Abstract
l-Glutaminases are enzymes that catalyze the cleavage of the gamma-amido bond of l-glutamine residues, producing ammonia and l-glutamate. These enzymes have several applications in food and pharmaceutical industries. However, the l-glutaminases that hydrolyze free l-glutamine (l-glutamine glutaminases, EC 3.5.1.2) have different structures and properties with respect to the l-glutaminases that hydrolyze the same amino acid covalently bound in peptides (peptidyl glutaminases, EC 3.5.1.43) and proteins (protein-glutamine glutaminase, EC 3.5.1.44). In the food industry, l-glutamine glutaminases are applied to enhance the flavor of foods, whereas protein glutaminases are useful to improve the functional properties of proteins. This review will focus on structural backgrounds and differences between these enzymes, the methodology available to measure the activity as well as strengths and limitations. Production methods, applications, and challenges in the food industry will be also discussed. This review will provide useful information to search and identify the suitable l-glutaminase that best fits to the intended application.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Not applicable.
Code availability
Not applicable.
References
Amirato GR, Borges JO, Marques DL, Santos JM, Santos CA, Andrade MS, Pithon-Curi TC (2021) l-Glutamine supplementation enhances strength and power of knee muscles and improves glycemia control and plasma redox balance in exercising elderly women. Nutrients 13:1025. https://doi.org/10.3390/nu13031025
Amobonye A, Singh S, Pillai S (2019) Recent advances in microbial glutaminase production and applications—a concise review. Crit Rev Biotechnol 39:944–963. https://doi.org/10.1080/07388551.2019.1640659
Amobonye A, Singh S, Mukherjee K, Jobichen C, Qureshi IA, Pillai S (2022) Structural and functional insights into fungal glutaminase using a computational approach. Process Biochem 117:76–89. https://doi.org/10.1016/j.procbio.2022.03.019
Bao XL, Lv Y, Yang BC, Ren CG, Guo ST (2008) A study of the soluble complexes formed during calcium binding by soybean protein hydrolysates. J Food Sci 73:C117–C121. https://doi.org/10.1111/j.1750-3841.2008.00673.x
Barzkar N, Sohail M, Tamadoni Jahromi S, Nahavandi R, Khodadadi M (2021) Marine microbial l-glutaminase: from pharmaceutical to food industry. Appl Microbiol Biotechnol 105:4453–4466. https://doi.org/10.1007/s00253-021-11356-1
Bazaraa W, Alian A, El-Shimi N, Mohamed R (2016) Purification and characterization of extracellular glutaminase from Aspergillus oryzae NRRL 32567. Biocatal Agric Biotechnol 6:76–81. https://doi.org/10.1016/j.bcab.2016.02.009
Binod P, Sindhu R, Madhavan A, Abraham A, Mathew AK, Beevi US, Sukumaran RK, Singh SP, Pandey A (2017) Recent developments in l-glutaminase production and applications—an overview. Bioresour Technol. https://doi.org/10.1016/j.biortech.2017.05.059
Boudier-Lemosquet A, Mahler A, Bobo C, Dufossée M, Priault M (2022) Introducing protein deamidation: landmark discoveries, societal outreach, and tentative priming workflow to address deamidation. Methods 200:3–14. https://doi.org/10.1016/j.ymeth.2021.11.012
Brown G, Singer A, Proudfoot M, Skarina T, Kim Y, Chang C, Dementieva I, Kuznetsova E, Gonzalez CF, Joachimiak A (2008) Functional and structural characterization of four glutaminases from Escherichia coli and Bacillus subtilis. Biochemistry 47:5724–5735. https://doi.org/10.1021/bi800097h
Cassago A, Ferreira AP, Ferreira IM, Fornezari C, Gomes ER, Greene KS, Pereira HM, Garratt RC, Dias SM, Ambrosio AL (2012) Mitochondrial localization and structure-based phosphate activation mechanism of glutaminase C with implications for cancer metabolism. Proc Natl Acad Sci USA 109:1092–1097. https://doi.org/10.1073/pnas.1112495109
Chakraborty SP (2019) Patho-physiological and toxicological aspects of monosodium glutamate. Toxicol Mech Methods 29:389–396. https://doi.org/10.1080/15376516.2018.1528649
Chen X, Fu W, Luo Y, Cui C, Suppavorasatit I, Liang L (2021) Protein deamidation to produce processable ingredients and engineered colloids for emerging food applications. Compr Rev Food Sci Food Saf 20:3788–3817. https://doi.org/10.1111/1541-4337.12759
Dhankhar R, Gupta V, Kumar S, Kapoor RK, Gulati P (2020) Microbial enzymes for deprivation of amino acid metabolism in malignant cells: biological strategy for cancer treatment. Appl Microbiol Biotechnol 104:2857–2869. https://doi.org/10.1007/s00253-020-10432-2
Durthi CP, Pola M, Rajulapati SB, Kola AK, Kamal MA (2020) Versatile and valuable utilization of amidohydrolase l-glutaminase in pharma and food industries: a review. Curr Drug Metab 21:11–24. https://doi.org/10.2174/1574884715666200116110542
Fang L, Xiang H, Sun-Waterhouse D, Cui C, Lin J (2020) Enhancing the usability of pea protein isolate in food applications through modifying its structural and sensory properties via deamidation by glutaminase. J Agric Food Chem. https://doi.org/10.1021/acs.jafc.9b06046
Ferreira FV, Herrmann-Andrade AM, Binolfi A, Calabrese CD, Mac Cormack WP, Musumeci MA (2021) Characteristics of a cold-adapted l-glutaminase with potential applications in the food industry. Appl Biochem Biotechnol 193:3121–3138. https://doi.org/10.1007/s12010-021-03596-8
Fu W, Chen X, Cheng H, Liang L (2022) Tailoring protein intrinsic charge by enzymatic deamidation for solubilizing chicken breast myofibrillar protein in water. Food Chem 385:132512. https://doi.org/10.1016/j.foodchem.2022.132512
Gervais D, O’Donnell J, Sung M-A, Smith S (2013) Control of process-induced asparaginyl deamidation during manufacture of Erwinia chrysanthemi l-asparaginase. Process Biochem 48:1311–1316. https://doi.org/10.1016/j.procbio.2013.06.024
Gu Y, Matsumura Y, Yamaguchi S, Mori T (2001) Action of protein-glutaminase on α-lactalbumin in the native and molten globule states. J Agric Food Chem 49:5999–6005. https://doi.org/10.1021/jf010287z
Hadidi M, Ibarz A, Pouramin S (2021) Optimization of extraction and deamidation of edible protein from evening primrose (Oenothera biennis L.) oil processing by-products and its effect on structural and techno-functional properties. Food Chem 334:127613. https://doi.org/10.1016/j.foodchem.2020.127613
Hamada J (1991) Peptidoglutaminase deamidation of proteins and protein hydrolysates for improved food use. J Am Oil Chem Soc 68:459–462. https://doi.org/10.1007/BF02663813
Hamada JS (1992) Effects of heat and proteolysis on deamidation of food proteins using peptidoglutaminase. J Agric Food Chem 40:719–723. https://doi.org/10.1021/jf00017a003
Hamada JS (1995) High performance liquid chromatography of Bacillus circulans peptidoglutaminase for laboratory and industrial uses. J Chromatogr A 702:163–172. https://doi.org/10.1016/0021-9673(94)01267-I
Hamada J, Marshall W (1989) Preparation and functional properties of enzymatically deamidated soy proteins. J Food Sci 54:598–601. https://doi.org/10.1111/j.1365-2621.1989.tb04661.x
Hamada JS, Swanson B (1994) Deamidation of food proteins to improve functionality. Crit Rev Food Sci Nutr 34:283–292. https://doi.org/10.1080/10408399409527664
Hashizume R, Maki Y, Mizutani K, Takahashi N, Matsubara H, Sugita A, Sato K, Yamaguchi S, Mikami B (2011) Crystal structures of protein glutaminase and its pro forms converted into enzyme-substrate complex. J Biol Chem 286:38691–38702. https://doi.org/10.1074/jbc.M111.255133
Hatami B, Saffaei A, Jamali F, Abbasinazari M (2020) Glutamine powder-induced hepatotoxicity: it is time to understand the side effects of sports nutritional supplements. Gastroenterol Hepatol Bed Bench 13:86–89
Heini HG, Gebhardt R, Brecht A, Mecke D (1987) Purification and characterization of rat liver glutaminase. Eur J Biochem 162:541–546. https://doi.org/10.1111/j.1432-1033.1987.tb10673.x
Holeček M (2022) Side effects of amino acid supplements. Physiol Res 71:29–45. https://doi.org/10.33549/physiolres.934790
Horstmann G, Ewert J, Stressler T, Fischer L (2020) A novel protein glutaminase from Bacteroides helcogenes—characterization and comparison. Appl Microbiol Biotechnol 104:187–199. https://doi.org/10.1007/s00253-019-10225-2
Immonen M, Myllyviita J, Sontag-Strohm T, Myllärinen P (2021) Oat protein concentrates with improved solubility produced by an enzyme-aided ultrafiltration extraction method. Foods 10:3050. https://doi.org/10.3390/foods10123050
Ito K, Umitsuki G, Oguma T, Koyama Y (2011) Salt-tolerant and thermostable glutaminases of Cryptococcus species form a new glutaminase family. Biosci Biotechnol Biochem. https://doi.org/10.1271/bbb.110092
Jiang ZQ, Sontag-Strohm T, Salovaara H, Sibakov J, Kanerva P, Loponen J (2015) Oat protein solubility and emulsion properties improved by enzymatic deamidation. J Cereal Sci 64:126–132. https://doi.org/10.1016/j.jcs.2015.04.010
Jiang Y, Wang Z, He Z, Zeng M, Qin F, Chen J (2022) Effect of heat-induced aggregation of soy protein isolate on protein-glutaminase deamidation and the emulsifying properties of deamidated products. LWT 154:112328. https://doi.org/10.1016/j.lwt.2021.112328
Kenny J, Bao Y, Hamm B, Taylor L, Toth A, Wagers B, Curthoys NP (2003) Bacterial expression, purification, and characterization of rat kidney-type mitochondrial glutaminase. Protein Expr Purif 31:140–148. https://doi.org/10.1016/S1046-5928(03)00161-X
Kikuchi M, Sakaguchi K (1973) Some enzymatic properties and substrate specificities of peptidoglutaminase-I and II. Agric Biol Chem 37:1813–1821. https://doi.org/10.1080/00021369.1973.10860916
Kikuchi M, Sakaguchi K (1976) Chemical and physical properties of peptidoglutaminase I and II from Bacillus circulans. Biochim Biophys Acta 427:285–294. https://doi.org/10.1016/0005-2795(76)90304-4
Kikuchi Y, Itaya H, Date M, Matsui K, Wu L-F (2008) Production of Chryseobacterium proteolyticum protein-glutaminase using the twin-arginine translocation pathway in Corynebacterium glutamicum. Appl Microbiol Biotechnol 78:67. https://doi.org/10.1007/s00253-007-1283-3
Kikuchi Y, Itaya H, Date M, Matsui K, Wu L-F (2009) TatABC overexpression improves Corynebacterium glutamicum Tat-dependent protein secretion. Appl Environ Microbiol 75:603–607. https://doi.org/10.1128/AEM.01874-08
Krug F, Růžička J, Hansen E (1979) Determination of ammonia in low concentrations with Nessler’s reagent by flow injection analysis. Analyst 104:47–54. https://doi.org/10.1039/AN9790400047
Kumar L, Singh B, Adhikari DK, Mukherjee J, Ghosh D (2012) A temperature and salt-tolerant l-glutaminase from Gangotri region of Uttarakhand Himalaya: enzyme purification and characterization. Appl Biochem Biotechnol 166:1723–1735. https://doi.org/10.1007/s12010-012-9576-0
Kumeta H, Miwa N, Ogura K, Kai Y, Mizukoshi T, Shimba N, Suzuki E-I, Inagaki F (2010) The NMR structure of protein-glutaminase from Chryseobacterium proteolyticum. J Biomol NMR 46:251–255. https://doi.org/10.1007/s10858-010-9399-7
Kunarayakul S, Thaiphanit S, Anprung P, Suppavorasatit I (2018) Optimization of coconut protein deamidation using protein-glutaminase and its effect on solubility, emulsification, and foaming properties of the proteins. Food Hydrocoll 79:197–207. https://doi.org/10.1016/j.foodhyd.2017.12.031
Li D, Zhao XH (2011) Glutaminase-induced deamidation and hydrolysis of casein and metal-chelating or ACE-inhibitory activity of the hydrolysates in vitro. Int J Food Sci Technol 46:324–332. https://doi.org/10.1111/j.1365-2621.2010.02493.x
Li D, Zhao XH (2012) Limited deamidation of soybean protein isolates by glutaminase and its impacts on the selected properties. Int J Food Prop 15:638–655. https://doi.org/10.1080/10942912.2010.494760
Li X, Liu Y, Li N, Xie D, Yu J, Wang F, Wang J (2016) Studies of phase separation in soluble rice protein/different polysaccharides mixed systems. LWT 65:676–682. https://doi.org/10.1016/j.lwt.2015.08.064
Liu Y, Li X, Zhou X, Yu J, Wang F, Wang J (2011) Effects of glutaminase deamidation on the structure and solubility of rice glutelin. LWT 44:2205–2210. https://doi.org/10.1016/j.lwt.2011.05.011
Liu X, Wang C, Zhang X, Zhang G, Zhou J, Chen J (2022) Application prospect of protein-glutaminase in the development of plant-based protein foods. Foods 11:440. https://doi.org/10.3390/foods11030440
Lu X, Poon TCW, Zhang H (2020) Mass production of active recombinant Chryseobacterium proteolyticum protein glutaminase in Escherichia coli using a sequential dual expression system and one-step purification. IUBMB Life 72:2391–2399. https://doi.org/10.1002/iub.2358
Masuo N, Ito K, Yoshimune K, Hoshino M, Matsushima K, Koyama Y, Moriguchi M (2004) Molecular cloning, overexpression, and purification of Micrococcus luteus K-3-type glutaminase from Aspergillus oryzae RIB40. Protein Expr Purif 38:272–278. https://doi.org/10.1016/j.pep.2004.09.003
Miwa N, Nio N, Sonomoto K (2014) Effect of enzymatic deamidation by protein-glutaminase on the textural and microstructural properties of set yoghurt. Int Dairy J 36:1–5. https://doi.org/10.1016/j.idairyj.2013.12.002
Moldovan OL, Rusu A, Tanase C, Vari CE (2021) Glutamate—a multifaceted molecule: endogenous neurotransmitter, controversial food additive, design compound for anti-cancer drugs. A critical appraisal. Food Chem Toxicol 153:112290. https://doi.org/10.1016/j.fct.2021.112290
Moriguchi M, Sakai K, Tateyama R, Furuta Y, Wakayama M (1994) Isolation and characterization of salt-tolerant glutaminases from marine Micrococcus luteus K-3. J Ferment Bioeng 77:621–625. https://doi.org/10.1016/0922-338X(94)90143-0
Mosallatpour S, Aminzadeh S, Shamsara M, Hajihosseini R (2019) Novel halo- and thermo-tolerant Cohnella sp. A01 l-glutaminase: heterologous expression and biochemical characterization. Sci Rep 9:1–14. https://doi.org/10.1038/s41598-019-55587-9
Mu W, Zhang T, Jiang B (2015) An overview of biological production of l-theanine. Biotechnol Adv 33:335–342. https://doi.org/10.1016/j.biotechadv.2015.04.004
Nandakumar R, Wakayama M, Nagano Y, Kawamura T, Sakai K, Moriguchi M (1999) Overexpression of salt-tolerant glutaminase from Micrococcus luteus K-3 in Escherichia coli and its purification. Protein Expr Purif 15:155–161. https://doi.org/10.1006/prep.1998.1005
Nandakumar R, Yoshimune K, Wakayama M, Moriguchi M (2003) Microbial glutaminase: biochemistry, molecular approaches and applications in the food industry. J Mol Catal B 23:87–100. https://doi.org/10.1016/S1381-1177(03)00075-4
Nguyen TTT, Ramachandran S, Hill MJ, Cerione RA (2022) High-resolution structures of mitochondrial glutaminase C tetramers indicate conformational changes upon phosphate binding. J Biol Chem 298:101564. https://doi.org/10.1016/j.jbc.2022.101564
Ouyang X, Liu Y, Qu R, Tian M, Yang T, Zhu R, Gao H, Jin M, Huang J (2021) Optimizing protein-glutaminase expression in Bacillus subtilis. Curr Microbiol 78:1752–1762. https://doi.org/10.1007/s00284-021-02404-0
Pandian SRK, Deepak V, Sivasubramaniam SD, Nellaiah H, Sundar K (2014) Optimization and purification of anticancer enzyme l-glutaminase from Alcaligenes faecalis KLU102. Biologia 69:1644–1651. https://doi.org/10.2478/s11756-014-0486-1
Perna S, Alalwan TA, Alaali Z, Alnashaba T, Gasparri C, Infantino V, Hammad L, Riva A, Petrangolini G, Allegrini P, Rondanelli M (2019) The role of glutamine in the complex interaction between gut microbiota and health: a narrative review. Int J Mol Sci 20:5232. https://doi.org/10.3390/ijms20205232
Qu R, Zhu X, Tian M, Liu Y, Yan W, Ye J, Gao H, Huang J (2018) Complete genome sequence and characterization of a protein-glutaminase producing strain, Chryseobacterium proteolyticum QSH1265. Front Microbiol 9:1975. https://doi.org/10.3389/fmicb.2018.01975
Riha WE, Izzo HV, Zhang J, Ho CT (1996) Nonenzymatic deamidation of food proteins. Crit Rev Food Sci Nutr 36:225–255. https://doi.org/10.1080/10408399609527724
Sabu A, Chandrasekaran M (1999) l-Glutaminase production by marine fungi. Cochin Univ Sci Technol. https://doi.org/10.1016/S0032-9592(99)00127-2
Sakai K, Sato Y, Okada M, Yamaguchi S (2022) Enhanced activity and stability of protein-glutaminase by Hofmeister effects. Mol Catal 517:112054. https://doi.org/10.1016/j.mcat.2021.112054
Savoca MP, Tonoli E, Atobatele AG, Verderio EA (2018) Biocatalysis by transglutaminases: a review of biotechnological applications. Micromachines 9:562. https://doi.org/10.3390/mi9110562
Singh P, Banik R (2013) Biochemical characterization and antitumor study of l-glutaminase from Bacillus cereus MTCC 1305. Appl Biochem Biotechnol 171:522–531. https://doi.org/10.1007/s12010-013-0371-3
Sinsuwan S, Yongsawatdigul J, Chumseng S, Yamabhai M (2012) Efficient expression and purification of recombinant glutaminase from Bacillus licheniformis (GlsA) in Escherichia coli. Protein Expr Purif 83:52–58. https://doi.org/10.1016/j.pep.2012.03.001
Suppavorasatit I, Cadwallader KR (2012) Effect of enzymatic deamidation of soy protein by protein-glutaminase on the flavor-binding properties of the protein under aqueous conditions. J Agric Food Chem 60:7817–7823. https://doi.org/10.1021/jf301719k
Suppavorasatit I, De Mejia EG, Cadwallader KR (2011) Optimization of the enzymatic deamidation of soy protein by protein-glutaminase and its effect on the functional properties of the protein. J Agric Food Chem 59:11621–11628. https://doi.org/10.1021/jf2028973
Suppavorasatit I, Lee SY, Cadwallader KR (2013) Effect of enzymatic protein deamidation on protein solubility and flavor binding properties of soymilk. J Food Sci 78:C1–C7. https://doi.org/10.1111/j.1750-3841.2012.03012.x
Sze SK, Jebamercy G, Ngan SC (2020) Profiling the ‘deamidome’ of complex biosamples using mixed-mode chromatography-coupled tandem mass spectrometry. Methods. https://doi.org/10.1016/j.ymeth.2020.05.005
Tambasco-Studart M, Tews I, Amrhein N, Fitzpatrick TB (2007) Functional analysis of PDX2 from Arabidopsis, a glutaminase involved in vitamin B6 biosynthesis. Plant Physiol 144:915–925. https://doi.org/10.1104/pp.107.096784
Temthawee W, Panya A, Cadwallader KR, Suppavorasatit I (2020) Flavor binding property of coconut protein affected by protein-glutaminase: vanillin-coconut protein model. LWT 130:109676. https://doi.org/10.1016/j.lwt.2020.109676
Vaintraub I, Kotova L, Shaha R (1996) Protein deamidases from germinating seeds. Physiol Plant 96:662–666. https://doi.org/10.1111/j.1399-3054.1996.tb00240.x
Wakayama M, Yamagata T, Kamemura A, Bootim N, Yano S, Tachiki T, Yoshimune K, Moriguchi M (2005) Characterization of salt-tolerant glutaminase from Stenotrophomonas maltophilia NYW-81 and its application in Japanese soy sauce fermentation. J Ind Microbiol Biotechnol 32:383–390. https://doi.org/10.1007/s10295-005-0257-7
Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, TaP DB, Rempfer C, Bordoli L (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 46:W296–W303. https://doi.org/10.1093/nar/gky427
Weatherburn M (1967) Phenol-hypochlorite reaction for determination of ammonia. Anal Chem 39:971–974. https://doi.org/10.1021/ac60252a045
Wieser H (2007) Chemistry of gluten proteins. Food Microbiol 24:115–119. https://doi.org/10.1016/j.fm.2006.07.004
Wu D, Tu M, Wang Z, Wu C, Yu C, Battino M, El-Seedi HR, Du M (2020) Biological and conventional food processing modifications on food proteins: structure, functionality, and bioactivity. Biotechnol Adv 40:107491. https://doi.org/10.1016/j.biotechadv.2019.107491
Xiang H, Sun-Waterhouse D, Cui C, Wang W, Dong K (2018) Modification of soy protein isolate by glutaminase for nanocomplexation with curcumin. Food Chem 268:504–512. https://doi.org/10.1016/j.foodchem.2018.06.059
Xu F, Oruna-Concha M-J, Elmore JS (2016) The use of asparaginase to reduce acrylamide levels in cooked food. Food Chem 210:163–171. https://doi.org/10.1016/j.foodchem.2016.04.105
Yamaguchi S, Yokoe M (2000) A novel protein-deamidating enzyme from Chryseobacterium proteolyticum sp. nov., a newly isolated bacterium from soil. Appl Environ Microbiol 66:3337–3343. https://doi.org/10.1128/AEM.66.8.3337-3343.2000
Yamaguchi S, Jeenes DJ, Archer DB (2001) Protein-glutaminase from Chryseobacterium proteolyticum, an enzyme that deamidates glutaminyl residues in proteins: purification, characterization and gene cloning. Eur J Biochem 268:1410–1421. https://doi.org/10.1046/j.1432-1327.2001.02019.x
Ye M, Liu X, Zhao L (2013) Production of a novel salt-tolerant l-glutaminase from Bacillus amyloliquefaciens using agro-industrial residues and its application in Chinese soy sauce fermentation. Biotechnology 12:25. https://doi.org/10.3923/biotech.2013.25.35
Yin X, Zhang G, Zhou J, Li J, Du G (2021) Combinatorial engineering for efficient production of protein-glutaminase in Bacillus subtilis. Enzym Microb Technol 150:109863. https://doi.org/10.1016/j.enzmictec.2021.109863
Ying Y, Li H (2020) Recent progress in the analysis of protein deamidation using mass spectrometry. Methods. https://doi.org/10.1016/j.ymeth.2020.06.009
Yong YH, Yamaguchi S, Gu YS, Mori T, Matsumura Y (2004) Effects of enzymatic deamidation by protein-glutaminase on structure and functional properties of α-zein. J Agric Food Chem 52:7094–7100. https://doi.org/10.1021/jf040133u
Yong YH, Yamaguchi S, Matsumura Y (2006) Effects of enzymatic deamidation by protein-glutaminase on structure and functional properties of wheat gluten. J Agric Food Chem 54:6034–6040. https://doi.org/10.1021/jf060344u
Yoshimune K, Shirakihara Y, Wakayama M, Yumoto I (2010) Crystal structure of salt-tolerant glutaminase from Micrococcus luteus K-3 in the presence and absence of its product l-glutamate and its activator Tris. FEBS J 277:738–748. https://doi.org/10.1111/j.1742-4658.2009.07523.x
Zhang Y, Jia C, He C, Kang L, Huang D, Cheng N, Ning X, Huang J, Jin M, Lu W, Bu G, Gao H (2015) Isolation and identification of nine bacteria strains producing protein-glutaminase. Sci Technol Food Ind 1:170–176. https://doi.org/10.13386/j.issn1002-0306.2015.01.027
Zhang X, Xu Z, Liu S, Qian K, Xu M, Yang T, Xu J, Rao Z (2019) Improving the production of salt-tolerant glutaminase by integrating multiple copies of Mglu into the protease and 16S rDNA genes of Bacillus subtilis 168. Molecules 24:592. https://doi.org/10.3390/molecules24030592
Zhang G, Ma S, Liu X, Yin X, Liu S, Zhou J, Du G (2021a) Protein-glutaminase: research progress and prospect in food manufacturing. Food Biosci 43:101314. https://doi.org/10.1016/j.fbio.2021.101314
Zhang J, Kang D, Zhang W, Lorenzo JM (2021b) Recent advantage of interactions of protein-flavor in foods: perspective of theoretical models, protein properties and extrinsic factors. Trends Food Sci Technol 111:405–425. https://doi.org/10.1016/j.tifs.2021.02.060
Zhou JX, Zhou J, Yang HM, Chen M, Huang F (2008) Characterization of two glutaminases from the filamentous cyanobacterium Anabaena sp. PCC 7120. FEMS Microbiol Lett 289:241–249. https://doi.org/10.1111/j.1574-6968.2008.01395.x
Acknowledgements
We apologize to colleagues whose work could not be cited due to space constraints. Yohanna Martínez, Flavia Ferreira and Matías Musumeci are staff members of The Argentinean National Research Council (CONICET).
Funding
This work was supported by ANPCyT (Grant No. PICT 2018-01372) and National University of Entre Rios (Grant No. PID-UNER 8129).
Author information
Authors and Affiliations
Contributions
YBM, FVF and MAM wrote the main manuscript text. MAM prepared figures. All authors reviewed the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
There is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Martínez, Y.B., Ferreira, F.V. & Musumeci, M.A. l-Glutamine-, peptidyl- and protein-glutaminases: structural features and applications in the food industry. World J Microbiol Biotechnol 38, 204 (2022). https://doi.org/10.1007/s11274-022-03391-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11274-022-03391-5