Overview of strategies for developing high thermostability industrial enzymes: Discovery, mechanism, modification and challenges

References

• Abraham, T., T. Abraham, S. Pil Pack, and Y. Je Yoo. 2005. Stabilization of Bacillus subtilis lipase A by increasing the residual packing. Biocatalysis and Biotransformation 23 (3–4):217–24. doi: 10.1080/10242420500193013.
   Web of Science ®Google Scholar
• Atalah, J., P. Cáceres-Moreno, G. Espina, and J. Blamey. 2019. Thermophiles and the applications of their enzymes as new biocatalysts. Bioresource Technology 280:478–88. doi: 10.1016/j.biortech.2019.02.008.
   PubMed Web of Science ®Google Scholar
• Ayuso-Tejedor, S., O. Abián, and J. Sancho. 2011. Underexposed polar residues and protein stabilization. Protein Engineering, Design & Selection: PEDS 24 (1–2):171–7. doi: 10.1093/protein/gzq072.
   PubMed Web of Science ®Google Scholar
• Ban, X., J. Wu, B. Kaustubh, P. Lahiri, A. S. Dhoble, Z. Gu, C. Li, L. Cheng, Y. Hong, Y. Tong, et al. 2020. Additional salt bridges improve the thermostability of 1,4-α-glucan branching enzyme. Food Chemistry 316:126348. doi: 10.1016/j.foodchem.2020.126348.
   PubMed Web of Science ®Google Scholar
• Barzegar, A., A. A. Moosavi-Movahedi, J. Z. Pedersen, and M. Miroliaei. 2009. Comparative thermostability of mesophilic and thermophilic alcohol dehydrogenases: Stability-determining roles of proline residues and loop conformations. Enzyme and Microbial Technology 45 (2):73–9. doi: 10.1016/j.enzmictec.2009.04.007.
   Web of Science ®Google Scholar
• Ben Ali, M., M. Ghram, H. Hmani, B. Khemakhem, R. Haser, and S. Bejar. 2011. Toward the smallest active subdomain of a TIM-barrel fold: Insights from a truncated α-amylase. Biochemical and Biophysical Research Communications 411 (2):265–70. doi: 10.1016/j.bbrc.2011.06.114.
   PubMed Web of Science ®Google Scholar
• Bommarius, A. S., and M. F. Paye. 2013. Stabilizing biocatalysts. Chemical Society Reviews 42 (15):6534–65. doi: 10.1039/c3cs60137d.
   PubMed Web of Science ®Google Scholar
• Brown, S. H., H. R. Costantino, and R. M. Kelly. 1990. Characterization of amylolytic enzyme activities associated with the hyperthermophilic archaebacterium Pyrococcus furiosus. Applied and Environmental Microbiology 56 (7):1985–91. https://aem.asm.org/content/aem/56/7/1985.full.pdf. doi: 10.1128/aem.56.7.1985-1991.1990.
   PubMed Web of Science ®Google Scholar
• Chadha, B., B. Kaur, N. Basotra, A. Tsang, and A. Pandey. 2019. Thermostable xylanases from thermophilic fungi and bacteria: Current perspective. Bioresource Technology 277:195–203. doi: 10.1016/j.biortech.2019.01.044.
   PubMed Web of Science ®Google Scholar
• Chakravarty, S., and R. Varadarajan. 2002. Elucidation of factors responsible for enhanced thermal stability of proteins: A structural genomics based study. Biochemistry 41 (25):8152–61. doi: 10.1021/bi025523t.
   PubMed Web of Science ®Google Scholar
• Chan, C. H., T. H. Yu, K. B. Wong, and A. Pastore. 2011. Stabilizing salt-bridge enhances protein thermostability by reducing the heat capacity change of unfolding. PLOS One 6 (6):e21624. doi: 10.1371/journal.pone.0021624.
   PubMed Web of Science ®Google Scholar
• Chen, K., A. C. Robinson, M. E. Van Dam, P. Martinez, C. Economou, and F. H. Arnold. 1991. Enzyme engineering for nonaqueous solvents. II. Additive effects of mutations on the stability and activity of subtilisin E in polar organic media. Biotechnology Progress 7 (2):125–9. doi: 10.1021/bp00008a007.
   PubMed Web of Science ®Google Scholar
• Chen, Q., Y. Xiao, W. Zhang, and W. Mu. 2020. Current methods and applications in computational protein design for food industry. Critical Reviews in Food Science and Nutrition 60 (19):3259–70. doi: 10.1080/10408398.2019.1682513.
   PubMed Web of Science ®Google Scholar
• Chettri, D., A. K. Verma, L. Sarkar, and A. K. Verma. 2021. Role of extremophiles and their extremozymes in biorefinery process of lignocellulose degradation. Extremophiles: Life under Extreme Conditions 25 (3):203–19. doi: 10.1007/s00792-021-01225-0.
   PubMed Web of Science ®Google Scholar
• Craig, D. B., and A. A. Dombkowski. 2013. Disulfide by Design 2.0: A web-based tool for disulfide engineering in proteins. BMC Bioinformatics 14 (1):346. doi: 10.1186/1471-2105-14-346.
   PubMed Web of Science ®Google Scholar
• Creighton, T. E. 1984. Disulfide bond formation in proteins, methods in enzymology, 305–29. Academic Press.
   Google Scholar
• D’Auria, S., A. Morana, F. Febbraio, C. Vaccaro, M. De Rosa, and R. Nucci. 1996. Functional and structural properties of the homogeneous beta-glycosidase from the extreme thermoacidophilic archaeon sulfolobus solfataricus expressed in Saccharomyces cerevisiae. Protein Expression and Purification 7 (3):299–308. doi: 10.1006/prep.1996.0043.
   PubMed Web of Science ®Google Scholar
• Dani, V. S., C. Ramakrishnan, and R. Varadarajan. 2003. MODIP revisited: Re-evaluation and refinement of an automated procedure for modeling of disulfide bonds in proteins. Protein Engineering 16 (3):187–93. doi: 10.1093/proeng/gzg024.
   PubMedGoogle Scholar
• de Bakker, P. I. W., P. H. Hünenberger, and J. A. McCammon. 1999. Molecular dynamics simulations of the hyperthermophilic protein Sac7d from Sulfolobus acidocaldarius: Contribution of salt bridges to thermostability. Journal of Molecular Biology 285 (4):1811–30. doi: 10.1006/jmbi.1998.2397.
   PubMed Web of Science ®Google Scholar
• Dehouck, Y., A. Grosfils, B. Folch, D. Gilis, P. Bogaerts, and M. Rooman. 2009. Fast and accurate predictions of protein stability changes upon mutations using statistical potentials and neural networks: PoPMuSiC-2.0. Bioinformatics (Oxford, England) 25 (19):2537–43. doi: 10.1093/bioinformatics/btp445.
   PubMed Web of Science ®Google Scholar
• Deutsch, C., and B. Krishnamoorthy. 2007. Four-body scoring function for mutagenesis. Bioinformatics (Oxford, England) 23 (22):3009–15. doi: 10.1093/bioinformatics/btm481.
   PubMed Web of Science ®Google Scholar
• Dotsenko, A. S., S. Pramanik, A. V. Gusakov, A. M. Rozhkova, I. N. Zorov, A. P. Sinitsyn, M. D. Davari, and U. Schwaneberg. 2019. Critical effect of proline on thermostability of endoglucanase II from Penicillium verruculosum. Biochemical Engineering Journal 152:107395. doi: 10.1016/j.bej.2019.107395.
   Web of Science ®Google Scholar
• Dotsenko, A. S., A. M. Rozhkova, I. N. Zorov, and A. P. Sinitsyn. 2020. Protein surface engineering of endoglucanase Penicillium verruculosum for improvement in thermostability and stability in the presence of 1-butyl-3-methylimidazolium chloride ionic liquid. Bioresource Technology 296:122370. doi: 10.1016/j.biortech.2019.122370.
   PubMed Web of Science ®Google Scholar
• Dougherty, D. A. 2007. Cation-pi interactions involving aromatic amino acids. The Journal of Nutrition 137 (6 Suppl 1):1504S–1508. doi: 10.1093/jn/137.6.1504S.
   PubMed Web of Science ®Google Scholar
• Ebaid, R., H. Wang, C. Sha, A. E. F. Abomohra, and W. Shao. 2019. Recent trends in hyperthermophilic enzymes production and future perspectives for biofuel industry: A critical review. Journal of Cleaner Production 238:117925. doi: 10.1016/j.jclepro.2019.117925.
   Web of Science ®Google Scholar
• Eriksson, A. E., W. A. Baase, X. J. Zhang, D. W. Heinz, M. Blaber, E. P. Baldwin, and B. W. Matthews. 1992. Response of a protein structure to cavity-creating mutations and its relation to the hydrophobic effect. Science (New York, NY) 255 (5041):178–83. doi: 10.1126/science.1553543.
   Google Scholar
• Ferrer, M., M. Martínez-Martínez, R. Bargiela, W. R. Streit, O. V. Golyshina, and P. N. Golyshin. 2016. Estimating the success of enzyme bioprospecting through metagenomics: Current status and future trends. Microbial Biotechnology 9 (1):22–34. doi: 10.1111/1751-7915.12309.
   PubMed Web of Science ®Google Scholar
• Folch, B., M. Rooman, and Y. Dehouck. 2008. Thermostability of salt bridges versus hydrophobic interactions in proteins probed by statistical potentials. Journal of Chemical Information and Modeling 48 (1):119–27. doi: 10.1021/ci700237g.
   PubMed Web of Science ®Google Scholar
• Ge, L., D. Li, T. Wu, L. Zhao, G. Ding, Z. Wang, and W. Xiao. 2018. B-factor-saturation mutagenesis as a strategy to increase the thermostability of α-L-rhamnosidase from Aspergillus terreus. Journal of Biotechnology 275:17–23. doi: 10.1016/j.jbiotec.2018.03.013.
   PubMed Web of Science ®Google Scholar
• Georis, J., F. de Lemos Esteves, J. Lamotte-Brasseur, V. Bougnet, B. Devreese, F. Giannotta, B. Granier, and J. M. Frère. 2000. An additional aromatic interaction improves the thermostability and thermophilicity of a mesophilic family 11 xylanase: Structural basis and molecular study. Protein Science 9 (3):466–75. doi: 10.1110/ps.9.3.466.
   PubMed Web of Science ®Google Scholar
• Grättinger, M., A. Dankesreiter, H. Schurig, and R. Jaenicke. 1998. Recombinant phosphoglycerate kinase from the hyperthermophilic bacterium Thermotoga maritima: Catalytic, spectral and thermodynamic properties. Journal of Molecular Biology 280 (3):525–33. doi: 10.1006/jmbi.1998.1861.
   PubMed Web of Science ®Google Scholar
• Gromiha, M. M., M. C. Pathak, K. Saraboji, E. A. Ortlund, and E. A. Gaucher. 2013. Hydrophobic environment is a key factor for the stability of thermophilic proteins. Proteins 81 (4):715–21. doi: 10.1002/prot.24232.
   PubMed Web of Science ®Google Scholar
• Guerois, R., J. E. Nielsen, and L. Serrano. 2002. Predicting changes in the stability of proteins and protein complexes: A study of more than 1000 mutations. Journal of Molecular Biology 320 (2):369–87. doi: 10.1016/S0022-2836(02)00442-4.
   PubMed Web of Science ®Google Scholar
• Guo, J., Z. Rao, T. Yang, Z. Man, X. Zhang, M. Xu, and X. Li. 2017. Enhancement of the thermostability of Streptomyces kathirae SC-1 Tyrosinase by rational sign and empirical mutation. Journal of Food Science and Biotechnology 36 (9):901–11. doi: 10.3969/j.issn.1673-1689.2017.09.002. (In Chinese).
   Google Scholar
• Han, H., Z. Ling, A. Khan, A. Virk, S. Kulshrestha, and X. Li. 2019. Improvements of thermophilic enzymes: From genetic modifications to applications. Bioresource Technology 279:350–61. doi: 10.1016/j.biortech.2019.01.087.
   PubMed Web of Science ®Google Scholar
• Herbert, R. A. 1992. A perspective on the biotechnological potential of extremophiles. Trends in Biotechnology 10 (11):395–402. doi: 10.1016/0167-7799(92)90282-Z.
   PubMed Web of Science ®Google Scholar
• Huang, P., S. E. Boyken, and D. Baker. 2016. The coming of age of de novo protein design. Nature 537 (7620):320–7. doi: 10.1038/nature19946.
   PubMed Web of Science ®Google Scholar
• Huang, L., J. Ma, J. Sang, N. Wang, S. Wang, C. Wang, H. Kang, F. Liu, F. Lu, and Y. Liu. 2020. Enhancing the thermostability of phospholipase D from Streptomyces halstedii by directed evolution and elucidating the mechanism of a key amino acid residue using molecular dynamics simulation. International Journal of Biological Macromolecules 164:3065–74. doi: 10.1016/j.ijbiomac.2020.08.160.
   PubMed Web of Science ®Google Scholar
• Huang, J., D. Xie, and Y. Feng. 2017. Engineering thermostable (R)-selective amine transaminase from Aspergillus terreus through in silico design employing B-factor and folding free energy calculations. Biochemical and Biophysical Research Communications 483 (1):397–402. doi: 10.1016/j.bbrc.2016.12.131.
   PubMed Web of Science ®Google Scholar
• Ikeda, M., and D. S. Clark. 1998. Molecular cloning of extremely thermostable esterase gene from hyperthermophilic archaeon. Biotechnology and Bioengineering 57 (5):624–9. doi: 10.1002/(SICI)­1097-0290(19980305)57:5<624::AID-BIT15>3.0.CO;2-B.
   PubMed Web of Science ®Google Scholar
• Ishak, S. N. H., N. H. A. Kamarudin, M. S. M. Ali, A. T. C. Leow, and R. N. Z. R. A. Rahman. 2020. Ion-pair interaction and hydrogen bonds as main features of protein thermostability in mutated T1 recombinant lipase originating from Geobacillus zalihae. Molecules 25 (15):3430. doi: 10.3390/molecules25153430.
   PubMed Web of Science ®Google Scholar
• Ishikawa, K., H. Nakamura, K. Morikawa, and S. Kanaya. 1993. Stabilization of Escherichia coli ribonuclease HI by cavity-filling mutations within a hydrophobic core. Biochemistry 32 (24):6171–8. doi: 10.1021/bi00075a009.
   PubMed Web of Science ®Google Scholar
• Jensen, M. S., L. Fredriksen, A. K. MacKenzie, P. B. Pope, I. Leiros, P. Chylenski, A. K. Williamson, T. Christopeit, H. Østby, G. Vaaje-Kolstad, et al. 2018. Discovery and characterization of a thermostable two-domain GH6 endoglucanase from a compost metagenome. PLoS One 13 (5):e0197862. doi: 10.1371/journal.pone.0197862.
   PubMed Web of Science ®Google Scholar
• Kannan, N., and S. Vishveshwara. 2000. Aromatic clusters: A determinant of thermal stability of thermophilic proteins. Protein Engineering 13 (11):753–61. doi: 10.1093/protein/13.11.753.
   PubMedGoogle Scholar
• Kapoor, S., A. Rafiq, and S. Sharma. 2017. Protein engineering and its applications in food industry. Critical Reviews in Food Science and Nutrition 57 (11):2321–9. doi: 10.1080/10408398.2014.1000481.
   PubMed Web of Science ®Google Scholar
• Karnaouri, A., I. Antonopoulou, A. Zerva, M. Dimarogona, E. Topakas, U. Rova, and P. Christakopoulos. 2019. Thermophilic enzyme systems for efficient conversion of lignocellulose to valuable products: Structural insights and future perspectives for esterases and oxidative catalysts. Bioresource Technology 279:362–72. doi: 10.1016/j.biortech.2019.01.062.
   PubMed Web of Science ®Google Scholar
• Karshikoff, A., and R. Ladenstein. 1998. Proteins from thermophilic and mesophilic organisms essentially do not differ in packing. Protein Engineering 11 (10):867–72. doi: 10.1093/protein/11.10.867.
   PubMedGoogle Scholar
• Kazlauskas, R. 2018. Engineering more stable proteins. Chemical Society Reviews 47 (24):9026–45. doi: 10.1039/c8cs00014j.
   PubMed Web of Science ®Google Scholar
• Kim, H. S., Q. A. T. Le, and Y. H. Kim. 2010. Development of thermostable lipase B from Candida antarctica (CalB) through in silico design employing B-factor and RosettaDesign. Enzyme and Microbial Technology 47 (1–2):1–5. doi: 10.1016/j.enzmictec.2010.04.003.
   Web of Science ®Google Scholar
• Kumar, S., A. Dangi, P. Shukla, D. Baishya, and S. Khare. 2019. Thermozymes: Adaptive strategies and tools for their biotechnological applications. Bioresource Technology 278:372–82. doi: 10.1016/j.biortech.2019.01.088.
   PubMed Web of Science ®Google Scholar
• Ladevèze, S., L. Tarquis, D. A. Cecchini, J. Bercovici, I. André, C. M. Topham, S. Morel, E. Laville, P. Monsan, V. Lombard, et al. 2013. Role of glycoside phosphorylases in mannose foraging by human gut bacteria. The Journal of Biological Chemistry 288 (45):32370–83. doi: 10.1074/jbc.M113.483628.
   PubMed Web of Science ®Google Scholar
• Lewin, A., T. A. Strand, T. Haugen, G. Klinkenberg, H. K. Kotlar, S. Valla, F. Drablos, and A. Wentzel. 2016. Discovery and characterization of a thermostable esterase from an oil reservoir metagenome. Advances in Enzyme Research 04 (02):68–86. doi: 10.4236/aer.2016.42008.
   Google Scholar
• Li, G., X. Chen, X. Zhou, R. Huang, L. Li, Y. Miao, D. Liu, and R. Zhang. 2019. Improvement of GH10 family xylanase thermostability by introducing of an extra α-helix at the C-terminal. Biochemical and Biophysical Research Communications 515 (3):417–22. doi: 10.1016/j.bbrc.2019.05.163.
   PubMed Web of Science ®Google Scholar
• Li, L., S. Zhang, W. Wu, W. Guan, Z. Deng, and H. Qiao. 2019. Enhancing thermostability of Yarrowia lipolytica lipase 2 through engineering multiple disulfide bonds and mitigating reduced lipase production associated with disulfide bonds. Enzyme and Microbial Technology 126:41–9. doi: 10.1016/j.enzmictec.2019.03.008.
   PubMed Web of Science ®Google Scholar
• Li, W., X. Zhou, and P. Lu. 2005. Structural features of thermozymes. Biotechnology Advances 23 (4):271–81. doi: 10.1016/j.biotechadv.2005.01.002.
   PubMed Web of Science ®Google Scholar
• Liu, Y., L. Huang, M. Shan, J. Sang, Y. Li, L. Jia, N. Wang, S. Wang, S. Shao, F. Liu, et al. 2019. Enhancing the activity and thermostability of Streptomyces mobaraensis transglutaminase by directed evolution and molecular dynamics simulation. Biochemical Engineering Journal 151:107333. doi: 10.1016/j.bej.2019.107333.
   Web of Science ®Google Scholar
• Liu, Q., Y. Wang, H. Luo, L. Wang, P. Shi, H. Huang, P. Yang, and B. Yao. 2015. Isolation of a novel cold-active family 11 xylanase from the filamentous fungus Bispora antennata and deletion of its N-terminal amino acids on thermostability. Applied Biochemistry and Biotechnology 175 (2):925–36. doi: 10.1007/s12010-014-1344-x.
   PubMed Web of Science ®Google Scholar
• Liu, Q., G. Xun, and Y. Feng. 2019. The state-of-the-art strategies of protein engineering for enzyme stabilization. Biotechnology Advances 37 (4):530–7. doi: 10.1016/j.biotechadv.2018.10.011.
   PubMed Web of Science ®Google Scholar
• Liu, Y., G. Luo, H. Ngo, W. Guo, and S. Zhang. 2020. Advances in thermostable laccase and its current application in lignin-first biorefinery: A review. Bioresource Technology 298:122511. doi: 10.1016/j.biortech.2019.122511.
   PubMed Web of Science ®Google Scholar
• Lorenz, P., and J. Eck. 2005. Metagenomics and industrial applications. Nature Reviews Microbiology 3 (6):510–6. doi: 10.1038/nrmicro1161.
   PubMed Web of Science ®Google Scholar
• Mabrouk, S. B., N. Aghajari, M. B. Ali, E. B. Messaoud, M. Juy, R. Haser, and S. Bejar. 2011. Enhancement of the thermostability of the maltogenic amylase MAUS149 by Gly312Ala and Lys436Arg substitutions. Bioresource Technology 102 (2):1740–6. doi: 10.1016/j.biortech.2010.08.082.
   PubMed Web of Science ®Google Scholar
• Madan, B., and P. Mishra. 2014. Directed evolution of Bacillus licheniformis lipase for improvement of thermostability. Biochemical Engineering Journal 91:276–82. doi: 10.1016/j.bej.2014.08.022.
   Web of Science ®Google Scholar
• Mao, S., X. Cheng, Z. Zhu, Y. Chen, C. Li, M. Zhu, X. Liu, F. Lu, and H. Qin. 2020. Engineering a thermostable version of D-allulose 3-epimerase from Rhodopirellula baltica via site-directed mutagenesis based on B-factors analysis. Enzyme and Microbial Technology 132:109441. doi: 10.1016/j.enzmictec.2019.109441.
   PubMed Web of Science ®Google Scholar
• Matthews, B. W., H. Nicholson, and W. J. Becktel. 1987. Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding. Proceedings of the National Academy of Sciences of the United States of America 84 (19):6663–7. doi: 10.1073/pnas.84.19.6663.
   PubMed Web of Science ®Google Scholar
• Mhiri, S., A. Bouanane-Darenfed, S. Jemli, S. Neifar, R. Ameri, M. Mezghani, K. Bouacem, B. Jaouadi, and S. Bejar. 2020. A thermophilic and thermostable xylanase from Caldicoprobacter algeriensis: Recombinant expression, characterization and application in paper biobleaching. International Journal of Biological Macromolecules 164:808–17. doi: 10.1016/j.ijbiomac.2020.07.162.
   PubMed Web of Science ®Google Scholar
• Modarres, H. P., M. R. Mofrad, and A. Sanati-Nezhad. 2016. Protein thermostability engineering. RSC Advances 6 (116):115252–70. doi: 10.1039/C6RA16992A.
   Web of Science ®Google Scholar
• Mohammadi, M., A. Sakhteman, S. Ahrari, K. Hassanpour, S. E. Hashemi, and G. Farnoosh. 2018. Disulfide bridge formation to increase thermostability of DFPase enzyme: A computational study. Computational Biology and Chemistry 77:272–8. doi: 10.1016/j.compbiolchem.2018.09.005.
   PubMed Web of Science ®Google Scholar
• Mollania, N., K. Khajeh, B. Ranjbar, and S. Hosseinkhani. 2011. Enhancement of a bacterial laccase thermostability through directed mutagenesis of a surface loop. Enzyme and Microbial Technology 49 (5):446–52. doi: 10.1016/j.enzmictec.2011.08.001.
   PubMed Web of Science ®Google Scholar
• Niehaus, F., A. Peters, T. Groudieva, and G. Antranikian. 2000. Cloning, expression and biochemical characterisation of a unique thermostable pullulan-hydrolysing enzyme from the hyperthermophilic archaeon Thermococcus aggregans. FEMS Microbiology Letters 190 (2):223–9. doi: 10.1016/S0378-1097(00)00339-6.
   PubMed Web of Science ®Google Scholar
• Ohmura, T., T. Ueda, K. Ootsuka, M. Saito, and T. Imoto. 2001. Stabilization of hen egg white lysozyme by a cavity-filling mutation. Protein Science 10 (2):313–20. doi: 10.1110/ps.37401.
   PubMed Web of Science ®Google Scholar
• Okada, J., T. Okamoto, A. Mukaiyama, T. Tadokoro, D. You, H. Chon, Y. Koga, K. Takano, and S. Kanaya. 2010. Evolution and thermodynamics of the slow unfolding of hyperstable monomeric proteins. BMC Evolutionary Biology 10:207. doi: 10.1186/1471-2148-10-207.
   PubMed Web of Science ®Google Scholar
• Pace, C. 1992. Contribution of the hydrophobic effect to globular protein stability. Journal of Molecular Biology 226 (1):29–35. doi: 10.1016/0022-2836(92)90121-Y.
   PubMed Web of Science ®Google Scholar
• Patel, A., R. Singhania, S. Sim, and A. Pandey. 2019. Thermostable cellulases: Current status and perspectives. Bioresource Technology 279:385–92. doi: 10.1016/j.biortech.2019.01.049.
   PubMed Web of Science ®Google Scholar
• Peng, H., L. Qian, Z. Fu, L. Xin, Z. Hua, J. Woolf, Y. Xiao, and Y. Gao. 2021. Using a novel hyperthermophilic amylopullulanase to simplify resistant starch preparation from rice starches. Journal of Functional Foods 80:104429. doi: 10.1016/j.jff.2021.104429.
   Web of Science ®Google Scholar
• Polizzi, K. M., A. S. Bommarius, J. M. Broering, and J. F. Chaparro-Riggers. 2007. Stability of biocatalysts. Current Opinion in Chemical Biology 11 (2):220–5. doi: 10.1016/j.cbpa.2007.01.685.
   PubMed Web of Science ®Google Scholar
• Reetz, M. T., and J. D. Carballeira. 2007. Iterative saturation mutagenesis (ISM) for rapid directed evolution of functional enzymes. Nature Protocols 2 (4):891–903. doi: 10.1038/nprot.2007.72.
   PubMed Web of Science ®Google Scholar
• Rothschild, L. J., and R. L. Mancinelli. 2001. Life in extreme environments. Nature 409 (6823):1092–101. doi: 10.1038/35059215.
   PubMed Web of Science ®Google Scholar
• Sakai, G., K. Kojima, K. Mori, Y. Oonishi, and K. Sode. 2015. Stabilization of fungi-derived recombinant FAD-dependent glucose dehydrogenase by introducing a disulfide bond. Biotechnology Letters 37 (5):1091–9. doi: 10.1007/s10529-015-1774-8.
   PubMed Web of Science ®Google Scholar
• Samson, M., T. Yang, M. Omar, M. Xu, X. Zhang, U. Alphonse, and Z. Rao. 2018. Improved thermostability and catalytic efficiency of overexpressed catalase from B. pumilus ML 413 (KatX2) by introducing disulfide bond C286-C289. Enzyme and Microbial Technology 119:10–6. doi: 10.1016/j.enzmictec.2018.08.002.
   PubMed Web of Science ®Google Scholar
• Schymkowitz, J., J. Borg, F. Stricher, R. Nys, F. Rousseau, and L. Serrano. 2005. The FoldX web server: An online force field. Nucleic Acids Research 33 (Web Server issue):W382–388. doi: 10.1093/nar/gki387.
   PubMedGoogle Scholar
• Scott, K. A., D. O. V. Alonso, S. Sato, A. R. Fersht, and V. Daggett. 2007. Conformational entropy of alanine versus glycine in protein denatured states. Proceedings of the National Academy of Sciences of the United States of America 104 (8):2661–6. doi: 10.1073/pnas.0611182104.
   PubMed Web of Science ®Google Scholar
• Shi, H., Q. Gan, D. Jiang, Y. Wu, Y. Yin, H. Hou, H. Chen, Y. Xu, L. Miao, Z. Yang, et al. 2019. Biochemical characterization and mutational studies of a thermostable uracil DNA glycosylase from the hyperthermophilic euryarchaeon Thermococcus barophilus Ch5. International Journal of Biological Macromolecules 134:846–55. doi: 10.1016/j.ijbiomac.2019.05.073.
   PubMed Web of Science ®Google Scholar
• Strickler, S. S., A. V. Gribenko, A. V. Gribenko, T. R. Keiffer, J. Tomlinson, T. Reihle, V. V. Loladze, and G. I. Makhatadze. 2006. Protein stability and surface electrostatics: A charged relationship. Biochemistry 45 (9):2761–6. doi: 10.1021/bi0600143.
   PubMed Web of Science ®Google Scholar
• Sumbalova, L., J. Stourac, T. Martinek, D. Bednar, and J. Damborsky. 2018. HotSpot Wizard 3.0: Web server for automated design of mutations and smart libraries based on sequence input information. Nucleic Acids Research 46 (W1):W356–362. doi: 10.1093/nar/gky417.
   PubMed Web of Science ®Google Scholar
• Sun, J., M. Liu, Y. Xu, Z. Xu, L. Pan, and H. Gao. 2005. Improvement of the thermostability and catalytic activity of a mesophilic family 11 xylanase by N-terminus replacement. Protein Expression and Purification 42 (1):122–30. doi: 10.1016/j.pep.2005.03.009.
   PubMed Web of Science ®Google Scholar
• Sun, Z., Q. Liu, G. Qu, Y. Feng, and M. T. Reetz. 2019. Utility of B-Factors in protein science: Interpreting rigidity, flexibility, and internal motion and engineering thermostability. Chemical Reviews 119 (3):1626–65. doi: 10.1021/acs.chemrev.8b00290.
   PubMed Web of Science ®Google Scholar
• Suresh, A., D. Ramgopal, K. Gopinath, J. Arun, P. SundarRajan, and A. Bhatnagar. 2021. Recent advancements in the synthesis of novel thermostable biocatalysts and their applications in commercially important chemoenzymatic conversion processes. Bioresource Technology 323:124558. doi: 10.1016/j.biortech.2020.124558.
   PubMed Web of Science ®Google Scholar
• Szilágyi, A., and P. Závodszky. 2000. Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: Results of a comprehensive survey. Structure (London, England: 1993) 8 (5):493–504. doi: 10.1016/S0969-2126(00)00133-7.
   PubMed Web of Science ®Google Scholar
• Tachibana, Y., A. Kuramura, N. Shirasaka, Y. Suzuki, T. Yamamoto, S. Fujiwara, M. Takagi, and T. Imanaka. 1999. Purification and characterization of an extremely thermostable cyclomaltodextrin glucanotransferase from a newly isolated hyperthermophilic archaeon, a Thermococcus sp. Applied and Environmental Microbiology 65 (5):1991–7. doi: 10.1128/AEM.65.5.1991-1997.1999.
   PubMed Web of Science ®Google Scholar
• Tang, F., D. Chen, B. Yu, Y. Luo, P. Zheng, X. Mao, J. Yu, and J. He. 2017. Improving the thermostability of Trichoderma reesei xylanase 2 by introducing disulfide bonds. Electronic Journal of Biotechnology 26:52–9. doi: 10.1016/j.ejbt.2017.01.001.
   Web of Science ®Google Scholar
• Tian, J., P. Wang, S. Gao, X. Chu, N. Wu, and Y. Fan. 2010. Enhanced thermostability of methyl parathion hydrolase from Ochrobactrum sp. M231 by rational engineering of a glycine to proline mutation. The FEBS Journal 277 (23):4901–8. doi: 10.1111/j.1742-4658.2010.07895.x.
   PubMed Web of Science ®Google Scholar
• Tompa, D. R., M. M. Gromiha, and K. Saraboji. 2016. Contribution of main chain and side chain atoms and their locations to the stability of thermophilic proteins. Journal of Molecular Graphics & Modelling 64:85–93. doi: 10.1016/j.jmgm.2016.01.001.
   PubMed Web of Science ®Google Scholar
• Tong, L., S. Liu, J. Li, G. Du, and J. Chen. 2018. Improvement of TGase thermal stability through site-directed mutagenesis based on analysis of folding free energy. Journal of Food Science and Biotechnology 37 (12):1278–83. doi: 10.3969/j.issn.1673-1689.2018.12.008. (In Chinese).
   Google Scholar
• Toogood, H. S., E. J. Hollingsworth, R. C. Brown, I. N. Taylor, S. J. Taylor, R. McCague, and J. A. Littlechild. 2002. A thermostable L-aminoacylase from Thermococcus litoralis: Cloning, overexpression, characterization, and applications in biotransformations. Extremophiles: Life under Extreme Conditions 6 (2):111–22. doi: 10.1007/s007920100230.
   PubMed Web of Science ®Google Scholar
• Ueno, K., M. Ibarra, and T. Gojobori. 2016. Structural adaption of extremophile proteins to the environments with special reference to hydrophobic networks. Ecological Genetics and Genomics 1:1–5. doi: 10.1016/j.egg.2015.10.001.
   Google Scholar
• van den Burg, B. 2003. Extremophiles as a source for novel enzymes. Current Opinion in Microbiology 6 (3):213–8. doi: 10.1016/S1369-5274(03)00060-2.
   PubMed Web of Science ®Google Scholar
• Vasudevan, U., A. Jaiswal, S. Krishna, and A. Pandey. 2019. Thermostable phytase in feed and fuel industries. Bioresource Technology 278:400–7. doi: 10.1016/j.biortech.2019.01.065.
   PubMed Web of Science ®Google Scholar
• Verma, S., G. K. Meghwanshi, and R. Kumar. 2021. Current perspectives for microbial lipases from extremophiles and metagenomics. Biochimie 182:23–36. doi: 10.1016/j.biochi.2020.12.027.
   PubMed Web of Science ®Google Scholar
• Vieille, C., and G. J. Zeikus. 2001. Hyperthermophilic enzymes: Sources, uses, and molecular mechanisms for thermostability. Microbiology and Molecular Biology Reviews: MMBR 65 (1):1–43. doi: 10.1128/MMBR.65.1.1-43.2001.
   PubMed Web of Science ®Google Scholar
• Vieira, D. S., and L. Degrève. 2009. An insight into the thermostability of a pair of xylanases: The role of hydrogen bonds. Molecular Physics 107 (1):59–69. doi: 10.1080/00268970902717959.
   Web of Science ®Google Scholar
• Vogt, G., S. Woell, and P. Argos. 1997. Protein thermal stability, hydrogen bonds, and ion pairs. Journal of Molecular Biology 269 (4):631–43. doi: 10.1006/jmbi.1997.1042.
   PubMed Web of Science ®Google Scholar
• Wang, K., H. Luo, J. Tian, O. Turunen, H. Huang, P. Shi, H. Hua, C. Wang, S. Wang, and B. Yao. 2014. Thermostability improvement of a streptomyces xylanase by introducing proline and glutamic acid residues. Applied and Environmental Microbiology 80 (7):2158–65. doi: 10.1128/AEM.03458-13.
   PubMed Web of Science ®Google Scholar
• Wang, R., S. Wang, Y. Xu, and X. Yu. 2020. Enhancing the thermostability of Rhizopus chinensis lipase by rational design and MD simulations. International Journal of Biological Macromolecules 160:1189–200. doi: 10.1016/j.ijbiomac.2020.05.243.
   PubMed Web of Science ®Google Scholar
• Wang, X., Y. Nie, and Y. Xu. 2019. Industrially produced pullulanases with thermostability: Discovery, engineering, and heterologous expression. Bioresource Technology 278:360–71. doi: 10.1016/j.biortech.2019.01.098.
   PubMed Web of Science ®Google Scholar
• Wang, Y., Z. Fu, H. Huang, H. Zhang, B. Yao, H. Xiong, and O. Turunen. 2012. Improved thermal performance of Thermomyces lanuginosus GH11 xylanase by engineering of an N-terminal disulfide bridge. Bioresource Technology 112:275–9. doi: 10.1016/j.biortech.2012.02.092.
   PubMed Web of Science ®Google Scholar
• Waterhouse, A., M. Bertoni, S. Bienert, G. Studer, G. Tauriello, R. Gumienny, F. T. Heer, T. A. P. de Beer, C. Rempfer, L. Bordoli, et al. 2018. SWISS-MODEL: Homology modelling of protein structures and complexes. Nucleic Acids Research 46 (W1):W296–303. doi: 10.1093/nar/gky427.
   PubMed Web of Science ®Google Scholar
• Wen, S., T. Tan, and H. Zhao. 2012. Improving the thermostability of lipase Lip2 from Yarrowia lipolytica. Journal of Biotechnology 164 (2):248–53. doi: 10.1016/j.jbiotec.2012.08.023.
   PubMed Web of Science ®Google Scholar
• Wu, H., M. Chen, C. Guang, W. Zhang, and W. Mu. 2020. Identification of a novel recombinant D-lyxose isomerase from Thermoprotei archaeon with high thermostable, weak-acid and nickel ion dependent properties. International Journal of Biological Macromolecules 164:1267–74. doi: 10.1016/j.ijbiomac.2020.07.222.
   PubMed Web of Science ®Google Scholar
• Wu, H., W. Zhang, and W. Mu. 2019. Recent studies on the biological production of D-mannose. Applied Microbiology and Biotechnology 103 (21–22):8753–61. doi: 10.1007/s00253-019-10151-3.
   PubMed Web of Science ®Google Scholar
• Xiao, Z., H. Bergeron, S. Grosse, M. Beauchemin, M.-L. Garron, D. Shaya, T. Sulea, M. Cygler, and P. C. K. Lau. 2008. Improvement of the thermostability and activity of a pectate lyase by single amino acid substitutions, using a strategy based on melting-temperature-guided sequence alignment. Applied and Environmental Microbiology 74 (4):1183–9. doi: 10.1128/AEM.02220-07.
   PubMed Web of Science ®Google Scholar
• Xing, H., G. Zou, C. Liu, S. Chai, X. Yan, X. Li, R. Liu, Y. Yang, and Z. Zhou. 2021. Improving the thermostability of a GH11 xylanase by directed evolution and rational design guided by B-factor analysis. Enzyme and Microbial Technology 143:109720. doi: 10.1016/j.enzmictec.2020.109720.
   PubMed Web of Science ®Google Scholar
• Xu, J., W. A. Baase, E. Baldwin, and B. W. Matthews. 1998. The response of T4 lysozyme to large-to-small substitutions within the core and its relation to the hydrophobic effect. Protein Science 7 (1):158–77. doi: 10.1002/pro.5560070117.
   PubMed Web of Science ®Google Scholar
• Xu, P., Z. Ni, M. Zong, X. Ou, J. Yang, and W. Lou. 2020. Improving the thermostability and activity of Paenibacillus pasadenensis chitinase through semi-rational design. International Journal of Biological Macromolecules 150:9–15. doi: 10.1016/j.ijbiomac.2020.02.033.
   PubMed Web of Science ®Google Scholar
• Xu, W., J. Peng, W. Zhang, T. Zhang, C. Guang, and W. Mu. 2019. Enhancement of the Brenneria sp. levansucrase thermostability by site-directed mutagenesis at Glu404 located at the “-TEAP-” residue motif. Journal of Biotechnology 290:1–9. doi: 10.1016/j.jbiotec.2018.11.021.
   PubMed Web of Science ®Google Scholar
• Xu, Z., T. Cai, N. Xiong, S. Zou, Y. Xue, and Y. Zheng. 2018. Engineering the residues on “A” surface and C-terminal region to improve thermostability of nitrilase. Enzyme and Microbial Technology 113:52–8. doi: 10.1016/j.enzmictec.2018.03.001.
   PubMed Web of Science ®Google Scholar
• Xu, Z., Y. Cen, S. Zou, Y. Xue, and Y. Zheng. 2020. Recent advances in the improvement of enzyme thermostability by structure modification. Critical Reviews in Biotechnology 40 (1):83–98. doi: 10.1080/07388551.2019.1682963.
   PubMed Web of Science ®Google Scholar
• Yi, Z., X. Pei, and Z. Wu. 2011. Introduction of glycine and proline residues onto protein surface increases the thermostability of endoglucanase CelA from Clostridium thermocellum. Bioresource Technology 102 (3):3636–8. doi: 10.1016/j.biortech.2010.11.043.
   PubMed Web of Science ®Google Scholar
• Yin, X., J. Li, C. Wang, D. Hu, Q. Wu, Y. Gu, and M. Wu. 2015. Improvement in the thermostability of a type A feruloyl esterase, AuFaeA, from Aspergillus usamii by iterative saturation mutagenesis. Applied Microbiology and Biotechnology 99 (23):10047–56. doi: 10.1007/s00253-015-6889-2.
   PubMed Web of Science ®Google Scholar
• Yoneda, K., M. Yoshioka, H. Sakuraba, T. Araki, and T. Ohshima. 2020. Structural and biochemical characterization of an extremely thermostable FMN-dependent NADH-indigo reductase from Bacillus smithii. International Journal of Biological Macromolecules 164:3259–67. doi: 10.1016/j.ijbiomac.2020.08.197.
   PubMed Web of Science ®Google Scholar
• Yu, H., and H. Huang. 2014. Engineering proteins for thermostability through rigidifying flexible sites. Biotechnology Advances 32 (2):308–15. doi: 10.1016/j.biotechadv.2013.10.012.
   PubMed Web of Science ®Google Scholar
• Yu, H., Y. Zhao, C. Guo, Y. Gan, and H. Huang. 2015. The role of proline substitutions within flexible regions on thermostability of luciferase. Biochimica et Biophysica Acta 1854 (1):65–72. doi: 10.1016/j.bbapap.2014.10.017.
   PubMed Web of Science ®Google Scholar
• Zeiske, T., K. A. Stafford, and A. G. Palmer. 2016. Thermostability of enzymes from molecular dynamics simulations. Journal of Chemical Theory and Computation 12 (6):2489–92. doi: 10.1021/acs.jctc.6b00120.
   PubMed Web of Science ®Google Scholar
• Zhang, S., and Z. Wu. 2011. Identification of amino acid residues responsible for increased thermostability of feruloyl esterase A from Aspergillus niger using the PoPMuSiC algorithm. Bioresource Technology 102 (2):2093–6. doi: 10.1016/j.biortech.2010.08.019.
   PubMed Web of Science ®Google Scholar
• Zhang, W., M. Jia, S. Yu, T. Zhang, L. Zhou, B. Jiang, and W. Mu. 2016. Improving the thermostability and catalytic efficiency of the d-psicose 3-epimerase from Clostridium bolteae ATCC BAA-613 using site-directed mutagenesis. Journal of Agricultural and Food Chemistry 64 (17):3386–93. doi: 10.1021/acs.jafc.6b01058.
   PubMed Web of Science ®Google Scholar
• Zhang, W., Y. Zhang, J. Huang, Z. Chen, T. Zhang, C. Guang, and W. Mu. 2018. Thermostability improvement of the d-allulose 3-epimerase from Dorea sp. CAG317 by site-directed mutagenesis at the interface regions. Journal of Agricultural and Food Chemistry 66 (22):5593–601. doi: 10.1021/acs.jafc.8b01200.
   PubMed Web of Science ®Google Scholar
• Zhang, Y., T. Geary, and B. K. Simpson. 2019. Genetically modified food enzymes: A review. Current Opinion in Food Science 25:14–8. doi: 10.1016/j.cofs.2019.01.002.
   Web of Science ®Google Scholar
• Zhang, Z., L. Wang, Y. Gao, J. Zhang, M. Zhenirovskyy, and E. Alexov. 2012. Predicting folding free energy changes upon single point mutations. Bioinformatics (Oxford, England) 28 (5):664–71. doi: 10.1093/bioinformatics/bts005.
   PubMed Web of Science ®Google Scholar
• Zhang, Z., J. Yang, P. Xie, Y. Gao, J. Bai, C. Zhang, L. Liu, Q. Wang, and X. Gao. 2020. Characterization of a thermostable phytase from Bacillus licheniformis WHU and further stabilization of the enzyme through disulfide bond engineering. Enzyme and Microbial Technology 142:109679. doi: 10.1016/j.enzmictec.2020.109679.
   PubMed Web of Science ®Google Scholar
• Zhou, Y., B. Pérez, W. Hao, J. Lv, R. Gao, and Z. Guo. 2019. The additive mutational effects from surface charge engineering: A compromise between enzyme activity, thermostability and ionic liquid tolerance. Biochemical Engineering Journal 148:195–204. doi: 10.1016/j.bej.2018.07.020.
   Web of Science ®Google Scholar
• Zhou, C., Y. Xue, and Y. Ma. 2010. Enhancing the thermostability of alpha-glucosidase from Thermoanaerobacter tengcongensis MB4 by single proline substitution. Journal of Bioscience and Bioengineering 110 (1):12–7. doi: 10.1016/j.jbiosc.2009.12.002.
   PubMed Web of Science ®Google Scholar
• Zouari Ayadi, D., A. Hmida Sayari, H. Ben Hlima, S. Ben Mabrouk, M. Mezghani, and S. Bejar. 2015. Improvement of Trichoderma reesei xylanase II thermal stability by serine to threonine surface mutations. International Journal of Biological Macromolecules 72:163–70. doi: 10.1016/j.ijbiomac.2014.08.014.
   PubMed Web of Science ®Google Scholar