Article pubs.acs.org/Langmuir
Electropolymerized Carbonic Anhydrase Immobilization for Carbon Dioxide Capture Geraldine Merle,† Sylvie Fradette,‡ Eric Madore,‡ and Jake E. Barralet*,†,§ †
Faculty of Dentistry, and §Division of Orthopedics, Department of Surgery, Faculty of Medicine, McGill University, Montreal, Quebec H3A 0C7, Canada ‡ CO2 Solutions, Incorporated Quebec City, Quebec G2C 1T9, Canada ABSTRACT: Biomimetic carbonation carried out with carbonic anhydrase (CA) in CO2-absorbing solutions, such as methyldiethanolamine (MDEA), is one approach that has been developed to accelerate the capture of CO2. However, there are several practical issues, such as high cost and limited enzyme stability, that need to be overcome. In this study, the capacity of CA immobilization on a porous solid support was studied to improve the instability in the tertiary amine solvent. We have shown that a 63% porosity macroporous carbon foam support makes separation and reuse facile and allows for an efficient supply and presentation of CO2 to an aqueous solvent and the enzyme catalytic center. These enzymatic supports conserved 40% of their initial activity after 42 days at 70 °C in an amine solvent, whereas the free enzyme shows no activity after 1 h in the same conditions. In this work, we have overcome the technical barrier associated with the recovery of the biocatalyst after operation, and most of all, these electropolymerized enzymatic supports have shown a remarkable increase of thermal stability in an aminebased CO2 sequestration solvent.
■
accelerates CO2 scrubbing from the flue gases. Major issues in using biological compounds in this process is that they can easily denature in organic solvent and are thermally instable.8 Immobilization is often the key to enhance the enzyme stability against thermal denaturation by preventing the unfolding of the protein9 and to allow for the recovery of the active enzyme for reuse, thereby reducing the cost of the enzymatic industrial processes. Diverse approaches have been developed to immobilize CA on solid supports to allow for the recovery and enhance the thermal stability without affecting the mass transfer. Physical methods, such as adsorption10−13 and encapsulation,13 are simple and inexpensive technics; however, they suffer from a progressive desorption of the enzyme after repeated operation and, with respect to the encapsulation, mass-transfer diffusion limitation. Preventing enzyme release while preserving macromolecular interactions can be achieved with the covalent grafting method.13−15 Immobilization on an electropolymerized polymer is a reproducible technique that affords the deposition of homogeneous polymeric coating in and on a porous support, the manipulation of a polymeric film thickness, owing to the conductivity, and allows for manipulation of the enzyme−polymer film composition. Among the conducting polymers, polypyrrole and its derivatives are attractive because a wide variety of functional groups can be covalently linked to the pyrrole motif.16 Here, we
INTRODUCTION In recent years, a great deal of concern has been heightened with regard to global climate change and its apparent link to rising atmospheric concentrations of the greenhouse gas carbon dioxide (CO2). With a total of 33.5 Gt of industrial CO2 emission worldwide in 1 year,1 there are several methods aimed at removing CO2 from the atmosphere, whereas others scrub CO2 from point emissions. While both approaches offer several benefits, the research of CO2 capture from the atmosphere is still in its infancy and the practicality of large-scale deployment needs to be further explored.2,3 The capture of CO2 from mixed gas streams at industrial and energy-related sources is the most energy-intensive stage of the process. To date, mainly monoethanolamine (MEA)-based absorption/desorption processes are currently available for CO2 capture4,5 for natural gas processing and ammonia manufacture; however, energy requirements and expensive operating costs related to the high-temperature process that can corrode the process equipment are prohibitive.6 Therefore, alternative approaches that can decrease the cost of CO2 capture are required. Methyldiethanolamine (MDEA) solvent is a tertiary amine solvent that offers the lowest regeneration energy; however, it requires an activator to accelerate the absorption of CO2 and achieve a better system combining fast absorption.6 Carbonic anhydrase (CA), a zinc metalloenzyme, can efficiently and quickly (from 104 to 106 molecules per second) catalyze the hydration of CO2 to form bicarbonate (HCO3−), and biologically, it serves in CO2 in living organisms.7 This enzyme can overcome the low hydration rate of CO2 in MDEA and © 2014 American Chemical Society
Received: April 8, 2014 Revised: May 13, 2014 Published: May 23, 2014 6915
dx.doi.org/10.1021/la501333s | Langmuir 2014, 30, 6915−6919
Langmuir
Article
corresponding to the oxidation of pyrrole motifs into a radical. The electropolymerization of the monomer (0.1 M) was carried out on the 1 cm long bare porous carbon support (mean total volume of the solid support including macropores = 0.871 cm3) in 0.1 M NBu4PF6 in acetonitrile. The oxidation of the monomer was performed at a controlled potential of +0.95 V versus Ag/AgCl after the introduction of 0.5 M perchloric acid. To obtain different film thicknesses, the transferred charge under the oxidation peak of the polyaminopropyl pyrrole during the oxidation was increased from 1 to 20 C. The subsequent support was then washed 3 times with acetonitrile and 0.1 M carbonate buffer at pH 9.4. For the direct grafting, glutaraldehyde was used as a bifunctional reagent to fix the enzyme to the amino groups of the polymer. The modified support was dipped in 3.2 mL of carbonate (0.1 M, pH 9.4) solution containing glutaraldehyde [5% (v/v)] per cm−3 of support at 20 °C for 3 h. The support was washed 3 times with carbonate buffer, rinsed with phosphate buffer (0.1 M, pH 7.4), and subsequently soaked for 2 h at 20 °C, followed by 7 h in CA solution (2.6 mg mL−1) at 4 °C. After the enzymatic support was rinsed in phosphate buffer, it was stored in the same buffer at 4 °C. Incorporation of poly(ethylene oxide) (PEO) as a spacer arm was carried out on five different electropolymerized charges (1, 5, 10, 15, and 20 C).20 After substitution of the amino group of the polyaminopropyl pyrrole with the carbonyl group of the glutaraldehyde, the support was soaked in acetonitrile solution (4 mL) containing PEO (0.1 g) and the reaction starts with the incorporation of HCl (0.01%, w/w) under stirring at room temperature for 4 h.20 Glutaraldehyde and enzyme were further attached to the support in carbonate buffer and phosphate buffer, respectively, as previously described. The modified supports were stored in a 0.1 M phosphate buffer (pH 7.4) at 4 °C before conducting the activity and stability measurements. The protein loading on the support was calculated by measuring the concentration in the CA solution before and after immobilization was determined using the Bradford method.21 Absorbance measurements were realized using a Molecular Devices, Spectramax M2E spectrophotometer. The samples were placed in Suprasil quartz glass cells with a light path of 1 cm. The difference in the protein concentration was used to calculate the loading of CA onto the modified support. To carry out the CA activity assay for the free and immobilized CA, the colorimetric assay with p-NPA was performed. The enzymatic activity was determined by measuring the amount of para-nitrophenol (p-NP) produced by absorbance in an ultraviolet/ visible (UV/vis) spectrometer.15 CA activity in solution was measured by the hydrolysis rate of 3 mM pNPA in 15.6 mM Tris−HCl buffer at pH 7.6 and 25 °C. The increase in absorbance, corresponding to the production rate of the p-NP product, was followed by spectrophotometry at 420 nm (ε420 = 18.5 mM−1 cm−1). The same procedure was used to determine the CA activity immobilized on the support. Measurements were performed by soaking the support in a 3 mM pNPA solution at pH 7.6 (V = 2 mL). The activity values were determined as being the mean of at least three measurements. Thermal stability of the immobilized CA on each support was tested in 0.1 M phosphate buffer at pH 7.4 and compared to the free enzyme in the same solution. The stability for free and immobilized CA was determined by assaying the enzyme activity after exposing the enzymatic support and the free enzyme at various temperatures (25, 50, 70, and 90 °C) for 1 h. Moreover, the stability of the immobilized CA was determined by monitoring the enzymatic activity of the supports periodically for a 42 day storage period in absorption solvent (1 M aqueous MDEA solution at pH 11) at 70 °C.
have developed an elegant approach involving the covalent binding of CA to polypyrrole films bearing an amine group. We determined the optimal conditions for each step by varying the film thicknesses and with the use of spacer molecules of varying length. The influence of film thickness and distance between enzyme and support were evaluated toward the activity and stability of the enzyme.
■
EXPERIMENTAL SECTION
CA (human carbonic anhydrase II17) was provided by CO2 Solutions, Inc. (Quebec City, Quebec, Canada). Uncoated carbon foam with a relative percent porosity of 63% was supplied by Technology Assessment and Transfer, Inc., Annapolis, MD. Cyanoethyl pyrrole, lithium aluminum hydride (AlLiH4), tetrabutylammonium hexafluorophosphate (NBu4PF6), poly(ethylene oxide) (8000 g mol−1), glutaraldehyde, N-methyldiethanolamine, and para-nitrophenylacetate (p-NPA) were purchased from Sigma-Aldrich (St. Louis, MO). All other chemicals used were of reagent grade or better and were supplied by Fisher Chemical, unless stated otherwise. Ultrapure water (resistivity = 18.2 MΩ at pH 6.82) was used in all experiments. The enzyme was grafted chemically on an electropolymerized poly(aminopropyl)pyrrole film onto a highly porous carbon support. The immobilization of CA was achieved as per the method described by Merle et al.18,19 Shortly, the aminopropyl pyrrole monomer (2) was synthetized via the chemical reduction of the commercial cyanoethyl pyrrole (1) (Figure 1).
Figure 1. Chemical synthesis of the aminopropyl pyrrole. A solution of compound 1 in anhydrous ether was incorporated to LiAlH4 in anhydrous ether, and the mixture was stirred overnight under an inert atmosphere. The excess of hydride was neutralized with the addition of water and NaOH, and the ether solution was decanted from the white, granular inorganic residue. This residue was washed with ether, and ether portions were all combined. A yellow oil was subsequently obtained and characterized electrochemically by cyclic voltammetry of a 0.1 M aminopropyl pyrrole solution in acetonitrile with 0.1 M NBu4PF6 (Figure 2). The monomer had the traditional electrochemical characteristics of functionalized pyrrole with an irreversible oxidation peak around 1.1 V
■
RESULTS AND DISCUSSION Chemical grafting is an immobilization technique defined as irreversible fixation, thereby preventing the leaching out of the enzyme over time compared to the adsorption, entrapment, or encapsulation and limiting the enzymatic conformational change because of a thermal denaturation, thus enabling their use in high thermal industrial processes. Here, we investigated
Figure 2. Cyclic voltammetry of aminopropyl pyrrole in CH3CN and 0.1 M NBu4PF6, with v = 5 mV s−1 versus reference Ag/AgCl. 6916
dx.doi.org/10.1021/la501333s | Langmuir 2014, 30, 6915−6919
Langmuir
Article
the effect of the enzyme loading as well as the influence of the enzyme distance to the support on the enzymatic activity and stability over time. The polyaminopropyl pyrrole was electrodeposed on the porous support, and by controlling the oxidation time, we were able to produce five different supports presenting different thicknesses, namely, 1, 5, 10, 15, 20 C, which were further modified with the use or not of a spacer arm. The loading of CA per unit volume of carbon support according to the film thickness and distance between enzyme/ support is shown in Table 1. The two immobilization techniques showed that the enzyme loading on the support increased with the increase in thickness. Table 1. Mean ± Standard Deviation (SD) Loading of CA Per Unit Volume of Supports Modified without a Spacer (N = 5) and Modified with a Spacer (N = 5), as a Function of Film Thickness, Calculated by Subtracting the Protein Concentration in Solution before and after Immobilization via the Bradford Methoda
Figure 3. Mean ± SD production rate of p-NP on supports modified (□) without a spacer (N = 5) and (○) with a spacer (N = 5) as a function of the deposition charge, measured by absorbance at 420 nm. The polymer thickness is proportional to the deposition charge.
CA loading per unit total volume of solid support including macropores (mg cm−3) without spacer 1C 5C 10 C 15 C 20 C a
0.23 0.28 0.39 0.37 0.71
± ± ± ± ±
0.02 0.01 0.01 0.01 0.02
with spacer 0.39 0.64 0.85 0.84 1.25
± ± ± ± ±
0.03 0.02 0.02 0.01 0.03
enzyme and the inherent flexibility of the spacer retains the active conformation of the enzyme. In this way, the apparent mass-transfer limitation of p-NPA to the enzyme is overcome. Although we went on to confirm long-term enzymatic stability of the PEO-containing materials, which correlates with the anticipated stability of the acetal bond,23,24 the possibility remains that the effect was purely physical. However, evidence against this eventuality came in the observation that PEO alone was not able to wet the support material. CA immobilized with PEO as a spacer arm on an electropolymerized film at 20 C charge exhibited the best trade off between enzymatic activity and loading. The catalytic activity of free and immobilized enzyme for the hydrolysis of p-NPA was investigated after consecutive 1 h heat treatments at increasing temperatures from 25 to 90 °C. The results in Figure 4 show a gradual loss of activity for free and immobilized enzyme with the temperature; however, the activity of free CA decreased rather rapidly at temperatures of 70 and 90 °C; only 8% of the initial activity remained after 1 h
Thickness is function of the charge (C).
Furthermore, the use of a spacer arm appears to double the loading of the enzyme, as compared to the loading observed for the immobilization without a spacer. The use of a spacer was envisaged to minimize the steric hindrance by separating the enzyme molecules from each other, thereby increasing the loading of CA on the support.22 Table 1 suggests that the presence of the spacer arm positively influenced the CA loading on the substrate by exposing a more polymeric amino group to the surface of the support, making them more accessible for reacting with the enzyme. The catalytic activity of the enzyme grafted with and without a spacer on the support with different thicknesses was studied by measuring the production rate of p-NP (Figure 3); measurement of the support alone confirmed no activity. The catalytic activity of CA per unit volume of the carbon support is summarized in Figure 3. We expected that an increase in the enzyme loading (Table 1) would have led to a higher enzymatic activity; however, this was not the case for the samples made without PEO. On the other hand, the highest p-NP production rate (22 M min−1 cm−3) was recorded for the support at the enzyme load of 1.25 mg cm−3, corresponding to the support modified with the thicker film and the spacer arm. The enzyme activity was positively correlated to polymer thickness above 5 C deposition charge for the spacer arm group, except for the 15 C deposition charge that appeared to be anomalous. The lack of correlation between activity and polymer thickness (Figure 2) for the no-spacer arm group may have been due to enzyme inactivation or an inability of the substrate to reach the engrafted enzyme. One might envisage that the presence of the polymer offers a “softer” environment to the enzyme compared to polypyrrole/gluteraldehyde (GA), and because of its hydrophilicity, it would create a more open polymer network and provide enhanced accessibility to the active site of the
Figure 4. Remaining activity after 1 h of storage at 25, 50, 70, and 90 °C of (dotted bars) free and (dashed bars) immobilized enzyme (N = 3) in 0.1 M phosphate buffer at pH 7.4. 6917
dx.doi.org/10.1021/la501333s | Langmuir 2014, 30, 6915−6919
Langmuir
Article
at 70 °C (Figure 4). This loss of activity is attributed to an irreversible denaturation of the protein, which undergoes a conformational alteration, thereby a loss of the biocatalytic activity.25 The immobilized enzymes on the modified support retained 40% of the initial activity after 1 h at 70 and 90 °C. The thermal stability of the immobilized enzyme at 70 °C in MDEA aqueous solvent was further investigated by measuring, over a 42 day period, the catalytic activity toward p-NPA hydrolysis (Figure 5).
group instead of PEO. These functionalities enhance the masstransfer diffusion and enzyme deactivation that could be encountered with encapsulation, followed by a random crosslinking. The electropolymerization method developed for the capture of CO2 at high concentrations and pH levels is very promising to enhance the useful life of this enzyme, which usually loses its activity rapidly. The work carried out in this paper was complementary to that performed at CO2 Solutions, Inc. that aimed to develop another technical method (materials and attachment chemistry) to maintain the activity of CA in MDEA and stabilize the enzyme for long periods. The direct benefits of this approach are reducing the costs of CO2 capture by increasing the stability and allowing for an easy recovery of the biocatalyst.
■
CONCLUSION Immobilization of CA on a cheap porous support has been successfully carried out. Carbon supports were modified using an electrodeposition method. Different thicknesses and architectures were investigated and compared by measuring the amount of immobilized enzyme as well as the enzymatic activity. It has been observed that the loading of the CA enzyme immobilized onto a modified carbon support increased with increasing the film thickness and the use of a spacer arm. The enzymatic activity study reveals that the activity of CA decreased with the increase of the film, indicating a possible steric hindrance of the enzyme and a slow mass transfer of the reactant from the media to the active center of the enzyme as well as through the film. This phenomenon appears reduced when PEO as a spacer arm is used, leading to a higher accessibility of the catalytic center of the enzyme. The thermal stability of the enzyme in phosphate buffer or MDEA solvent was also significantly improved by the immobilization. In comparison to its free enzyme counterpart, the immobilized enzyme retained by up to 50% of its initial activity over a 42 day test period at 70 °C. We have designed an enzymatic system that is highly active and long-lived in a desirable carbon capture solvent that shows some promise for CO2 capture for coal-fired power plants for instance.
Figure 5. Effect of the aging time in 1 M MDEA solution at 70 °C on the remaining enzymatic activity of immobilized enzyme (N = 3) at pH 11.
The enzymatic activity is decreasing up to 50% initial activity after 5 days and remains stable until 42 days (Figure 5), as compared to the free enzyme, which is completely denatured at 70 °C after 1 day;26 our electropolymerized enzymatic support kept approximately 50% of its initial activity after a 42 day period in tertiary amine solvent at 70 °C. The gain of this immobilization method is distinctly established by the exceptional thermal stability of CA, where conformational changes are minimized, as compared to the free enzyme. It is very difficult to compare the efficiency of the CA immobilized system with the literature because of the different methodologies used. For instance, the majority of the stability measurements performed for immobilized CA are in buffer solution at 4 °C or room temperature; however, even in these soft conditions, the enzymatic technologies show their activities decreasing. Chitosan-based nanoparticles,27 alginate beads,28 or iron mesh29 retain only 28% at 4 °C after 30 days, 70% after 50 days, and 50% after 20 days at 25 °C of their activity, respectively. The activity of the immobilized enzymes monitored for 42 days by measuring the p-NP production after incubation in MDEA at 70 °C showed a greater stability than CA cross-linked on polyurethane foam,15 immobilized on surfactant-modified silylated chitosan,30 or immobilized on mesoporous silica,10 which lost all of its activity at 60 °C in buffer or decreased by 70 and 30% at 55 and 50 °C in buffer, respectively. This remarkable increase of stability of the enzyme at high temperatures and in an alkaline environment is an asset for CO2 capture post-combustion. The electropolymerization chemical bonding to the substrate overcame the desorption of the enzyme over time and prevents the enzyme from conformational change and unfolding compared to the adsorption and encapsulation method. Because of the versatility of our approach, the amount of enzyme and the distance to the substrate can be controlled by varying the polymer thickness and/or the arm spacer functionality, for instance, using a lysine
■
AUTHOR INFORMATION
Corresponding Author
*Fax: 514-398-8900. E-mail:
[email protected]. Notes
The authors declare no competing financial interest.
■
ACKNOWLEDGMENTS The authors gratefully acknowledge the support of an Engage Grant from the Natural Sciences and Engineering Research Council of Canada. The authors gratefully acknowledge the support of Technology Assessment and Transfer, Inc. for the donation of porous carbon foam.
■ ■
ABBREVIATIONS USED CA, carbonic anhydrase; p-NPA, para-nitrophenylacetate; pNP, para-nitrophenol; MDEA, methyldiethanolamine REFERENCES
(1) Singh, U. Carbon capture and storage: An effective way to mitigate global warming. Curr. Sci. 2013, 105 (7), 914−922. (2) Lackner, K. S.; Brennan, S.; Matter, J. M.; Park, A. H. A.; Wright, A.; van der Zwaan, B. The urgency of the development of CO2 capture
6918
dx.doi.org/10.1021/la501333s | Langmuir 2014, 30, 6915−6919
Langmuir
Article
from ambient air. Proc. Natl. Acad. Sci. U. S. A. 2012, 109 (33), 13156− 13162. (3) Mahmoudkhani, M.; Keith, D. W. Low-energy sodium hydroxide recovery for CO2 capture from atmospheric airThermodynamic analysis. Int. J. Greenhouse Gas Control 2009, 3 (4), 376−384. (4) Choi, S.; Drese, J. H.; Jones, C. W. Adsorbent materials for carbon dioxide capture from large anthropogenic point sources. ChemSusChem 2009, 2 (9), 796−854. (5) Gouedard, C.; Picq, D.; Launay, F.; Carrette, P. L. Amine degradation in CO2 capture. I. A review. Int. J. Greenhouse Gas Control 2012, 10, 244−270. (6) Chowdhury, F. A.; Yamada, H.; Higashii, T.; Goto, K.; Onoda, M. CO2 capture by tertiary amine absorbents: A performance comparison study. Ind. Eng. Chem. Res. 2013, 52 (24), 8323−8331. (7) Elliott, S.; Lackner, K. S.; Ziock, H. J.; Dubey, M. K.; Hanson, H. P.; Barr, S.; Ciszkowski, N. A.; Blake, D. R. Compensation of atmospheric CO2 buildup through engineered chemical sinkage. Geophys. Res. Lett. 2001, 28 (7), 1235−1238. (8) Davy, R.; Shanks, R. A.; Periasamy, S.; Gustafason, M. P.; Zambergs, B. M. Development of high stability catalysts to facilitate CO2 capture into waterAn alternative to monoethanolamine and amine solvents. Greenhouse Gas Control Technol., Proc. Int. Conf., 10th 2011, 4, 1691−1698. (9) Ekrem, O. Biomimetic CO2 sequestration: 1. Immobilization of carbonic anhydrase within polyurethane foam. Energy Fuels 2009, 23, 5725−5730. (10) Vinoba, M.; Bhagiyalakshmi, M.; Jeong, S. K.; Yoon, Y., II; Nam, S. C. Immobilization of carbonic anhydrase on spherical SBA-15 for hydration and sequestration of CO2. Colloids Surf., B 2012, 90, 91−96. (11) Wanjari, S.; Prabhu, C.; Satyanarayana, T.; Vinu, A.; Rayalu, S. Immobilization of carbonic anhydrase on mesoporous aluminosilicate for carbonation reaction. Microporous Mesoporous Mater. 2012, 160, 151−158. (12) Zhang, S.; Lu, Y.; Ye, X. Catalytic behavior of carbonic anhydrase enzyme immobilized onto nonporous silica nanoparticles for enhancing CO2 absorption into a carbonate solution. Int. J. Greenhouse Gas Control 2013, 13, 17−25. (13) Boone, C. D.; Gill, S.; Habibzadegan, A.; McKenna, R. Carbonic anhydrase: An efficient enzyme with possible global implications. Int. J. Chem. Eng. 2013, 2013, 6. (14) Vinoba, M.; Bhagiyalakshmi, M.; Jeong, S. K.; Nam, S. C.; Yoon, Y. Carbonic anhydrase immobilized on encapsulated magnetic nanoparticles for CO2 sequestration. Chem.Eur. J. 2012, 18 (38), 12028−12034. (15) Kanbar, B.; Ozdemir, E. Thermal stability of carbonic anhydrase immobilized within polyurethane foam. Biotechnol. Prog. 2010, 26 (5), 1474−1480. (16) Merle, G.; Habrioux, A.; Servat, K.; Rolland, M.; Innocent, C.; Kokoh, K. B.; Tingry, S. Long-term activity of covalent grafted biocatalysts during intermittent use of a glucose/O2 biofuel cell. Electrochim. Acta 2009, 54 (11), 2998−3003. (17) Daigle, R.; Desrochers, M. Carbonic anhydrase having increased stability under high temperature conditions. U.S. Patent 8,263,383 B2, 2012. (18) Merle, G.; Brunel, L.; Tingry, S.; Cretin, M.; Rolland, M.; Servat, K.; Jolivalt, C.; Innocent, C.; Seta, P. Electrode biomaterials based on immobilized laccase. Application for enzymatic reduction of dioxygen. Mater. Sci. Eng., C 2008, 28 (5−6), 932−938. (19) Habrioux, A.; Merle, G.; Servat, K.; Kokoh, K. B.; Innocent, C.; Cretin, M.; Tingry, S. Concentric glucose/O2 biofuel cell. J. Electroanal. Chem. 2008, 622 (1), 97−102. (20) Kang, M.-S.; Kim, J. H.; Won, J.; Kang, Y. S. Dye-sensitized solar cells based on crosslinked poly(ethylene glycol) electrolytes. J. Photochem. Photobiol., A 2006, 183 (1−2), 15−21. (21) Belzil, A.; Parent, C. Mét hodes de qualification des immobilisations chimiques d’une enzyme sur un support solide. Biochem. Cell Biol. 2005, 83 (1), 70−77. (22) Shanmugam, S. Enzyme Technology; I.K. International Publishing House Pvt. Ltd.: New Delhi, India, 2009.
(23) Cordes, E. H.; Bull, H. G. Mechanism and catalysis for hydrolysis of acetals, ketals, and ortho esters. Chem. Rev. 1974, 74 (5), 581−603. (24) Fife, T. H.; Jao, L. K. Substituent effects in acetal hydrolysis. J. Org. Chem. 1965, 30 (5), 1492−1495. (25) Sheldon, R. A. Enzyme immobilization: The quest for optimum performance. Adv. Synth. Catal. 2007, 349 (8−9), 1289−1307. (26) Savile, C.; Nguyen, L.; Balatskaya, S.; Choi, G.; Benoit, M.; Fusman, I.; Geilhufe, J.; Ghose, S.; Gitin, S.; Grate, J.; Liang, J.; Newman, L.; Novick, S.; Parsons, J.; Riggins, J.; Zimmerman, S.; Lalonde, J. Low-cost biocatalyst for acceleration of energy efficient CO2 capture. Proceedings of the ARPA-E Energy Innovation Summit; Washington, D.C., Feb 28−March 2, 2011. (27) Yadav, R.; Satyanarayanan, T.; Kotwal, S.; Rayalu, S. Enhanced carbonation reaction using chitosan-based carbonic anhydrase nanoparticles. Curr. Sci. 2011, 100 (4), 520−524. (28) Yadav, R. R.; Mudliar, S. N.; Shekh, A. Y.; Fulke, A. B.; Devi, S. S.; Krishnamurthi, K.; Juwarkar, A.; Chakrabarti, T. Immobilization of carbonic anhydrase in alginate and its influence on transformation of CO2 to calcite. Process Biochem. 2012, 47 (4), 585−590. (29) Bhattacharya, S.; Schiavone, M.; Chakrabarti, S.; Bhattacharya, S. K. CO2 hydration by immobilized carbonic anhydrase. Biotechnol. Appl. Biochem. 2003, 38 (2), 111−117. (30) Yadav, R.; Wanjari, S.; Prabhu, C.; Kumar, V.; Labhsetwar, N.; Satyanarayanan, T.; Kotwal, S.; Rayalu, S. Immobilized carbonic anhydrase for the biomimetic carbonation reaction. Energy Fuels 2010, 24 (11), 6198−6207.
6919
dx.doi.org/10.1021/la501333s | Langmuir 2014, 30, 6915−6919
