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Protein & Peptide Letters

Author(s): Fatima Akram*, Rabia Akram, Ikram ul Haq, Ali Nawaz, Zuriat Jabbar and Zeeshan Ahmed

DOI: 10.2174/0929866528666210218215359

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Biotechnological Eminence of Chitinases: A Focus on Thermophilic Enzyme Sources, Production Strategies and Prominent Applications

Page: [1009 - 1022] Pages: 14

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Abstract

Background: Chitin, the second most abundant polysaccharide in nature, is a constantly valuable and renewable raw material after cellulose. Due to advancement in technology, industrial interest has grown to take advantage of the chitin.

Objective: Now, biomass is being treated with diverse microbial enzymes or cells for the production of desired products under best industrial conditions. Glycosidic bonds in chitin structure are degraded by chitinase enzymes, which are characterized into number of glycoside hydrolase (GHs) families.

Methods: Thermophilic microorganisms are remarkable sources of industrially important thermostable enzymes, having ability to survive harsh industrial processing conditions. Thermostable chitinases have an edge over mesophilic chitinases as they can hydrolyse the substrate at relatively high temperatures and exhibit decreased viscosity, significantly reduced contamination risk, thermal and chemical stability and increased solubility. Various methods are employed to purify the enzyme and increase its yield by optimizing various parameters such as temperature, pH, agitation, and by investigating the effect of different chemicals and metal ions etc.

Results: Thermostable chitinase enzymes show high specific activity at elevated temperature which distinguish them from mesophiles. Genetic engineering can be used for further improvement of natural chitinases, and unlimited potential for the production of thermophilic chitinases has been highlighted due to advancement in synthetic biological techniques. Thermostable chitinases are then used in different fields such as bioremediation, medicine, agriculture and pharmaceuticals.

Conclusion: This review will provide information about chitinases, biotechnological potential of thermostable enzyme and the methods by which they are being produced and optimized for several industrial applications. Some of the applications of thermostable chitinases have also been briefly described.

Keywords: Biocontrol, chitin, chitinase, genetic engineering, thermostability, bio-pesticides.

Graphical Abstract

[1]
Vani, R.; Stanley, S.A. Studies on the extraction of chitin and chitosan from different aquatic organisms. Adv. BioTech., 2013, 12, 12-15.
[2]
Aam, B.B.; Heggset, E.B.; Norberg, A.L.; SA,rlie, M.; Varum, K.M.; Eijsink, V.G. Production of chitooligosaccharides and their potential applications in medicine. Mar. Drugs, 2010, 8(5), 1482-1517.[http://dx.doi.org/10.3390/md8051482] [PMID: 20559485]
[3]
Stoykov, Y.M.; Pavlov, A.I.; Krastanov, A.I. Chitinase biotechnology: production, purification, and application. Eng. Life Sci., 2015, 15, 30-38.[http://dx.doi.org/10.1002/elsc.201400173]
[4]
Langner, T.; GAhre, V. Fungal chitinases: function, regulation, and potential roles in plant/pathogen interactions. Curr. Genet., 2016, 62(2), 243-254.[http://dx.doi.org/10.1007/s00294-015-0530-x] [PMID: 26527115]
[5]
Adrangi, S.; Faramarzi, M.A.; Shahverdi, A.R.; Sepehrizadeh, Z. Purification and characterization of two extracellular endochitinases from Massilia timonae. Carbohydr. Res., 2010, 345(3), 402-407.[http://dx.doi.org/10.1016/j.carres.2009.11.015] [PMID: 19962135]
[6]
Hamid, R.; Khan, M.A.; Ahmad, M.; Ahmad, M.M.; Abdin, M.Z.; Musarrat, J.; Javed, S. Chitinases: An update. J. Pharm. Bioallied Sci., 2013, 5(1), 21-29.[http://dx.doi.org/10.4103/0975-7406.106559] [PMID: 23559820]
[7]
Annamalai, N.; Giji, S.; Arumugam, M.; Balasubramanian, T. Purification and characterization of chitinase from Micrococcus sp. AG84 isolated from marine environment. Afr. J. Microbiol. Res., 2010, 4, 2822-2827.
[8]
Wang, S.L.; Chen, S.J.; Wang, C.L. Purification and characterization of chitinases and chitosanases from a new species strain Pseudomonas sp. TKU015 using shrimp shells as a substrate. Carbohydr. Res., 2008, 343(7), 1171-1179.[http://dx.doi.org/10.1016/j.carres.2008.03.018] [PMID: 18378219]
[9]
Aliabadi, N.; Aminzadeh, S.; Karkhane, A.A.; Haghbeen, K. Thermostable chitinase from Cohnella sp. A01: isolation and product optimization. Braz. J. Microbiol., 2016, 47(4), 931-940.[http://dx.doi.org/10.1016/j.bjm.2016.07.009] [PMID: 27528085]
[10]
Neeraja, C.; Anil, K.; Purushotham, P.; Suma, K.; Sarma, P.; Moerschbacher, B.M.; Podile, A.R. Biotechnological approaches to develop bacterial chitinases as a bioshield against fungal diseases of plants. Crit. Rev. Biotechnol., 2010, 30(3), 231-241.[http://dx.doi.org/10.3109/07388551.2010.487258] [PMID: 20572789]
[11]
Frederiksen, R.F.; Paspaliari, D.K.; Larsen, T.; Storgaard, B.G.; Larsen, M.H.; Ingmer, H.; Palcic, M.M.; Leisner, J.J. Bacterial chitinases and chitin-binding proteins as virulence factors. Microbiology (Reading), 2013, 159(Pt 5), 833-847.[http://dx.doi.org/10.1099/mic.0.051839-0] [PMID: 23519157]
[12]
Patil, R.S.; Ghormade, V.; Deshpande, M.V. Chitinolytic enzymes: an exploration. Enzyme Microb. Technol., 2000, 26(7), 473-483.[http://dx.doi.org/10.1016/S0141-0229(00)00134-4] [PMID: 10771049]
[13]
Bhattacharya, D.; Nagpure, A.; Gupta, R.K. Bacterial chitinases: properties and potential. Crit. Rev. Biotechnol., 2007, 27(1), 21-28.[http://dx.doi.org/10.1080/07388550601168223] [PMID: 17364687]
[14]
Dahiya, N.; Tewari, R.; Hoondal, G.S. Biotechnological aspects of chitinolytic enzymes: a review. Appl. Microbiol. Biotechnol., 2006, 71(6), 773-782.[http://dx.doi.org/10.1007/s00253-005-0183-7] [PMID: 16249876]
[15]
Stephens, D.E.; Khan, F.I.; Singh, P.; Bisetty, K.; Singh, S.; Permaul, K. Creation of thermostable and alkaline stable xylanase variants by DNA shuffling. J. Biotechnol., 2014, 187, 139-146.[http://dx.doi.org/10.1016/j.jbiotec.2014.07.446] [PMID: 25093937]
[16]
Meena, S.; Gothwal, R.K.; Krishna Mohan, M.; Ghosh, P. Production and purification of a hyperthermostable chitinase from Brevibacillus formosus BISR-1 isolated from the Great Indian Desert soils. Extremophiles, 2014, 18(2), 451-462.[http://dx.doi.org/10.1007/s00792-014-0630-4] [PMID: 24473902]
[17]
Thirunavukkarasu, N.; Dhinamala, K.; Inbaraj, R.M. Production of chitin from two marine stomatopods Oratosquilla spp.(Crustacea). J. Chem. Pharm. Res., 2011, 2011(3), 353-359.
[18]
Adrangi, S.; Faramarzi, M.A. From bacteria to human: a journey into the world of chitinases. Biotechnol. Adv., 2013, 31(8), 1786-1795.[http://dx.doi.org/10.1016/j.biotechadv.2013.09.012] [PMID: 24095741]
[19]
Chandrasekaran, R.; Revathi, K.; Nisha, S.; Kirubakaran, S.A.; Sathish-Narayanan, S.; Senthil-Nathan, S. Physiological effect of chitinase purified from Bacillus subtilis against the tobacco cutworm Spodoptera litura Fab. Pestic. Biochem. Physiol., 2012, 104, 65-71.[http://dx.doi.org/10.1016/j.pestbp.2012.07.002]
[20]
Felse, P.A.; Panda, T. Production of microbial chitinases-A revisit. Bioprocess Eng., 2000, 23, 127-134.[http://dx.doi.org/10.1007/PL00009117]
[21]
Hartl, L.; Zach, S.; Seidl-Seiboth, V. Fungal chitinases: diversity, mechanistic properties and biotechnological potential. Appl. Microbiol. Biotechnol., 2012, 93(2), 533-543.[http://dx.doi.org/10.1007/s00253-011-3723-3] [PMID: 22134638]
[22]
Itoh, T.; Hibi, T.; Fujii, Y.; Sugimoto, I.; Fujiwara, A.; Suzuki, F.; Iwasaki, Y.; Kim, J.K.; Taketo, A.; Kimoto, H. Cooperative degradation of chitin by extracellular and cell surface-expressed chitinases from Paenibacillus sp. strain FPU-7. Appl. Environ. Microbiol., 2013, 79(23), 7482-7490.[http://dx.doi.org/10.1128/AEM.02483-13] [PMID: 24077704]
[23]
Nagpure, A.; Choudhary, B.; Gupta, R.K. Chitinases: in agriculture and human healthcare. Crit. Rev. Biotechnol., 2014, 34(3), 215-232.[http://dx.doi.org/10.3109/07388551.2013.790874] [PMID: 23859124]
[24]
Islam, R.; Datta, B. Diversity of chitinases and their industrial potential. Int. J. Appl. Res., 2015, 1, 55-60.
[25]
Horn, S.J.; Sarbotten, A.; Synstad, B.; Sikorski, P.; Sarlie, M.; Varum, K.M.; Eijsink, V.G. Endo/exo mechanism and processivity of family 18 chitinases produced by Serratia marcescens. FEBS J., 2006, 273(3), 491-503.[http://dx.doi.org/10.1111/j.1742-4658.2005.05079.x] [PMID: 16420473]
[26]
Oyeleye, A.; Normi, Y.M. Chitinase: diversity, limitations, and trends in engineering for suitable applications. Biosci. Rep., 2018, 38(4), 38.[http://dx.doi.org/10.1042/BSR20180323] [PMID: 30042170]
[27]
Lombard, V.; Golaconda Ramulu, H.; Drula, E.; Coutinho, P.M.; Henrissat, B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res., 2014, 42(Database issue), D490-D495.[http://dx.doi.org/10.1093/nar/gkt1178] [PMID: 24270786]
[28]
Seidl, V. Chitinases of filamentous fungi: a large group of diverse proteins with multiple physiological functions. Fungal Biol. Rev., 2008, 22, 36-42.[http://dx.doi.org/10.1016/j.fbr.2008.03.002]
[29]
Liu, T.; Zhou, Y.; Chen, L.; Chen, W.; Liu, L.; Shen, X.; Zhang, W.; Zhang, J.; Yang, Q. Structural insights into cellulolytic and chitinolytic enzymes revealing crucial residues of insect β-N-acetyl-D-hexosaminidase. PLoS One, 2012, 7(12), e52225.[http://dx.doi.org/10.1371/journal.pone.0052225] [PMID: 23300622]
[30]
Isogawa, D.; Fukuda, T.; Kuroda, K.; Kusaoke, H.; Kimoto, H.; Suye, S.; Ueda, M. Demonstration of catalytic proton acceptor of chitosanase from Paenibacillus fukuinensis by comprehensive analysis of mutant library. Appl. Microbiol. Biotechnol., 2009, 85(1), 95-104.[http://dx.doi.org/10.1007/s00253-009-2041-5] [PMID: 19517107]
[31]
Xia, W.; Liu, P.; Liu, J. Advance in chitosan hydrolysis by non-specific cellulases. Bioresour. Technol., 2008, 99(15), 6751-6762.[http://dx.doi.org/10.1016/j.biortech.2008.01.011] [PMID: 18328693]
[32]
Khan, F.I.; Govender, A.; Permaul, K.; Singh, S.; Bisetty, K. Thermostable chitinase II from Thermomyces lanuginosus SSBP: Cloning, structure prediction and molecular dynamics simulations. J. Theor. Biol., 2015, 374, 107-114.[http://dx.doi.org/10.1016/j.jtbi.2015.03.035] [PMID: 25861869]
[33]
Itoh, Y.; Kawase, T.; Nikaidou, N.; Fukada, H.; Mitsutomi, M.; Watanabe, T.; Itoh, Y. Functional analysis of the chitin-binding domain of a family 19 chitinase from Streptomyces griseus HUT6037: substrate-binding affinity and cis-dominant increase of antifungal function. Biosci. Biotechnol. Biochem., 2002, 66(5), 1084-1092.[http://dx.doi.org/10.1271/bbb.66.1084] [PMID: 12092819]
[34]
Van Aalten, D.M.; Synstad, B.; Brurberg, M.B.; Hough, E.; Riise, B.W.; Eijsink, V.G.; Wierenga, R.K. Structure of a two-domain chitotriosidase from Serratia marcescens at 1.9-Å resolution. Proc. Natl. Acad. Sci. (PNAS) USA., 2000, 97, 5842-5847.
[35]
Hoell, I.A.; Dalhus, B.; Heggset, E.B.; Aspmo, S.I.; Eijsink, V.G. Crystal structure and enzymatic properties of a bacterial family 19 chitinase reveal differences from plant enzymes. FEBS J., 2006, 273(21), 4889-4900.[http://dx.doi.org/10.1111/j.1742-4658.2006.05487.x] [PMID: 17010167]
[36]
Huet, J.; Rucktooa, P.; Clantin, B.; Azarkan, M.; Looze, Y.; Villeret, V.; Wintjens, R. X-ray structure of papaya chitinase reveals the substrate binding mode of glycosyl hydrolase family 19 chitinases. Biochemistry, 2008, 47(32), 8283-8291.[http://dx.doi.org/10.1021/bi800655u] [PMID: 18636748]
[37]
Ubhayasekera, W.; Rawat, R.; Ho, S.W.; Wiweger, M.; Von Arnold, S.; Chye, M.L.; Mowbray, S.L. The first crystal structures of a family 19 class IV chitinase: the enzyme from Norway spruce. Plant Mol. Biol., 2009, 71(3), 277-289.[http://dx.doi.org/10.1007/s11103-009-9523-9] [PMID: 19629717]
[38]
Yang, J.; Gan, Z.; Lou, Z.; Tao, N.; Mi, Q.; Liang, L.; Sun, Y.; Guo, Y.; Huang, X.; Zou, C.; Rao, Z.; Meng, Z.; Zhang, K.Q. Crystal structure and mutagenesis analysis of chitinase CrChi1 from the nematophagous fungus Clonostachys rosea in complex with the inhibitor caffeine. Microbiology (Reading), 2010, 156(Pt 12), 3566-3574.[http://dx.doi.org/10.1099/mic.0.043653-0] [PMID: 20829286]
[39]
Kezuka, Y.; Kojima, M.; Mizuno, R.; Suzuki, K.; Watanabe, T.; Nonaka, T. Structure of full-length class I chitinase from rice revealed by X-ray crystallography and small-angle X-ray scattering. Proteins, 2010, 78(10), 2295-2305.[http://dx.doi.org/10.1002/prot.22742] [PMID: 20544965]
[40]
Hsieh, Y.C.; Wu, Y.J.; Chiang, T.Y.; Kuo, C.Y.; Shrestha, K.L.; Chao, C.F.; Huang, Y.C.; Chuankhayan, P.; Wu, W.G.; Li, Y.K.; Chen, C.J. Crystal structures of Bacillus cereus NCTU2 chitinase complexes with chitooligomers reveal novel substrate binding for catalysis: a chitinase without chitin binding and insertion domains. J. Biol. Chem., 2010, 285(41), 31603-31615.[http://dx.doi.org/10.1074/jbc.M110.149310] [PMID: 20685646]
[41]
Busby, J.N.; Landsberg, M.J.; Simpson, R.M.; Jones, S.A.; Hankamer, B.; Hurst, M.R.; Lott, J.S. Structural analysis of Chi1 Chitinase from Yen-Tc: the multisubunit insecticidal ABC toxin complex of Yersinia entomophaga. J. Mol. Biol., 2012, 415(2), 359-371.[http://dx.doi.org/10.1016/j.jmb.2011.11.018] [PMID: 22108167]
[42]
Bibra, M.; Krishnaraj, R.N.; Sani, R.K. An overview on extremophilic chitinases.In Extremophilic Enzymatic Processing of Lignocellulosic Feedstocks to Bioenergy. Springer International Publishing AG Cham Switzerland, 2017, 225-247.[http://dx.doi.org/10.1007/978-3-319-54684-1_12]
[43]
Satyanarayana, T.; Littlechild, J.; Kawarabayasi, Y. Thermophilic microbes in environmental and industrial biotechnology. Springer: Dordrecht, 2013.[http://dx.doi.org/10.1007/978-94-007-5899-5]
[44]
Sarma, P.V.; Prakash, J.M.; Das, S.N.; Kaur, M.; Purushotham, P.; Podile, A.R. Microbial chitinases: natural sources, mutagenesis, and directed evolution to obtain thermophilic counterparts.In Thermophilic Microbes in Environmental and Industrial Biotechnology, Satyanarayana, T.; Littlechild, J.; Kawarabayasi, Y. Eds.; Springer: Dordrecht, 2013, , 649-669.[http://dx.doi.org/10.1007/978-94-007-5899-5_24]
[45]
Gao, J.; Bauer, M.W.; Shockley, K.R.; Pysz, M.A.; Kelly, R.M. Growth of hyperthermophilic archaeon Pyrococcus furiosus on chitin involves two family 18 chitinases. Appl. Environ. Microbiol., 2003, 69(6), 3119-3128.[http://dx.doi.org/10.1128/AEM.69.6.3119-3128.2003] [PMID: 12788706]
[46]
Andronopoulou, E.; Vorgias, C.E. Purification and characterization of a new hyperthermostable, allosamidin-insensitive and denaturation-resistant chitinase from the hyperthermophilic archaeon Thermococcus chitonophagus. Extremophiles, 2003, 7(1), 43-53.[http://dx.doi.org/10.1007/s00792-002-0294-3] [PMID: 12579379]
[47]
Tanaka, T.; Fukui, T.; Imanaka, T. Different cleavage specificities of the dual catalytic domains in chitinase from the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1. J. Biol. Chem., 2001, 276(38), 35629-35635.[http://dx.doi.org/10.1074/jbc.M105919200] [PMID: 11468293]
[48]
Hobel, C.F.; Hreggvidsson, G.O.; Marteinsson, V.T.; Bahrani-Mougeot, F.; Einarsson, J.M.; Kristjansson, J.K. Cloning, expression, and characterization of a highly thermostable family 18 chitinase from Rhodothermus marinus. Extremophiles, 2005, 9(1), 53-64.[http://dx.doi.org/10.1007/s00792-004-0422-3] [PMID: 15583965]
[49]
Tsujibo, H.; Kubota, T.; Yamamoto, M.; Miyamoto, K.; Inamori, Y. Characterization of chitinase genes from an alkaliphilic actinomycete, Nocardiopsis prasina OPC-131. Appl. Environ. Microbiol., 2003, 69(2), 894-900.[http://dx.doi.org/10.1128/AEM.69.2.894-900.2003] [PMID: 12571009]
[50]
Kudan, S.; Pichyangkura, R. Purification and characterization of thermostable chitinase from Bacillus licheniformis SK-1. Appl. Biochem. Biotechnol., 2009, 157(1), 23-35.[http://dx.doi.org/10.1007/s12010-008-8328-7] [PMID: 19190863]
[51]
Zverlov, V.V.; Fuchs, K.P.; Schwarz, W.H. Chi18A, the endochitinase in the cellulosome of the thermophilic, cellulolytic bacterium Clostridium thermocellum. Appl. Environ. Microbiol., 2002, 68(6), 3176-3179.[http://dx.doi.org/10.1128/AEM.68.6.3176-3179.2002] [PMID: 12039789]
[52]
Gohel, V.; Naseby, D.C. Thermalstabilization of chitinolytic enzymes of Pantoea dispersa. Biochem. Eng. J., 2007, 35, 150-157.[http://dx.doi.org/10.1016/j.bej.2007.01.009]
[53]
Bhushan, B. Production and characterization of a thermostable chitinase from a new alkalophilic Bacillus sp. BG-11. J. Appl. Microbiol., 2000, 88(5), 800-808.[http://dx.doi.org/10.1046/j.1365-2672.2000.01016.x] [PMID: 10792540]
[54]
Nawani, N.N.; Kapadnis, B.P. Optimization of chitinase production using statistics based experimental designs. Process Biochem., 2005, 40, 651-660.[http://dx.doi.org/10.1016/j.procbio.2004.01.048]
[55]
Gomes, R.C.; Semedo, L.T.; Soares, R.M.; Linhares, L.F.; Ulhoa, C.J.; Alviano, C.S.; Coelho, R.R. Purification of a thermostable endochitinase from Streptomyces RC1071 isolated from a cerrado soil and its antagonism against phytopathogenic fungi. J. Appl. Microbiol., 2001, 90(4), 653-661.[http://dx.doi.org/10.1046/j.1365-2672.2001.01294.x] [PMID: 11309080]
[56]
Lien, T.S.; Yu, S.T.; Wu, S.T.; Too, J.R. Induction and purification of a thermophilic chitinase produced by Aeromonas sp. DYU-too7 using glucosamine. Biotechnol. Bioprocess. Engr, 2007, 12, 610-617.[http://dx.doi.org/10.1007/BF02931076]
[57]
Li, A.N.; Yu, K.; Liu, H.Q.; Zhang, J.; Li, H.; Li, D.C. Two novel thermostable chitinase genes from thermophilic fungi: cloning, expression and characterization. Bioresour. Technol., 2010, 101(14), 5546-5551.[http://dx.doi.org/10.1016/j.biortech.2010.02.058] [PMID: 20223653]
[58]
Karthik, N.; Akanksha, K.; Pandey, A.; Pandey, A. Production, purification and properties of fungal chitinases--a review. Indian J. Exp. Biol., 2014, 52(11), 1025-1035.[PMID: 25434097]
[59]
Chen, W.M.; Chen, C.S.; Jiang, S.T. Purification and characterization of an extracellular chitinase from Rhizopus oryzae. J. Mar. Sci. Technol., 2013, 21, 361-366.
[60]
Alves, T.B.; de Oliveira Ornela, P.H.; de Oliveira, A.H.C.; Jorge, J.A.; Guimaraes, L.H.S. Production and characterization of a thermostable antifungal chitinase secreted by the filamentous fungus Aspergillus niveus under submerged fermentation. 3 Biotech., 2018, 8(8), 369.
[61]
Wang, S.; Moyne, A.; Thottappilly, G.; Wu, S.; Locy, R.D.; Singh, N.K. Purification and characterization of a Bacillus cereus exochitinase. Enzyme Microb. Technol., 2001, 28(6), 492-498.[http://dx.doi.org/10.1016/S0141-0229(00)00362-8] [PMID: 11267643]
[62]
Yuli, P.E.; Suhartono, M.T.; Rukayadi, Y.; Hwang, J.K.; Pyun, Y.R. Characteristics of thermostable chitinase enzymes from the indonesian Bacillus sp. 13.26. Enzyme Microb. Technol., 2004, 35, 147-153.[http://dx.doi.org/10.1016/j.enzmictec.2004.03.017]
[63]
Kuzu, S.B.; GA1/4venmez, H.K.; Denizci, A.A. Production of a thermostable and alkaline chitinase by Bacillus thuringiensis subsp. kurstaki strain HBK-51. Biotechnol. Res. Int., 2012, 2012, 135498.[http://dx.doi.org/10.1155/2012/135498] [PMID: 23304523]
[64]
Vahed, M.; Motalebi, E.; Rigi, G.; Akbari Noghabi, K.; Soudi, M.R.; Sadeghi, M.; Ahmadian, G. Improving the chitinolytic activity of Bacillus pumilus SG2 by random mutagenesis. J. Microbiol. Biotechnol., 2013, 23(11), 1519-1528.[http://dx.doi.org/10.4014/jmb.1301.01048] [PMID: 23867702]
[65]
Singh, A.K.; Chhatpar, H.S. Purification and characterization of chitinase from Paenibacillus sp. D1. Appl. Biochem. Biotechnol., 2011, 164(1), 77-88.[http://dx.doi.org/10.1007/s12010-010-9116-8] [PMID: 21049291]
[66]
Guo, R.F.; Shi, B.S.; Li, D.C.; Wen, M.A.; Qing, W.E. Purification and characterization of a novel thermostable chitinase from Thermomyces lanuginosus SY2 and cloning of its encoding gene. Agric. Sci. China, 2008, 7, 1458-1465.[http://dx.doi.org/10.1016/S1671-2927(08)60403-4]
[67]
Malik, A. Purification and properties of plant chitinases: a review. J. Food Biochem., 2019, 43(3), e12762.[http://dx.doi.org/10.1111/jfbc.12762]
[68]
Rao, D.H.; Gowda, L.R. Abundant class III acidic chitinase homologue in tamarind (Tamarindus indica) seed serves as the major storage protein. J. Agric. Food Chem., 2008, 56(6), 2175-2182.[http://dx.doi.org/10.1021/jf073183i] [PMID: 18298067]
[69]
Onaga, S.; Chinen, K.; Ito, S.; Taira, T. Highly thermostable chitinase from pineapple: cloning, expression, and enzymatic properties. Process Biochem., 2011, 46, 695-700.[http://dx.doi.org/10.1016/j.procbio.2010.11.015]
[70]
Li, Y.C.; Chang, C.T.; Hsiao, E.S.; Hsu, J.S.; Huang, J.W.; Tzen, J.T. Purification and characterization of an antifungal chitinase in jelly fig (Ficus awkeotsang) achenes. Plant Cell Physiol., 2003, 44(11), 1162-1167.[http://dx.doi.org/10.1093/pcp/pcg141] [PMID: 14634152]
[71]
Kopparapu, N.K.; Liu, Z.; Yan, Q.; Jiang, Z.; Zhang, S. A novel thermostable chitinase (PJC) from pomegranate (Punica granatum) juice. Food Chem., 2011, 127(4), 1569-1575.[http://dx.doi.org/10.1016/j.foodchem.2011.02.020]
[72]
Kopparapu, N.K.; Liu, Z.; Fei, F.; Yan, Q.; Jiang, Z. Purification and characterization of a chitinase (sAMC) with antifungal activity from seeds of Astragalus membranaceus. Process Biochem., 2011, 46(6), 1370-1374.[http://dx.doi.org/10.1016/j.procbio.2011.02.015]
[73]
Wang, S.; Ye, X.; Chen, J.; Rao, P. A novel chitinase isolated from Vicia faba and its antifungal activity. Food Res. Int., 2012, 45(1), 116-122.[http://dx.doi.org/10.1016/j.foodres.2011.10.010]
[74]
Matsumoto, Y.; Saucedo-Castaneda, G.; Revah, S.; Shirai, K. Production of β-N-acetylhexosaminidase of Verticillium lecanii by solid state and submerged fermentations utilizing shrimp waste silage as substrate and inducer. Process Biochem., 2004, 39(6), 665-671.[http://dx.doi.org/10.1016/S0032-9592(03)00140-7]
[75]
Jholapara, R.J.; Mehta, R.S.; Bhagwat, A.M.; Sawant, C.S. Exploring and optimizing the potential of chitinase production by isolated Bacillus spp. Int. J. Pharm. Pharm. Sci., 2013, 5, 412-418.
[76]
Cheba, B.A.; Zaghloul, T.I.; El-Mahdy, A.R. EL-Massry, M.H. Enhanced production of Bacillus sp. R2 chitinase through cell immobilization. ACT-Biotechnol. Res. Commun., 2011, 1, 8-13.
[77]
Aunpad, R.; Panbangred, W. Cloning and characterization of the constitutively expressed chitinase C gene from a marine bacterium, Salinivibrio costicola strain 5SM-1. J. Biosci. Bioeng., 2003, 96(6), 529-536.[http://dx.doi.org/10.1016/S1389-1723(04)70145-0] [PMID: 16233569]
[78]
Bouacem, K.; Laribi-Habchi, H.; Mechri, S.; Hacene, H.; Jaouadi, B.; Bouanane-Darenfed, A. Biochemical characterization of a novel thermostable chitinase from Hydrogenophilus hirschii strain KB-DZ44. Int. J. Biol. Macromol., 2018, 106, 338-350.[http://dx.doi.org/10.1016/j.ijbiomac.2017.08.026] [PMID: 28827133]
[79]
Oku, T.; Ishikawa, K. Analysis of the hyperthermophilic chitinase from Pyrococcus furiosus: activity toward crystalline chitin. Biosci. Biotechnol. Biochem., 2006, 70(7), 1696-1701.[http://dx.doi.org/10.1271/bbb.60031] [PMID: 16861805]
[80]
Nimlos, M.R.; Matthews, J.F.; Crowley, M.F.; Walker, R.C.; Chukkapalli, G.; Brady, J.W.; Adney, W.S.; Cleary, J.M.; Zhong, L.; Himmel, M.E. Molecular modeling suggests induced fit of Family I carbohydrate-binding modules with a broken-chain cellulose surface. Protein Eng. Des. Sel., 2007, 20(4), 179-187.[http://dx.doi.org/10.1093/protein/gzm010] [PMID: 17430975]
[81]
Varnai, A.; Siika-Aho, M.; Viikari, L. Carbohydrate-binding modules (CBMs) revisited: reduced amount of water counterbalances the need for CBMs. Biotechnol. Biofuels, 2013, 6(1), 30.[http://dx.doi.org/10.1186/1754-6834-6-30] [PMID: 23442543]
[82]
Zakariassen, H.; Aam, B.B.; Horn, S.J.; Varum, K.M.; SA,rlie, M.; Eijsink, V.G. Aromatic residues in the catalytic center of chitinase A from Serratia marcescens affect processivity, enzyme activity, and biomass converting efficiency. J. Biol. Chem., 2009, 284(16), 10610-10617.[http://dx.doi.org/10.1074/jbc.M900092200] [PMID: 19244232]
[83]
Andreini, C.; Bertini, I.; Cavallaro, G.; Holliday, G.L.; Thornton, J.M. Metal ions in biological catalysis: from enzyme databases to general principles. J. Biol. Inorg. Chem., 2008, 13(8), 1205-1218.[http://dx.doi.org/10.1007/s00775-008-0404-5] [PMID: 18604568]
[84]
Dai, D.H.; Hu, W.L.; Huang, G.R.; Li, W. Purification and characterization of a novel extracellular chitinase from thermophilic Bacillus sp. Hu1. Afr. J. Biotechnol., 2011, 10, 2476-2485.
[85]
Nawani, N.N.; Kapadnis, B.P.; Das, A.D.; Rao, A.S.; Mahajan, S.K. Purification and characterization of a thermophilic and acidophilic chitinase from Microbispora sp. V2. J. Appl. Microbiol., 2002, 93, 965-75.[http://dx.doi.org/10.1046/j.1365-2672.2002.01766.x]
[86]
Lee, Y.S.; Park, I.H.; Yoo, J.S.; Chung, S.Y.; Lee, Y.C.; Cho, Y.S.; Ahn, S.C.; Kim, C.M.; Choi, Y.L. Cloning, purification, and characterization of chitinase from Bacillus sp. DAU101. Bioresour. Technol., 2007, 98(14), 2734-2741.[http://dx.doi.org/10.1016/j.biortech.2006.09.048] [PMID: 17107787]
[87]
Han, Y.; Yang, B.; Zhang, F.; Miao, X.; Li, Z. Characterization of antifungal chitinase from marine Streptomyces sp. DA11 associated with South China Sea sponge Craniella australiensis. Mar. Biotechnol. (NY), 2009, 11(1), 132-140.[http://dx.doi.org/10.1007/s10126-008-9126-5] [PMID: 18626709]
[88]
Kuddus, M.; Ahmad, L.Z. Isolation of novel chitinolytic bacteria and production optimization of extracellular chitinase. J. Genet. Eng. Biotechnol., 2013, 11, 39-46.[http://dx.doi.org/10.1016/j.jgeb.2013.03.001]
[89]
Cheba, B.A.; Zaghloul, T.I. EL-Massry, M.H.; EL-Mahdy, A.R. Effect of metal ions, chemical agents, and organic solvent on Bacillus sp. R2 chitinase activity. Procedia. Technol., 2016, 22, 465-470.[http://dx.doi.org/10.1016/j.protcy.2016.01.090]
[90]
Prakash, D.; Nawani, N.; Kapadnis, B. Cloning, expression and characterization of thermophilic and alkalophilic N-acetylglucosaminidase from Streptomyces sp. NK52 for the targeted production of N-acetylglucosamine. Proc. Natl. Acad. Sci., 2014, 83, 431-437.[http://dx.doi.org/10.1007/s40011-013-0158-x]
[91]
Toharisman, A.; Suhartono, M.T.; Spindler-Barth, M.; Hwang, J.K.; Pyun, Y.R. Purification and characterization of a thermostable chitinase from Bacillus licheniformis Mb-2. World J. Microbiol. Biotechnol., 2005, 21, 733-738.[http://dx.doi.org/10.1007/s11274-004-4797-1]
[92]
Liu, D.; Cai, J.; Xie, C.C.; Liu, C.; Chen, Y.H. Purification and partial characterization of a 36-kDa chitinase from Bacillus thuringiensis subsp. colmeri, and its biocontrol potential. Enzyme Microb. Technol., 2010, 46, 252-256.[http://dx.doi.org/10.1016/j.enzmictec.2009.10.007]
[93]
Chrisnasari, R.; Yasaputera, S.; Christianto, P.; Santoso, V.I.; Pantjajani, T. Production and characterization of chitinases from thermophilic bacteria isolated from prataan hot spring, East Java. J. Math. Fundamental Sci., 2016, 48, 149-163.[http://dx.doi.org/10.5614/j.math.fund.sci.2016.48.2.6]
[94]
Wen, C.M.; Tseng, C.S.; Cheng, C.Y.; Li, Y.K. Purification, characterization and cloning of a chitinase from Bacillus sp. NCTU2. Biotechnol. Appl. Biochem., 2002, 35(3), 213-219.[http://dx.doi.org/10.1042/BA20020001] [PMID: 12074700]
[95]
Li, J.G.; Jiang, Z.Q.; Xu, L.P.; Sun, F.F.; Guo, J.H. Characterization of chitinase secreted by Bacillus cereus strain CH2 and evaluation of its efficacy against Verticillium wilt of eggplant. BioControl, 2008, 53, 931-944.[http://dx.doi.org/10.1007/s10526-007-9144-7]
[96]
Karthik, N.; Binod, P.; Pandey, A. Chitinases. In: Current Developments in Biotechnology and Bioengineering, Pandey, A.; Negi, S.; Soccol, C.R. Eds.; Elsevier , 2017, , 335-368.[http://dx.doi.org/10.1016/B978-0-444-63662-1.00015-4]
[97]
Hjort, K.; Presti, I.; ElvAng, A.; Marinelli, F.; SjAling, S. Bacterial chitinase with phytopathogen control capacity from suppressive soil revealed by functional metagenomics. Appl. Microbiol. Biotechnol., 2014, 98(6), 2819-2828.[http://dx.doi.org/10.1007/s00253-013-5287-x] [PMID: 24121932]
[98]
Ramírez, M.V.; CalzadA-az, L. Industrial enzymes and metabolites from Actinobacteria in food and medicine industry.In Actinobacteria - Basics and Biotechnological Applications, Dhanasekaran, D.; Jiang, Y. 2016, , 315.[http://dx.doi.org/10.5772/61286]
[99]
Subbanna, A.R.; Rajasekhara, H.; Stanley, J.; Mishra, K.K.; Pattanayak, A. Pesticidal prospectives of chitinolytic bacteria in agricultural pest management. Soil Biol. Biochem., 2018, 116, 52-66.[http://dx.doi.org/10.1016/j.soilbio.2017.09.019]
[100]
Nurdebyandaru, N.; Mubarik, N.R.; Prawasti, T.S. Chitinolytic bacteria isolated from Chili rhizosphere: chitinase characterization and application as biocontrol for Aphis gossypii. Microbiology Indonesia, 2010, 4(3), 103-107.
[101]
Koga, D. Application of chitinase in agriculture. J. Metals. Mater. Min., 2005, 15, 33-36.
[102]
Wang, J.; Chen, Z.; Du, J.; Sun, Y.; Liang, A. Novel insect resistance in Brassica napus developed by transformation of chitinase and scorpion toxin genes. Plant Cell Rep., 2005, 24(9), 549-555.[http://dx.doi.org/10.1007/s00299-005-0967-3] [PMID: 16028062]
[103]
Kabir, K.E.; Sugimoto, H.; Tado, H.; Endo, K.; Yamanaka, A.; Tanaka, S.; Koga, D. Effect of Bombyx mori chitinase against Japanese pine sawyer (Monochamus alternatus) adults as a biopesticide. Biosci. Biotechnol. Biochem., 2006, 70(1), 219-229.[http://dx.doi.org/10.1271/bbb.70.219] [PMID: 16428840]
[104]
Suganthi, M.; Senthilkumar, P.; Arvinth, S.; Chandrashekara, K.N. Chitinase from Pseudomonas fluorescens and its insecticidal activity against Helopeltis theivora. J. Gen. Appl. Microbiol., 2017, 63(4), 222-227.[http://dx.doi.org/10.2323/jgam.2016.11.001] [PMID: 28680004]
[105]
Al-Ahmadi, K.J.; Yazdi, M.T.; Najafi, M.F.; Shahverdi, A.R.; Faramarzi, M.A.; Zarrini, G.; Behravan, J. Optimization of medium and cultivation conditions for chitinase production by the newly isolated: Aeromonas sp. Biotechnol., 2008, 7, 266-272.[http://dx.doi.org/10.3923/biotech.2008.266.272]
[106]
Yano, S.; Wakayama, M.; Tachiki, T. Cloning and expression of an α-1,3-glucanase gene from Bacillus circulans KA-304: the enzyme participates in protoplast formation of Schizophyllum commune. Biosci. Biotechnol. Biochem., 2006, 70(7), 1754-1763.[http://dx.doi.org/10.1271/bbb.60095] [PMID: 16861810]
[107]
Manivasagan, P.; Venkatesan, J.; Sivakumar, K.; Kim, S.K. Pharmaceutically active secondary metabolites of marine actinobacteria. Microbiol. Res., 2014, 169(4), 262-278.[http://dx.doi.org/10.1016/j.micres.2013.07.014] [PMID: 23958059]
[108]
Waghmare, S.R.; Ghosh, J.S. Chitobiose production by using a novel thermostable chitinase from Bacillus licheniformis strain JS isolated from a mushroom bed. Carbohydr. Res., 2010, 345(18), 2630-2635.[http://dx.doi.org/10.1016/j.carres.2010.09.023] [PMID: 20970120]