Skip to main content
SpringerLink
Log in

Activation and thermal stabilization of a recombinant γ-glutamyltranspeptidase from Bacillus licheniformis ATCC 27811 by monovalent cations

  • Biotechnologically Relevant Enzymes and Proteins
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The regulation of enzyme activity through complexation with certain metal ions plays an important role in many biological processes. In addition to divalent metals, monovalent cations (MVCs) frequently function as promoters for efficient biocatalysis. Here, we examined the effect of MVCs on the enzymatic catalysis of a recombinant γ-glutamyltranspeptidase (BlrGGT) from Bacillus licheniformis ATCC 27,811 and the application of a metal-activated enzyme to L-theanine synthesis. The transpeptidase activity of BlrGGT was enhanced by Cs+ and Na+ over a broad range of concentrations with a maximum of 200 mM. The activation was essentially independent of the ionic radius, but K+ contributed the least to enhancing the catalytic efficiency. The secondary structure of BlrGGT remained mostly unchanged in the presence of different concentrations of MVCs, but there was a significant change in its tertiary structure under the same conditions. Compared with the control, the half-life (t1/2) of the Cs+-enriched enzyme at 60 and 65 °C was shown to increase from 16.3 and 4.0 min to 74.5 and 14.3 min, respectively. The simultaneous addition of Cs+ and Mg2+ ions exerted a synergistic effect on the activation of BlrGGT. This was adequately reflected by an improvement in the conversion of substrates to L-theanine by 3.3–15.1% upon the addition of 200 mM MgCl2 into a reaction mixture comprising the freshly desalted enzyme (25 μg/mL), 250 mM L-glutamine, 600 mM ethylamine, 200 mM each of the MVCs, and 50 mM borate buffer (pH 10.5). Taken together, our results provide interesting insights into the complexation of MVCs with BlrGGT and can therefore be potentially useful to the biocatalytic production of naturally occurring γ-glutamyl compounds.

Key points

• The transpeptidase activity of B. licheniformis γ-glutamyltranspeptidase can be activated by monovalent cations.

• The thermal stability of the enzyme was profoundly increased in the presence of 200 mM Cs+.

• The simultaneous addition of Cs+and Mg2+ions to the reaction mixture improves L-theanine production.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Ahmad A, Akhtar S, Bhakuni V (2001) Monovalent cation-induced conformational change in glucose oxidase leading to stabilization of the enzyme. Biochemistry 40:1945–1955

    Article  CAS  PubMed  Google Scholar 

  • Andersson CE, Mowbray SL (2002) Activation of ribokinase by monovalent cations. J Mol Biol 315(3):409–419

    Article  CAS  PubMed  Google Scholar 

  • Andreini C, Bertini I, Cavallaro G, Holliday GL, Thornton JM (2008) Metal ions in biological catalysis: from enzyme databases to general principles. J Biol Inorg Chem 13:1205–1218

    Article  CAS  PubMed  Google Scholar 

  • Asante-Appiah E, Skalka AM (1997) A metal-induced conformational change and activation of HIV-1 integrase. J Biol Chem 272:16196–16205

    Article  CAS  PubMed  Google Scholar 

  • Atanasov V, Stoykova S, Kolev H, Mitewa M, Petrova S, Pantcheva I (2013) Effect of some divalent metal ions on enzymatic activity of secreted phospholipase A2 (sPLA2) isolated from Bulgarian Vipera ammodytes meridionalis. Biotechnol Biotechnol Eq 27(5):4181–4185

    Article  CAS  Google Scholar 

  • Avery SV (1995) Caesium accumulation by microorganisms: uptake mechanisms, cation competition, compartmentalization and toxicity. J Ind Microbiol 14(2):76–84

    Article  CAS  PubMed  Google Scholar 

  • Bindal S, Gupta R (2014) L-Theanine synthesis using γ-glutamyl transpeptidase from Bacillus licheniformis ER-15. J Agric Food Chem 62:9151–9159

    Article  CAS  PubMed  Google Scholar 

  • Boanca G, Sand A, Okada T, Suzuki H, Kumagai H, Fukuyama K, Barycki JJ (2007) Autoprocessing of Helicobacter pylori γ-glutamyltranspeptidase leads to the formation of a threonine-threonine catalytic dyad. J Biol Chem 282:534–541

    Article  CAS  PubMed  Google Scholar 

  • Bougie I, Charpentier S, Bisaillon M (2003) Characterization of the metal ion binding properties of the hepatitis C virus RNA polymerase. J Biol Chem 278:3868–3875

    Article  CAS  PubMed  Google Scholar 

  • Castellano I, Merlino A (2012) γ-Glutamyl transpeptidases: sequence, structure, biochemical properties, and biotechnological applications. Cell Mol Life Sci 69:3381–3394

    Article  CAS  PubMed  Google Scholar 

  • Chaudhuri TK, Arai M, Terada TP, Ikura T, Kuwajima K (2000) Equilibrium and kinetic studies on folding of the authentic and recombinant forms of human α-lactalbumin by circular dichroism spectroscopy. Biochemistry 39:15643–15651

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Su L, Wu D, Wu J (2014) Application of recombinant Bacillus subtilis γ-glutamyltranspeptidase to the production of L-theanine. Process Biochem 49:1429–1439

    Article  CAS  Google Scholar 

  • Chen YY, Lo HF, Wang TF, Lin MG, Lin LL, Chi MC (2015) Enzymatic synthesis of γ-L-glutamyl-S-allyl-L-cysteine, a naturally occurring organosulfur compound from garlic, by Bacillus licheniformis γ-glutamyltranspeptidase. Enzyme Microb Technol 75–76:18–24

    PubMed  Google Scholar 

  • Chi MC, Chen YY, Lo HF, Lin LL (2012) Experimental evidence for the involvement of amino acid residue Glu398 in the autocatalytic processing of Bacillus licheniformis γ-glutamyltranspeptidase. FEBS Open Bio 2:298–304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chi MC, Huang YF, Lu BY, Lin MG, Wang TF, Lin LL (2021) Magnetic cross-linked enzyme aggregates of a transpeptidase-specialized variant (N450D) of Bacillus licheniformis γ-glutamyl transpeptidase: an efficient and stable biocatalyst for L-theanine synthesis. Catalysts 11:243

    Article  CAS  Google Scholar 

  • Chi MC, Liao TY, Lin MG, Lin LL, Wang TF (2020) Expression and physiochemical characterization of an N-terminal polyhistidine-tagged phosphotriesterase from the soil bacterium Brevundimonas diminuta. Biocatal Agric Biotechnol 29:101811

    Article  Google Scholar 

  • Chi MC, Lin MG, Huang YF, Chen YY, Wang TF, Lin LL (2019) Enzymatic synthesis of L-theanine from L-glutamine and ethylamine by Bacillus licheniformis γ-glutamyltranspeptidase and its mutants specialized in transpeptidase activity. Biocatal Agric Biotechnol 22:101393

    Article  Google Scholar 

  • Chi MC, Lo YH, Chen YY, Lin LL, Merlino A (2014) γ-Glutamyl transpeptidase architecture: effect of extra sequence deletion on autoprocessing, structure and stability of the protein from Bacillus licheniformis. Biochim Biophys Acta 1844:2290–2297

    Article  CAS  PubMed  Google Scholar 

  • Chi MC, Lo HF, Lin MG, Chen YY, Lin LL, Wang TF (2017) Application of Bacillus licheniformis γ-glutamyltranspeptidase to the biocatalytic synthesis of γ-glutamyl-phenylalanine. Biocatal Agric Biotechnol 10:278–284

    Article  CAS  Google Scholar 

  • Collins KD (1995) Sticky ions in biological systems. Proc Natl Acad Sci USA 92:5553–5557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Cera E (2006) A structural perspective on enzymes activated by monovalent cations. J Biol Chem 20:1305–1308

    Article  Google Scholar 

  • Dionisi HM, Alvarez CV, Viale AM (1999) Alkali metal ions protect mitochondrial rhodanese against thermal inactivation. Arch Biochem Biophys 361:202–206

    Article  CAS  PubMed  Google Scholar 

  • Frick DN, Banik S, Rypma RS (2007) Role of divalent cations in ATP hydrolysis catalyzed by the hepatitis C virus NS3 helicase: magnesium provides a bridge for ATP to fuel unwinding. J Mol Biol 365:1017–1032

    Article  CAS  PubMed  Google Scholar 

  • Frolow F, Harel M, Sussman JL, Mevarech M, Shoham M (1996) Insights into protein adaptation to a saturated salt environment from the crystal structure of a halophilic 2Fe–2S ferredoxin. Nat Struct Biol 3:452–458

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Gohara DW, Di Cera E (2016) Molecular mechanisms of enzyme activation by monovalent cations. J Biol Chem 291:20840–20848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gouzi H, Depagne C, Coradin T (2011) Kinetics and thermodynamics of the thermal inactivation of polyphenol oxidase in an aqueous extract from Agaricus bisporus. J Agric Food Chem 60(1):500–506

    Article  PubMed  Google Scholar 

  • Graziano G, Merlino A (2014) Molecular bases of protein haloterance. Biochim Biophys Acta 1844:850–858

    Article  CAS  PubMed  Google Scholar 

  • Grochowski P, Trylska J (2008) Continuum molecular electrostatics, salt effects, and counter ion binding –a review of the Poisson-Boltzmann theory and its modifications. Biopolymers 89:93–113

    Article  CAS  PubMed  Google Scholar 

  • Guo G, Fang T, Wang C, Huang Y, Tian F, Cui Q, Wang H (2015) Isolation and characterization of two novel halotolerant catechol 2,3-dioxygenases from a halophilic bacterial consortium. Sci Rep 5:17603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hákansson K, Doherty AJ, Shuman S, Wigley DB (1997) X-ray crystallography reveals a large conformational change during guanyl transfer by mRNA capping enzymes. Cell 89:545–553

    Article  PubMed  Google Scholar 

  • Hase T, Matsurbara H, Koike H, Katoh S (1983) Amino acid sequence of ferredoxin from a thermophilic blue-green alga, Synechococcus sp. Biochim Biophys Acta 744:46–52

    Article  CAS  Google Scholar 

  • Hoppert M (2011) Metalloenzymes. In: Reitner J, Thiel V (eds) Encyclopedia of Geobiology, Encyclopedia of Earth Sciences Series. Springer, Dordrecht, pp 558–563

    Google Scholar 

  • Hunaiti AR, Kolattukudy PE (1982) Isolation and characterization of an acyl-coenzyme A carboxylase from an erythromycin-producing Streptomyces erythreus. Arch Biochem Biophys 216(1):362–371

    Article  CAS  PubMed  Google Scholar 

  • Inoue M, Hiratake J, Suzuki H, Kumagai H, Sakata K (2000) Identification of catalytic nucleophile of Escherichia coli γ-glutamyltranspeptidase by γ-monofluorophosphono derivative of glutamic acid: N-terminal Thr-391 in small subunit is the nucleophile. Biochemistry 39:7764–7771

    Article  CAS  PubMed  Google Scholar 

  • Ishibashi M, Arakawa T, Philo JS, Sakashita K, Yonezawa Y, Kunaga H, Tokunaga M (2002) Secondary and quaternary structural transition of the halophilic archaeon nucleoside diphosphate kinase under high- and low-salt conditions. FEMS Microbiol Lett 216:235–241

    Article  CAS  PubMed  Google Scholar 

  • Jaspers C, Penniuckx M (1984) Glutathione metabolism in Saccharomyces cerevisiae: evidence that γ-glutamyltranspeptidase is a vacuolar enzyme. Biochimie 66:71–74

    Article  CAS  PubMed  Google Scholar 

  • Kaufman SB, González-Flecha L, González-Lebrero RM (2012) Opposing effects of Na+ and K+ on the thermal stability of Na+, K+-ATPase. J Phys Chem B 116:3421–3429

    Article  CAS  PubMed  Google Scholar 

  • Keillor JW, Castonguay R, Lherbet C (2005) γ-Glutamyl transpeptidase: substrate specificity and catalytic mechanism. Methods Enzymol 401:449–467

    Article  CAS  PubMed  Google Scholar 

  • Kuntz ID (1971) Hydration of macromolecules. IV. Polypeptide conformation in frozen solutions. J Am Chem Soc 93:516–518

    Article  CAS  PubMed  Google Scholar 

  • Lardner AL (2014) Neurobiological effects of the green tea constituent theanine and its potential role in the treatment of psychiatric and neurodegenerative disorders. Nutr Neurosci 17(4):145–155

    Article  CAS  PubMed  Google Scholar 

  • Larsen TM, Laughlin LT, Holden HM, Rayment I, Reed GH (1994) Structure of rabbit muscle pyruvate kinase complexed with Mn2+, K+, and pyruvate. Biochemistry 33:6301–6309

    Article  CAS  PubMed  Google Scholar 

  • Lee YC, Chi MC, Lin MG, Chen YY, Lin LL, Wang TF (2018) Biocatalytic synthesis of γ-glutamyl-L-leucine, a kokumi-imparting dipeptide, by Bacillus licheniformis γ-glutamyltranspeptidase. Food Biotechnol 32:130–147

    Article  CAS  Google Scholar 

  • Lees JG, Smith BR, Wien F, Miles AJ, Wallac BA (2004) CDtool – an integrated software package for circular dichroism spectroscopic data processing, analysis, and archiving. Anal Biochem 332:285–289

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Zhu R, Liu Y, Li J, Gao H, Hu N (2020) γ-Glutamyltranspeptidase from Bacillus amyloliquefaciens: transpeptidation activity enhancement and L-theanine production. Enzyme Microb Technol 140:109644

    Article  CAS  PubMed  Google Scholar 

  • Liang C, Xue Y, Fioroni M, Rodriguez-Ropero F, Schwaneberg U, Ma Y (2011) Cloning and characterization of a thermostable and halo-tolerant endoglucanase from Thermoanaerobacter tengcongenesis. Appl Microbiol Biotechnol 89:315–326

    Article  CAS  PubMed  Google Scholar 

  • Lin LL, Chen YY, Chi MC, Merlino A (2014) Low resolution X-ray structure of γ-glutamyltranspeptidase from Bacillus licheniformis: opened active site cleft and a cluster of acid residues potentially involved in the recognition of a metal ion. Biochim Biophys Acta 1844:1523–1529

    Article  CAS  PubMed  Google Scholar 

  • Lin LL, Chou PR, Hua YW, Hsu WH (2006) Overexpression, one-step purification, and biochemical characterization of a recombinant γ-glutamyltranspeptidase from Bacillus licheniformis. Appl Microbiol Biotechnol 73:103–112

    Article  CAS  PubMed  Google Scholar 

  • Lin MG, Chi MC, Chen YY, Wang TF, Lo HF, Lin LL (2016) Site-directed mutagenesis of a conserved Asn450 residue of Bacillus licheniformis γ-glutamyltranspeptidase. Int J Biol Macromol 91:416–425

    Article  CAS  PubMed  Google Scholar 

  • Lyu RC, Hu HY, Kuo LY, Lo HF, Ong PL, Chang HP, Lin LL (2009) Role of the conserved Thr399 and Thr417 residues of Bacillus licheniformis γ-glutamyltranspeptidase as evaluated by site-directed mutagenesis. Curr Microbiol 59:101–106

    Article  CAS  PubMed  Google Scholar 

  • Neville MC, Ling GN (1967) Synergistic activation of β-galactosidase by Na+ and Cs+. Arch Biochem Biophys 118(3):596–610

    Article  CAS  PubMed  Google Scholar 

  • Madern D, Ebel C, Zaccai G (2000) Halophilic adaption of enzymes. Extremophiles 4:91–98

    Article  CAS  PubMed  Google Scholar 

  • Maguire ME, Cowan JA (2002) Magnesium chemistry and biochemistry. Biometals 15:203–210

    Article  CAS  Google Scholar 

  • Minami H, Suzuki H, Kumagai H (2003) Salt-tolerant γ-glutamyltranspeptidase from Bacillus subtilis 168 with glutaminase activity. Enzyme Microb Technol 32:431–438

    Article  CAS  Google Scholar 

  • Miroshnikova AD, Kuznetsova AA, Voeobjev YN, Kuznetsov NA, Fedorova OS (2016) Effects of mono- and divalent-metal ions on DNA binding and catalysis of human apurinic/apyrimidinic endonuclease 1. Mol BioSyst 12:1527–1539

    Article  CAS  PubMed  Google Scholar 

  • Monsellier E, Bedouelle H (2005) Quantitative measurement of protein stability from unfolding equilibria monitored with the fluorescence maximum wavelength. Protein Eng Des Sel 18:445–456

    Article  CAS  PubMed  Google Scholar 

  • Mu W, Zhang T, Jiang B (2015) An overview of biological production of L-theanine. Biotechnol Adv 33:335–342

    Article  CAS  PubMed  Google Scholar 

  • Pace CN, Grimsley GR (1988) Ribonuclease T1 is stabilized by cation and anion binding. J Biol Chem 27:3242–3246

    CAS  Google Scholar 

  • Page MJ, Di Cera E (2006) Role of Na+ and K+ in enzyme function. Physiol Rev 86:1049–1092

    Article  CAS  PubMed  Google Scholar 

  • Pederick JL, Thompson AP, Bell SG, Bruning JB (2020) D-Alanine-D-alanine ligase as a model for the activation of ATP-grasp enzymes by monovalent cations. J Biol Chem 295(23):7894–7904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perutz MF, Raidt H (1978) Electrostatic effects in proteins. Science 201:1187–1191

    Article  CAS  PubMed  Google Scholar 

  • Pica A, Chi MC, D’Ischia M, Chen YY, Lin LL, Merlino A (2016) The maturation mechanism of γ-glutamyltranspeptidase: insights from the crystal structure of a precursor mimic of the enzyme from Bacillus licheniformis. Biochim Biophys Acta 1864:195–203

    Article  CAS  PubMed  Google Scholar 

  • Pica A, Krauss IR, Castellano I, La Cara F, Graziano G, Sica F, Merlino A (2013) Effect of NaCl on the conformational stability of the thermophilic γ-glutamyltranspeptidase from Geobacillus thermodenitrificans: implication for globular protein halotolerance. Biochim Biophys Acta 1834:149–157

    Article  CAS  PubMed  Google Scholar 

  • Pineda AO, Carrell CJ, Bush LA, Prasad S, Caccia S, Chen ZW, Mathews FS, Di Cera E (2004) Molecular dissection of Na+ binding to thrombin. J Biol Chem 279:31842–31853

    Article  CAS  PubMed  Google Scholar 

  • Premkumar L, Greenblatt HM, Bageshwar UK, Savchenko T, Gokhman I, Sussman JL, Zamir A (2005) Three-dimensional structure of a halotolerant algal carbonic anhydrase predicts halotolerance of a mammalian homolog. Proc Natl Acad Sci USA 102:7493–7498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quiroga-Roger D, Babul J, Guixé V (2015) Role of monovalent and divalent metal cations in human ribokinase catalysis and regulation. Biometals 28:401–413

    Article  CAS  PubMed  Google Scholar 

  • Radfar R, Leaphart A, Brewer JM, Minor W, Odom JD, Dunlap RB, Lovell CR, Lebioda L (2000) Cation binding and thermostability of FTHFS monovalent cation binding sites and thermostability of N10-formyltetrahydrofolate synthetase from Moorella thermoacetica. Biochemistry 39:14481–14486

    Article  CAS  PubMed  Google Scholar 

  • Rawlings ND, Barrett AJ, Bateman A (2020) MEROPS: the peptidase database. Nucleic Acids Res 38:D227–D233

    Article  Google Scholar 

  • Rochu D, Viguié N, Renault F, Crouzier D, Froment MT, Masson P (2004) Contribution of the active-site metal cation to the catalytic activity and to the conformational stability of phosphotriesterase: temperature- and pH-dependence. Biochem J 380:627–633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Royer CA, Mann CJ, Matthews CR (1993) Resolution of the fluorescence equilibrium unfolding profile of trp aporepressor using single tryptophan mutants. Protein Sci 2:1844–1852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saini M, Kashyap A, Bindal S, Saini K, Gupta R (2021) Bacterial γ-glutamyl transpeptidase, an emerging biocatalyst: insights into structure-function relationship and its biotechnological applications. Front Microbiol 12:641251

    Article  PubMed  PubMed Central  Google Scholar 

  • Schulz H (1975) On the structure-function relationship of acyl carrier protein of Escherichia coli. J Biol Chem 250(6):2299–2304

    Article  CAS  PubMed  Google Scholar 

  • Shuai Y, Zhang T, Jiang B, Mu W (2010) Development of efficient enzymatic production of theanine by γ-glutamyltranspeptidase from a newly isolated strain of Bacillus subtilis, SK11.004. J Sci Food Agric 90:2563–2567

    Article  CAS  PubMed  Google Scholar 

  • Siglioccolo A, Paiardini A, Piscitelli M, Pascarella S (2011) Structural adaption of extreme halophilic proteins through decrease of conserved hydrophobic contact surface. BMC Struct Biol 11:50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki H (2019) Bacterial γ-glutamyltranspeptidase: food and medicinal applications. ScienceAsia 245:503–508

    Article  Google Scholar 

  • Suzuki H, Hashimoto W, Kumagai H (1999) Glutathione metabolism in Escherichia coli. J Mol Catal B Enzym 6:175–184

    Article  CAS  Google Scholar 

  • Suzuki H, Izuka S, Miyakawa N, Kumagai H (2002) Enzymatic production of theanine, an “umami” component of tea, from glutamine and ethylamine with bacterial γ-glutamyltranspeptidase. Enzyme Microb Technol 31:884–889

    Article  CAS  Google Scholar 

  • Suzuki H, Kumagai H (2002) Autocatalytic processing of γ-glutamyltranspeptidase. J Biol Chem 277:43536–43543

    Article  CAS  PubMed  Google Scholar 

  • Szajn H, Csopak H (1977) Metal ion-induced conformational changes in Escherichia coli alkaline phosphatase. Biochim Biophys Acta 480(1):143–153

    Article  CAS  PubMed  Google Scholar 

  • Toyokawa Y, Takahara H, Reungsang A, Fukuta M, Hachimine Y, Tachibana S, Yasuda M (2010) Purification and characterization of a halotolerant serine proteinase from thermotolerant Bacillus licheniformis RKK-04 isolated from Thai fish sauce. Appl Microbiol Biotechnol 86:1867–1875

    Article  CAS  PubMed  Google Scholar 

  • Villeret V, Huang S, Fromm HJ, Lipscomb WN (1995) Crystallographic evidence for the action of potassium, thallium, and lithium ions on fructose-1,6-bisphosphatase. Proc Natl Acad Sci USA 92:8916–8920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wada K, Irie M, Suzuki H, Fukuyama K (2010) Crystal structure of the halotolerant γ-glutamyltranspeptidase from Bacillus subtilis in complex with glutamate reveals a unique architecture of the solvent-exposed catalytic pocket. FEBS J 277:1000–1009

    Article  CAS  PubMed  Google Scholar 

  • Wang CY, Hsieh YR, Ng CC, Chan H, Lin HT, Tzeng WS, Shyu YT (2009) Purification and characterization of a novel halostable cellulase from Salinivibrio sp. strain NTU-05. Enzyme Microb Technol 44:373–379

    Article  CAS  Google Scholar 

  • Warden AC, Williams M, Peat TS, Seabrook SA, Newman J, Dojchinov G, Haritos VS (2015) Rational engineering of a mesophilic carbonic anhydrase to an extreme halotolerant biocatalyst. Nat Commun 6:10278

    Article  CAS  PubMed  Google Scholar 

  • West MB, Chen Y, Wickham S, Heroux A, Cahill K, Hanigan MH, Mooers BHM (2013) Novel insights into eukaryotic γ-glutamyltranspeptidase 1 from the crystal structure of the glutamate-bound human enzyme. J Biol Chem 288:31902–31913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams J, Kellett J, Roach PD, McKune A, Mellor D, Thomas J, Naumovski N (2016) L-Theanine as a functional food additive: its role in disease prevention and health promotion. Beverages 2:13

    Article  Google Scholar 

  • Wright DB, Banks DD, Lohman JR, Hilsenbeck JL, Gloss LM (2002) The effect of salts on the activity and stability of Escherichia coli and Haloferax volcanii dihydrofolate reductases. J Mol Biol 323:327–344

    Article  CAS  PubMed  Google Scholar 

  • Yang G, Chen H, Liu Y (2009) Effect of additives on thermostability of Trichoderma viride JQF-04 cellulase. Chin J Appl Environ Biol 15(1):134–138

    Article  Google Scholar 

  • Yang J, Bai W, Zeng X, Cui C (2019) Gamma glutamyl peptides: the food source, enzymatic synthesis, kokumi-active and the potential functional properties- a review. Trends Food Sci Technol 91:339–346

    Article  CAS  Google Scholar 

  • Yang JC, Liang WC, Chen YY, Chi MC, Lo HF, Chen HL, Lin LL (2011) Biophysical characterization of Bacillus licheniformis and Escherichia coli γ-glutamyltranspeptidases: a comparative analysis. Int J Biol Macromol 48:414–422

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Forman HJ, Choi J (2005) γ-Glutamyl transpeptidase in glutathione biosynthesis. Methods Enzymol 401:468–483

    Article  CAS  PubMed  Google Scholar 

  • Zhang P, Idota Y, Yano K, Negishi M, Kawabata H, Arakawa H, Morimoto K, Tsuji A, Ogihara T (2014) Characterization of cesium uptake mediated by a potassium transport system of bacteria in a soil conditioner. Biol Pharm Bull 37(4):604–607

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

The authors are greatly indebted to the Ministry of Science and Technology of Taiwan for financial support (MOST 109–2313-B-415–006; MOST 109–2320-B-415–003).

Author information

Author notes

  1. Long-Liu Lin and Bo-Yuan Lu contributed equally to this paper.

Authors and Affiliations

  1. Department of Applied Chemistry, National Chiayi University, 300 Syuefu Road, Chiayi City, 60004, Taiwan

    Long-Liu Lin, Bo-Yuan Lu, Meng-Chun Chi, Yu-Fen Huang & Tzu-Fan Wang

  2. Institute of Molecular Biology, Academia Sinica, Nangang District, Taipei City, 11529, Taiwan

    Min-Guan Lin

Authors
  1. Long-Liu Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bo-Yuan Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Meng-Chun Chi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yu-Fen Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Min-Guan Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tzu-Fan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tzu-Fan Wang.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lin, LL., Lu, BY., Chi, MC. et al. Activation and thermal stabilization of a recombinant γ-glutamyltranspeptidase from Bacillus licheniformis ATCC 27811 by monovalent cations. Appl Microbiol Biotechnol 106, 1991–2006 (2022). https://doi.org/10.1007/s00253-022-11836-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-022-11836-y

Keywords

Search

Navigation