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1 Supporting Information Study of molecular conformation and activity-related properties of lipase immobilized onto core-shell structured polyacrylic acid-coated magnetic silica nanocomposite particles Parvaneh Esmaeilnejad-Ahranjani a,b, Mohammad Kazemeini b, Gurvinder Singh, c Ayyoob Arpanaei a,* a Department of Industrial and Environmental Biotechnology, National Institute of Genetic Engineering and Biotechnology, PO Box: 14965/161, Tehran, Iran. *Corresponding author address: arpanaei@yahoo.com b Department of Chemical and Petroleum Engineering, Sharif University of Technology, Tehran, Iran. c Department of Materials Science and Engineering, Norwegian University of Science and Technology, Trondheim, Norway. 1
2 Experimental Preparation of Fe 3 O 4 clusters@sio 2 (MS) particles The core-shell MS particles were synthesized by the Stöber method in the presence of magnetite particles. The magnetite nanoparticles prepared by the co-precipitation method (75 mg) and dispersed in toluene (5 ml) were added in ml mixed solution of ethanol, water and ammonia (32:8:1 v/v). A homogeneous solution of particles were obtained at ambient temperature under continuous stirring at 400 rpm for 20 min. Then, TEOS (1 ml) was added drop-wise to the resulting solution over 30 min. The synthesis of MS particles was allowed to complete at room temperature for 4 h. The resulting particles were collected by magnetic separation, thoroughly washed with ethanol and water and finally dried at 50 o C. washing of lipase-immobilized samples after immobilization procedure After completion of immobilization procedure, the samples were first washed three times with the buffer solution of ph 7.4. To ensure the removal of all the noncovalently-attached lipase molecules, the further wshing of the samples were done by considering the surface charge states of the lipase and partilces. Therefore, the samples were then washed twice with sodium phosphate buffer solutions (0.1 mol L -1 ) of ph 9, where it is expected that the repulsive forces between the lipase and particles to be high because of their high negative surface charges. The samples were then washed twice with phosphate buffer solutions of ph 8 and then ph 6. Finally, the smaple were washed twice with acetate buffer solutions (0.1 mol L -1, ph 3 or 5). It is noted as we fond which buffer solution is required for completely removing of unattached lipase molecules, the washing steps were carried out only with those tested buffer solutions, i.e., buffer solutions of ph 7.4, 8, and 9, in this study. Surface charge states of lipase molecules and the nanocomposite particles as a function of ph. 2
3 Enzyme activity assay Catalytic activity of free and immobilized lipases was studied in hydrolysis reaction of 4-Nitrophenyl palmitate (pnpp). The reactions were conducted in 2 ml screw-caped bottle containing 0.1 mg lipase either in free or immobilized state and 450 µl of 1 mmol L -1 pnpp. It is emphasized that, in order to investigate the activity of immobilized lipases, with respect to the loading capacity of particles, desirable amounts of the solution of both lipase-immobilized particles (IL-PMS1 and IL-PMS2) were taken which contained the same amount of lipase molecules. The solutions of buffer and particles without the immobilized lipase were taken as controls. After completion of reactions and recovering of the particles, NaOH solution was added to the reaction mixture to adjust the ph value of solution on 10. This step was necessary because the exact enzyme activity measurement requires complete conversion of p-nitrophenol (pnp) product into 4-nitrophenoxide, which occurs at ph 10. The molar concentration of 4-nitrophenoxide, equaling to the pnp molar concentration, was measured using a T80+ UV/VIS spectrophotometer (PG Company, Germany) at 405 nm. The lipase specific activity was defined as one unit lipase activity (U, the amount of lipase required to liberate 1 µmol of p-nitrophenol (pnp) from pnpp substrate per minute) per mg of lipase (U mg -1 ). Results Size distribution of PMS2 particles Figure S1. Size distribution analysis of core diameter, shell thickness and particles diameter of the PMS2 particles. The size distribution of PMS1 particles were almost similar to that of PMS2 particles. 3
4 STEM images of magnetite (Fe 3 O 4 ) and magnetic silica (MS) particles Figure S2. (a) Bright field (BF) STEM image of magnetite and (b) dark field (DF) STEM image of core-shell structured MS particles. FC-ZFC analysis of magnetite and MS particles The superparamagnetic properties of the magnetite, MS, PMS1 and PMS2 particles through the FC-ZFC analysis are shown in Figure S3. The superparamagnetic behavior of these particles can also be deduced from the maximum of ZFC curve indicating blocking temperatures ~65 K. The FC and ZFC curves of MS particles are almost similar to those of PAA-coated MS particles. It is observed that the slopes of FC curves increase with the decrease of the temperature and the composite particles blocking temperature is lower than that of the magnetite particles (~80 K), fairly suggesting that the nonmagnetic silica/polymer shell around the magnetite nanoparticles reduces the dipolar coupling between the magnetite nanoparticles. Figure 3Sb inset displays the simple separation of particles from the 5 mg ml -1 particles solution using a magnet within 30 sec at ambient condition. After the magnetic separation, the particles could be re-dispersed completely by manual shaking. 4
5 Figure S3 FC-ZFC curves of (a) magnetite and MS particles and (b) PMS1 and PMS2 particles. 5
6 Zeta potential values of Particles The ζ potential values of the prepared particles recorded in an aqueous solution of ph 7.4 also verified the surface modification of MS particles with PAA molecules, as discussed in detail in the Supporting Information. The surface charge of bare MS particles was negative (-34.8±2.3 mv), which is due to the presence of a large number of hydroxyl groups on its surface. 1 After functionalization of the particle surface with AAS molecules, which contain amine groups, a considerable increase in ζ potential value of particles was noticed, i.e., 8.2±1.2 mv. After attachment of PAA molecules on the AAS-MS particles the surface charges of PMS1 and PMS2 were lowered to ±2.0 mv and -39.3±1.9 mv, respectively, due to presence of the carboxyl functional groups. The more negative surface charge of PMS2 sample in comparison to that of PMS1 one is the result of the high concentration of carboxyl groups on the former. Lipase immobilization efficiency and loading capacity of the particles as a function of lipase initial concentration The lipase immobilization efficiency and loading capacity of the particles were studied as a function of lipase initial concentration utilized in immobilization procedure, as illustrated in Figure S4a. To calculated the amount of immobilized lipases, the content of un-immobilized lipase in supernatant and collected washing solutions (Figure S4b) were subtracted from the content of lipase in the initial lipase solution. For both prepared samples, the lipase immobilization efficiency continuously decreases with the increase of lipase concentration, while an initial increase in the loading capacity of particles is observed with the increase of lipase initial concentration up to 2 mg ml -1 followed by decreasing as the initial lipase concentration increase further (Figure S4a). Due to the interactions among enzyme molecules, enzyme aggregates are formed at high enzyme concentrations, 2,3, e.g., above 2 mg ml -1 in this study, which in turn limit the immobilization of enzymes onto the particles. According to the zeta potential values results in this file, the free lipase exhibits an isoelectric point of 5; however its surface charge does not significantly change at various ph values as the enzyme molecules involve different functional molecules and can tune its surface charge at various buffer solutions. It is also indicated that the surface charge of the PMS1 and PMS2 particles at all the ph values are negative. To remove possible unattached lipase molecules adsorbed on these particles via electristatical interactions, the prepared samples were washed several times with various buffer solutions. Figure S4b shows the amount of the loosly-bonded lipase molecules removed after each washing step with various 1 mol L -1 buffer solutions (ph 3, 5, 6, 7.4, 8 and 9). The immobilization procedure was carried out at ph 7.4 with 2 mg ml -1 lipase initial concentration equaling to a lipase content of 5 mg in the immobilization media. The IL-PMS1 and IL-PMS2 were first washed three times with a sodium phosphate buffer solution of ph 7.4 until we did not measure any lipase molecules in the washig solution, as it was analysized by the Bradford method. Then, considering the surface charge state of the particles, the samples were then washed twice with a sodium acetate buffer solution of ph 9. It was expected that most of the unattached lipase molecules to 6
7 remove as the zeta potential of lipase and particles are very negative and repulsive forces are high at this ph value. Figure S4b shows that the most of the loosely bonded lipase molecules was removed over this washig step (ph 9). Then, the samples were washed with other buffer solutions and no significant amount of the unatached lipase were observed in those washing solutions. Figure S4. (a) lipase immobilization efficiency and loading capacity of particles as a function of lipase initial concentration applied in the immobilization procedure and (b) the amount of un-immobilized lipase removed through the washings with various buffer solutions. Lipase iniital concentration of 2 mg ml -1 (= 5 mg in the system) was used in the immobilization procedure. 7
8 Study of the kinetics of the enzymatic hydrolysis reactions Figure S5 Effect of initial substrate concentration on initial reaction rate at ph 7.4 and 40 o C. 8
9 Circular dichroism (CD) analysis results performed on the free and immobilized lipases at various ph values and constant temperature of 40 o C Structural element Table S1 Secondary structural content (%) of lipase in free and different immobilized states at various ph values and constant temperature of 40 o C. Free lipase IL-PMS1 IL-PMS2 ph 6 [a] ph 7.4 [b] ph 8 [c] ph 9 [d] ph6 ph 7.4 ph 8 ph 9 ph 6 ph 7.4 ph 8 ph 9 α-helix (%) β-sheet (%) β-turn (%) Random coil (%) [a] fresh lipases dispersed in a buffer solution of ph 6, [b] fresh lipases dispersed in a buffer solution of ph 7.4, [c] fresh lipases dispersed in a buffer solution of ph 8, and [d] fresh lipases dispersed in a buffer solution of ph 9. Circular dichroism (CD) analysis results performed on the free and immobilized lipases in thermal and storage stability assays Sample Table S2 Secondary structural content (%) of lipase in free and different immobilized states pretreated under various conditions at constant ph 7.4. α-helix (%) β-sheet (%) β-turn (%) Random coil (%) 4 o C [a] S-4 o C [b] 50 o C [c] T-50 o C [d] 4 o C S-4 o C 50 o C T-50 o C 4 o C S-4 o C 50 o C T-50 o C 4 o C S-4 o C 50 o C T-50 o C Free lipase IL-PMS IL-PMS [a] fresh lipases dispersed in a buffer solution at 4 o C and CD recorded at 4 o C (also reported in the paper), [b] lipases pretreated in a buffer solution at 4 o C for 20 days and CD recorded at 4 o C, [c] lipases pretreated in a buffer solution at 50 o C for 15 min and CD recorded at 50 o C (also reported in the paper), and [d] lipases pretreated at 50 o C for 10 h and CD recorded at 50 o C. References (1) Mohammad-Beigi, H.; Yaghmaei, S.; Roostaazad, R.; Bardania, H.; Arpanaei, A. Effect of ph, Citrate Treatment and Silane-Coupling Agent Concentration on the Magnetic, Structural and Surface Properties of Functionalized Silica-Coated Iron Oxide Nanocomposite Particles. Phys. E. 2011, 44, (2) Jiang, Y.; Guo, C.; Xia, H.; Iram, M.; Liu, C.; Liu, H. Magnetic Nanoparticles Supported Ionic Liquids for Lipase Immobilization: Enzyme Activity in Catalyzing Esterification. J. Mol. Catal. B: Enzym. 2009, 58, (3) Ranjbakhsh, E.; Bordbara, A. K.; Abbasi, M.; Khosropour, A. R.; Shams, E. Enhancement of Stability and Catalytic Activity of Immobilized Lipase on Silica-Coated Modified Magnetite Nanoparticles. Chem. Eng. J. 2012, 179,
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