Electron transfer reactions of ruthenium(II)-bipyridine complexes carrying tyrosine moiety with quinones

Research article

Received: 31 July 2013, Revised: 7 October 2013, Accepted: 27 October 2013 Published online in Wiley Online Library: 17 December 2013

(wileyonlinelibrary.com) DOI 10.1002/bio.2617

754

Electron transfer reactions of ruthenium(II)–bipyridine complexes carrying tyrosine moietywith quinonesPaulpandian Muthu Mareeswaran,a Eswaran Rajkumar,a,b

Veerasamy Sathisha and Seenivasan Rajagopala*

ABSTRACT: Three ruthenium(II)–bipyridine complexes carrying a tyrosine moiety were synthesized and photophysical andelectron transfer studies with quinones were carried out using absorption and emission spectral techniques. The bindingefficiency of quinones with ruthenium(II)–bipyridine complexes was also studied using these techniques. The bindingefficiency was moderate and similar for all complexes with all quinones. The quenching modes were also similar and efficientfor all complexes with all quinones. The quenching processes were diffusion controlled. The rate of electron transfer wascalculated using semiclassical theory. Copyright © 2013 John Wiley & Sons, Ltd.

Additional supporting information may be found in the online version of this article at the publisher’s web-site.

Keywords: electron transfer; photophysics; ruthenium(II)–bipyridine–tyrosine; quinones; semiclassical theory

* Correspondence to: Seenivasan Rajagopal, School of Chemistry,Madurai Kamaraj University, Madurai, Tamil Nadu, India. E-mail:[email protected]

a School of Chemistry, Madurai Kamaraj University, Madurai, Tamil Nadu, India

b Vel Tech University, Avadi, Chennai, Tamil Nadu, India

IntroductionElectrons shuttle between water and CO2 during photosynthesis(1). Water is split and transfers its electron on the water oxida-tion catalyst (WOC, manganese cluster) (1,2). The reaction centerof photosystem II (PSII) receives the electron from WOC via atyrosine moiety attached to the active center of PSII, which isalso undergoing a hydrogen bonding interaction with theWOC (3–5). In the excited state, PSII transfers its electron tonearby electron acceptors, pheophytin and quinones (QA andQB) (6–8). These quinones deliver the electron to photosystemI (PSI) in the excited state, which is further used in reduction ofCO2 to form carbohydrates (1,9). Thus, the excited states of PSIand PSII attached to tyrosine and nearby quinones are the media-tors of electron transfer (ET) between the WOC and PSI (6–11).Therefore, it is essential that the tyrosine–reaction center–quinonesystem is mimicked exactly in order to understand more preciselythe redox processes occuring in photosynthesis (9–14).

Ruthenium(II) polypyridyl complexes ([Ru(NN)3]2+) are widely

used to mimic the ET behavior of the PSII reaction center(15–17). The advantage with [Ru(NN)3]

2+ complexes is that theproperties of the excited state can be varied systematically byintroducing electron-donating and electron-withdrawing subs-titutents in the 4,4′-position of the 2,2′-bipyridine (bpy) ligand(17–21). Various amino acid moieties have been introduced intoligand bpy of [Ru(bpy)3]

2+ complexes via peptide linkage, andthe photophysical properties have been studied widely (22–25).However in PSII, tyrosineZ is the amino acid that mediates ET fromthe manganese cluster (3,11). Therefore, [Ru(NN)3]

2+ complexescarrying the tyrosine moiety may be an excellent mimic of the PSIIreaction center carrying tyrosine (26). Excitation of a [Ru(NN)3]

2+

complex by a photon leads to the formation of a triplet metal-to-ligand charge transfer (3MLCT) excited state and transfer ofits electron to the electron acceptor (quinones). Ru3+ is then

Luminescence 2014; 29: 754–761 Copyright © 2013 John

reduced in two ways: (i) back ET from the electron acceptor(quinones) and (ii) intramolecular electron transfer from thetyrosine moiety (27–30).

Quinones are ubiquitous in nature. They are ET mediatorsbetween PSI and PSII, and act as anticancer drugs in medicine(31–38). Quinones appear to be predestined as electronacceptors in nature for a variety of reasons (39–41). In order to un-derstand the electron-accepting properties of quinones in naturalphotosynthesis, several model photosensitizers (metal–porphyrin,[Ru(NN)3]

2+ complexes) have been designed and inter- and intra-molecular ET reactions with quinones have been studied (42–44).The ET reactions of several quinones with excited state [Ru(NN)3]

2+

complexes have been reported previously (42–45). ET fromphenolate to [Ru(NN)3]

2+ has been reported extensively from thislaboratory (46–49). Herein, we report a detailed study on the excitedstate ET reactions of [Ru(NN)3]

2+ complexes carrying a tyrosinemoiety with quinones using steady-state and time-resolvedmeasurements. The semiclassical theory of ET has also been appliedsuccessfully for the excited state ET reactions of [Ru(NN)3]

2+

complexes carrying a tyrosine moiety with quinones.

ExperimentalThe compounds bpy (98.9%), RuCl3·3H2O (99.98%) were fromMerck and used without further purification. Benzoquinone

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A photophysic approach

(BQ; > 98.0%); naphthoquinone (NQ; 97.0%); 2,5-dichlo-robenzoquinone (DCBQ; 99.0%); tetrachloro-1,4-benzoquinone(TCBQ; 99.0%); and 7,7,8,8-tetracyanoquinodimethane (TCNQ;98.0%) were from Sigma-Aldrich and their structures are shownin Scheme 1. The compounds 4,4′-dimethyl-2,2′-bipyridine(dmbpy; 99%); 2,2′-bipyridine-4,4′-dicarboxylic acid (dcbpy; 98%)and tyrosine ethyl ester (99.0%) were also from Sigma-Aldrich.

Synthesis of ruthenium(II)–bipyridinecomplexes carrying a tyrosine moietyThe ligands 4-methyl-4′-carboxy-2,2′-bipyridine (cmbpy), 4,4′-dicarboxyethyl ester-2,2′-bipyridine (dcet) and the complexes [Ru(bpy)2]Cl2, [Ru(dmbpy)2]Cl2, [Ru(dcet)2]Cl2, [Ru(bpy)2(cmbpy)]·2PF6,[Ru(dmbpy)2(cmbpy)]·2PF6 and [Ru(dcet)2(cmbpy)]·2PF6 weresynthesized using reported procedures (50–53). [Ru(NN)3]

2+

complexes carrying a tyrosine moiety, Ru(bpy)3–T, Ru(dmbpy)3–T, Ru(dcet)3–T, were synthesized using the following procedureand characterized using ESI-MS spectral techniques. The spectralresults were similar to existing reports (22,53,54).

Preparation of [Ru(bpy)3–T)]·2PF6[Ru(bpy)2(cmbpy)]·2PF6 (400 mg, 0.43 mmol) was dissolved in 30mL of thionyl chloride and the solution was heated to refluxunder nitrogen for 2 h. Evaporation of the excess thionylchloride in vacuum gave a dark red oil, which was immediatelyused for the next step of the reaction. Tyrosine ethyl ester (160mg, 0.65 mmol) was suspended in acetonitrile (15 mL, 99.9%)and the solid in the suspension was dissolved after addtion oftriethylamine (0.4 mL, 2.5 mmol). The clear solution was addeddropwise to the above complex in acetonitrile (5 mL). White

Scheme 1. Structure of ruthenium (II) complexes and quinones used in this study.


75

smoke formed above the solution in the reaction flask, and thesolution was heated to reflux under nitrogen for 2.5 h and thencooled to room temperature. White crystals of triethylaminehydrochloride formed and were filtered off. The filtrate wasconcentrated to ~ 5 mL. The crude product was purified byrepetitive column chromatography on neutral aluminum oxidewith gradient eluents, CH2Cl2 and CH2Cl2/CH3OH (90:10 v/v). Thedesired fractions were combined and the solvents evaporatedto dryness to give a red solid. The red solid was dissolved in waterand to this aqueous solution was added concentrated aqueoussolution of NH4PF6 to produce a red precipitate. Filtration andwashing with water and petroleum ether gave a red solid with70% yield. ESI-MS (M-PF6+ Na) 1074.44 m/z.

Preparation of [Ru(dmbpy)3–T)]·2PF6The same synthetic procedure was adopted for the synthesis of[Ru(dmbpy)2(c-t)]·2PF6 complex. The product yield is 66%.ESI-MS (M-2PF6) 875.03 m/z.

Preparation of [Ru(dcet)3–T)]·2PF6[Ru(dcet)2(cmbpy)]·2PF6 (470 mg, 0.39 mmol) was refluxed in 15mL of thionyl chloride for 3 h. Excess of thionyl chloride wasremoved under reduced pressure, and the residue dried undervacuum at 50°C for 1 h. The resulting solid (acid chloride) wasredissolved in 5 mL of dry CH2Cl2. The solution was addeddropwise to a solution of tyrosine ethyl ester (265 mg, 0.42mmol) and triethylamine (0.5 mL) in dry CH2Cl2 (10 mL). Theresulting solution was stirred under nitrogen at room temperatureovernight. The solvent was removed, and water (50 mL) addedand extracted with CH2Cl2 (4 × 50 mL). The crude product waspurified on a silica gel column using a mixture of MeCN/H2O/KNO3 (saturated) (40/3/1) as the eluent. After purification, thesolvent was evaporated, the solid dissolved in a minimum amountof water, and a saturated aqueous solution of NH4PF6 was added.Themixture was extracted with CH2Cl2, and the combined organicphase was washed with a diluted aqueous Na2CO3 solution andthen dried over Na2SO4. Solvent was removed under reducedpressure to afford 63% yield of the desired product. ESI-MS(M-PF6 + Na) 1335.63 m/z.

Absorption and emission spectralmeasurementsSample solutions of the [Ru(NN)3–T]

2+ complexes and the quinoneswere freshly prepared for each measurement. The [Ru(NN)3–T]

2+

concentration was fixed at 2 × 10-5 M and the quinone concentra-tion was varied between 2 × 10-5 and 2 × 10-4 M. The same samplesolutions were used for both absorption and emission studies. Theabsorption spectrum was recorded using an Analtik-Jena SpecordS100 spectrometer and the emission spectrum using a JASCOspectrofluorometer. All the sample solutions used for emissionmeasurements were deaerated for ~ 30 min using dry N2 gaspurging by keeping solutions in cold water to ensure that therewas no change in the volume of the solution. All measurementswere carried out at room temperature.

Electrochemical measurementsElectrochemical measurements were carried out using cyclicvoltammetric technique with a EG&G Princeton Applied

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Research Potentiostat/Galvanostate Model 273A. Measurementswere taken in acetonitrile using a platinum electrode as theworking electrode with 0.1 M tert-butyl ammonium perchlorateas the supporting electrolyte and platinum wire as the auxiliaryelectrode. The separation between the cathodic and anodicpeaks and the relative intensities of the cathodic and anodiccurrents were taken as criteria for reversibility.

Determination of binding constants usingabsorption and emission techniquesThe binding constant (Ka

abs) for the binding of [Ru(NN)3–T]2+ com-

plexes with quinones was evaluated using Benesi–Hildebrandmethod (equation (1)) (55).

1=ΔA ¼ 1=KaabsΔε Ru NNð Þ3–T

� �2þh iþ 1=Δε Q½ � (1)

Here, ΔA is the change in the absorbance of the [Ru(NN)3–T]2+

complex on the addition of quinone. Δε is the difference in themolar extinction coefficient between the free and quinone-bound[Ru(NN)3–T]

2+ complex. [[Ru(NN)3–T]2+] is the total concentration

of [Ru(NN)3–T]2+and [Q] is the total concentration of quinone.

We have calculated the binding constant for the system fromthe luminescence intensity data using the following modifiedStern–Volmer equation (equation (2)) (18,56).

log I0–Ið Þ=I½ � ¼ nlog Q½ � þ log Kaem (2)

where, I0, I, [Q], Kaem and n are the emission intensity in the ab-

sence of quencher, emission intensity in the presence ofquencher, concentration of quinone, binding constant andstoichiometric ratio, respectively.

Determination of luminescence quenchingconstant kqThe observed quenching rate constant kq for the oxidativequenching of [Ru(bpy)3–T]

2+ with quinones used in the study wasobtained from the Stern–Volmer plots using equation (3)(56).

Io=I ¼ 1þ Ksv Q½ � (3)

Ksv¼ kqτ (4)

where, Ksv, kq and τ are the Stern–Volmer constant, quenching con-stant and excited sate lifetime, respectively. The plot of Iο/I vs [Q] is a

Figure 1. (a) Absorption spectra and (b) normalized emission spectra of [Ru(bpy)3]2+

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straight line with an intercept of unity in all quenching studies. TheStern–Volmer plots for the quenching of [Ru(NN)3–T]

2+ withquinones are shown in Figs S8-S10. The slope of this plot, theStern–Volmer constant, Ksv is related to kq through equation (4).

Results and discussion[Ru(NN)3]

2+ complexes carrying tyrosine moiety ([Ru(bpy)3–T]2+,

[Ru(dmbpy)3–T]2+ and [Ru(dcet)3–T]

2+) were synthesized, asgiven in the Experimental section and characterized using massspectra (22). The structures of complexes are shown in Scheme 1and the mass spectra are shown in Figs S1–S3.

Steady-state absorption and emission prop-erties of [Ru(NN)3–T]2+ complexesThe 1MLCT state of the parent complex [Ru(bpy)3]

2+ has absorp-tion in the visible region at 450 nm. Introduction of a tyrosinemoiety via amide linkage produces a red-shift in the absorptionmaximum to a λmax of 458 nm. The electron-releasing methylgroup is a good σ donor, but a poor π acceptor and the reverseis the case with the electron-withdrawing carboxyethyl estergroup. Thus, the operation of σ-donor and π-acceptor propertiesof the substituents in the ligand bipyridine increases theelectron density on the metal–ligand bond, thereby stabilizingthe 1MLCT state, leading to a red-shift in the absorptionmaximum. Therefore, the absorption, maximum correspondingto the MLCT transition of [Ru(dmbpy)3–T]

2+ and [Ru(dcet)3–T]2+

is shifted towards the red region with respect to the [Ru(bpy)3–T]

2+ complex. The overlayed spectra of [Ru(bpy)3]2+, [Ru(bpy)

3–T]2+, [Ru(dmbpy)3–T]

2+ and [Ru(dcet)3–T]2+ are shown in Fig. 1

(a). The respective absorption λmax values are shown in Table S1.The emission maximum of [Ru(bpy)3]

2+ in CH3CN is 612 nm.Introduction of a tyrosine moiety via amide linkage produces ared-shift in the emission maximum to a λmax of 644 nm. Becauseof the σ electron donation capacity of methyl group, the energygap between the ground and 3MLCT states decreases. Therefore,a red-shift is observed when a –CH3 group is introduced intobpy. However, when the carboxyethyl ester group is introduced,the ligand becomes highly π accepting. Therefore, the energygap between 3MLCT and the ground state increased. Thus, forthe complex [Ru(dcet)3–T]

2+, a blue-shift to the tune of 22 nmis observed compared with [Ru(dmbpy)3–T]

2+. The normalizedemission spectra of four Ru(II) complexes are shown in Fig. 1(b). The respective emission λmax values are given in Table S1.

(----), [Ru(bpy)2C–T)]2+(—), [Ru(dmbpy)2(C–T)]

2+(- - - ) and [Ru(dcEt)2(C–T)]

2+(-.-.-).

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Excited state lifetime and redox propertiesThe excited state lifetime of parent [Ru(bpy)3]

2+ in CH3CN is 850ns. Introduction of a tyrosine moiety via an amide groupincreases the excited state lifetime of the complex (1250 ns).However, introduction of an electron-releasing group in the liganddestabilizes the 3MLCT state by higher σ-donating ability and poorπ-accepting ability. Thus lifetime is reduced. Even though it hashigher lifetime than the parent complex [Ru(bpy)3]

2+, it haslifetime of 985 ns which is 265 ns less than that of the similarcomplex [Ru(bpy)3–T]

2+. However, introduction of the carboxyethylester group into the 2,2′-bipyridine ligand increases the π-acceptingcapacity. It stabilizes the system up to 1350 ns, which is 100 nshigher than the [Ru(bpy)3–T]

2+ and of 500 ns higher than theparent complex. The respective excited state lifetime values aregiven in Table S1.

The parent complex, [Ru(bpy)3]2+, has an oxidation potential of

+1.26 V and introduction of the tyrosine moiety via amide bondingincreases the oxidation potential to +1.39 V. However, the introduc-tion of substituents into the 2,2′-bipyridne ligand produces little shiftin the oxidation potential of the Ru(II) complex. The complex[Ru(dmbpy)3–T]

2+ has an oxidation potential of +1.37 V and[Ru(dcEt)3–T]

2+ has an oxidation potential of +1.29 V. The cyclicvoltammogram of [Ru(dmbpy)3–T]

2+ is shown in Fig. 2.

Figure 2. Cyclic voltagram of [Ru(dmbpy)2(C–T)]2+.

Figure 3. Absorption spectrum of Ru(dcet)3–T (2 × 10-5M) with incremental addit


Study of the binding of *[Ru(NN)3–T]2+ withquinones using absorption spectral techniqueThe changes in the absorption spectra of [Ru(NN)3–T]

2+ com-plexes in the presence of increasing concentrations of quinonesare shown in Figs 3, S4–S6. There is a slight change in theabsorption intensity of MLCT of [Ru(NN)3–T]

2+, which issufficient for the determination of binding constant for thebinding of quinone with [Ru(NN)3–T]

2+ complexes. Li et al.(57–59) have already established the importance of the π–πstacking between phenols and [Ru(bpy)3]

2+. We have usedBenesi–Hildebrand method to calculate the binding constant.The binding constants (Ka

abs) are given in Table 1. TheBenesi–Hildebrand plots are shown in Figs S7–S9. From thebinding constant values it can be inferred that the efficiencyof binding is moderate and similar to all quinones in therange of 9–33 M-1.

Binding and oxidative quenching of*[Ru(NN)3–T]2+ with quinones usingemission spectral techniqueThe increase in the concentration of quinones quenchedthe emission intensity of [Ru(NN)3–T]

2+ complexes. Thequenching of [Ru(NN)3–T]

2+ complexes with quinones isshown in Figs 4, S10–S12. The binding constant (Ka

em) forthe binding of quencher with the sensitizer is calculated usingthe modified Stern–Volmer equation (18). The modified Stern–Volmer plots are shown in Figs S13–S15. The binding constantvalues are given in Table 1. In this case, the binding efficiencyfor all five quinones is similar with all three [Ru(NN)3–T]

2+

complexes. The bimolecular quenching rate constants, kq, of the*[Ru(NN)3–T]

2+ complex by quinones in CH3CN were calculatedusing the Stern–Volmer equation (51). Stern–Volmer plots areshown in Figs S16–S18. From the slope of the Stern–Volmerplots, the bimolecular quenching rate constants, kq, arecalculated and these values are given in Table 2.Although the quenching constant kq is similar for both[Ru(bpy)3–T]

2+ and [Ru(dmbpy)3–T]2, the value is one order

higher for [Ru(dcet)3–T]2+. This is because of the favorable

ΔG0 value for [Ru(dcet)3–T]2+. Although there is a possibility

of quenching due to energy transfer, it has already beenestablished that quenching of the emission of [Ru(NN)3–T]

2+

ion of quinones (a) BQ (2 × 10-5to 2 × 10

-4M), (b) NQ (2 × 10

-5to 2 × 10

-4M).


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Table 1. Binding constants of [Ru(NN)3–T] complexes with quinones using absorption (Kaabs, M-1) and emission (Ka

em, M-1)techniques

Quinones [Ru(bpy)3–T]2+ [Ru(dmbpy)3–T]

2+ [Ru(dcet)3–T]2+

Kaabs n Ka

em Kaabs n Ka

em Kaabs n Ka

em

BQ 9.9 ± 0.34 0.71 18.1 ± 0.43 8.3 ± 0.22 0.82 17.6 ± 0.41 10.6 ± 0.57 0.66 25.7 ± 0.91NQ 10.2 ± 0.12 0.94 20.1 ± 0.61 9.7 ± 0.78 0.78 22.6 ± 0.77 11.1 ± 0.33 0.73 32.8 ± 1.10TCNQ 10.7 ± 0.55 0.67 22.6 ± 0.21 10.8 ± 0.67 0.69 19.1 ± 0.24 9.8 ± 0.63 0.85 31.4 ± 0.22DCBQ 9.6 ± 0.10 0.58 20.5 ± 0.32 10.4 ± 0.34 0.72 27.5 ± 0.54 10.1 ± 0.42 0.59 29.1 ± 0.13TCBQ 10.5 ± 0.78 0.95 25.8 ± 0.89 11.1 ± 0.54 0.55 30.3 ± 0.32 11.7 ± 0.12 0.91 33.7 ± 0.58

Figure 4. Emission spectrum of Ru(dmbpy)3–T (2 × 10-5M) with incremental addition of quinones (a) BQ (2 × 10

-5to 2 × 10

-4M), (b) NQ (2 × 10

-5to 2 × 10

-4M).

Table 2. Rate constants for oxidative quenching, rate of electron transfer, equilibrium constant and free energy

Quencher Equilibriumconstant, Keq

Rate of oxidativequenching, kq

Rate of electrontransfer, k23

log k23 ΔGο, eV

[Ru(bpy)3–T]BQ 6.6 1.2 × 109 2.9 × 109 9.46 0.13NQ 8.4 6.5 × 109 9.6 × 108 8.98 0.29TCNQ 7.1 2 × 1010 7.2 × 109 9.86 -0.28DCBQ 7.6 1.9 × 109 5.9 × 109 9.77 -0.39TCBQ 10.3 2.6 × 1010 1.2 × 1010 10.08 -0.55[Ru(dmbpy)3–T]BQ 5.2 8.0 × 109 8.7 × 108 8.94 0.11NQ 6.7 4.4 × 109 3.4 × 108 8.53 0.27TCNQ 6.9 1.0 × 109 2.6 × 109 9.43 -0.57DCBQ 7.2 9.1 × 109 2.3 × 109 9.38 -0.30TCBQ 9.7 8.7 × 109 3.8 × 109 9.59 -0.41[Ru(dcet)3–T]BQ 7.1 5.2 × 1010 2.0 × 109 9.31 0.23NQ 8.7 3.4 × 1010 1.3 × 109 9.14 0.32TCNQ 7.7 2.5 × 1010 6.3 × 109 9.88 -0.65DCBQ 8.1 2.1 × 1010 7.4 × 109 9.87 -0.42TCBQ 11.1 1.8 × 1010 4.5 × 109 9.66 -0.67


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with quinones is due to ET (22). The probability of reduction ofoxidized [Ru(NN)3–T]

2+ by intramolecular ET from a tyrosinemoiety in acetonitrile medium is also negligible (22).Therefore, we have assigned the quenching as ET and usedthe quenching constant values for calculating rate ofelectron transfer.


Dynamics of ET reactions of [Ru(NN)3–T]2+

with quinones

The rate of ET from a donor molecule to an acceptor in a solventis controlled by the change in free energy of the reaction (ΔG0),the reorganization energy (λ) and the ET distance (d) between



the donor and the acceptor. The ET rate constant (ket) in boththe classical and semiclassical theories can be represented byequation (5)(17)(38).

ket ¼ кelυnexp �ΔG #= RTð Þ� �(5)

where, кel is the electronic transmission coefficient, υn the nu-clear frequency and ΔG# is the free energy of activation. Whenthe ET distance, d, is kept constant, the rate of the ET processis decided by ΔG0 and the reorganization energy, λ throughthe Marcus equation (equation (6)) (17,60).

ΔG # ¼ λþ ΔG0� �2

= 4λð Þ (6)

Substitution of the above expression into equation (5) givesthe basic relation for ket in terms of ΔG0 and λ:

ket ¼ кelυnexp � λ þ ΔG0� �2

= 4λRTð Þh i

(7)

According to classical Marcus theory, ET can occur only at theintersection of the two potential energy surfaces. In such case, amore effective route for the ET rate is derived from the semiclassicaltheory, which can be represented by equation (8).

ket ¼ 4π2=h HDAj j2 4πλokTð Þ�1=2 ∑∞

m¼0e�SSm=m!� �

exp � λo þ ΔG° þmhvð Þ2=4λokTh i

(8)

In equation (8) HDA is the electronic coupling coefficientbetween the redox centers, the reorganization energy λ iscomposed of solvational λo and vibrational λi contributions withs = λi/hν, ν is the high-energy vibrational frequency associatedwith the acceptor and m is the density of product vibrationallevels. The terms h and k are Planck’s and Boltzmann’sconstants, respectively

According to Rehm and Weller, the free-energy change of ET(ΔG°) can be calculated from equation (9) (61-62).

ΔG° ¼ EðD=DþÞ � EðA=A�Þ � Eo�o � e2=aε (9)

where E(D/D+;) is the oxidation potential of donors, E(A/A�), thereduction potential of acceptor, Eo-o the lowest excited stateenergy of Ru(II) complexes, and e2/aε is a columbic term.The ΔG° values thus estimated for different donor and acceptorpairs in CH3CN are given in the Table 2.

The value of λo can be evaluated classically by using dielectriccontinuum model, equation (10).

λo ¼ e2=4πεo 1=2rD þ 1=2rA–1=dð Þ 1=Dop–1=Ds� �

(10)

Where e is the transferred electronic charge, εo is the permittiv-ity of free space, Dop and Ds are the optical and static dielectric

Scheme 2. Mechanism for the oxidative qu


constants, respectively. The terms rD and rA are the radii of theelectron donor and acceptor, respectively and d is the separationdistance between the donor and acceptor in the encountercomplex. This model is most applicable in cases where the donorand acceptor are roughly spherical, and their center-to-centerdistance (rDA) is large compared with the sum of the sphere radii.The values of rD and rA can be estimated by the semi-empirical(PM6 level) molecular model (10.8 Å for [Ru(bpy)3–T]

2+; 11.2 Åfor [Ru(dmbpy)3–T]

2+ and 12.9 Å for [Ru(dcet)3–T]2+ and for

quinones in the range 2.97–5.0 Å). Because the ΔG0 and λvalues are known, the rate constant for ET from the excitedstate of [Ru(NN)3–T]

2+ to quinone can be calculated. Inequation (8), HDA = 2 × 10�3 eV, λ = 0.81–0.92 eV, ν = 1000–1500cm�1 and T = 298 K. These are the optimum values for the reaction,chosen by a trial and error method (63).Because quenching occurs via ET, the redox quenching

process can be discussed in terms of the mechanism shown inScheme 2. By applying steady-state treatments to the short-livedspecies in Scheme 2, the following expression (equation (11)) forthe observed bimolecular quenching rate constant, kobs(kq) canbe derived.

kq ¼ k121þ k12=k23Keq

� � (11)

where Keq is the equilibrium constant for the formation of theencounter complex and k12 is the rate constant for the diffusionprocess to form the encounter complex. The value of k12 is calcu-lated from equation (12) (61-63).

k12 ¼ 2RT=3000η 2þ rD=rA þ rA=rD½ �f (12)

where f�1 = d∫eu/kT dr/r2 with u = ZDZAe2/DS[e

Kd/1 + Kd] e�Kr/rwhere K = (8πe2Nη/1000DSkT)

1/2, rD and rA are the radii of thereactants and η is the viscosity of the medium.The diffusion rate constant, k12, calculated according to

Smoluchowski (64) for non-charged molecules, has a value of1.9 × 1010 dm3 mol-1 s-1. Keq was estimated using the Fuossand Eigen equation (equation (13)) (65).

Keq ¼ 4πNd3=3000� �

exp �wr=RTð Þ (13)

where w r is the work required to bring the reactants to theseparation distance d. Because we use neutral quenchersthroughout this study, wr is zero. The value of Keq is in the range5.2–11.1 M-1 for the oxidative quenching of [Ru(NN)3–T]

2+ withquinones. Keq values given in Table 2 are close to the bindingconstant values obtained from absorption and emissiontechniques (Ka

abs and Kaem) in Table 1. Because the values of k12

and Keq are known, the value for k23, the rate constant for theprocess of ET in the encounter complex, can be calculated fromthe observed kq values using equation (11).In order to treat the dynamic quenching process in terms of ther-

modynamic function (ΔG0), we correlated the ET rate constant, k23,

enching of *[Ru(NN)3–T]2+

with quinones.


759

Figure 5. Plot of log k23, M-1s-1vsΔG

0, eV for the oxidative quenching of [Ru(NN)3–T]

2+

complexes with quinones.


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values estimated from the kq values with the free energy change(ΔG0) of the electron transfer process (equation (7)). The plot oflog k23 vs ΔG

0 is shown in Fig. 5 and the ET rate constant increaseswith increasing the driving force (ΔG0) of the ET reaction and at-tains saturation at high ΔGo values (�0.4 eV). The values of k23(ket) can also be calculated using semiclassical theory from equa-tion (8). The experimental k23 values along with the calculated ket(solid line) values were plotted against �ΔG° values (Fig. 5) for all[Ru(NN)3–T]

2+ complexes. Figure 5 shows that the rate constantsfor ET reaction of chosen redox system are in accordance withRhem–Weller model.

ConclusionThe tyrosine–reaction center–quinone system in PSII is success-fully mimicked by studying the ET reaction of [Ru(NN)3–T]

2+

complexes with quinones. Modification of periphery of the 2,2′-bipyridine ligands affects the photophysical properties andhence, the ET properties of [Ru(NN)3–T]

2+ complexes. Thebinding constant values obtained from absorption and emissiontechniques (Ka

abs and Kaem) and equilibrium constant values (Keq)

obtained from equation (13) established the interaction ofquinones with [Ru(NN)3–T]

2+ complexes. The quenching rateconstants are varied with respect to the nature of the (elec-tron releasing and withdrawing) substituents. The plot oflog k23 vs ΔG0 shows that the ET process from [Ru(NN)3]

2+

carrying a tyrosine moiety with quinones is in accordancewith the Rhem–Weller model.

Acknowledgements

We sincerely thank Prof. P. Ramamurthy, National Center forUltrafast Processes, University of Madras, Taramani, Chennai forhis help in time resolved measurements. We sincerely thank DrM. Vairamani, IICT, Hyderabad for his help in HR-MS.

References1. Scheuring S. The supramolecular architecture of the bacterial photo-

synthetic apparatus studied by atomic force microscopy (AFM). In:Aartsma T, Matysik J, editors. Biophysical techniques in photosynthe-sis. Advances in photosynthesis and respiration. 26. Dordtrecht:Springer, 2008:1–11.


2. Kalyanasundaram K. Photochemistry of polypyridine and porphyrincomplexes. London: Academic Press, 1992.

3. Barber J. Photosynthetic generation of oxygen. Phil Trans B.2008;363:2665–74.

4. Vermaas WJ, Styring S, SchröderW, Andersson B. Photosynthetic wateroxidation: the protein framework. Photosynth Res 1993;38:249–63.

5. Dau H, Andrews JC, Roelofs TA, Latimer MJ, Liang W, Yachandra VK,et al. Structural consequences of ammonia binding to the manga-nese center of the photosynthetic oxygen-evolving complex: an X-ray absorption spectroscopy study of isotropic and oriented photo-system II particles. Biochemistry 1995;34:5274–87.

6. Sun L, Burkitt M, Tamm M, Raymond MK, Abrahamsson M,LeGourriérec D, et al. Hydrogen-bond promoted intramolecular ETto photogenerated Ru(III): a functional mimic of tyrosine Z andhistidine 190 in photosystem II. J Am Chem Soc 1999;121:6834–42.

7. Magnuson A, Berglund H, Korall P, Hammarström L, Åkermark B,Styring S, et al. Mimicking electron transfer reactions in photosystemII: synthesis and photochemical characterization of a ruthenium(II)tris(bipyridyl) complex with a covalently linked tyrosine. J Am ChemSoc 1997;119:10720–5.

8. Diner BA, Bautista JA, Nixon PJ, Berthomieu C, Hienerwadel R, BrittRD, et al. Coordination of proton and electron transfer from theredox-active tyrosine, YZ, of photosystem II and examination of theelectrostatic influence of oxidized tyrosine, YD[radical dot](H+). PhysChem Chem Phys 2004;6:4844–50.

9. Oja V, Laisk A. Photosystem II antennae are not energetically connected:evidence based on flash-induced O2 evolution and chlorophyll fluores-cence in sunflower leaves. Photosynth Res 2012;114:15–28.

10. Sjödin M, Irebo T, Utas JE, Lind J, Merényi G, Åkermark B, et al. Kineticeffects of hydrogen bonds on proton-coupled electron transfer fromphenols. J Am Chem Soc 2006;128:13076–83.

11. Najafpour M, Moghaddam A, Yang Y, Aro E-M, Carpentier R, Eaton-Rye J, et al. Biological water-oxidizing complex: a nano-sized manga-nese–calcium oxide in a protein environment. Photosynth Res2012;114:1–13.

12. Irebo T, Reece SY, Sjödin M, Nocera DG, Hammarström L. Proton-coupled electron transfer of tyrosine oxidation: buffer dependenceand parallel mechanisms. J Am Chem Soc 2007;129:15462–4.

13. Sjödin M, Styring S, Wolpher H, Xu Y, Sun L, Hammarström L.Switching the redox mechanism: models for proton-coupled elec-tron transfer from tyrosine and tryptophan. J Am Chem Soc2005;127:3855–63.

14. Sjödin M, Styring S, Åkermark B, Sun L, Hammarström L. Proton-coupledelectron transfer from tyrosine in a tyrosine�ruthenium�tris-bipyridinecomplex: comparison with tyrosine Z oxidation in photosystem II. J AmChem Soc 2000;122:3932–6.

15. Nazeeruddin MK, Kalyanasundaram K. Acid-base behavior in theground and excited states of ruthenium(II) complexes containingtetraimines or dicarboxybipyridines as protonatable ligands. InorgChem 1989;28:4251–9.

16. Darwent JR, Kalyanasundaram K. Electron-transfer reactions of qui-nones, hydroquinones and methyl viologen, photosensitized bytris(2,2[prime or minute]-bipyridine)-ruthenium(II). J Chem Soc Fara-day Trans 1981;77:373–82.

17. Juris A, Balzani V, Barigelletti F, Campagna S, Belser P, von ZelewskyA. Ru(II) polypyridine complexes: photophysics, photochemistry,eletrochemistry, and chemiluminescence. Coord Chem Rev1988;84:85–277.

18. Bae E, Choi W. Effect of the anchoring group (carboxylate vsphosphonate) in Ru-complex-sensitized TiO2 on hydrogen produc-tion under visible light. J Phys Chem B 2006;110:14792–9.

19. Csjernyik G, Éll AH, Fadini L, Pugin B, Bäckvall J-E. Efficientruthenium-catalyzed aerobic oxidation of alcohols using a biomi-metic coupled catalytic system. J Org Chem 2002;67:1657–62.

20. Kuang D, Ito S, Wenger B, Klein C, Moser J-E, Humphry-Baker R, et al.High molar extinction coefficient heteroleptic ruthenium complexesfor thin film dye-sensitized solar cells. J Am Chem Soc2006;128:4146–54.

21. Waern JB, Desmarets C, Chamoreau L-M, Amouri H, Barbieri A,Sabatini C, et al. Luminescent Cyclometalated RhIII, IrIII, and (DIP)2RuII complexes with carboxylated bipyridyl ligands: synthesis,X-ray molecular structure, and photophysical properties. Inorg Chem2008;47:3340–8.

22. Rajkumar E, Rajagopal S, Ramamurthy P, Vairamani M. Photophysicsof ruthenium(II) complexes carrying amino acids in the ligand 2,2′-



bipyridine and intramolecular electron transfer from methionine tophotogenerated Ru(III). Inorg Chim Acta 2009;362:1629–36.

23. Geißer B, Alsfasser R. A peptide approach to covalently linked[Ru(bipy)3]2+–ferrocene and [Ru(bipy)3]

2+–tyrosine conjugates.Inorg Chim Acta 2003;344:102–8.

24. Ozawa H, Haga M-a, Sakai K. A photo-hydrogen-evolving moleculardevice driving visible-light-induced EDTA-reduction of water intomolecular hydrogen. J Am Chem Soc 2006;128:4926–7.

25. Striplin DR, Reece SY, McCafferty DG, Wall CG, Friesen DA, Erickson BW,et al. Solvent dependence of intramolecular electron transfer in a heli-cal oligoproline assembly. J Am Chem Soc 2004;126:5282–91.

26. Irebo T, Zhang M-T, Markle TF, Scott AM, Hammarström L. Spanningfour mechanistic regions of intramolecular proton-coupled electrontransfer in a Ru(bpy)3

2+–tyrosine complex. J Am Chem Soc2012;134:16247–54.

27. Kodera Y, Hara H, Astashkin AV, Kawamori A, Ono T-a. EPR study oftrapped tyrosine Z+ in Ca-depleted photosystem II. Biochim BiophysActa 1995;1232:43–51.

28. Svensson B, Etchebest C, Tuffery P, van Kan P, Smith J, Styring S. Amodelfor the photosystem II reaction center core including the structure of theprimary donor P680. Biochemistry 1996;35:14486–502.

29. Grätzel M. Solar energy conversion by dye-sensitized photovoltaiccells. Inorg Chem 2005;44:6841–51.

30. Clifford JN, Palomares E, Nazeeruddin MK, Grätzel M, Nelson J, Li X,et al. Molecular control of recombination dynamics in dye-sensitized nanocrystalline TiO2 films: free energy vs distance depen-dence. J Am Chem Soc 2004;126:5225–33.

31. Saito K, Rutherford AW, Ishikita H. Mechanism of proton-coupledquinone reduction in photosystem II. Proc Natl Acad Sci U S A2013;110:954–9.

32. Hasan SS, Yamashita E, Baniulis D, Cramer WA. Quinone-dependentproton transfer pathways in the photosynthetic cytochrome b6fcomplex. Proc Natl Acad Sci 2013;110:4297–302.

33. Johnsson Wass JRT, Ahlberg E, Panas I, Schiffrin DJ. Quantum chem-ical modeling of the reduction of quinones. J Phys Chem A2006;110:2005–20.

34. Ishikita H, Knapp E-W. Control of quinone redox potentials in photo-system II: electron transfer and photoprotection. J Am Chem Soc2005;127:14714–20.

35. Lenaz G. Quinone specificity of complex I. Biochim Biophys Acta1998;1364:207–21.

36. Itoh S, Ohshiro Y. The chemistry of heterocyclic o-quinone cofactors.Nat Prod Rep 1995;12:45–53.

37. Nohl H, Jordan W, Youngman RJ. Quinones in biology: functions inelectron transfer and oxygen activation. Adv Free Radal Biol Med1986;2:211–79.

38. Marcus RA, Sutin N. Electron transfers in chemistry and biology.Biochim Biophys Acta 1985;811:265–322.

39. Kurreck H, Huber M. Model reactions for photosynthesis – photoin-duced charge and energy transfer between covalently linked por-phyrin and quinone units. Angew Chem Int Ed 1995;34:849–66.

40. Luque NB, Schmickler W. Are the reactions of quinones on graphiteadiabatic? Electrochim Acta 2013;88:892–4.

41. Kasson TD, Barry B. Reactive oxygen and oxidative stress: N-formylkynurenine in photosystem II and non-photosynthetic proteins.Photosynth Res 2012;114:97–110.

42. Eugster N, Fermín DJ, Girault HH. Photoinduced electron transfer atliquid–liquid interfaces: dynamics of the heterogeneous photore-duction of quinones by self-assembled porphyrin ion pairs. J AmChem Soc 2003;125:4862–9.

43. Szrebowaty P, Kapturkiewicz A. Free energy dependence on tris(2,2′-bipyridine)ruthenium(II) electrochemiluminescence efficiency. ChemPhys Lett 2000;328:160–8.

44. D’Souza F, Deviprasad GR. Studies on porphyrin�quinhydronecomplexes: molecular recognition of quinone and hydroquinonein solution. J Org Chem 2001;66:4601–9.

45. Okamoto K, Fukuzumi S. Hydrogen bonds not only provide astructural scaffold to assemble donor and acceptor moieties of zincporphyrin�quinone dyads but also control the photoinducedelectron transfer to afford the long-lived charge-separated states.J Phys Chem B 2005;109:7713–23.


46. Rajendran T, Thanasekaran P, Rajagopal S, Gnanaraj GA, Srinivasan C,Ramamurthy P, et al. Steric effects in the photoinduced electron transferreactions of ruthenium(II)-polypyridine complexes with 2,6-disubstitutedphenolate ions. Phys Chem Chem Phys 2001;3:2063–9.

47. Thanasekaran P, Rajagopal S, Srinivasan C. Photoredox reactions oftris(2,2′-bipyrazine)-tris(2,2′-bipyrimidine)- and tris(2,3-bis[2-pyridyl]pyrazine)ruthenium(II) cations with phenolate ions in aqueous ace-tonitrile. J Chem Soc Faraday Trans 1998;94:3339–44.

48. Thanasekaran P, Rajendran T, Rajagopal S, Srinivasan C, Ramaraj R,Ramamurthy P. Marcus inverted region in the photoinduced elec-tron transfer reactions of ruthenium(II)�polypyridine complexeswith phenolate ions. J Phys Chem A 1997;101:8195–9.

49. Rajagopal S, Gnanaraj GA, Mathew A, Srinivasan C. Excited state elec-tron transfer reactions of tris(4,4′-dialkyl-2,2′-bipyridine)ruthenium(II)complexes with phenolate ions: structural and solvent effects. JPhotochem Photobiol A 1992;69:83–9.

50. Sprintschnik G, Sprintschnik HW, Kirsch PP, Whitten DG. Photochem-ical reactions in organized monolayer assemblies. 6. Preparation andphotochemical reactivity of surfactant ruthenium(II) complexes inmonolayer assemblies and at water-solid interfaces. J Am ChemSoc 1977;99:4947–54.

51. McCafferty DG, Bishop BM, Wall CG, Hughes SG, Mecklenberg SL,Meyer TJ, et al. Synthesis of redox derivatives of lysine and theiruse in solid-phase synthesis of a light-harvesting peptide. Tetrahe-dron 1995;51:1093–106.

52. Sullivan BP, Salmon DJ, Meyer TJ. Mixed phosphine 2,2’-bipyridinecomplexes of ruthenium. Inorg Chem 1978;17:3334–41.

53. Mecklenburg SL, McCafferty DG, Schoonover JR, Peek BM, EricksonBW, Meyer TJ. Spectroscopic study of electron transfer in atrifunctional lysine with anthraquinone as the electron acceptor.Inorg Chem 1994;33:2974–83.

54. Sjodin M, Ghanem R, Polivka T, Pan J, Styring S, Sun L, et al. Tuningproton coupled electron transfer from tyrosine: a competition be-tween concerted and step-wise mechanisms. Phys Chem Chem Phys2004;6:4851–8.

55. Connors KA. Binding constants: the measurement of molecular com-plex stabilit. New York: Wiley, 1987.

56. Lakowicz JR. Quenching of fluorescence. In: Principles of fluorescencespectroscopy. New York: Springer, 2006:277–330.

57. Li C, Hoffman MZ, Pizzocaro C, Maihot G, Bolte M. Ground-stateinteractions between ruthenium(II)�diimine complexes andphenol and monochlorophenols in aqueous solution. InorgChem 1998;37:3078–82.

58. Li C, Hoffman MZ, Pizzocaro C, Mailhot G, Bolte M. Interactions be-tween the excited states of ruthenium(II)�diimine complexes andphenols in aqueous solution. J Phys Chem A 1998;102:7370–4.

59. Cang L, Sun H, Hoffman MZ. Ground- and excited-state interactionsbetween the tris(2,2′-bipyridine)ruthenium(2+) ion and phenol inaqueous solution. J Photochem Photobiol A 1997;108:129–33.

60. Marcus RA. Electron transfer reactions in chemistry: theory and ex-periment (Nobel lecture). Angew Chem Int Ed 1993;32:1111–21.

61. Rehm D, Weller A. Kinetics of fluorescence quenching by electronand H-atom transfer. Israel J Chem 1970;8:259–71.

62. Rehm D, Weller A. Kinetik und Mechanismus der Elektronübertragungbei der Fluoreszenzlöschung in Acetonitril. Ber Bunsen Phys Chem1969;73:834–9.

63. Kavarnos GJ, Turro NJ. Photosensitization by reversible electrontransfer: theories, experimental evidence, and examples. Chem Rev1986;86:401–49.

64. Smolunchouski MZ. Versuch einer mathematischen Theorie derKoagulationskinetik kolloider Lösungen. Phys Chem 1917;92:129–68.

65. Fuoss RM. Ionic association. III. The equilibrium between ion pairsand free ions. J Am Chem Soc 1958;80:5059–61.

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Electron transfer reactions of ruthenium(II)-bipyridine complexes carrying tyrosine moiety with quinones