteristic patterns of codon usage, amino acid composition and nucleotide content. Gene 317:39–47PubMedCrossRefGoogle Scholar
  196. Spassov VZ, Karshikoff AD, Ladenstein R (1995) The optimization of protein-solvent interactions: Thermostability and the role of hydrophobic and electrostatic interactions. Protein science 4:1516–1527PubMedPubMedCentralCrossRefGoogle Scholar
  197. Spector S et al (2000) Rational modification of protein stability by the mutation of charged surface residues. BioChemistry 39:872–879PubMedCrossRefGoogle Scholar
  198. Srivastava A, Sinha S (2014) Thermostability of in vitro evolved Bacillus subtilis lipase A: a network and dynamics perspective. PloS one 9:e102856PubMedPubMedCentralCrossRefGoogle Scholar
  199. Sunna A, Gibbs MD, Bergquist PL (2000) A novel thermostable multidomain 1, 4-β-xylanase from ‘Caldibacillus cellulovorans’ and effect of its xylan-binding domain on enzyme activity. Microbiology 146(11):2947–2955PubMedCrossRefGoogle Scholar
  200. Suplatov D, Panin N, Kirilin E, Shcherbakova T, Kudryavtsev P, Švedas V (2014) Computational design of a pH stable enzyme: understanding molecular mechanism of penicillin acylase’s adaptation to alkaline conditions. PloS one 9:e100643PubMedPubMedCentralCrossRefGoogle Scholar
  201. Swaim MW, Pizzo SV (1988) Methionine sulfoxide and the oxidative regulation of plasma proteinase inhibitors. J Leukocyte Biol 43:365–379PubMedGoogle Scholar
  202. Szilágyi A, Závodszky P (2000) Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey. Structure 8:493–504PubMedCrossRefGoogle Scholar
  203. Taguchi H, Konishi J, Ishii N, Yoshida M (1991) A chaperonin from a thermophilic bacterium, Thermus thermophilus, that controls refoldings of several thermophilic enzymes. J Biol Chem 266(33):22411–22418PubMedGoogle Scholar
  204. Takagi H, Takahashi T, Momose H, Inouye M, Maeda Y, Matsuzawa H, Ohta T (1990) Enhancement of the thermostability of subtilisin E by introduction of a disulfide bond engineered on the basis of structural comparison with a thermophilic serine protease. J Biol Chem 265:6874–6878PubMedGoogle Scholar
  205. Takami H, Horikoshi K (2000) Analysis of the genome of an alkaliphilic Bacillus strain from an industrial point of view. Extremophiles 4:99–108PubMedCrossRefGoogle Scholar
  206. Tanaka Y et al (2004) How oligomerization contributes to the thermostability of an archaeon protein protein l-isoaspartyl-o-methyltransferase from Sulfolobus tokodaii. J Biol Chem 279:32957–32967PubMedCrossRefGoogle Scholar
  207. Tanner JJ, Hecht RM, Krause KL (1996) Determinants of enzyme thermostability observed in the molecular structure of Thermus aquaticus d-glyceraldehyde-3-phosphate dehydrogenase at 2.5 Å resolution. BioChemistry 35:2597–2609PubMedCrossRefGoogle Scholar
  208. Tatko CD, Waters ML (2002) Selective aromatic interactions in β-hairpin peptides. J Am Chem Soc 124:9372–9373PubMedCrossRefGoogle Scholar
  209. Teng S, Srivastava AK, Wang L (2010) Sequence feature-based prediction of protein stability changes upon amino acid substitutions. BMC Genomics 11:1CrossRefGoogle Scholar
  210. Tian J, Wu N, Chu X, Fan Y (2010) Predicting changes in protein thermostability brought about by single-or multi-site mutations. BMC Bioinform 11:1CrossRefGoogle Scholar
  211. Tina K, Bhadra R, Srinivasan N (2007) PIC: protein interactions calculator. Nucleic Acids Res 35:W473–W476PubMedPubMedCentralCrossRefGoogle Scholar
  212. Tiwari A, Panigrahi SK (2007) HBAT: a complete package for analysing strong and weak hydrogen bonds in macromolecular crystal structures. In Silico Biol 7:651–661PubMedGoogle Scholar
  213. Tokunaga H, Arakawa T, Tokunaga M (2008) Engineering of halophilic enzymes: Two acidic amino acid residues at the carboxy-terminal region confer halophilic characteristics to Halomonas and Pseudomonas nucleoside diphosphate kinases. Protein Sci 17:1603–1610PubMedPubMedCentralCrossRefGoogle Scholar
  214. Toniolo C, Benedetti E (1980) Intramolecularly Hydrogen-Bonded Peptide Conformation. CRC Crit Rev Biochem 9:1–44PubMedCrossRefGoogle Scholar
  215. Trivedi S, Gehlot H, Rao S (2006) Protein thermostability in Archaea and Eubacteria. Genet Mol Res 5:816–827PubMedGoogle Scholar
  216. Turner P, Mamo G, Karlsson EN (2007) Potential and utilization of thermophiles and thermostable enzymes in biorefining. Microb Cell Fact 6:1CrossRefGoogle Scholar
  217. Tyson GW et al (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:37–43PubMedCrossRefGoogle Scholar
  218. Ventura S, Vega MC, Lacroix E, Angrand I, Spagnolo L, Serrano L (2002) Conformational strain in the hydrophobic core and its implications for protein folding and design. Na Struct Mol Biol 9:485–493CrossRefGoogle Scholar
  219. Vetriani C et al (1998) Protein thermostability above 100 C: a key role for ionic interactions. Proc Natl Acad Sci 95:12300–12305PubMedPubMedCentralCrossRefGoogle Scholar
  220. Vieille C, Zeikus GJ (2001) Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability. Microbiol Mol Biol Rev 65:1–43PubMedPubMedCentralCrossRefGoogle Scholar
  221. Violot S et al (2005) Structure of a full length psychrophilic cellulase from Pseudoalteromonas haloplanktis revealed by X-ray diffraction and small angle X-ray scattering. J Mol Biol 348:1211–1224PubMedCrossRefGoogle Scholar
  222. Vogt G, Argos P (1997) Protein thermal stability: hydrogen bonds or internal packing? Fold Des 2:S40–S46PubMedCrossRefGoogle Scholar
  223. Vogt G, Woell S, Argos P (1997) Protein thermal stability, hydrogen bonds, and ion pairs. J Mol Biol 269:631–643PubMedCrossRefGoogle Scholar
  224. Voorhorst WG, Eggen RI, Luesink EJ, De Vos WM (1995) Characterization of the celB gene coding for beta-glucosidase from the hyperthermophilic archaeon Pyrococcus furiosus and its expression and site-directed mutation in Escherichia coli. J Bacteriol 177:7105–7111PubMedPubMedCentralCrossRefGoogle Scholar
  225. Wagner A (2008) Neutralism and selectionism: a network-based reconciliation. Nat Rev Genet 9:965–974PubMedCrossRefGoogle Scholar
  226. Wang XY, Meng FG, Zhou HM (2004) The role of disulfide bonds in the conformational stability and catalytic activity of phytase. Biochem Cell Biol 82:329–334PubMedCrossRefGoogle Scholar
  227. Watson JD (2008) Molecular biology of the gene. vol QH506. M6627Google Scholar
  228. Whitaker JR, Feeney RE, Sternberg MM (1983) Chemical and physical modification of proteins by the hydroxide ion. Crit Rev Food Sci Nutr 19:173–212PubMedCrossRefGoogle Scholar
  229. Widderich N, Höppner A, Pittelkow M, Heider J, Smits SH, Bremer E (2014) Biochemical properties of ectoine hydroxylases from extremophiles and their wider taxonomic distribution among microorganisms. PloS one 9(4):e93809PubMedPubMedCentralCrossRefGoogle Scholar
  230. Willard L, Ranjan A, Zhang H, Monzavi H, Boyko RF, Sykes BD, Wishart DS (2003) VADAR: a web server for quantitative evaluation of protein structure quality. Nucleic Acids Res 31:3316–3319PubMedPubMedCentralCrossRefGoogle Scholar
  231. Worth CL, Preissner R, Blundell TL (2011) SDM—a server for predicting effects of mutations on protein stability and malfunction. Nucleic Acids Res gkr363Google Scholar
  232. Wu S, Skolnick J, Zhang Y (2007) Ab initio modeling of small proteins by iterative TASSER simulations. BMC Biol 5:17PubMedPubMedCentralCrossRefGoogle Scholar
  233. Xiao L, Honig B (1999) Electrostatic contributions to the stability of hyperthermophilic proteins. J Mol Biol 289:1435–1444PubMedCrossRefGoogle Scholar
  234. Xie Y, An J, Yang G, Wu G, Zhang Y, Cui L, Feng Y (2014) Enhanced enzyme kinetic stability by increasing rigidity within the active site. J Biol Chem 289:7994–8006PubMedPubMedCentralCrossRefGoogle Scholar
  235. Yafremava LS, Di Giulio M, Caetano-Anollés G (2013) Comparative analysis of barophily-related amino acid content in protein domains of Pyrococcus abyssi and Pyrococcus furiosus. ArchaeaGoogle Scholar
  236. Yang H, Liu L, Shin H-d, Chen RR, Li J, Du G, Chen J (2013) Structure-based engineering of histidine residues in the catalytic domain of α-amylase from Bacillus subtilis for improved protein stability and catalytic efficiency under acidic conditions. J Biotechnol 164:59–66PubMedCrossRefGoogle Scholar
  237. Yaseen A, Li Y (2013) Dinosolve: a protein disulfide bonding prediction server using context-based features to enhance prediction accuracy. BMC Bioinform 14:S9CrossRefGoogle Scholar
  238. Yin S, Ding F, Dokholyan NV (2007) Eris: an automated estimator of protein stability. Nat Methods 4:466–467PubMedCrossRefGoogle Scholar
  239. Zavodszky M, Chen CW, Huang JK, Zolkiewski M, Wen L, Krishnamoorthi R (2001) Disulfide bond effects on protein stability: designed variants of Cucurbita maxima trypsin inhibitor-V. Protein Sci 10:149–160PubMedPubMedCentralCrossRefGoogle Scholar
  240. Zeldovich KB, Berezovsky IN, Shakhnovich EI (2007) Protein and DNA sequence determinants of thermophilic adaptation. PLoS Comput Biol 3:e5PubMedPubMedCentralCrossRefGoogle Scholar
  241. Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinform 9:40CrossRefGoogle Scholar
  242. Zhang JH, Lin Y, Sun YF, Ye YR, Zheng SP, Han SY (2012) High-throughput screening of B factor saturation mutated Rhizomucor miehei lipase thermostability based on synthetic reaction. Enzyme Microb Technol 50:325–330PubMedCrossRefGoogle Scholar
  243. Zuber H (1988) Temperature adaptation of lactate dehydrogenase Structural, functional and genetic aspects. Biophys Chem 29(1):171–179PubMedCrossRefGoogle Scholar

Copyright information

© Springer Japan 2017

Authors and Affiliations

  • Debamitra Chakravorty
    • 1
  • Mohd Faheem Khan
    • 1
  • Sanjukta Patra
    • 1
  1. 1.Department of Biosciences and BioengineeringIndian Institute of Technology GuwahatiGuwahatiIndia

Personalised recommendations