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Encapsulated laccases as effective electrocatalysts for oxygen reduction reactions Ana Franco, Soledad Cebrián-García, Daily Rodríguez-Padrón, Alain Rafael Puente Santiago, Mario J. Muñoz Batista, Alvaro Caballero, Alina Mariana Balu, Antonio A. Romero, and Rafael Luque ACS Sustainable Chem. Eng., Just Accepted Manuscript • DOI: 10.1021/acssuschemeng.8b02529 • Publication Date (Web): 02 Jul 2018 Downloaded from http://pubs.acs.org on July 3, 2018

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Encapsulated laccases as effective electrocatalysts for oxygen reduction reactions Ana Franco,[a] ‡ S. Cebrián-García,[a] ‡ Daily Rodríguez-Padrón,[a] Alain R. PuenteSantiago,[a]* Mario J. Muñoz-Batista,[a] Alvaro Caballero,[b ] Alina M. Balu,[a] Antonio A. Romero,[a] Rafael Luque[a, c]* [a]

Department of Organic Chemistry, Institute of Fine Chemistry, University of Cordoba,

Campus de Rabanales, Edificio Marie Curie (C-3), Ctra Nnal IV-A, Km 396, E14014, Cordoba (Spain). [b]

Department of Inorganic Chemistry, Institute of Fine Chemistry, University of Cordoba,

Campus de Rabanales, Edificio Marie Curie (C-3), Ctra Nnal IV-A, Km 396, E14014, Cordoba (Spain). [c]

Peoples Friendship University of Russia (RUDN University), 6 Miklukho-Maklaya str.,

117198, Moscow, Russia Emails of Corresponding authors: [email protected], [email protected]

ABSTRACT. The efficient electronic wiring of silica encapsulated laccases has been applied for the first time to the bioelectrocatalytic reduction of oxygen. The synthesized silica/laccase composites were evaluated electrochemically and characterized by UV-vis, FT-IR, DLS and XPS. FT-IR measurements showed that laccase preserved its native-like structure after the bio-

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silicification process. The one-pot biosilicification synthesis facilitated the accommodation of the enzymes in highly effective orientations for the direct electron transfer (DET) of the T1 redox centers. Consequently, the biosilicified laccase deposited on Ni electrodes exhibited an efficient bioelectrocatalytic oxygen reduction, with current densities of up to 0.94 mA/cm2.

KEYWORDS:

encapsulated

laccases,

direct

electron

transfer

(DET),

orientation,

bioelectrocatalysis.

Introduction Direct electron transfer (DET) between the enzymes and electrodes provide inherent advantages in the design and fabrication of electronic nanoscale biomaterials for several industrial, environmental, biomedical and energy applications.1-3 Specially, the use of simple and innovative immobilitation techniques to design bioinorganic materials that can be used for the construction of highly efficient bioelectrocatalytic devices, have gained a lot of attention.4 To reach a desirable electronic communication between a redox enzyme modified material and the electrode surface, a number of factors need to be taken into account. These include the surface properties of the electrodes, the pH and ionic strength of the solutions and the interfacial electric field.5-8 Among them, the orientation play a crucial role in the ET function of the redox enzymes coupled to functional materials.9-12 In fact, Gui-Xia Wang and coworkers have reported that the DET is tuned by the heme orientation plane in cytochrome C coated mixed self-assembled monolayers.13 Consequently, the immobilization strategy can directly modulate the conformation and/or orientation of the redox sites of the enzymes. Recently a novel encapsulation method denoted as bio-silicification was reported by our group to stabilize enzymes without affecting its catalytic

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activity.14 Silica is a promising candidate due to its structural, chemical, thermal stability and toxicological safety.15,16 In this sense, enzyme bio-silicification is a one-pot process in which enzyme are partially encapsulated by a silica crust following a simple sol-gel silica formation by the addition of a silicate precursor (e.g tetraethyl orthosilicate, TEOS) under mild conditions.17, 18 Laccases are multicopper oxidases that couple one-electron oxidation of four substrate equivalents with the four-electron reduction of dioxygen to water. Electroreduction mechanism occurs via a ping-pong mechanism. Substrates are oxidized near the solvent accessible T1 site, and then electrons are transferred through the protein, via a Cys-His pathway, over a distance of ~12 Å to the trinuclear copper (TNC) center where the oxygen reduction reaction (ORR) takes place.19 A large battery of highly efficient electrocatalysts towards ORR reaction have been developed in the recent years.20-24 Specially, the development of new biomaterials with potential applications to functional bio-fuel cells has gained a lot of attention in the scientific community.25-27 In this letter, an unprecedented electrically active encapsulated laccase material with an efficient bielectrocatalytic activity for oxygen reduction reactions was synthesized following a facile and eco-environmental one-pot bio-silicification proccess (Scheme 1).

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Scheme 1. Overview of the bio-silicification process and the subsequent electrocatalytic function of the biocomposite. Results and discussion UV–vis spectroscopy of the bio-silicified laccases revealed a characteristic adsorption peak at 287 nm (Figure 1A), which can be attributed to the adsorption of tryptophan and tyrosine aminoacids.28 FT-IR was used to evaluate if laccase preserve its native-like structure after the bio-silicification step. FT-IR spectrum exhibited two characteristics bands at 1646 cm-1 and 1568 cm-1, which correspond to amide I and amide II groups in the enzyme structure, respectively (Figure 1.B). The amide I band is characteristic from C=O stretching vibration in carbonyl groups of the peptide linkages. In addition, the band at 1568 cm-1 can be attributed to the combination of C–N stretching and N H bending of the peptide groups in the backbone of the protein. Compared to the commercial free laccase,29 the FT-IR spectrum of bio-silicified laccase does not displayed

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considerable changes, suggesting that laccase does not in principle undergoes major structural changes in its secondary structure preserving a native-like structure after the bio-silicification process.

Figure 1. A) UV-vis and B) FT-IR spectra of the bio-silicified laccase system. The dynamic light scattering (DLS) data of bio-silicified laccase system (Figure 2A.) displayed an average hydrodynamic size of 188 nm. This value is in accordance with the expected after encapsulation process. The zeta potential of bio-silicified laccase was -12 mV (Figure 2B.), with a negative net electrical charge within the range of the expected value for a stable bioconjugate colloidal solution.30

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Figure 2. A) DLS and B) z-potential measurements of biosilicified laccase system. XPS measurements were also carried out to study the chemical properties of the bioconjugate. Figure 3 displays XPS data of the sample for carbon 1s (C1s), nitrogen 1s (N1s), and oxygen 1s (O1s) experimental regions and fitting results. For C1s, C-C signal (284.6 eV) as well as those contributions of C-N and C-O at 286.4 and 288.1 eV, respectively, were detected. They are mainly ascribable to the polypeptide chain of the immobilized laccase. Both, the energy of the

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N1s peaks as well as their characteristic energy difference are indicative of the peptide bonds (399.9 eV) and pyrimidinic groups (401.2 eV) of the immobilized protein.31,32 Contribution from the bioconjugate system can be detected also from the O1s XPS region. Peaks at 532.5 eV and 530.8 eV can be associated to O-Si and O-C bonds, respectively. Finally, the silica phase shows the well-known binding energy of the Si 2p peak which is located at 103.5 eV.33 X-ray diffraction analyses were conducted for the first time, at the best of our knowledge, to investigate how laccase immobilization influences the silica structure (Figure S1, ESI†). It is observed a sharp peak on a broad hump at 22º (2θ) that is associated to a cristobalite structure.35 The changes from the sharp peak of the silica platform to a broad peak observed for the biosilicified laccase material indicated both the successfully immobilization of the laccases and the silica structural changes by the incorporation of the enzymes. Additionally the morphology of the silica/laccase composite was characterized by Scanning Electron Microscopy (Figure S2 ESI†).

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Figure 3. A) C1s, B) N1s and C) O1s XPS spectra of the bioconjugates. Fitting results display the different contributions to each XPS peak. The free and biosilicified laccases were examined by cyclic voltammetry respectively for ORR reactions (figure 4). As shown in figure 4A, laccases deposited on Ni electrodes did not exhibit electrocatalytic responses for the ORR process in the studied conditions most likely owed to the

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denaturalization and/or electroinactive orientations of the immobilized enzymes. In contrast, a well-defined sigmoidal waveshape signal for the biosilicified laccases (figure 4A) with an onset potential of +0.64 V (vs. Ag/AgCl) was observed in the same potential range indicating that the bio-hybrid material enable the efficient direct electron transfer (DET) of the encapsulated laccases and consequently the electrocatalytic function via T1 copper center.25 Along with cyclic voltammetry, chronoamperometric measurements were conducted at Ep=0.2 V (vs Ag/AgCl 3M) for the biosilicified laccases (figure 4B). Noticeably, under a constant oxygen flow, a maximum current density of 0.94 mA/cm2 was observed for the electrocatalytic oxygen reduction, which is similar to the bioelectrocatalytic current responses of laccases covalently attached to high conductive nanomaterials such carbon nanotubes and graphene assemblies.35,36 This significant bioelectrocatalytic activity is mainly attributed to the efficient ET orientations adopted by the redox T1 groups of the entrapped laccases in the biosilification process.

Figure 4. Cyclic voltammograms of A) a) free laccase and b) biosilicified laccase under oxygen purging in 0.1M PBS at pH=6. Scan rate: 0.01 V/s and B) Chronoamperometric responses for biosilicified electrodes performed at Ep=0.2 V in the same experimental conditions under oxygen purging.

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The stability of the biocomposites was assessed by a number of chronoamperometric experiments performed during a period of 1 month (figure 5). The biosilicified laccase electrodes maintained good bioelectrocatalytic performances during the time. After 10 days of storage the electrodes retained nearly the 75% of the initial bioelectrocatalytic activity which decreased to 65% after one month.

Figure 5. Stability of the biosilicified laccases electrodes investigated by several chronoamperometric measurements performed at Ep=0.2 V over 1 month. Conclusion In summary, the silica framework acts as soft-platforms for the immobilization of the redox enzymes favouring their active ET orientations. The resulting composite showed an efficient biolectrocatalytic performance toward the reduction of the oxygen. Additionally, biosilicified laccases electrodes displayed significant stability in the bioelectrochemical response over one month. Bearing in mind these results, the synthesized biomaterials could be successfully integrated into functional bio-fuel cell devices.

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ASSOCIATED CONTENT Supporting Information. The Electronic Supporting Information provides the experimental section, XRD and SEM images of the biosilicified laccases composites.

AUTHOR INFORMATION Corresponding Authors *Email: [email protected] *Email: [email protected] Author Contributions ‡These authors contributed equally. Notes The authors declare no competing financial interest. ACKNOWLEDGMENT Rafael Luque gratefully acknowledges MINECO for funding project CTQ2016-78289-P, cofinanced with FEDER funds. Mario J. Munoz-Batista gratefully acknowledges MINECO for a JdC contract (Ref. FJCI-2016-29014). The publication has been prepared with suport from RUDN University Program 5-100. REFERENCES

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Table of Content graphic:

Environmentally friendly, one-pot synthesis of efficient encapsulated laccases bioelectrocatalysts and their applications to oxygen reduction reactions (ORR).

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