Osmium(II) Complexes Bearing Chelating N ... - ACS Publications

Aug 16, 2016 - Noémie Lalaoui, Bertrand Reuillard, Christian Philouze, Michael Holzinger, Serge Cosnier, and Alan Le Goff. Université Grenoble Alpes...
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Osmium(II) Complexes Bearing Chelating N‑Heterocyclic Carbene and Pyrene-Modified Ligands: Surface Electrochemistry and Electron Transfer Mediation of Oxygen Reduction by Multicopper Enzymes Noémie Lalaoui, Bertrand Reuillard, Christian Philouze, Michael Holzinger, Serge Cosnier, and Alan Le Goff* Université Grenoble Alpes, DCM UMR 5250, F-38000 Grenoble, France CNRS, DCM UMR 5250, F-38000 Grenoble, France S Supporting Information *

ABSTRACT: We report the synthesis of original osmium(II) complexes bearing chelating N-heterocyclic (NHC) and bipyridine ligands. The pincer ligand 1,1′-dimethyl3,3′-methylenediimidazole-2,2′-diylidene was used to tune the redox properties of osmium complexes. Bipyridine ligands modified with pyrene groups were chosen to study the electrosynthesis of OsII-NHC-based metallopolymers as well as the noncovalent immobilization of these complexes on carbon-nanotube (CNT) electrodes. Poly-[OsIINHC] polypyrene polymer was electrogenerated on a GC electrode, whereas the pyrenemodified [OsII-NHC] could interact with the CNTs’ sidewalls through π−π interactions, allowing the immobilization of the NHC complexes at the surface of π-extended nanostructured electrodes. Furthermore, an OsII-NHC complex was studied in water, showing electron transfer mediation with multicopper enzymes. UV−visible and electrochemical experiments demonstrate that redox properties of the OsII-NHC complex provide sufficient driving force for electron transfer with bilirubin oxidase from Myrothecium verrucaria while achieving high potential electroenzymatic oxygen reduction at E = +0.45 V vs Ag/AgCl at pH 6.5.



INTRODUCTION Polypyridyl osmium(II) complexes have been widely studied as efficient redox mediators for bioelectrocatalysis with many types of enzymes, especially for biofuel cells and biosensors.1−5 Their well-defined electrochemical behavior associated with their high stability in both of the Os(II) and Os(III) redox states makes them particularly suitable as redox shuttles between enzyme active sites and electrode surface. The redox potential of the Os(III)/Os(II) redox system can easily be modulated by modification of the surrounding ligands and their substituents, mainly pyridines or imidazoles, allowing these complexes to wire both multicopper enzymes for oxygen reduction and glucose oxidases for glucose oxidation.6,7 In addition, their immobilization onto the electrode surface has widely been investigated in order to design enzyme electrodes for biosensing and biofuel cell applications.6,7 These advances have led to high power glucose biofuel cells, which have now demonstrated their ability to operate in living organisms.8−12 Recently, an immobilization strategy for osmium complexes has successfully been developed on advanced graphitic nanomaterials, i.e., carbon nanotubes (CNTs) and graphene, which possess an ideal combination of high conductivity, high stability, and high electroactive surface.13−15 In particular, noncovalent strategies based on the π−π interactions between π-extended molecules and CNT sidewalls have been employed. Grafting transition-metal complexes on these carbon nano© XXXX American Chemical Society

structures provides excellent electron transfer properties and increases the number of redox centers per surface unit without destroying CNT conductivity at these redox nanomaterials.15−21 NHC ligands have been growingly employed in many applications such as catalysis,22,23 electrocatalysis,24−28 medicinal chemistry,22 and photochemistry.29 Among metal-NHC complexes, several osmium-NHC complexes have been characterized showing photochemical properties30−33 and catalytic activity toward olefin metathesis34 or O−H bond activation.35 However, the properties of NHC-metal complexes toward transferring electrons to enzymes, acting as redox mediators, have never been investigated so far. Due to the possibility to tune their electronic properties as well as their strong σ-donor character, these ligands could represent an original alternative to other neutral two-electron donors such as pyridines or imidazoles, which have been investigated for the design of transition-metal-based redox mediators. In this work, we describe the synthesis of novel osmium-NHC complexes using the pincer ligand 1,1′-dimethyl-3,3′-methylenediimidazole-2,2′-diylidene (bis-NHC). While stabilizing osmium complexes in different redox states, these ligands allow a finetuning of redox potentials of the osmium center with stronger Received: June 21, 2016

A

DOI: 10.1021/acs.organomet.6b00508 Organometallics XXXX, XXX, XXX−XXX

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Organometallics electron-donating properties as compared to well-known pyridine ligands. When designing an enzymatic bioelectrode for a fuel cell, it is crucial to use a redox mediator with redox potentials close enough to the redox potentials of an enzyme’s active sites while providing minimal driving force for efficient electron transfer.1,4 This allows minimizing overpotentials toward the given electrocatalytic reaction at the electrode and the achievement of a high fuel cell voltage. An original osmium complex 1, bearing two bipyridines (bpy) and a bis-NHC ligand, was synthesized. In addition, the synthesis of an original [bis(2,2′-bipyridine)(4,4′-bis(4-pyrenyl1-ylpentyloxy)(bis-NHC)] osmium(II) hexafluorophosphate complex 2 bearing pyrene groups was also realized. Their electrochemical study was achieved in both organic and aqueous media. The ability of complex 2 to form metallopolymer by electropolymerization of the pyrene groups was investigated on GC electrodes.15,19,36 Its interaction with multiwalled CNT (MWCNT) electrodes was also investigated in order to form nanostructured redox electrodes based on a OsII-NHC complex. Thanks to its pyrene groups, complex 2 not only can be electropolymerized on an electrode but can also strongly interact with CNT-based electrodes by π−π interactions. As the bis-NHC ligand allows the Os(III)/Os(II) redox couple to be shifted in the negative region, complex 1 was synthesized in order to match the redox potentials of multicopper oxidases (MCOs) such as bilirubin oxidase from Myrothecium verrucaria (MvBOD). These enzymes are widely used as cathode catalysts for enzymatic fuel cells.4,37 The active site of MCOs is composed of a trinuclear copper cluster, where oxygen is reduced, and a mononuclear T1 copper center, involved in the electron transfers between the phenolic substrate and the trinuclear copper center. For MvBOD, the T1 copper redox potential has been measured at E = 0.49 V vs ECS.38−40 The ability of osmium-NHC complexes to act as high-potential redox mediators of MvBOD is shown.

ppm, respectively, which falls in the typical high-frequency region for such a metalated carbon bond.31 The structure of 1 was determined by X-ray diffraction. The ORTEP diagram of 1 is displayed in Figure 2. The structure of 1 is in agreement with

RESULTS AND DISCUSSION Synthesis and Characterization of Bis-NHC-Osmium Complexes. OsII-NHC complexes were synthesized in two steps. The first step uses a widely employed carbene transfer reaction between the metal precursor, here [OsCl(μ-Cl)(η6-pcymene)]2, and a dimeric [AgI(bis-NHC)]22+ starting complex. Transmetalation and chloride substitution afford the osmium intermediate [OsCl(bis-NHC)(η6-p-cymene)]PF6, bearing a pcymene ligand and the chelating bis-NHC ligand. This intermediate was characterized by 1H NMR and mass spectroscopy. This complex further reacts with bipyridine or pyrene-modified bipyridine, affording the OsII-NHC complexes 1 and 2, respectively (Figure 1). Both 1 and 2 were fully characterized by mass spectroscopy, 1 H NMR, and 13C NMR. The 13C NMR spectra of 1 and 2 exhibit a signal attributed to the carbene at 175.3 and 160.1

Table 1. Selected Bond Lengths and Angles for 1

Figure 2. ORTEP view of 1. PF6− anions were omitted for clarity.

the spectroscopic data. The osmium center is surrounded by the three bidentate ligands, two bipyridines, and the bis-NHC ligands, adopting an octahedral geometry. The most representative bond distances and angles are given in Table 1. The Os−C distances (2.022(11) and 2.064(10) Å) are in agreement with the bond lengths observed for related osmium complexes bearing NHC ligands.30,32



atom

atom

bond distance (Å)

angle

angle (deg)

Os Os Os Os Os Os

C22 C24 N3 N1 N2 N4

2.022(11) 2.064(10) 2.079(8) 2.093(9) 2.108(8) 2.115(9)

C22−Os−C24 N1−Os−N2 N3−Os−N4 N4−Os−C24 N3−Os−N1 N2−Os−C22

85.6(5) 77.1(3) 77.9(3) 172.0(4) 171.2(3) 172.5(3)

Electrochemistry and Surface Chemistry of OsNHC Complexes at GC and MWCNT Electrodes. Electrochemistry of 1 and 2 was performed in MeCN−TBAP (Figure 3A and B). For both complexes, two reversible reductions were attributed to the ligand-centered reduction of the two bipyridine ligands, while the reversible oxidation is attributed to the metal-centered Os(III)/Os(II) redox couple. For 2, an irreversible oxidation peak was attributed to the irreversible oxidation of the two pyrene groups. Table 2 displays the values of redox potentials for both complexes. Complex 2 can undergo oxidative electropolymerization via the formation of a polymerized pyrene film.15,19,36 We therefore investigated the electrosynthesis of a poly-[2] metallopolymer at the surface of GC electrodes by successive CV scans above the irreversible oxidation of pyrene. Figure 4 displays the successive 20 scans performed on a GC electrode in a 0.2 mM solution of 2. The growth of the polymer is confirmed by the

Figure 1. Synthesis of 1 and 2. B

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backbone.41 These systems are attributed to the cathodic and anodic polypyrene electroactivity. Two intense anodic and cathodic irreversible peaks of same intensity are observed at Epox = 0.16 V and Epred = −1.89 V vs Fc+/0 and marked with an asterisk. These peaks are commonly observed in redox polymers with multiple redox systems.42−44 This chargetrapping phenomenon involves the release of trapped charges in the domain of electroactivity of the polymer; trapped reduced charges are released at Epox = 0.16 V vs Fc+/0, at the foot of the Os(II)/Os(III) oxidation (E1/2ox1 = 0.18 V vs Fc+/0), while trapped oxidized charges are released at the foot of the bpy/bpy•− redox system (E1/2red1 = −1.84 V vs Fc+/0). After transferring the electrodes in monomer-free solution (Figure 5), the electroactivity of the metallopolymer is observed, assessing the electrodeposition of the poly-[2] at the surface of the electrode.

Figure 3. CV of (A) a 0.3 mM solution of 1 and (B) a 0.2 mM solution of 2 in MeCN−0.1 TBAP: (dashed line) CV of a 0.54 mM solution of ferrocene (v = 0.1 mV s−1).

Table 2. Electrochemical Data for 1 and 2 in MeCN (Potentials vs Fc+/0) complex

E1/2ox1

Epox2

E1/2red1

E1/2red2

1 2

0.25 0.18

+ 0.93

−1.78 −1.84

−2.02 −2.07

Figure 5. (A) CV of the poly-[2]-functionalized GC electrode in monomer free MeCN−0.1 M TBAP solution (v = 100 mV s−1). (B) Plot of the anodic and cathodic peak currents against scan rate and associated linear fitting curves (dotted line).

As expected, the anodic and cathodic irreversible peaks related to charge-trapping effect almost disappear if the scan range is restricted to the positive or negative potential range, respectively. A ΔEp of 30 mV, close to the theoretical value of 0 mV, was measured for the Os(III)/Os(II) redox system, accompanied by a ratio Ipox/Ipred = 1. Furthermore, linear dependence of the peak current intensity on scan rate unambiguously confirms a surface-confined redox process.45 By integration of the charge under the Os(III)/Os(II) redox system, a surface concentration for complex 2 of 2.2 × 10−11 mol cm−2 was estimated at the surface of the electrode. Owing to the presence of one pyrene group per bipyridine ligand in 2, this Os(II) complex interacts with the π-extended surface of MWCNT sidewalls via π−π interactions. By simply soaking an MWCNT electrode in a 0.2 mM MeCN solution of 2, followed by several washings in MeCN and acetone, this complex can be grafted on the surface of MWCNTs. Figure 6 shows the schematic representation of the functionalized MWCNT and its electrochemical behavior. Figure 6B shows a SEM image of the functionalized electrode surface, which underlines the high specific surface brought by the MWCNT film. On the CV performed in pure electrolyte (Figure 6C), a reversible redox system is observed at E1/2 = +0.18 V vs Fc+/0 with a ΔEp of 40 mV. In addition to the linear dependence of peak current intensities on scan rate, these features confirm the stable immobilization of 2 on MWCNTs. Integration of the charge under the Os(III)/Os(II) redox systems gives a surface coverage of 1.2 × 10−10 mol cm−2, considering the geometrical surface of the electrode (0.07 cm−2). This correspond to a 5fold increase as compared to electrodeposition of the complex

Figure 4. (A) Scheme of electropolymerization of complex 2. (B) Electropolymerization of 2 performed by 20 successive scans between −2.3 and 1.1 V in MeCN−TBAP (v = 0.1 mV s−1).

increase of the reversible systems that belong to complex 2, at E1/2 = −2.07, −1.84, and +0.18 V vs Fc+/0. The irreversible oxidation of pyrene decreases as the pyrene unit becomes increasingly difficult to oxidize as the polymer grows on the surface of the electrode. Two novel reversible redox systems appear at E1/2 = −0.73 V and E1/2 = +0.41 V vs Fc+/0, corresponding to the electroactivity of the polypyrene C

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these enzymes. MvBOD was chosen, as it is a well-studied MCO for enzymatic fuel cell application.37 UV−visible spectroscopy was first conducted to confirm the role of 1 as substrate of MvBOD in air-saturated solution at pH 6.5, the enzyme optimum pH. As MvBOD is added to a solution of 1, it turns rapidly from green to red, indicating the fast formation of an OsIII-NHC complex. The enzymatic reaction can be followed by measuring the UV−visible spectrum of 1 during the course of the reaction (Figure 7B). Characteristic absorption bands of the Os(II) complex at 330 (ε = 5170 M−1 cm−1), 450 (4380 M−1 cm−1), 484 (4520 M−1 cm−1), and 630 nm (1340 M−1 cm−1) decrease, while new bands appear at 570 (1500 M−1 cm−1) and 317 nm (8900 M−1 cm−1), corresponding to the formation of an OsIII-NHC complex. This confirms the enzymatic oxidation of complex 1 by MvBOD and the concomitant reduction of O2 into H2O. This enzymatic reaction follows a classic Michaelis−Menten dependence. Km, Vmax, and kcat were thus determined by monitoring the initial reaction rate for different concentrations of 1 in air-saturated McIlvaine buffer at pH 6.5 (Figure S1). Table 3 displays kinetic parameters obtained from UV−visible and electrochemical experiments.

Figure 6. (A) Schematic representation of MWCNT functionalized by 2. (B) SEM image of the OsNHC-functionalized MWCNT electrode. (C) CV of the 2-functionalized MWCNT electrode (full line) and the poly-[2]-functionalized GC electrode (dotted line) in MeCN−0.1 M TBAP (v = 10 mV s−1). (D) Plot of the anodic and cathodic peak currents against scan rate and associated linear fitting curves (dotted line).

Table 3. Redox-Mediating Parameters for 1 Measured in McIlvaine Buffer pH 6.5 E1/2(OsIII/II), V

on a GC electrode, underlining the high specific surface of MWCNTs. Electron Transfer Mediation Properties of 1 toward Enzymatic and Electroenzymatic Oxygen Reduction. Contrary to complex 2, complex 1 is water-soluble and was studied in McIlvaine buffer pH 6.5 (Figure 7). A reversible redox system (Ipa/Ipred = 1 and ΔEp = 60 mV) is observed at E = +0.45 V vs Ag/AgCl or +0.65 V vs NHE (Figure 7C, curve a). For comparison, the redox potential of the parent Os(bpy)32+ complex was measured at +0.63 V vs Ag/AgCl.46 The 180 mV negative shift confirms that the bis-NHC ligand is a strong electron donor as compared to the bipyridine ligand.47 The redox potential of 1 is therefore very close to the redox potential of ABTS (E = +0.50 V vs Ag/AgCl at pH 7), the mainly used redox mediator for oxygen reduction by multicopper oxidases.48 Thus, complex 1 has a well-suited redox potential for mediating the high potential oxygen reduction by

+0.45

D0, cm2 s−1 −6

7.12 × 10

Km, mM

kcat, min−1

kcat/Km, M−1 s−1

2.0

84

7.0 × 102

Km is higher while kcat value is lower, as compared to Km (0.25 mM) and kcat (7 × 103 min−1) values measured for ABTS.49 This indicates a lower affinity of MvBOD for complex 1, as compared to ABTS. Figure 7B shows the schematic representation of 1, acting as a redox mediator for electrocatalytic oxygen reduction by MvBOD. CV experiments were performed to investigate the electroenzymatic reduction of oxygen (Figure 7C, curve b). In oxygen-saturated solution, an irreversible cathodic wave is observed at the redox potential of the Os(III)/Os(II) redox couple of complex 1, corresponding to oxygen bioelectrocatalytic reduction. These experiments unambiguously confirm the role of 1 as a redox mediator of MCOs. Owing to a driving force of 40 mV between redox potentials of 1 and MvBOD, these NHC complexes are able to mediate the oxygen

Figure 7. (A) UV−visible spectra of a 29 μM solution of 1 before (a, black) and after addition of MvBOD at 4 (b, red), 8 (c, orange), 10 (d, green), 15 (e, purple), and 20 min (f, blue) (McIlvaine buffer pH 6.5). (B) Schematic representation of the mediated electron transfer between MvBOD and electrode via 1. (C) CV of a 0.25 mM solution of 1 and 36 μM MvBOD (a) under argon and (b) under oxygen (v = 5 mV s−1, McIlvaine buffer pH 6.5). D

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reduction reaction at a close potential, as compared to the enzyme redox potential, and at a final high potential of +0.45 V vs Ag/AgCl (+0.65 V vs NHE), comparable to ABTS.48



CONCLUSION This work describes the synthesis and the electrochemical uses of novel OsII-NHC complexes. These complexes can be easily grafted at the surface of planar electrodes and nanostructured CNT electrodes either by electrogeneration of a redox polymer or by supramolecular π interactions. Furthermore, the lower redox potentials of these complexes match almost exactly with those of multicopper enzymes. Accompanied with their welldefined spectroscopic properties, these complexes represent a novel family of redox mediator for enzymes. Using the rich and growing chemistry of NHC ligands and complexes opens vast possibilities in the design of novel redox entities for interactions with redox enzymes and electrode surfaces. The design of novel NHC-based complexes to study the structure−activity relationship of this novel family of redox mediators with several redox enzymes is currently under way.



ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.organomet.6b00508. Experimental details, synthetic and electrochemical procedures, enzymatic assays, and Figure S1 (PDF) Crystallographic data complex 1 (CIF)



AUTHOR INFORMATION

Corresponding Author

*E-mail: alan.le-goff@univ-grenoble-alpes.fr. Notes

The authors declare no competing financial interest.



ACKNOWLEDGMENTS The authors wish to acknowledge the support from the platform Chimie NanoBio ICMG FR 2607 (PCN-ICMG) and from the LabEx ARCANE (ANR-11-LABX-0003-01). They gratefully acknowledge funding from the Agence Nationale de la Recherche through the project CAROUCELL (ANR-13BIOME-0003-02). They also thank the GDR CNRS 3540 “Biopiles” for partial financial support. Electron microscopy was performed at the CMTC characterization platform of Grenoble INP supported by the Centre of Excellence of Multifunctional Architectured Materials “CEMAM” no. AN-10-LABX-44-01 funded by the “Investments for the Future” Program. The authors are grateful to the “Service de Diffraction des RX de l’Université de Bretagne Occidentale, Brest” for crystallographic measurements (Dr. F. Michaud).



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