Abstract
Mesoporous cuttlebone powder of Sepia officinalis (CBP) was characterized and used as matrix for the immobilization of Bacillus subtilis AKL 13 lipase (BsL). Particle size and surface area of the matrix used for enzyme immobilization were 89.95 µm and 1.631 m2 g−1, respectively. Remarkable thermostability (54% of weight loss at 700 °C) of CBP was determined in TGA profile. The lipase immobilization process parameters were sequentially optimized by response surface methodology followed by artificial neural network and genetic algorithm. The maximum lipase loading capacity of CBP was 255 mg g−1 of support. Immobilized lipase (CBP-BsL) showed maximum specific activity of 5808 U mg−1 of protein in p-nitrophenol palmitate hydrolysis. Adsorption isotherm study revealed that the binding of lipase on the surface of CBP was Langmuir and the binding was physical adsorption. CBP-BsL showed lower activation energy (51.4 KJ mol−1) and higher thermal stability with half-lives of 13.3 h at 50 °C. Higher activity retention in nonpolar solvents and 69% of operational stability after 15 cycle of reaction were measured.
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References
Adeogun AI, Kareeem SO, Adebayo OS, Balogun SA (2017) Comparative adsorption of amylase, protease and lipase on ZnFe(2)O(4): kinetics, isothermal and thermodynamics studies. 3 Biotech 7:198. https://doi.org/10.1007/s13205-017-0859-6
Adlercreutz P (2013) Immobilisation and application of lipases in organic media. Chem Soc Rev 42:6406–6436. https://doi.org/10.1039/c3cs35446f
Amirkhani L, Moghaddas J, Jafarizadeh-Malmiri H (2016) Candida rugosa lipase immobilization on magnetic silica aerogel nanodispersion. RSC Adv 6:12676–12687. https://doi.org/10.1039/c5ra24441b
Balcar H, Čejka J, Sedláček J, Svoboda J, Bastl Z, Pacovská M, Vohlídal J (2003) Mesoporous molecular sieves immobilized catalysts for polymerization of phenylacetylene and its derivatives. In: Imamoglu Y, Bencze L (eds) Novel metathesis chemistry: well-defined initiator systems for specialty chemical synthesis, tailored polymers and advanced material applications. Springer, Netherlands, pp 155–165. https://doi.org/10.1007/978-94-010-0066-6_11
Biji GD, Arun A, Muthulakshmi E, Vijayaraghavan P, Arasu MV, Al-Dhabi NA (2016) Bio-prospecting of cuttle fish waste and cow dung for the production of fibrinolytic enzyme from Bacillus cereus IND5 in solid state fermentation. 3 Biotech 6:231. https://doi.org/10.1007/s13205-016-0553-0
Brito MJP, Veloso CM, Bonomo RCF, Fontan RDCI, Santos LS, Monteiro KA (2017) Activated carbons preparation from yellow mombin fruit stones for lipase immobilization. Fuel Process Technol 156:421–428. https://doi.org/10.1016/j.fuproc.2016.10.003
Cadman J, Zhou S, Chen Y, Li Q (2012) Cuttlebone: characterisation, application and development of biomimetic materials. J Bionic Eng 9:367–376. https://doi.org/10.1016/S1672-6529(11)60132-7
da Silva TM, Pessela BC, da Silva JCR, Lima MS, Jorge JA, Guisan JM, Polizeli MdLTM (2014) Immobilization and high stability of an extracellular β-glucosidase from Aspergillus japonicus by ionic interactions. J Mol Catal B Enzym 104:95–100. https://doi.org/10.1016/j.molcatb.2014.02.018
Díaz Ramos M, Giraldo Gómez GI, Sanabria González N (2014) Immobilization of Candida rugosa lipase on bentonite modified with benzyltriethylammonium chloride. J Mol Catal B Enzym 99:79–84. https://doi.org/10.1016/j.molcatb.2013.10.021
Dong H, Li J, Li Y, Hu L, Luo D (2012) Improvement of catalytic activity and stability of lipase by immobilization on organobentonite. Chem Eng J 181–182:590–596. https://doi.org/10.1016/j.cej.2011.11.095
Dong H, Li Y, Li J, Sheng G, Chen H (2013) Comparative study on lipases immobilized onto bentonite and modified bentonites and their catalytic properties. Ind Eng Chem Res 52:9030–9037. https://doi.org/10.1021/ie4001986
Fan M, Li T, Hu J, Cao R, Wei X, Shi X, Ruan W (2017) Artificial neural network modeling and genetic algorithm optimization for cadmium removal from aqueous solutions by reduced graphene oxide-supported nanoscale zero-valent iron (nZVI/rGO) composites. Materials (Basel) 10:544. https://doi.org/10.3390/ma10050544
Fatiha B, Sameh B, Youcef S, Zeineddine D, Nacer R (2013) Comparison of artificial neural network (ANN) and response surface methodology (RSM) in optimization of the immobilization conditions for lipase from Candida rugosa on Amberjet((R)) 4200-Cl. Prep Biochem Biotechnol 43:33–47. https://doi.org/10.1080/10826068.2012.693899
Ghodsinia SSE, Akhlaghinia B, Jahanshahi R (2016) Direct access to stabilized CuI using cuttlebone as a natural-reducing support for efficient CuAAC click reactions in water. RSC Adv 6:63613–63623. https://doi.org/10.1039/c6ra13314b
Gholamzadeh P, Mohammadi Ziarani G, Badiei A (2017) Immobilization of lipases onto the SBA-15 mesoporous silica. Biocatalysis Biotransform. https://doi.org/10.1080/10242422.2017.1308495
Gricajeva A, Bendikiene V, Kalediene L (2016) Lipase of Bacillus stratosphericus L1: cloning, expression and characterization. Int J Biol Macromol 92:96–104. https://doi.org/10.1016/j.ijbiomac.2016.07.015
Gupta R, Gupta N, Rathi P (2004) Bacterial lipases: an overview of production, purification and biochemical properties. Appl Microbiol Biotechnol 64:763–781. https://doi.org/10.1007/s00253-004-1568-8
Jacoby J, Pasc A, Carteret C, Dupire F, Stébé MJ, Coupard V, Blin JL (2013) Ordered mesoporous materials containing Mucor Miehei Lipase as biocatalyst for transesterification reaction. Process Biochem 48:831–837. https://doi.org/10.1016/j.procbio.2013.04.003
Jia X, Qian W, Wu D, Wei D, Xu G, Liu X (2009) Cuttlebone-derived organic matrix as a scaffold for assembly of silver nanoparticles and application of the composite films in surface-enhanced Raman scattering. Colloids Surf B 68:231–237. https://doi.org/10.1016/j.colsurfb.2008.10.017
Lage FA, Bassi JJ, Corradini MC, Todero LM, Luiz JH, Mendes AA (2016a) Preparation of a biocatalyst via physical adsorption of lipase from Thermomyces lanuginosus on hydrophobic support to catalyze biolubricant synthesis by esterification reaction in a solvent-free system. Enzyme Microb Technol 84:56–67. https://doi.org/10.1016/j.enzmictec.2015.12.007
Lage FAP, Bassi JJ, Corradini MCC, Todero LM, Luiz JHH, Mendes AA (2016b) Preparation of a biocatalyst via physical adsorption of lipase from Thermomyces lanuginosus on hydrophobic support to catalyze biolubricant synthesis by esterification reaction in a solvent-free system. Enzyme Microbial Technol 84:56–67. https://doi.org/10.1016/j.enzmictec.2015.12.007
Lorenzoni ASG, Graebin NG, Martins AB, Fernandez-Lafuente R, Ayub MAZ, Rodrigues RC (2012) Optimization of pineapple flavour synthesis by esterifcation catalysed by immobilized lipase from Rhizomucor miehei. Flavour Fragrance J 27:196–200. https://doi.org/10.1002/ffj.3088
Macha IJ, Ben-Nissan B (2018) Marine skeletons: towards hard tissue repair and regeneration. Mar Drugs. https://doi.org/10.3390/md16070225
Manoel EA, dos Santos JCS, Freire DMG, Rueda N, Fernandez-Lafuente R (2015) Immobilization of lipases on hydrophobic supports involves the open form of the enzyme. Enzyme Microbial Technol 71:53–57. https://doi.org/10.1016/j.enzmictec.2015.02.001
Miranda JS, Silva NCA, Bassi JJ, Corradini MCC, Lage FAP, Hirata DB, Mendes AA (2014) Immobilization of Thermomyces lanuginosus lipase on mesoporous poly-hydroxybutyrate particles and application in alkyl esters synthesis: isotherm, thermodynamic and mass transfer studies. Chem Eng J 251:392–403. https://doi.org/10.1016/j.cej.2014.04.087
Olusesan AT et al (2011) Purification, characterization and thermal inactivation kinetics of a non-regioselective thermostable lipase from a genotypically identified extremophilic Bacillus subtilis NS 8. New Biotechnol 28:738–745. https://doi.org/10.1016/j.nbt.2011.01.002
Orrego CE, Valencia JS, Zapata C (2009) Candida rugosa lipase supported on high crystallinity chitosan as biocatalyst for the synthesis of 1-butyl oleate. Catal Lett 129:312. https://doi.org/10.1007/s10562-009-9857-6
Pahujani S, Kanwar SS, Chauhan G, Gupta R (2008) Glutaraldehyde activation of polymer Nylon-6 for lipase immobilization: enzyme characteristics and stability. Bioresour Technol 99:2566–2570. https://doi.org/10.1016/j.biortech.2007.04.042
Palaveniene A, Tamburaci S, Kimna C, Glambaite K, Baniukaitiene O, Tihminlioglu F, Liesiene J (2019) Osteoconductive 3D porous composite scaffold from regenerated cellulose and cuttlebone-derived hydroxyapatite. J Biomater Appl 33:876–890. https://doi.org/10.1177/0885328218811040
Periasamy K, Mohankumar GC (2015) Sea coral-derived cuttlebone reinforced epoxy composites: characterization and tensile properties evaluation with mathematical models. J Compos Mater 50:807–823. https://doi.org/10.1177/0021998315581512
Poompradub S, Ikeda Y, Kokubo Y, Shiono T (2008) Cuttlebone as reinforcing filler for natural rubber. Eur Polymer J 44:4157–4164. https://doi.org/10.1016/j.eurpolymj.2008.09.015
Raghuvanshi S, Gupta R (2010) Advantages of the immobilization of lipase on porous supports over free enzyme. Protein Pept Lett 17:1412–1416
Rodrigues D, Cavalcante G, Ferreira A, Gonçalves L (2008) Immobilization of Candida antarctica lipase type B by adsorption on activated carbon. Chem Biochem Eng Q 22:9
Saleem M, Rashid MH, Jabbar A, Perveen R, Khalid AM, Rajoka MI (2005) Kinetic and thermodynamic properties of an immobilized endoglucanase from Arachniotus citrinus. Process Biochem 40:849–855. https://doi.org/10.1016/j.procbio.2004.02.026
Sankar K, Achary A (2017) Synthesis of feruloyl ester using Bacillus subtilis AKL 13 Lipase Immobilized on Celite(R) 545. Food Technol Biotechnol 55:542–552
Sankar K, Achary A, Mehala N, Rajendran L (2017) Empirical and analytical correlation of the reaction kinetics parameters of cuttle bone powder immobilized lipase catalyzed ethyl ferulate synthesis. Catal Lett 147:2232–2245. https://doi.org/10.1007/s10562-017-2108-3
Singh AK, Mukhopadhyay M (2014) Immobilization of Candida antarctica lipase onto cellulose acetate-coated Fe2O3 nanoparticles for glycerolysis of olive oil. Korean J Chem Eng 31:1225–1232. https://doi.org/10.1007/s11814-014-0020-8
Souissi N, Ellouz-Triki Y, Bougatef A, Blibech M, Nasri M (2008) Preparation and use of media for protease-producing bacterial strains based on by-products from Cuttlefish (Sepia officinalis) and wastewaters from marine-products processing factories. Microbiol Res 163:473–480. https://doi.org/10.1016/j.micres.2006.07.013
Tran DT, Chen CL, Chang JS (2012) Immobilization of Burkholderia sp. lipase on a ferric silica nanocomposite for biodiesel production. J Biotechnol 158:112–119
Ulker C, Gokalp N, Guvenilir Y (2016) Immobilization of Candida antarctica lipase B (CALB) on surface-modified rice husk ashes (RHA) via physical adsorption and cross-linking methods. Biocatal Biotransform 34:172–180. https://doi.org/10.1080/10242422.2016.1247818
van Pouderoyen G, Eggert T, Jaeger K-E, Dijkstra BW (2001) The crystal structure of Bacillus subtilis lipase: a minimal α/β hydrolase fold enzyme1. J Mol Biol 309:215–226. https://doi.org/10.1006/jmbi.2001.4659
Yu WH, Tong DS, Fang M, Shao P, Zhou CH (2015) Immobilization of Candida rugosa lipase on MSU-H type mesoporous silica for selective esterification of conjugated linoleic acid isomers with ethanol. J Mol Catal B Enzym 111:43–50. https://doi.org/10.1016/j.molcatb.2014.11.003
Yücel Y (2012) Optimization of immobilization conditions of Thermomyces lanuginosus lipase on olive pomace powder using response surface methodology. Biocatal Agric Biotechnol 1:39–44. https://doi.org/10.1016/j.bcab.2011.08.009
Yücel Y, Demir C, Dizge N, Keskinler B (2011) Lipase immobilization and production of fatty acid methyl esters from canola oil using immobilized lipase. Biomass Bioenerg 35:1496–1501. https://doi.org/10.1016/j.biombioe.2010.12.018
Zdarta J et al (2014) Immobilization of Amano Lipase A onto Stöber silica surface: process characterization and kinetic studies. Open Chem 13:1. https://doi.org/10.1515/chem-2015-0017
Zeng H-Y, Liu X-Y, He P, Peng D-H, Fan B, Xia K (2014) Lipase adsorption on woven nylon-6 membrane: Optimization, kinetic and thermodynamic analyses. Biocatal Biotransform 32:188–197. https://doi.org/10.3109/10242422.2014.895334
Zhou L, Wan J, Cao X (2010) Synthesis of thermo-sensitive copolymer with affinity butyl ligand and its application in lipase purification. J Chromatogr B Analyt Technol Biomed Life Sci 878:1025–1030
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The authors gratefully acknowledge the management of Kamaraj College of Engineering and Technology, Virudhunagar-626001, Tamil Nadu, India, for the support of research facilities.
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Sankar, K., Achary, A. Bio-ceramic, mesoporous cuttlebone of Sepia officinalis is an ideal support for the immobilization of Bacillus subtilis AKL13 lipase: optimization, adsorption, thermodynamic and reaction kinetic studies. Chem. Pap. 74, 459–470 (2020). https://doi.org/10.1007/s11696-019-00891-x
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DOI: https://doi.org/10.1007/s11696-019-00891-x