Strategies for tailoring pH performances of glycoside hydrolases

References

• Watanabe M, Matsuzawa T, Yaoi K. Rational protein design for thermostabilization of glycoside hydrolases based on structural analysis. Appl Microbiol Biotechnol. 2018;102(20):8677–8684.
   PubMed Web of Science ®Google Scholar
• Lombard V, Golaconda Ramulu H, Drula E, et al. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014;42(Database issue):D490–D495.
   PubMedGoogle Scholar
• Koshland DE. Stereochemistry and the mechanism of enzymatic reactions. Biol Rev. 1953;28(4):416–436.
   Web of Science ®Google Scholar
• Vuong TV, Wilson DB. Glycoside hydrolases: catalytic base/nucleophile diversity. Biotechnol Bioeng. 2010;107(2):195–205.
   PubMed Web of Science ®Google Scholar
• Vocadlo DJ, Davies GJ. Mechanistic insights into glycosidase chemistry. Curr Opin Chem Biol. 2008;12(5):539–555.
   PubMed Web of Science ®Google Scholar
• Bu L, Crowley MF, Himmel ME, et al. Computational investigation of the pH dependence of loop flexibility and catalytic function in glycoside hydrolases. J Biol Chem. 2013;288(17):12175–12186.
   PubMed Web of Science ®Google Scholar
• Paës G, Berrin J-G, Beaugrand J. GH11 xylanases: structure/function/properties relationships and applications. Biotechnol Adv. 2012;30(3):564–592.
   PubMed Web of Science ®Google Scholar
• Sharma A, Kawarabayasi Y, Satyanarayana T. Acidophilic bacteria and archaea: acid stable biocatalysts and their potential applications. Extremophiles. 2012;16(1):1–19.
   PubMed Web of Science ®Google Scholar
• Fujinami S, Fujisawa M. Industrial applications of alkaliphiles and their enzymes-past, present and future. Environ Technol. 2010;31(8–9):845–856.
   PubMed Web of Science ®Google Scholar
• Nielsen JE. Analysing the pH-dependent properties of proteins using pKa calculations. J Mol Graph Model. 2007;25(5):691–699.
   PubMed Web of Science ®Google Scholar
• Harris TK, Turner GJ. Structural basis of perturbed pKa values of catalytic groups in enzyme active sites. IUBMB Life. 2002;53(2):85–98.
   PubMed Web of Science ®Google Scholar
• Urry DW, Gowda DC, Peng S, et al. Nanometric design of extraordinary hydrophobic-induced pKa shifts for aspartic acid: relevance to protein mechanisms. Biopolymers. 1994;34(7):889–896.
   PubMed Web of Science ®Google Scholar
• Rostkowski M, Olsson MHM, Søndergaard CR, et al. Graphical analysis of pH-dependent properties of proteins predicted using PROPKA. BMC Struct Biol. 2011;11:6.
   PubMed Web of Science ®Google Scholar
• Nielsen JE, Borchert TV, Vriend G. The determinants of alpha-amylase pH-activity profiles. Protein Eng. 2001;14(7):505–512.
   PubMedGoogle Scholar
• Ishikawa K, Matsui I, Honda K. Optimum pH control mechanism for porcine pancreatic alpha-amylase. Biosci Biotechnol Biochem. 1995;59(6):1175–1176.
   PubMed Web of Science ®Google Scholar
• Tollinger M, Crowhurst KA, Kay LE, et al. Site-specific contributions to the pH dependence of protein stability. Proc Natl Acad Sci USA. 2003;100(8):4545–4550.
   PubMed Web of Science ®Google Scholar
• Lee SJ, Lee SJ, Lee YJ, et al. Homologous alkalophilic and acidophilic L-arabinose isomerases reveal region-specific contributions to the pH dependence of activity and stability. Appl Environ Microbiol. 2012;78(24):8813–8816.
   PubMed Web of Science ®Google Scholar
• Becker D, Braet C, Brumer H, et al. Engineering of a glycosidase family 7 cellobiohydrolase to more alkaline pH optimum: the pH behaviour of Trichoderma reesei Cel7A and its E223S/A224H/L225V/T226A/D262G mutant. Biochem J. 2001;356(1):19–30.
   PubMedGoogle Scholar
• Nielsen JE, Beier L, Otzen D, et al. Electrostatics in the active site of an alpha-amylase. Eur J Biochem. 1999;264(3):816–824.
   PubMedGoogle Scholar
• Joshi MD, Sidhu G, Pot I, et al. Hydrogen bonding and catalysis: a novel explanation for how a single amino acid substitution can change the ph optimum of a glycosidase. J Mol Biol. 2000;299(1):255–279.
   PubMed Web of Science ®Google Scholar
• Sajedi RH, Taghdir M, Naderi-Manesh H, et al. Nucleotide sequence, structural investigation and homology modeling studies of a Ca2+-independent alpha-amylase with acidic pH-profile. J Steroid Biochem. 2007;40:315–324.
   Google Scholar
• Huang Y, Krauss G, Cottaz S, et al. A highly acid-stable and thermostable endo-beta-glucanase from the thermoacidophilic archaeon Sulfolobus solfataricus. Biochem J. 2005;385(Pt 2):581–588.
   PubMedGoogle Scholar
• Zhao J, Shi P, Luo H, et al. An acidophilic and acid-stable beta-mannanase from phialophora sp. p13 with high mannan hydrolysis activity under simulated gastric conditions. J Agric Food Chem. 2010;58(5):3184–3190.
   PubMed Web of Science ®Google Scholar
• Juturu V, Wu JC. Microbial xylanases: Engineering, production and industrial applications. Biotechnol Adv. 2012;30(6):1219–1227.
   PubMed Web of Science ®Google Scholar
• Fushinobu S, Ito K, Konno M, et al. Crystallographic and mutational analyses of an extremely acidophilic and acid-stable xylanase: biased distribution of acidic residues and importance of Asp37 for catalysis at low pH. Protein Eng. 1998;11(12):1121–1128.
   PubMedGoogle Scholar
• Schwermann B, Pfau K, Liliensiek B, et al. Purification, properties and structural aspects of a thermoacidophilic alpha-amylase from Alicyclobacillus acidocaldarius atcc 27009. Insight into acidostability of proteins. Eur J Biochem. 1994;226(3):981–991.
   PubMedGoogle Scholar
• Lemos Esteves F, Ruelle V, Lamotte-Brasseur J, et al. Acidophilic adaptation of family 11 endo-beta-1,4-xylanases: modeling and mutational analysis. Protein Sci. 2004;13(5):1209–1218.
   PubMed Web of Science ®Google Scholar
• Ge HH, Qiu Y, Yi ZW, et al. π-π stacking interaction is a key factor for the stability of GH11 xylanases at low pH. Int J Biol Macromol. 2019;124:895–902.
   PubMed Web of Science ®Google Scholar
• Shirai T, Ishida H, Noda JI, et al. Crystal structure of alkaline cellulase K: insight into the alkaline adaptation of an industrial enzyme. J Mol Biol. 2001;310(5):1079–1087.
   PubMed Web of Science ®Google Scholar
• Bai W, Zhou C, Zhao Y, et al. Structural insight into and mutational analysis of family 11 xylanases: implications for mechanisms of higher pH catalytic adaptation. PLOS One. 2015;10(7):e0132834.
   PubMed Web of Science ®Google Scholar
• Mamo G, Thunnissen M, Hatti-Kaul R, et al. An alkaline active xylanase: Insights into mechanisms of high pH catalytic adaptation. Biochimie. 2009;91(9):1187–1196.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Zhang Y, Cao Y, et al. Structural analysis of alkaline β-mannanase from alkaliphilic bacillus sp. N16-5: implications for adaptation to alkaline conditions. PLOS One. 2011;6(1):e14608.
   PubMed Web of Science ®Google Scholar
• Shirai T, Suzuki A, Yamane T, et al. High-resolution crystal structure of M-protease: phylogeny aided analysis of the high-alkaline adaptation mechanism. Protein Eng. 1997;10(6):627–634.
   PubMedGoogle Scholar
• Ma F, Xie Y, Luo M, et al. Sequence homolog-based molecular engineering for shifting the enzymatic pH optimum. Synth. Syst. Biotechnol. 2016;1(3):195–206.
   PubMed Web of Science ®Google Scholar
• Tenu JP, Viratelle OM, Garnier J, et al. pH dependence of the activity of beta-galactosidase from Escherichia coli. Eur J Biochem. 1971;20(3):363–370.
   PubMedGoogle Scholar
• Xie X, Cane DE. pH-Rate profiles establish that polyketide synthase dehydratase domains utilize a single-base mechanism. Org Biomol Chem. 2018;16(47):9165–9170.
   PubMed Web of Science ®Google Scholar
• Li C, Zhang R, Wang J, et al. Protein engineering for improving and diversifying natural product biosynthesis. Trends Biotechnol. 2020;38(7):729–744.
   PubMed Web of Science ®Google Scholar
• Perperopoulou F, Pouliou F, Labrou NE. Recent advances in protein engineering and biotechnological applications of glutathione transferases. Crit Rev Biotechnol. 2018;38(4):511–528.
   PubMed Web of Science ®Google Scholar
• Kumar A, Singh S. Directed evolution: tailoring biocatalysts for industrial applications. Crit Rev Biotechnol. 2013;33(4):365–378.
   PubMed Web of Science ®Google Scholar
• Li YX, Yi P, Yan QJ, et al. Directed evolution of a β-mannanase from rhizomucor miehei to improve catalytic activity in acidic and thermophilic conditions. Biotechnol Biofuels. 2017;10:143.
   PubMed Web of Science ®Google Scholar
• Bessler C, Schmitt J, Maurer KH, et al. Directed evolution of a bacterial alpha-amylase: toward enhanced pH-performance and higher specific activity. Protein Sci. 2003;12(10):2141–2149.
   PubMed Web of Science ®Google Scholar
• Chiu FWY, Stavrakis S. High-throughput droplet-based microfluidics for directed evolution of enzymes. Electrophoresis. 2019;40(21):2860–2872.
   PubMed Web of Science ®Google Scholar
• Ding Y, Howes PD, deMello AJ. Recent advances in droplet microfluidics. Anal Chem. 2020;92(1):132–149.
   PubMed Web of Science ®Google Scholar
• Chica RA, Doucet N, Pelletier JN. Semi-rational approaches to engineering enzyme activity: combining the benefits of directed evolution and rational design. Curr Opin Biotechnol. 2005;16(4):378–384.
   PubMed Web of Science ®Google Scholar
• Shakeel T, Gupta M, Fatma Z, et al. A consensus-guided approach yields a heat-stable alkane-producing enzyme and identifies residues promoting thermostability. J Biol Chem. 2018;293(24):9148–9161.
   PubMed Web of Science ®Google Scholar
• Shivange AV, Hoeffken HW, Haefner S, et al. Protein consensus-based surface engineering (ProCoS): a computer-assisted method for directed protein evolution. Biotechniques. 2016;61(6):305–314.
   PubMed Web of Science ®Google Scholar
• Xu W, Zhang W, Zhang T, et al. L-arabinose isomerases: characteristics, modification, and application. Trends Food Sci Tech. 2018;78:25–33.
   Web of Science ®Google Scholar
• Tishkov VI, Gusakov AV, Cherkashina AS, et al. Engineering the pH-optimum of activity of the GH12 family endoglucanase by site-directed mutagenesis. Biochimie. 2013;95(9):1704–1710.
   PubMed Web of Science ®Google Scholar
• Li S, Yang Q, Tang B. Improving the thermostability and acid resistance of rhizopus oryzae α-amylase by using multiple sequence alignment based site-directed mutagenesis. Biotechnol Appl Biochem. 2020;67(4):677–684.
   PubMed Web of Science ®Google Scholar
• Bartlett GJ, Porter CT, Borkakoti N, et al. Analysis of catalytic residues in enzyme active sites. J Mol Biol. 2002;324(1):105–121.
   PubMed Web of Science ®Google Scholar
• Yang, H., Liu, L., Li, J, et al. Rational design to improve protein thermostability: recent advances and prospects. Chembioeng Rev. 2015;2(2):87–94.
   Google Scholar
• Ludwiczek ML, D'Angelo I, Yalloway GN, et al. Strategies for modulating the pH-dependent activity of a family 11 glycoside hydrolase. Biochemistry. 2013;52(18):3138–3156.
   PubMed Web of Science ®Google Scholar
• Lu Y, Zen KC, Muthukrishnan S, et al. Site-directed mutagenesis and functional analysis of active site acidic amino acid residues D142, D144 and E146 in manduca sexta (tobacco hornworm) chitinase. Insect Biochem Molec. 2002;32(11):1369–1382.
   PubMed Web of Science ®Google Scholar
• Pokhrel S, Joo JC, Yoo YJ. Shifting the optimum pH of Bacillus circulans xylanase towards acidic side by introducing arginine. Biotechnol Bioproc E. 2013;18(1):35–42.
   Web of Science ®Google Scholar
• Wind RD, Uitdehaag JC, Buitelaar RM, et al. Engineering of cyclodextrin product specificity and pH optima of the thermostable cyclodextrin glycosyltransferase from Thermoanaerobacterium thermosulfurigenes EM1. J Biol Chem. 1998;273(10):5771–5779.
   PubMed Web of Science ®Google Scholar
• Pace CN, Fu H, Lee Fryar K, et al. Contribution of hydrogen bonds to protein stability. Protein Sci. 2014;23(5):652–661.
   PubMed Web of Science ®Google Scholar
• Kuriki T, Imanaka T. The concept of the alpha-amylase family: structural similarity and common catalytic mechanism. J Biosci Bioeng. 1999;87(5):557–565.
   PubMed Web of Science ®Google Scholar
• Chen A, Xu T, Ge Y, et al. Hydrogen-bond-based protein engineering for the acidic adaptation of bacillus acidopullulyticus pullulanase. Enzyme Microb Technol. 2019;124:79–83.
   PubMed Web of Science ®Google Scholar
• Wang QY, Xie NZ, Du QS, et al. Active hydrogen bond network (AHBN) and applications for improvement of thermal stability and pH-sensitivity of pullulanase from Bacillus naganoensis. PLoS One. 2017;12(1):e0169080.
   PubMed Web of Science ®Google Scholar
• Yang H, Liu L, Shin HD, et al. 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. 2013;164(1):59–66.
   PubMed Web of Science ®Google Scholar
• Fang TY, Ford C. Protein engineering of Aspergillus awamori glucoamylase to increase its pH optimum. Protein Eng. 1998;11(5):383–388.
   PubMedGoogle Scholar
• Hirata A, Adachi M, Sekine A, et al. Structural and enzymatic analysis of soybean beta-amylase mutants with increased pH optimum. J Biol Chem. 2004;279(8):7287–7295.
   PubMed Web of Science ®Google Scholar
• Hirata A, Adachi M, Utsumi S, et al. Engineering of the pH optimum of Bacillus cereus beta-amylase: conversion of the pH optimum from a bacterial type to a higher-plant type. Biochemistry-US. 2004;43(39):12523–12531.
   PubMed Web of Science ®Google Scholar
• Russell AJ, Fersht AR. Rational modification of enzyme catalysis by engineering surface charge. Nature. 1987;328(6130):496–500.
   PubMed Web of Science ®Google Scholar
• Spector S, Wang M, Carp SA, et al. Rational modification of protein stability by the mutation of charged surface residues. Biochemistry-US. 2000;39(5):872–879.
   PubMed Web of Science ®Google Scholar
• Sokalingam S, Raghunathan G, Soundrarajan N, et al. A study on the effect of surface lysine to arginine mutagenesis on protein stability and structure using green fluorescent protein. PLOS One. 2012;7(7):e40410.
   PubMed Web of Science ®Google Scholar
• Strub C, Alies C, Lougarre A, et al. Mutation of exposed hydrophobic amino acids to arginine to increase protein stability. BMC Biochem. 2004;5:9.
   PubMedGoogle Scholar
• Jakob F, Martinez R, Mandawe J, et al. Surface charge engineering of a Bacillus gibsonii subtilisin protease. Appl Microbiol Biotechnol. 2013;97(15):6793–6802.
   PubMed Web of Science ®Google Scholar
• Li Q, Jiang T, Liu R, et al. Tuning the pH profile of β-glucuronidase by rational site-directed mutagenesis for efficient transformation of glycyrrhizin. Appl Microbiol Biotechnol. 2019;103(12):4813–4823.
   PubMed Web of Science ®Google Scholar
• Deng Z, Yang H, Shin HD, et al. Structure-based rational design and introduction of arginines on the surface of an alkaline α-amylase from Alkalimonas amylolytica for improved thermostability. Appl Microbiol Biotechnol. 2014;98(21):8937–8945.
   PubMed Web of Science ®Google Scholar
• Turunen O, Vuorio M, Fenel F, et al. Engineering of multiple arginines into the ser/thr surface of Trichoderma reesei endo-1,4-beta-xylanase II increases the thermotolerance and shifts the pH optimum towards alkaline pH. Protein Eng. 2002;15(2):141–145.
   PubMedGoogle Scholar
• Cockburn DW, Clarke AJ. Modulating the pH-activity profile of cellulase a from Cellulomonas fimi by replacement of surface residues. Protein Eng Des Sel. 2011;24(5):429–437.
   PubMed Web of Science ®Google Scholar
• Zheng F, Vermaas JV, Zheng J, et al. Activity and thermostability of GH5 endoglucanase chimeras from mesophilic and thermophilic parents. Appl Environ Microb. 2019;85:e02079–18.
   PubMed Web of Science ®Google Scholar
• Pardo I, Rodríguez-Escribano D, Aza P, et al. A highly stable laccase obtained by swapping the second cupredoxin domain. Sci Rep. 2018;8(1):15669.
   PubMedGoogle Scholar
• Xu Y, Liu Y, Rasool A, et al. Sequence editing strategy for improving performance of β-glucuronidase from Aspergillus terreus. Chem Eng Sci. 2017;167:145–153.
   Web of Science ®Google Scholar
• Du L, Pang H, Wang Z, et al. Characterization of an invertase with pH tolerance and truncation of its N-terminal to shift optimum activity toward neutral pH. PLOS One. 2013;8(4):e62306.
   PubMed Web of Science ®Google Scholar
• Saadat F. A review on chimeric xylanases: methods and conditions. 3 Biotech. 2017;7(1):67.
   PubMedGoogle Scholar
• Fan Z, Wagschal K, Lee CC, et al. The construction and characterization of two xylan-degrading chimeric enzymes. Biotechnol Bioeng. 2009;102(3):684–692.
   PubMed Web of Science ®Google Scholar
• Niu C, Luo H, Shi P, et al. N-Glycosylation improves the pepsin resistance of histidine acid phosphatase phytases by enhancing their stability at acidic pHs and reducing pepsin's accessibility to its cleavage sites. Appl Environ Microbiol. 2016;82(4):1004–1014.
   PubMed Web of Science ®Google Scholar
• Amann T, Schmieder V, Faustrup Kildegaard H, et al. Genetic engineering approaches to improve posttranslational modification of biopharmaceuticals in different production platforms. Biotechnol Bioeng. 2019;116(10):2778–2796.
   PubMed Web of Science ®Google Scholar
• Han C, Wang Q, Sun Y, et al. Improvement of the catalytic activity and thermostability of a hyperthermostable endoglucanase by optimizing N-glycosylation sites. Biotechnol Biofuels. 2020;13:30.
   PubMed Web of Science ®Google Scholar
• Ge F, Zhu L, Aang A, et al. Recent advances in enhanced enzyme activity, thermostability and secretion by N-glycosylation regulation in yeast. Biotechnol Lett. 2018;40(5):847–854.
   PubMed Web of Science ®Google Scholar
• Xia W, Xu X, Qian L, et al. Engineering a highly active thermophilic β-glucosidase to enhance its pH stability and saccharification performance. Biotechnol Biofuels. 2016;9:147.
   PubMed Web of Science ®Google Scholar
• Dotsenko AS, Gusakov AV, Rozhkova AM, et al. Effect of N-linked glycosylation on the activity and other properties of recombinant endoglucanase IIa (Cel5A) from penicillium verruculosum. Protein Eng Des Sel. 2016;29(11):495–502.
   PubMed Web of Science ®Google Scholar
• Gordon JC, Myers JB, Folta T, et al. H++: a server for estimating pKas and adding missing hydrogens to macromolecules. Nucleic Acids Res. 2005;33(Web Server issue):W368–W371.
   PubMed Web of Science ®Google Scholar
• Tynan-Connolly BM, Nielsen JE. Redesigning protein pKa values. Protein Sci. 2007;16(2):239–249.
   PubMed Web of Science ®Google Scholar
• Xiao K, Yu H. Rationalising pKa shifts in Bacillus circulans xylanase with computational studies. Phys Chem Chem Phys. 2016;18(44):30305–30312.
   PubMed Web of Science ®Google Scholar
• Wang CH, Liu XL, Huang RB, et al. Enhanced acidic adaptation of Bacillus subtilis Ca-independent alpha-amylase by rational engineering of pKa values. Biochem Eng J. 2018;139:146–153.
   Web of Science ®Google Scholar
• Beliën T, Joye IJ, Delcour JA, et al. Computational design-based molecular engineering of the glycosyl hydrolase family 11 B. subtilis XynA endoxylanase improves its acid stability. Protein Eng Des Sel. 2009;22(10):587–596.
   PubMed Web of Science ®Google Scholar
• Yang JH, Park JY, Kim SH, et al. Shifting pH optimum of Bacillus circulans xylanase based on molecular modeling. J Biotechnol. 2008;133(3):294–300.
   PubMed Web of Science ®Google Scholar
• Cheng F, Zhu L, Schwaneberg U. Directed evolution 2.0: improving and deciphering enzyme properties. Chem Commun (Camb)). 2015;51(48):9760–9772.
   PubMed Web of Science ®Google Scholar
• Fox RJ, Davis SC, Mundorff EC, et al. Improving catalytic function by ProSAR-driven enzyme evolution. Nat Biotechnol. 2007;25(3):338–344.
   PubMed Web of Science ®Google Scholar
• Novoa C, Dhoke GV, Mate DM, et al. KnowVolution of a fungal laccase toward alkaline pH. Chembiochem. 2019;20(11):1458–1466.
   PubMed Web of Science ®Google Scholar
• Körfer G, Novoa C, Kern J, et al. Directed evolution of an acid Yersinia mollaretii phytase for broadened activity at neutral pH. Appl Microbiol Biotechnol. 2018;102(22):9607–9620.
   PubMed Web of Science ®Google Scholar
• Wu X, Zhang Q, Zhang L, et al. Insights into the role of exposed surface charged residues in the alkali-tolerance of GH11 xylanase. Front Microbiol. 2020;11:872.
   PubMed Web of Science ®Google Scholar
• Jia H, Li Y, Liu Y, et al. Engineering a thermostable β-1,3-1,4-glucanase from paecilomyces thermophila to improve catalytic efficiency at acidic pH. J Biotechnol. 2012;159(1–2):50–55.
   PubMed Web of Science ®Google Scholar
• Park YM, Ghim SY. Enhancement of the activity and pH-performance of chitosanase from Bacillus cereus strains by DNA shuffling. Biotechnol Lett. 2009;31(9):1463–1467.
   PubMed Web of Science ®Google Scholar
• Li F, Xie J, Zhang X, et al. Improvement of the optimum pH of Aspergillus niger xylanase towards an alkaline pH by site-directed mutagenesis. J Microbiol Biotechnol. 2015;25(1):11–17.
   PubMed Web of Science ®Google Scholar
• Liu Y, Huang L, Jia L, et al. Improvement of the acid stability of Bacillus licheniformis alpha amylase by site-directed mutagenesis. Process Biochem. 2017;58:174–180.
   Web of Science ®Google Scholar
• Marana SR, Mendonça LMF, Andrade EHP, et al. The role of residues R97 and Y331 in modulating the pH optimum of an insect beta-glycosidase of family 1. Eur J Biochem. 2003;270(24):4866–4875.
   PubMedGoogle Scholar
• Kato A, Tanimoto S, Muraki Y, et al. Structural and functional properties of hen egg-white lysozyme deamidated by protein engineering. Biosci Biotechnol Biochem. 1992;56(9):1424–1428.
   PubMed Web of Science ®Google Scholar
• Zeng Y, Xu J, Fu X, et al. Effects of different carbohydrate-binding modules on the enzymatic properties of pullulanase. Int J Biol Macromol. 2019;137:973–981.
   PubMed Web of Science ®Google Scholar
• Somera AF, Pereira MG, Souza Guimarães LH, et al. Effect of glycosylation on the biochemical properties of beta-xylosidases from Aspergillus versicolor. J Microbiol. 2009;47(3):270–276.
   PubMed Web of Science ®Google Scholar
• Pokhrel S, Joo JC, Kim YH, et al. Rational design of a Bacillus circulans xylanase by introducing charged residue to shift the pH optimum. Process Biochem. 2012;47(12):2487–2493.
   Web of Science ®Google Scholar
• Sheldon RA, van Pelt S. Enzyme immobilisation in biocatalysis: why, what and how. Chem Soc Rev. 2013;42(15):6223–6235.
   PubMed Web of Science ®Google Scholar
• Rodrigues RC, Ortiz C, Berenguer-Murcia Á, et al. Modifying enzyme activity and selectivity by immobilization. Chem Soc Rev. 2013;42(15):6290–6307.
   PubMed Web of Science ®Google Scholar
• Jesionowski T, Zdarta J, Krajewska B. Enzyme immobilization by adsorption: a review. Adsorption. 2014;20(5–6):801–821.
   Web of Science ®Google Scholar
• Tüzmen N, Kalburcu T, Denizli A. α-Amylase immobilization onto dye attached magnetic beads: optimization and characterization. J Mol Catal B-Enzym. 2012;78:16–23.
   Web of Science ®Google Scholar
• Novick SJ, Rozzell JD. Immobilization of enzymes by covalent attachment. Microb. Enzym. Biotransformations. 2005;:247–271.
   Google Scholar
• Wang Y, Chen D, Wang G, et al. Immobilization of cellulase on styrene/maleic anhydride copolymer nanoparticles with improved stability against pH changes. Chem Eng J. 2018;336:152–159.
   Web of Science ®Google Scholar
• Karav S, Cohen JL, Barile D, et al. Recent advances in immobilization strategies for glycosidases. Biotechnol Prog. 2017;33(1):104–112.
   PubMed Web of Science ®Google Scholar
• Long J, Pan T, Xie Z, et al. Co-immobilization of β-fructofuranosidase and glucose oxidase improves the stability of Bi-enzymes and the production of lactosucrose. LWT-Food Sci Technol. 2020;128:109460.
   Web of Science ®Google Scholar
• Richards FM, Knowles JR. Glutaraldehyde as a protein cross-linking reagent. J Mol Biol. 1968;37(1):231–233.
   PubMed Web of Science ®Google Scholar
• Schoevaart R, Wolbers MW, Golubovic M, et al. Preparation, optimization, and structures of cross-linked enzyme aggregates (CLEAs). Biotechnol Bioeng. 2004;87(6):754–762.
   PubMed Web of Science ®Google Scholar
• Nadar SS, Muley AB, Ladole MR, et al. Macromolecular cross-linked enzyme aggregates (M-CLEAs) of α-amylase. Int J Biol Macromol. 2016;84:69–78.
   PubMed Web of Science ®Google Scholar
• Talekar S, Pandharbale A, Ladole M, et al. Carrier free co-immobilization of alpha amylase, glucoamylase and pullulanase as combined cross-linked enzyme aggregates (combi-CLEAs): a tri-enzyme biocatalyst with one pot starch hydrolytic activity. Bioresour Technol. 2013;147:269–275.
   PubMed Web of Science ®Google Scholar
• Klein MP, Hackenhaar CR, Lorenzoni ASG, et al. Chitosan crosslinked with genipin as support matrix for application in food process: support characterization and β-D-galactosidase immobilization. Carbohydr Polym. 2016;137:184–190.
   PubMed Web of Science ®Google Scholar
• Gürdaş S, Güleç HA, Mutlu M. Immobilization of aspergillus oryzae β-galactosidase onto duolite A568 resin via simple adsorption mechanism. Food Bioprocess Technol. 2012;5(3):904–911.
   Web of Science ®Google Scholar
• Lorenzoni ASG, Aydos LF, Klein MP, et al. Fructooligosaccharides synthesis by highly stable immobilized β-fructofuranosidase from Aspergillus aculeatus. Carbohydr Polym. 2014;103:193–197.
   PubMed Web of Science ®Google Scholar
• Díaz-Rodríguez A, Davis BG. Chemical modification in the creation of novel biocatalysts. Curr Opin Chem Biol. 2011;15(2):211–219.
   PubMed Web of Science ®Google Scholar
• Pedersen JN, Zhou Y, Guo Z, et al. Genetic and chemical approaches for surface charge engineering of enzymes and their applicability in biocatalysis: a review. Biotechnol Bioeng. 2019;116(7):1795–1812.
   PubMed Web of Science ®Google Scholar
• Goldstein L, Levin Y, Katchalski EA. A water-insoluble polyanionic derivative of trypsin. II. Effect of the polyelectrolyte carrier on the kinetic behavior of the bound trypsin. Biochemistry-US. 1964;3:1913–1919.
   PubMed Web of Science ®Google Scholar
• Nwagu TN, Okolo B, Aoyagi H, et al. Chemical modification with phthalic anhydride and chitosan: Viable options for the stabilization of raw starch digesting amylase from Aspergillus carbonarius. Int J Biol Macromol. 2017;99:641–647.
   PubMed Web of Science ®Google Scholar
• Murata H, Cummings CS, Koepsel RR, et al. Polymer-based protein engineering can rationally tune enzyme activity, pH-dependence, and stability. Biomacromolecules. 2013;14(6):1919–1926.
   PubMed Web of Science ®Google Scholar
• Liang X, Zhang W, Ran J, et al. Chemical modification of sweet potato β-amylase by mal-mPEG to improve its enzymatic characteristics. Molecules. 2018;23(11):2754.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Wang Q, Hess H. Increasing enzyme Cascade throughput by pH-engineering the microenvironment of individual enzymes. ACS Catal. 2017;7(3):2047–2051.
   Web of Science ®Google Scholar
• Wang L, Li X, Yuan L, et al. Improving the protein activity and stability under acidic conditions via site-specific conjugation of a pH-responsive polyelectrolyte. J Mater Chem B. 2015;3(3):498–504.
   PubMed Web of Science ®Google Scholar
• Cockburn DW, Vandenende C, Clarke AJ. Modulating the pH-activity profile of cellulase by substitution: replacing the general base catalyst aspartate with cysteinesulfinate in cellulase a from Cellulomonas fimi. Biochemistry-US. 2010;49(9):2042–2050.
   PubMed Web of Science ®Google Scholar
• Fierobe HP, Clarke AJ, Tull D, et al. Enzymatic properties of the cysteinesulfinic acid derivative of the catalytic-base mutant Glu400->Cys of glucoamylase from Aspergillus awamori. Biochemistry-US. 1998;37(11):3753–3759.
   PubMed Web of Science ®Google Scholar
• Pan S, Gu Z, Ding N, et al. Calcium and sodium ions synergistically enhance the thermostability of a maltooligosaccharide-forming amylase from Bacillus stearothermophilus STB04. Food Chem. 2019;283:170–176.
   PubMed Web of Science ®Google Scholar
• Stepankova V, Bidmanova S, Koudelakova T, et al. Strategies for stabilization of enzymes in organic solvents. ACS Catal. 2013;3(12):2823–2836.
   Web of Science ®Google Scholar
• Van-Thuoc D, Hashim SO, Hatti-Kaul R, et al. Ectoine-mediated protection of enzyme from the effect of pH and temperature stress: a study using Bacillus halodurans xylanase as a model. Appl Microbiol Biotechnol. 2013;97(14):6271–6278.
   PubMed Web of Science ®Google Scholar
• Liu M, Peng Y, Wang S, et al. Enhancement of anammox activity by addition of compatible solutes at high salinity conditions. Bioresour Technol. 2014;167:560–563.
   PubMed Web of Science ®Google Scholar
• Norouzi S, Birgani NH, Maghami P, et al. Improvement of PersiXyn2 activity and stability in presence of trehalose and proline as a natural osmolyte. Int J Biol Macromol. 2020;163:348–357.
   PubMed Web of Science ®Google Scholar
• Vathipadiekal V, Verma A, Rao M. Glycine-assisted enhancement of 1,4-beta-d-xylan xylanohydrolase activity at alkaline pH with a pH optimum shift. Biol Chem. 2007;388(1):61–65.
   PubMed Web of Science ®Google Scholar
• Arakawa T, Timasheff SN. Mechanism of protein salting in and salting out by divalent cation salts: balance between hydration and salt binding. Biochemistry-US. 1984;23(25):5912–5923.
   PubMed Web of Science ®Google Scholar
• Bowers EM, Ragland LO, Byers LD. Salt effects on beta-glucosidase: pH-profile narrowing. Biochim Biophys Acta. 2007;1774(12):1500–1507.
   PubMed Web of Science ®Google Scholar
• Bernal C, Rodríguez K, Martínez R. Integrating enzyme immobilization and protein engineering: an alternative path for the development of novel and improved industrial biocatalysts. Biotechnol Adv. 2018;36(5):1470–1480.
   PubMed Web of Science ®Google Scholar