Abstract
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.
Similar content being viewed by others
Abbreviations
- ΔG u :
-
Difference in Gibbs free energy of stability
- T s :
-
Stability temperature
- ΔH m :
-
Change in enthalpy
- ΔC p :
-
Change in heat capacity
- T m :
-
Melting temperature
References
Abe F, Kato C, Horikoshi K (1999) Pressure-regulated metabolism in microorganisms. Trends Microbiol 7:447–453
Ahern TJ, Klibanov AM (1988) Analysis of processes causing thermal inactivation of enzymes. Methods Biochem Anal 33:91–128
Allers T, Mevarech M (2005) Archaeal genetics—the third way. Nat Rev Genet 6:58–73
Alvarez M et al (1998) Triose-phosphate Isomerase (TIM) of the Psychrophilic Bacterium Vibrio marinus kinetic and structural properties. J Biol Chem 273:2199–2206
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 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 184:2634–2641
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 45:725–738
Bagautdinov B et al. (2014) Thermodynamic analysis of unusually thermostable CutA1 protein from human brain and its protease susceptibility. J Biochem mvu062
Baker-Austin C, Dopson M (2007) Life in acid: pH homeostasis in acidophiles. Trends Microbiol 15:165–171
Bao Q et al (2002) A complete sequence of the T. tengcongensis genome. Genome Res 12:689–700
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 22:205–214
Benedix A, Becker CM, de Groot BL, Caflisch A, Böckmann RA (2009) Predicting free energy changes using structural ensembles. Nat Methods 6:3–4
Berger F, Morellet N, Menu F, Potier P (1996) Cold shock and cold acclimation proteins in the psychrotrophic bacterium Arthrobacter globiformis SI55. J Bacteriol 178:2999–3007
Betz SF (1993) Disulfide bonds and the stability of globular proteins. Protein Sci 2:1551–1558
Bhaskara RM, Srinivasan N (2011) Stability of domain structures in multi-domain proteins. Sci Rep 8(1):40
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 461:225–234
Braxton S (1996) Protein engineering for stability. Protein engineering. Wiley-Liss, New York, pp 299–316
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 229:688–695
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 10:1
Bukau B, Horwich AL (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92(3):351–366
Bukau B, Weissman J, Horwich A (2006) Molecular chaperones and protein quality control. Cell 125(3):443–451
BURG B, Dijkstra BW, Vriend G, VINNE B, Venema G, Eijsink VG (1994) Protein stabilization by hydrophobic interactions at the surface. Eur J Biochem 220:981–985
Burley S, Petsko G (1985) Aromatic-aromatic interaction: a mechanism of protein structure stabilization. Science 229:23–28
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):24762–24769
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):1136–1143
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 150:3051–3063
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–W310
Ceroni A, Passerini A, Vullo A, Frasconi P (2006) DISULFIND: a disulfide bonding state and cysteine connectivity prediction server. Nucleic Acids Res 34:W177–W181
Chakravarty S, Varadarajan R (2000) Elucidation of determinants of protein stability through genome sequence analysis. Febs Lett 470:65–69
Chakravarty S, Varadarajan R (2002) Elucidation of factors responsible for enhanced thermal stability of proteins: a structural genomics based study. BioChemistry 41(25):8152–8161
Chakravorty D, Patra S (2012) Attaining extremophiles and extremolytes: methodologies and limitations. Extremophiles Sustain Resour Biotechnol Implications 29–74
Chakravorty D, Parameswaran S, Dubey VK, Patra S (2011) In silico characterization of thermostable lipases. Extremophiles 15:89–103
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:e21624
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 288:623–634
Chen C-W, Lin J, Chu Y-W (2013) iStable: off-the-shelf predictor integration for predicting protein stability changes. BMC Bioinform 14:1
Cheng J, Randall A, Baldi P (2006) Prediction of protein stability changes for single-site mutations using support vector machines. Proteins Struct Funct Bioinform 62:1125–1132
Costantini S, Colonna G, Facchiano AM (2008) ESBRI: a web server for evaluating salt bridges in proteins. Bioinformation 3:137–138
Creighton TE (1997) Protein structure: a practical approach
D’Amico S, Collins T, Marx JC, Feller G, Gerday C (2006) Psychrophilic microorganisms: challenges for life. EMBO Rep 7:385–389
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 21–31
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 269:17448–17453
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):16506–16511
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 25:2537–2543
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):461–470
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 4:2594–2604
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 346:1–6
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:e0149208
Dym O, Mevarech M, Sussman J (1995) Structural features that stabilize halophilic malate dehydrogenase from an archaebacterium. Science 267:1344
Edmondson SP, Qiu L, Shriver JW (1995) Solution structure of the DNA-binding protein Sac7d from the hyperthermophile Sulfolobus acidocaldarius. BioChemistry 34:13289–13304
Eiberweiser A, Nazet A, Kruchinin SE, Fedotova MV, Buchner R (2015) Hydration and ion binding of the osmolyte ectoine. J Phys Chem B 119:15203–15211
Eijsink VG, Bjørk A, Gåseidnes S, Sirevåg R, Synstad B, van den Burg B, Vriend G (2004) Rational engineering of enzyme stability. J Biotechnol 113:105–120
Elcock AH (1998) The stability of salt bridges at high temperatures: implications for hyperthermophilic proteins. J Mol Biol 284:489–502
Elcock AH, McCammon JA (1998) Electrostatic contributions to the stability of halophilic proteins. J Mol Biol 280:731–748
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 4:734–741
Farias ST, Bonato M (2003) Preferred amino acids and thermostability. Genet Mol Res 2:383–393
Feller G, Gerday C (2003) Psychrophilic enzymes: hot topics in cold adaptation. Nat Rev Microbiol 1:200–208
Feller G, Arpigny J, Narinx E, Gerday C (1997) Molecular adaptations of enzymes from psychrophilic organisms. Comparative biochemistry and physiology Part A. Physiology 118:495–499
Ferrè F, Clote P (2006) DiANNA 1.1: an extension of the DiANNA web server for ternary cysteine classification. Nucleic Acids Res 34:W182–W185
Frank A, Lobry J (1999) Asymmetric substitution patterns: a review of possible underlying mutational or selective mechanisms. Gene 238:65–77
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:e1003569
Fujinami S, Fujisawa M (2010) Industrial applications of alkaliphiles and their enzymes–past, present and future. Environ Technol 31:845–856
Fukuchi S, Yoshimune K, Wakayama M, Moriguchi M, Nishikawa K (2003) Unique amino acid composition of proteins in halophilic bacteria. J Mol Biol 327:347–357
Galinski EA, Pfeiffer HP, Trüper HG (1985) 1, 4, 5, 6-Tetrahydro-2-methyl-4-pyrimidinecarboxylic acid. Eur J Biochem 149:135–139
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 9:466–475
Gessesse A (1998) Purification and properties of two thermostable Alkaline xylanases from an Alkaliphilic Bacillus sp. Appl Environ Microbiol 64:3533–3535
Gianese G, Argos P, Pascarella S (2001) Structural adaptation of enzymes to low temperatures. Protein Eng 14:141–148
Gibson G, Muse SV (2004) Précis de génomique. De Boeck Supérieur
Gilbert HF (1993) Molecular and cellular aspects of thiol-disulfide exchange. Adv Enzymol Relat Areas Mol Biol 63:69–69
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 15:1
Goldstein RA (2007) Amino-acid interactions in psychrophiles, mesophiles, thermophiles, and hyperthermophiles: Insights from the quasi-chemical approximation. Protein Sci 16:1887–1895
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 407:30–41
Grocock RJ, Sharp PM (2002) Synonymous codon usage in Pseudomonas aeruginosa PA01. Gene 289:131–139
Gromiha MM, Thomas S, Santhosh C (2002) Role of cation-π interactions to the stability of thermophilic proteins. Prep Biochem Biotechnol 32:355–362
Gromiha MM, Santhosh C, Ahmad S (2004) Structural analysis of cation–π interactions in DNA binding proteins. Int J Biol Macromol 34:203–211
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 320:369–387
Gupta RS (1995) Evolution of the chaperonin families (HSP60, HSP 10 and TCP-1) of proteins and the origin of eukaryotic cells. Mol Microbiol 15:1–11
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 96:3578–3583
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 57:504–512
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
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(:):51–60
Horikoshi K (1999) Alkaliphiles: some applications of their products for biotechnology. Microbiol Mol Biol Rev 63:735–750
Huang L-T, Gromiha MM (2009) Reliable prediction of protein thermostability change upon double mutation from amino acid sequence. Bioinformatics 25:2181–2187
Huang L-T, Gromiha MM, Ho S-Y (2007) iPTREE-STAB: interpretable decision tree based method for predicting protein stability changes upon mutations. Bioinformatics 23:1292–1293
Hubbard RE, Kamran Haider M (2010) Hydrogen bonds in proteins: role and strength. eLS
Hutchinson EG, Thornton JM (1996) PROMOTIF—a program to identify and analyze structural motifs in proteins. Protein Sci 5:212–220
Jaenicke R (1991a) Protein stability and molecular adaptation to extreme conditions. In: EJB Reviews 1991. Springer, Berlin Heidelberg, pp 291–304
Jaenicke R (1991b) Protein folding: local structures, domains, subunits, and assemblies. BioChemistry 30:3147–3161
Jaenicke R (1996) Structure and stability of hyperstable proteins: glycolytic enzymes from hyperthermophilic bacterium Thermotoga maritima. Adv Protein Chem 48:181–269
Jaenicke R (2000) Do ultrastable proteins from hyperthermophiles have high or low conformational rigidity? Proc Natl Acad Sci 97:2962–2964
Jaenicke R, Böhm G (1998) The stability of proteins in extreme environments. Curr Opin Struct Biol 8:738–748
Johnson CM, Oliveberg M, Clarke J, Fersht AR (1997) Thermodynamics of denaturation of mutants of barnase with disulfide crosslinks. J Mol Biol 268:198–208
Jorda J, Yeates TO (2011) Widespread disulfide bonding in proteins from thermophilic archaea. Archaea
Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577–2637
Karplus PA, Schulz GE (1985) Prediction of chain flexibility in proteins. Naturwissenschaften 72:212–213
Karshikoff A, Ladenstein R (1998) Proteins from thermophilic and mesophilic organisms essentially do not differ in packing. Protein Eng 11:867–872
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):167–172
Kato C, Bartlett DH (1997) The molecular biology of barophilic bacteria. Extremophiles 1:111–116
Kato C, Sato T, Horikoshi K (1995) Isolation and properties of barophilic and barotolerant bacteria from deep-sea mud samples. Biodiversity Conserv 4:1–9
Kato C, Li L, Tamaoka J, Horikoshi K (1997) Molecular analyses of the sediment of the 11000-m deep Mariana Trench. Extremophiles 1:117–123
Kaur H, Raghava G (2003) A neural-network based method for prediction of γ-turns in proteins from multiple sequence alignment. Protein Sci 12:923–929
Kaur H, Raghava GPS (2006) Prediction of Cα-H· O and Cα-H· π interactions in proteins using recurrent neural network. In Silico Biol 6:111–125
Khan S, Vihinen M (2010) Performance of protein stability predictors. Hum Mutat 31:675–684
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 24:255–262
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 274:11761–11767
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 26:1038–1046
Klumpp M, Baumeister W (1998) The thermosome: archetype of group II chaperonins. FEBS Lett 430:73–77
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 262:502–515
Kollman PA (1972) Theory of hydrogen bond directionality. J Am Chem Soc 94:1837–1842
Kreil DP, Ouzounis CA (2001) Identification of thermophilic species by the amino acid compositions deduced from their genomes. Nucleic Acids Res 29:1608–1615
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 74:4560–4563
Kumar S, Tsai C-J, Nussinov R (2000) Factors enhancing protein thermostability. Protein Eng 13:179–191
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 65:3633–3640
Lanyi JK (1974) Salt-dependent properties of proteins from extremely halophilic bacteria. Bacteriol Rev 38:272
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):41–51
Lehmann M, Wyss M (2001) Engineering proteins for thermostability: the use of sequence alignments versus rational design and directed evolution. Curr Opin Biotechnol 12:371–375
Lentzen G, Schwarz T (2006) Extremolytes: natural compounds from extremophiles for versatile applications. Appl Microbiol Biotechnol 72:623–634
Li Y, Fang J (2012) PROTS-RF: a robust model for predicting mutation-induced protein stability changes. PloS one 7:e47247
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 14:1
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 255–257
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 237
Lu J-L, Hu X-H, Hu D-G (2012) A new hybrid fractal algorithm for predicting thermophilic nucleotide sequences. J Theor Biol 293:74–81
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 155:593–600
Macario AJ, de Macario EC (2004) The pathology of cellular anti-stress mechanisms: a new frontier. Stress 7:243–249
Madern D, Ebel C (2007) Influence of an anion-binding site in the stabilization of halophilic malate dehydrogenase from Haloarcula marismortui. Biochimie 89:981–987
Madigan MT (2000) Extremophilic bacteria and microbial diversity. Ann Mo Bot Garden 3–12
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):663–670
Makhatadze GI, Privalov PL (1995) Energetics of protein structure. Adv Protein Chem 47:307–425
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 99:9679–9684
Mally A, Witt SN (2001) GrpE accelerates peptide binding and release from the high affinity state of DnaK. Nat Struct Mol Biol 8(3):254–257
Manjunath K, Sekar K (2013) Molecular dynamics perspective on the protein thermal stability: a case study using SAICAR synthetase. J Chem Inf Model 53:2448–2461
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 448:265–268
Marcus Y (2009) Effect of ions on the structure of water: Structure making and breaking. Chem Rev (ACS Publications) 109:1346–1370
Marshall CJ (1997) Cold-adapted enzymes. Trends Biotechnol 15:359–364
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 3225–3228
Matsumura M, Matthews BW (1990) Stabilization of functional proteins by introduction of multiple disulfide bonds. Methods Enzymol 202:336–356
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 5
Mattos C (2002) Protein–water interactions in a dynamic world. Trends Biochem Sci 27:203–208
McDonald IK, Thornton JM (1994) Satisfying hydrogen bonding potential in proteins. J Mol Biol 238:777–793
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 10:1
Michels PC, Clark DS (1997) Pressure-enhanced activity and stability of a hyperthermophilic protease from a deep-sea methanogen. Appl Environ Microbiol 63:3985–3991
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 54:3039–3042
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 204:777–782
Najafabadi HS, Goodarzi H, Torabi N (2005) Optimality of codon usage in Escherichia coli due to load minimization. J Theor Biol 237:203–209
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):1000–1011
Nayek A, Gupta PSS, Banerjee S, Mondal B, Bandyopadhyay AK (2014) Salt-bridge energetics in halophilic proteins. Plos one 9:e93862
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):10308–10323
Norris PR, Burton NP, Foulis NA (2000) Acidophiles in bioreactor mineral processing. Extremophiles 4:71–76
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 286:31915–31923
Okada J et al (2010) Evolution and thermodynamics of the slow unfolding of hyperstable monomeric proteins. BMC Evol Biol 10:1
Olsen O, Thomsen KK (1991) Improvement of bacterial β-glucanase thermostability by glycosylation. Microbiology 137:579–585
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):797–807
Pace CN (1992) Contribution of the hydrophobic effect to globular protein stability. J Mol Biol 226:29–35
Pack SP, Yoo YJ (2004) Protein thermostability: structure-based difference of amino acid between thermophilic and mesophilic proteins. J Biotechnol 111:269–277
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):3417–3422
Palmer B, Angus K, Taylor L, Warwicker J, Derrick JP (2008) Design of stability at extreme alkaline pH in streptococcal protein G. J Biotechnol 134:222–230
Panigrahi P, Sule M, Ghanate A, Ramasamy S, Suresh C (2015) Engineering Proteins for Thermostability with iRDP Web Server. PloS one 10:e0139486
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):e0131495
Parthasarathy S, Murthy MR (2000) Protein thermal stability: insights from atomic displacement parameters (B values). Protein Eng 13:9–13
Parthiban V (2006) Prediction of factors determining changes in stability in protein mutants. Universität zu, Köln
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):782–801
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 9:1
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 32:928–949
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):13510–13515
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):2032–2043
Petsko GA (2001) Structural basis of thermostability in hyperthermophilic proteins, or “ there’s more than one way to skin a cat”. Methods Enzymol 334:469
Petsko GA, Ringe D (2004) Protein structure and function. New Science Press
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 6:75–88
Podar M, Reysenbach A-L (2006) New opportunities revealed by biotechnological explorations of extremophiles. Curr Opin Biotechnol 17:250–255
Privalov PL, Gill SJ (1988) Stability of protein structure and hydrophobic interaction. Adv Protein Chem 39:191–238
Rao JM, Argos P (1981) Structural stability of halophilic proteins. BioChemistry 20:6536–6543
Rathi PC, Jaeger K-E, Gohlke H (2015) Structural rigidity and protein thermostability in variants of lipase A from Bacillus subtilis. PloS one 10:e0130289
Reed CJ, Lewis H, Trejo E, Winston V, Evilia C (2013) Protein adaptations in archaeal extremophiles. Archaea 2013
Reetz MT (2013) Biocatalysis in organic chemistry and biotechnology: past, present, and future. J Am Chem Soc 135:12480–12496
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 45:7745–7751
Robinson NE (2002) Protein deamidation. Proc Natl Acad Sci 99:5283–5288
Rohl CA, Strauss CE, Misura KM, Baker D (2004) Protein structure prediction using Rosetta. Methods Enzymol 383:66–93
Rose GD, Gierasch L, Smith JA (1985) Turns in peptides and proteins. Adv Protein Chem 37:1
Rothschild LJ, Mancinelli RL (2001) Life in extreme environments. Nature 409:1092–1101
Russell NJ (1998) Molecular adaptations in psychrophilic bacteria: potential for biotechnological applications. In: Biotechnology of extremophiles. Springer, Berlin Heidelberg. pp 1–21
Russell RJ, Gerike U, Danson MJ, Hough DW, Taylor GL (1998) Structural adaptations of the cold-active citrate synthase from an Antarctic bacterium. Structure 6:351–361
Sahlan M, Yohda M (2013a) Molecular chaperones in thermophilic eubacteria and archaea. In: Thermophilic microbes in environmental and industrial biotechnology. Springer, pp 375–394
Sahlan M, Yohda M (2013b) Molecular chaperones in thermophilic eubacteria and archaea. In: Thermophilic microbes in environmental and industrial biotechnology. Springer, Netherlands, pp 375–394
Santos SR, Ochman H (2004) Identification and phylogenetic sorting of bacterial lineages with universally conserved genes and proteins. Environ Microbiol 6:754–759
Saunders NF et al. (2003) Mechanisms of thermal adaptation revealed from the genomes of the Antarctic Archaea Methanogenium frigidum and Methanococcoides burtonii. Genome Res 13:1580–1588
Schlessinger A, Yachdav G, Rost B (2006) PROFbval: predict flexible and rigid residues in proteins. Bioinformatics 22:891–893
Schumann J, Böhm G, Jaenicke R, Schumacher G, Rudolph R (1993) Stabilization of creatinase from Pseudomonas putida by random mutagenesis. Protein Sci 2:1612–1620
Seeliger D, De Groot BL (2010) Protein thermostability calculations using alchemical free energy simulations. Biophys J 98:2309–2316
Serrano L, Bycroft M, Fersht AR (1991) Aromatic-aromatic interactions and protein stability: investigation by double-mutant cycles. J Mol Biol 218:465–475
Setati ME (2010) Diversity and industrial potential of hydrolaseproducing halophilic/halotolerant eubacteria. Afr J Biotechnol 9:1555–1560
Sharma A, Kawarabayasi Y, Satyanarayana T (2012) Acidophilic bacteria and archaea: acid stable biocatalysts and their potential applications. Extremophiles 16:1–19
Shental-Bechor D, Levy Y (2008) Effect of glycosylation on protein folding: a close look at thermodynamic stabilization. Proc Natl Acad Sci 105:8256–8261
Shirley BA (1995) Protein stability and folding: theory and practice. Humana Press, pp 387
Siddiqui KS, Thomas T (2008) Protein adaptation in extremophiles. Nova Publishers
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 11:1
Singer GA, Hickey DA (2003) Thermophilic prokaryotes have characteristic patterns of codon usage, amino acid composition and nucleotide content. Gene 317:39–47
Spassov VZ, Karshikoff AD, Ladenstein R (1995) The optimization of protein-solvent interactions: Thermostability and the role of hydrophobic and electrostatic interactions. Protein science 4:1516–1527
Spector S et al (2000) Rational modification of protein stability by the mutation of charged surface residues. BioChemistry 39:872–879
Srivastava A, Sinha S (2014) Thermostability of in vitro evolved Bacillus subtilis lipase A: a network and dynamics perspective. PloS one 9:e102856
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):2947–2955
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:e100643
Swaim MW, Pizzo SV (1988) Methionine sulfoxide and the oxidative regulation of plasma proteinase inhibitors. J Leukocyte Biol 43:365–379
Szilágyi A, Závodszky P (2000) Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey. Structure 8:493–504
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):22411–22418
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 265:6874–6878
Takami H, Horikoshi K (2000) Analysis of the genome of an alkaliphilic Bacillus strain from an industrial point of view. Extremophiles 4:99–108
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 279:32957–32967
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 35:2597–2609
Tatko CD, Waters ML (2002) Selective aromatic interactions in β-hairpin peptides. J Am Chem Soc 124:9372–9373
Teng S, Srivastava AK, Wang L (2010) Sequence feature-based prediction of protein stability changes upon amino acid substitutions. BMC Genomics 11:1
Tian J, Wu N, Chu X, Fan Y (2010) Predicting changes in protein thermostability brought about by single-or multi-site mutations. BMC Bioinform 11:1
Tina K, Bhadra R, Srinivasan N (2007) PIC: protein interactions calculator. Nucleic Acids Res 35:W473–W476
Tiwari A, Panigrahi SK (2007) HBAT: a complete package for analysing strong and weak hydrogen bonds in macromolecular crystal structures. In Silico Biol 7:651–661
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 17:1603–1610
Toniolo C, Benedetti E (1980) Intramolecularly Hydrogen-Bonded Peptide Conformation. CRC Crit Rev Biochem 9:1–44
Trivedi S, Gehlot H, Rao S (2006) Protein thermostability in Archaea and Eubacteria. Genet Mol Res 5:816–827
Turner P, Mamo G, Karlsson EN (2007) Potential and utilization of thermophiles and thermostable enzymes in biorefining. Microb Cell Fact 6:1
Tyson GW et al (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:37–43
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 9:485–493
Vetriani C et al (1998) Protein thermostability above 100 C: a key role for ionic interactions. Proc Natl Acad Sci 95:12300–12305
Vieille C, Zeikus GJ (2001) Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability. Microbiol Mol Biol Rev 65:1–43
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 348:1211–1224
Vogt G, Argos P (1997) Protein thermal stability: hydrogen bonds or internal packing? Fold Des 2:S40–S46
Vogt G, Woell S, Argos P (1997) Protein thermal stability, hydrogen bonds, and ion pairs. J Mol Biol 269:631–643
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 177:7105–7111
Wagner A (2008) Neutralism and selectionism: a network-based reconciliation. Nat Rev Genet 9:965–974
Wang XY, Meng FG, Zhou HM (2004) The role of disulfide bonds in the conformational stability and catalytic activity of phytase. Biochem Cell Biol 82:329–334
Watson JD (2008) Molecular biology of the gene. vol QH506. M6627
Whitaker JR, Feeney RE, Sternberg MM (1983) Chemical and physical modification of proteins by the hydroxide ion. Crit Rev Food Sci Nutr 19:173–212
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):e93809
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 31:3316–3319
Worth CL, Preissner R, Blundell TL (2011) SDM—a server for predicting effects of mutations on protein stability and malfunction. Nucleic Acids Res gkr363
Wu S, Skolnick J, Zhang Y (2007) Ab initio modeling of small proteins by iterative TASSER simulations. BMC Biol 5:17
Xiao L, Honig B (1999) Electrostatic contributions to the stability of hyperthermophilic proteins. J Mol Biol 289:1435–1444
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 289:7994–8006
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. Archaea
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 164:59–66
Yaseen A, Li Y (2013) Dinosolve: a protein disulfide bonding prediction server using context-based features to enhance prediction accuracy. BMC Bioinform 14:S9
Yin S, Ding F, Dokholyan NV (2007) Eris: an automated estimator of protein stability. Nat Methods 4:466–467
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 10:149–160
Zeldovich KB, Berezovsky IN, Shakhnovich EI (2007) Protein and DNA sequence determinants of thermophilic adaptation. PLoS Comput Biol 3:e5
Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinform 9:40
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 50:325–330
Zuber H (1988) Temperature adaptation of lactate dehydrogenase Structural, functional and genetic aspects. Biophys Chem 29(1):171–179
Acknowledgements
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by S. Albers.
Debamitra Chakravorty and Mohd Faheem Khan are contributed equally.
Rights and permissions
About this article
Cite this article
Chakravorty, D., Khan, M.F. & Patra, S. Multifactorial level of extremostability of proteins: can they be exploited for protein engineering?. Extremophiles 21, 419–444 (2017). https://doi.org/10.1007/s00792-016-0908-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00792-016-0908-9