Excited states relaxation in covalently linked dyads and triads based on tryptophan, deuteroporphyrin and naphthoquinone Текст научной статьи по специальности «Физика»

Порфирины

Porphyrins

Макрогэтэроцмклы

Статья

Paper

http://macroheterocycles.isuct.ru

DOI: 10.6060/mhc181224z

Excited States Relaxation in Covalently Linked Dyads and Triads Based on Tryptophan, Deuteroporphyrin and Naphthoquinone

Eduard I. Zenkevich,a@ Ekaterina A. Larkina,b Nadezhda V. Konovalova,b and Alexander P. Stupakc

aNational Technical University of Belarus, 220013 Minsk, Belarus

hMIREA - Russian Technological University, M.V. Lomonosov Institute of Fine Chemical Technologies, 119571 Moscow, Russia

cB.I. Stepanov Institute of Physics NAS B, 220072 Minsk, Belarus @Corresponding author E-mail: zenkev@tut.by

Steady-state and time-resolved spectral-fluorescent characteristics have been measured for covalently linked dyads and triads consisting of deuteroporphyrin IX being attached via b-positions either to naphthoquinone or to one or two tryptophan residues in solutions of various polarity at 293 K. For the tryptophan-porphyrin dyad it was shown that experimental (FETexper=0.75) and theoretical (FETtheor=0.87) values of the energy transfer efficiency are in a reasonable agreement and the Foerster theory of inductive resonance is still applicable to weakly interacting donor-acceptor systems at intercenter distances RDA& 19+25 A. For the porphyrin-quinone dyad and tryptophan-porphyrin-quinone triad in dimethylformamide at 293 K, it was argued that the porphyrin fluorescence quenching may be appropriately described by the semi-classical Marcus theory as an endergonic or moderately exergonic non-adiabatic photoinduced electron transfer occurring within the "normal" region with the rate constant kpET=2.7-108s-1. The quantitative experimental and theoretical analysis of both energy and photoinduced electron transfer processes for the systems under study leads to the conclusion that the formation of folded conformations is hardly realized for the dyads and triads in liquid solvents at ambient temperature.

Keywords: Deuteroporphyrin, tryptophan, quinone, covalently linked dyads and triads, non-radiative deactivation of singlet excited states, Foerster resonance energy transfer, photoinduced electron transfer.

Релаксация возбужденных состояний в ковалентно связанных диадах и триадах на основе триптофана, дейтеропорфирина и хинона

Э. И. Зенькевич,^ Е. А. Ларкинаь Н. В. Коновалова^ А. П. Ступав

aБелорусский национальный технический университет, 220013 Минск, Беларусь

ЬМИРЭА - Российский технологический университет, Институт тонких химических технологий

им. М.В. Ломоносова, 119571 Москва, Россия

cИнститут физики им. Б.И. Степанова НАН Б, 220072 Минск, Беларусь @E-mail: zenkev@tut.by

Для диад и триад, состоящих из дейтеропорфирина IX и хинона или одной либо двух молекул триптофана, ковалентно присоединенных по остаткам пропионовой кислоты в ß-положениях порфирина, выполнены измерения стационарных и время-разрешенных спектрально-флуоресцентных характеристик в растворах различной полярности при 295 К. Для диад триптофан-порфирин было показано, что экспериментальные (ФпЭэкспер=0.75) и теоретические (ФПЭтеор=0.87) значения эффективности переноса энергии находятся в разумном соответствии, и теория индуктивного резонанса Ферстера применима для слабо взаимодействующих донорно-акцепторных систем на расстояниях R&19+25 Ä. Для диады порфирин-хинон и триады триптофан-

МЛ

порфирин-хинон в диметилформамиде при 293 К обосновано, что тушение флуоресценции порфирина может

быть адекватно описано полуклассической теорией Маркуса как эндотермический или слабо экзотермический неадиабатический фотоиндуцированный перенос электрона, происходящий в «нормальной» области с вероятностью k0^3=2.7-108 с-1. На основании количественного экспериментального и теоретического анализа процессов переноса энергии и фотоиндуцированного переноса электрона обосновано, что формирование свернутых конформаций диад и триад маловероятно в жидких растворителях при комнатной температуре.

Ключевые слова: Дейтеропорфирин, триптофан, хинон, ковалентно связанные диады и триады, безызлучательная дезактивация синглетных возбужденных состояний, ферстеровский резонансный перенос энергии, фотоиндуцированный перенос электрона.

Introduction

At the moment, on the basis of a combination of X-ray measurements together with steady-state, time-resolved and single molecule spectroscopy data it is well documented^"6, and ref- herein] that photosynthesis is one of the finest piece of nanoscale molecular machinery where Nature utilizes the self-assembly principles to form multicom-ponent arrays of tetrapyrrole molecules and other organic substances for the directed fast and efficient energy transfer (ET) among light-harvesting pigment-protein antenna complexes to the photochemical reaction center where the energy of excited states is converted into a stable transmembrane charge separation through a sequence of photoinduced electron transfer (PET) reactions. In fact, the most complex and spectacular sets of tetrapyrrole containing self-organized arrays are found in photosynthetic objects. The elucidation of the mechanisms and dynamics of ET processes in light-harvesting antenna complexes as well as the intrinsic features of PET (such as charge separation and charge recombination of the product ion pair state) in vivo, are still the most fundamental and important problems. In fact, some aspects of the light collection and distant electron transfer reactions remain still non-understood yet in great detail from both experimental and theoretical background: i) the role of pigment-protein interactions and electronic couplings via bridge in the directed ET and PET processes, ii) electronic couplings and optimized energy transfer in confined molecular assemblies, iii) the relatively weak temperature dependence and high efficiency of charge separation, etc.

In this respect, the formation and study of artificial multiporphyrin/multichlorophyll assemblies and/or nano-structures containing tetrapyrrolic compounds and other functional organic/inorganic components are of fundamental importance as models for mimicking and the detailed study of ET and PET processes taking place within in vivo objects.[7-15, and ref- herein] The covalent linkage between supposedly essential components is considered to be one way of the supramolecular chemistry which provides a vast range of diverse supramolecular systems. Covalently linked multichromophoric systems possess favorable characteristics for light harvesting and/or charge separation.

On the other hand, the bottom-up construction of supramolecular nanodevices including organic and inorganic subunits offers a formidable challenge on the road towards modern nanotechnology.[16-20] This field is a new frontier of research that combines the building blocks of life and synthetic structures, both of them at a tiny, molecular-

sized level. Its focus is on the development of powerful techniques and methods that merge the strengths of nanotechnol-ogy, working typically in the range of 1 to 100 nanometers, and biophysics, to generate a new type of 'bionanomaterial' which has some uniquely designed properties. In this respect, the interest in emerging nanostructures (including those based on tetrapyrrolic macrocycles) is growing exponentially since they are not only good models for the mimicking the primary photoevents in vivo but seems to be considered as promising building blocks for advanced multifunctional nanocomposites with potential applications in various fields of material science and nanobiomedicine.[2122]

With these ideas in mind, on the first step we have prepared covalently linked organic dyads on the basis of deu-teroporphyrin attached via b-positions to naphthoquinone or to one or two tryptophane residues. The detailed analysis of the structure and energy relaxation processes in these complexes have been used on the next step upon study regularities and mechanisms of the non-radiative deactiva-tion of excited singlet states for tryptophane and porphyrin subunits in covalently linked tryptophane-porphyrin-qui-none triad complex. Presumably the quantitative study of the non-radiative energy transfer and photoinduced electron transfer processes was mainly carried out for the given dyads and triad with known composition and morphology. The choice of deuteroporphyrin IX for the formation of dyads and triad is caused by the fact that the existence of two carboxylic groups permits to covalently attach two other subunits possessing variable donor or acceptor properties with respect to energy/electron transfer. In addition, the existence of propionic acid residues in deuteroporphyrin IX molecule gives the possibility to form conformations of the multicomponent complexes in which the intercenter distances between interacting moieties seem to be enough for appropriate energetic interactions. Amino acid component, tryptophan, was used as a potential donor of the energy or electron. In addition, it is known that amino acid residues in reaction centers in vivo may stabilize the charge transfer state in the energy scale,[23,24] and the existence of the dipole moment in tryptophan molecule may promotes the effective charge transfer.[2526] It is well documented also that the fast and effective transformation of the electronic excitation energy into the energy of charge separated states in reaction centers in vivo is realized with participation of quinone molecules.[27-29] Correspondingly, like in the most artificial multimolecular systems modelling the primary photosyn-thetic events[eg- 30-37] we have used quinone molecule also.

Finally, we would like to mention that this contribution is dedicated to the 85th anniversary of the world-known

%

expert in photophysics and photochemistry of chlorophyll and related compounds academician G.P. Gurinovich (born in 1933), who was a real leader in this field, being an initiator and participant of a lot of pioneering and fruitful experimental investigations of spectral and energetic properties of tetrapyrrolic pigments in molecular state as well as in structurally organized complexes of various composition and morphology. Within few decades his book «Spectroscopy of Chlorophyll and Related Compounds»[38] was a real textbook for beginners, PhD students and other scientists working in this interesting and promising area of science.

Experimental

Materials

Covalently linked dyads and triads. Basic compound 2,7,12,18-tetramethyl-13,17-bis(2-methoxycarbonylethyl)porphine (deuteroporphyrin IX, Dp) has been obtained from haemin by method described earlier.[39] The synthesis of dyad containing naphthoquinone (Q) and deuteroporphyrin IX (1,3,5,8-tetra-methyl-6(7)-{2-[2-(3-methyl-1,4-naphthoquinon-2-yl)thioethyl] oxycarbonylethyl}-7(6)-(2-carboxyethyl)porphyrin) has been carried using method described in.[40] The synthesis of tryptophan (Trp)-containing derivatives of deuteroporphyrin IX and triad containing molecules of Dp, Q and Trp has been carried using method described in.[41,42] The structures of dyads and triads have been supported by UV-VIS, IR and NMR spectroscopy and mass spectrometry.[40,42] Chemical structures of Dp, Trp and Q molecules as well covalently linked dyads and triads are presented in Figure 1.

For further analysis of experimental results on ET/PET rate constants the optimized geometries have been calculated for

Vnh n=/ y

Vn J \

— '—

NH N=

HN-

H3COOC COOCH3 COR-, COR2 Dp Dp-Q: R1 = Q, R2 = OH

Dp-Trp: R1 = Trp, R2 = OH Trp-Dp-Trp: R1 = R2 = Trp Trp-Dp-Q: R1 = Trp, R2 = Q O

Trp = -NH

Figure 1. Chemical structures of dimethyl ester of deuteroporphyrin IX (Dp), tryptophan (Trp), quinone (Q) as well as dyads and triads under investigation.

some dyads and triad (Figure 2). It was found (using HyperChem 7.0 Pro, semiempirical methods AMI or PM3) that two possible conformations may be realized: unfolded and folded (more optimized) (see Figure 2A and 2B, correspondingly). For the dyad Dp-Q, estimated intercenter distance is 19 A (case A) and 4 A (case B). Optimized geometry for triad Trp-Dp-Q has been calculated using Autodesk HyperChem (versions 2.0 and 3.0, MM+ method) (Figure 2C, D). Because of flexibility of the covalent spacer the triad geometry is determined by the rotation of its fragments. At the beginning the calculation of the geometry with the minimal energy has been carried out by a sequential changing of pair of torsion angles (from 0 to 350°, 10 ° iteration, optimization by Newton-Rafson method with gradient 0.01 kcal/(A-mol)). Final optimization has been done by Fleatcher-Rives method with gradient 0.01 kcal/(A-mol). The whole energy of the optimized geometry for the triad Trp-Dp-Q was estimated to be 86.73 kcal/ mol. In this case, the quinone subunit plane is practically parallel to the porphyrin plane with interplane distance of 3.23-3.96 A, while the angle between the tryptophan and the porphyrin planes is ~ 45-50° with estimated distance 3.10-3.28 A (Figure 2C). Calculations show also that from energetic point of view another geometry for the triad Trp-Dp-Q may be realized where both Q and Trp subunits are located together with respect to Dp macrocycle plane (Figure 2D).

Nevertheless, the flexibility of a covalent spacer may lead to the existence of few other conformations for the triad in which the indole ring may be moved away from the porphyrin subunit. Such fast transitions between conformations in liquid solutions at ambient temperature (compared to a time-scale of NMR measurements) manifest themselves in the broadening of proton peaks for tryptophan indole ring in NMR 1H spectra and the absence of registered proton signals for C51 and N atoms of tryptophan indole ring. However, the addition of 5 vol.% trifluoroacetic acid to solutions of compounds Dp-Trp and Trp-Dp-Trp in CDCl3 or introduction of a Zn atom into the porphyrin macrocycle restrict the conformational mobility of the complexes which manifests itself in the appearance of two signals due to protons at the C51 and N atoms in the 1H NMR spectra. The detailed analysis of NMR data for the systems under study is presented in.[42] In addition, some structural properties of the dyad and triad were confirmed also on the basis of IR- and mass-spectrometry measurements.

Figure 2. Optimized unfolded (A, D) and folded (B, C) geometries for the dyad Dp-Q (A, B) and for the triad Trp -Dp-Q (C, D).

Solvents

Solvents of various polarity (Aldrich, spectroscopic grade) such as methylcyclohexane, chloroform, toluene, tetrahydrofurane and dimethylformamide have been used at ambient temperature without further purification. Spectral steady-state and time-resolved measurements have been carried out in quartz optical cuvettes (Hellma QS 27 111, path length 1 cm). Optical density of solutions was 0D<0.15 in order to avoid reabsorption effects. Experiments have been completed during 1-2 h after sample preparation.

Spectral and Time-resolved Measurements

Absorption spectra were recorded with a Shimadzu 3001 UV/Vis or a Cary-500 M Varian spectrophotometer. Emission spectra were measured using spectrofluorophotometer SFL 1211A (Solar) as well as a home-built high-sensitive temperature variable laboratory set-up described earlier.[43] The fluorescence quantum yields 9f of the systems under investigation were measured

by the relative method,[44] tetraphenylporphyrin in non-degassed toluene (9f=0.09 at 293 K[45]) was used as a standard.

Time-resolved photoluminescence (PL) measurements on ensembles were performed in a time-correlated single photon counting mode under right-angle geometry using a laboratory pulse fluorometer PRA-3000 equipped with computer module TCC900 (Edinburg Instruments) and light emitting diodes PLS-8-2-130 (X =457 nm, FWHM ~ 713 ps) or PLS-8-2-135 (X =409 nm,

v max ' r ' v max

FWHM ~ 990 ps; PicoQuant GmbH). In most cases, repetition rate was 2.5 MHz, average power range was ~30 mW, the duration of kinetic measurements in every experiment have been adjusted to 10000 counts at decay curve maximum. In some cases multi-exponential decay curves A(t) were fitted by few components A. according to A(t)=ZAiexp(-t/T.). A commercial software program was used for decay analysis with the minimisation of chi-square values x2.

Scheme 1 shows the relative position of excited states in the energy scale as well as main deactivation processes in the systems under study.

Scheme 1. Diagram of excited states and main relaxation processes in dyads Trp -Dp and Dp-Q. Rate constants of the main channels are as follows: absorption (A), fluorescence (f), non-radiative recombination of radical ion pair (k).

3 1,0

n 0

P 0,6

300

400 500

X, nm

600

600

650 700 750

X, nm

Figure 3. Absorption (1A) and fluorescence (2A, 3B) spectra of Trp (2) and Dp (1, 3) in toluene at ambient temperature (2A: 1exc=240 nm; 3B: l =410 nm ).

exc '

Results and Discussion

Spectral-kinetic Properties of Precursors, Dyads and Triads

It was found that absorption spectra of the triad Trp-Dp-Trp and dyad Trp-Dp are a linear combination of the corresponding spectra of monomeric precursors Trp and Dp without differences in wavelength maxima and band shapes (Figures. 3 and 4A). It means that the interaction between the two subunits is weak in the ground state, and they retain their individual identities.

At the same time, fluorescence spectra of the triad Trp-Dp-Trp and dyad Trp-Dp do show strong quenching of the Trp fluorescence (1max=330 nm) upon excitation at 1exc=270 nm (Trp absorption band). In all cases the fluorescence spectra of the complexes mainly consist of Dp bands. Namely, in the dyad Trp-Dp the Trp fluorescence is absent practically (full quenching), while at low excitation level for the triad Trp-Dp-Trp, this band remains still visible but its intensity is quenched by >10 times with respect to that for the individual Trp at the same molar concentration. It is seen from Table 1 that the energetic interaction between Trp and Dp subunits in covalently linked complexes Trp-Dp-Trp and Trp-Dp manifesting in the strong quenching of Trp excited singlet state do not lead to the quenching of Dp excited singlet state (Table 1).

Data presented in Table 1 show that in toluene for alone Dp fluorescence lifetime ts is smaller than that mea-

sured in dimethylformamide. This difference is explained by two reasons. In toluene, the concentration of dissolved molecular oxygen [O2] is higher and viscosity is smaller with respect to these values for dimethylformamide.[46] Thus, the quenching of Dp S1 state by molecular oxygen is higher in toluene solutions compared to dimethylfor-mamide. Our measurements have shown that in degassed solutions ts0=18.1 ns for Dp. Based on these results one may conclude that fluorescence parameters of Dp in the triad Trp-Dp-Trp and dyad Trp-Dp do not change practically with respect to those for individual Dp molecules what is typical for acceptor molecules upon weak interaction with donor ones.[1011,47"49] Energetic interactions between Trp and Dp in the dyad Trp-Dp manifest themselves in fluorescence spectra of the complex: upon excitation of the dyad at 1exc=270 nm (Trp absorption band) Dp fluorescence intensity is stronger by 2 times compared to that for the individual Dp at the same molar concentration. Finally, it is seen from Figure 4B that fluorescence excitation spectra of the triad and dyad detected at Dp fluorescence band (1de>640 nm) in tetrahydrofurane at 295 K clearly show the existence of absorption bands of Trp component in the region of 250-300 nm.

In the case of the triad Trp-Dp-Trp and dyad Trp-Dp, it seems reasonable to explain all the observed experimental findings as the manifestation of the inductive resonance energy transfer Trp^Dp with participation of excited singlet states of donor (D) and acceptor (A) molecules (S-S ET).[101147-49] With respect to the given complexes,

Table 1. Fluorescence parameters for individual Dp, dyads and triad in solvents of various polarity at 295 K.

Solvent Compound Fluorescence quantum yield q>F , % Fluorescence decay t, ns

Dp 7.8 12.1

Dp-Trp 8 12.3

Toluene

Dp-Q 3 9.3

Trp-Dp-Q 5 8.7

Dp 7.3 15.4

Dimethylformamide Dp-Q 2 11.8 / 3.6

Trp-Dp-Q 2.5 12.7 / 5.4

1 Dp

2 Trp-Dp

3 Trp-Dp-Trp

250 300 350

400 450 500 X, nm

0,8 -

550 600 650

250 300 350

400 450 X, nm

500 550 600

Figure 4. Absorption (A) and fluorescence excitation (1det=640 nm) (B) spectra of monomeric Dp (1), the dyad Trp-Dp (2) and the triad Trp -Dp-Trp (3) in tetrahydrofurane at 295 K.

the corresponding detailed analysis of these processes will be presented below.

Now let us consider properties of the dyad Dp-Q and triad Trp-Dp-Q containing electron accepting quinone subunit. Basic arguments showing that in these complexes the interaction between Dp and Q takes place with participation of the Dp excited singlet states are evident from fluorescence decay measurements and ps/ns pump-probe experiments (see Table 1 and Figure 5).

Compared to individual Dp molecules, in the dyad Dp-Q and triad Trp-Dp-Q the fluorescence of the porphyrin subunit is noticeably quenched manifesting in the decrease of the fluorescence quantum efficiency 9 and decay t shortening (Table 1, Figure 5A). In fact, these effects are typical for porphyrin-quinone systems of various morphology where the photoinduced electron transfer (PET) processes porphyrin-quinone are more or less effective depending on the system geometry, flexibility and D-A distances.[30-37] It is also seen from data presented in Table 1 that in toluene at ambient temperature,

quenching effects are practically the same for both Dp-Q and Trp-Dp-Q complexes. On the other hand, in polar dimethylformamide Dp fluorescence quenching becomes more pronounced and, additionally, Dp emission decay becomes non-exponential. In addition, transient absorption spectra of Dp-Q show a noticeable spectral dynamics (Figure 5B). The rising absorption near 650-670 nm may be ascribed to Dp+ species by referring to the corresponding spectra obtained by electrochemical oxidation of a porphyrin free base.[50,51] It should be mentioned also that relative quantum yields of Dp fluorescence in dyad (9dyad/90) and triad (<trmd/<0) with respect to that for individual Dp (<0) are weakly dependent on the solvent nature being slightly higher for triad in comparison with dyad: <dyad/<0=0.38, 0.4, 0.4, 0.28 and <trmd/<0=0.64, 0.60, 0.55, 0.45 in toluene, chloroform, methylcyclohexane and dimethylformamide, correspondingly. This variation in relative quantum yields values may reflect different conformational mobility of subunits and steric interactions in the triad and dyad which may also be dependent

1600 -■f 1400 -

> 1000

800 -600 400 200 -

10 12 14 16 18 Time, ns

450 500 550 600 650 700 750 X, nm

£ 1200

0

Figure 5. Fluorescence decays (A, Xdet=640 nm) detected for Dp (1) and the dyad Dp-Q (2) and time-resolved absorption spectra (B, 1pump=540 nm) of the dyad Dp-Q at delay times 0, 2 and 7 ns in dimethylformamide at 295 K. IRF in (A) corresponds to the experimental response function. Details on pump-probe measurements and home-made experimental setup were described earlier in.[37]

on the solvent polarity. Main details of PET in the systems under study will be discussed later on.

Quantitative Analysis of the Non-radiative Energy Transfer

It was concluded above that the observed experimental findings for the dyad Trp-Dp and triad Trp-Dp-Trp may be connected with the realization of the non-radiative inductive resonance energy transfer Trp^Dp via excited singlet states of D (Trp) and A (Dp) molecules. Correspondingly, using theoretical considerations discussed in[101147-49] one could carry out a quantitative analysis of S-S ET processes for the systems under study.

Currently, because of lack of light emitting diodes in 250-300 nm UV range we have not succeeded to collect time-resolved data for fluorescence decay of Trp alone and in the complexes. But it is possible to estimate S-S ET efficiencies in the dyad via the sensibilization of the Dp emission (fluorescence enhancement) using fluorescence excitation and absorption data and approach described in.[5253] In this case, experimental efficiencies (®ET) of Dp fluorescence enhancement caused by S-S ET have been calculated from the direct measurements of the corresponding intensities (I) in fluorescence excitation spectra and optical densities (OD) in absorption spectra of the dyad Trp-Dp using the equation

® ET =

I-iad (X, )- I Dp (X, )

IDp (X 2 )

ODdiad (X,)- ODDp (X,)

ODDp (X2 )

Here, Idyad corresponds to the Dp fluorescence intensity in the dyad Trp-Dp, whereas I is the fluorescence intensity of the individual Dp at the same molar ratio, and 11=280 nm, 12=398 nm. Based on experimental data it has been estimated that S-S ET efficiencies are as follows: F-T=0.75 for the dyad Trp-Dp and F-T=0.65 for the triad Trp-D p-Trp.

In its turn, based on these data one can estimate the mean donor-acceptor distance RDA using the well-known expression for pair transfer:[47-49]

where R0 is the critical transfer distance at which the whole deactivation rate constant of S1 state of the D molecule is equal to the ET rate constant;

R6 =

9000 • /»10 • k2 128n5 • n4N.

•V°d J fD (VK (v)

, (3)

j = jId (v)Sa (v)4 is spectral overlap integral,

o v

fD(v) is the D fluorescence spectrum in wave number scale and normalized to 1 by square, eA(v) is the A absorption spectrum measured in M"1cm"1, NA is Avogadro number. The meanings of other parameters are presented in notes for Table 2 collected all calculated parameters for S-S ET in the dyad Trp-Dp.

It follows from data presented in Table 2 that for the dyad Trp-Dp experimental and theoretical values of ET efficiency are in a reasonable agreement (FETexper=0.75 and FET'heor=0.87). It indicates that the Foerster theory of inductive resonance is still applicable to weakly interacting porphyrin and tryptophan n-conjugated systems. Nevertheless, intercenter D-A distances RDAexper (estimated from ET parameters) are relatively high compared to the corresponding values evaluated from the optimized geometries (see Figure 2). This difference may be explained by the overestimation of the orientational factor . (1) k2 values (and thus, R0theor critical distances) for the dyad Trp-Dp. In reality, Trp fluorescence band overlaps with few electronic transitions (forming Soret band in absorption spectra of tetrapyrroles[101315'3739]) being differently oriented with respect to tetrapyrrole macrocycle. There -fore, the direct calculation of the orientational factor k2 seems to be very complicated problem. In addition, a high flexibility of a covalent spacer -CH2-CH2-COO- followed by a rotation of D and A molecular subunits (depending on the solvent nature and properties) may also lead to a strong variation of a mutual displacement of interacting dipoles. But in any case, from the obtained results it is evidently clear that folded geometries of A and C types (Figure 2) for the dyad Trp-Dp and triad Trp-Dp-Trp are thought to be (2) low probable in various liquid solvents.

0

Table 2. Energy transfer parameters for dyad Trp-Dp (toluene, 295 K, refractive index n=1.4968).

< e/v;,b M"1-cm-1 J(v), cm3'M-1 k2 c R^"', A R exper d A DA ' F theor e -T

0.2a 17.5-104 12.4-10"14 0.42 4- 0.70 34.0438.2 25427 0.87

Notes: "quantum yield of Trp fluorescence was taken from;[54,55] bdecimal molar extinction coefficient for Dp in the maximum of Soret band; corientational factors were calculated on the basis of an optimized geometries for the dyad and the inductive-resonant theory[47-49] as k2=[cos(^, _ - 3 cos(^, O'cosK, rDA)]2=0.47^0.75, (4)

where (^D, ^A) is the angle between the transition dipole moments of the D and A subunits, (^D, rDA) and (^A, rDA) denote the angles between the dipole vectors of D and A and the direction vector between D and A, respectively; ty***' values were calculated using Eq. (2) and experimentally estimated F data; 'theoretical value F^"* was calculated according to[47] as F-/-'=(k V(k-^^V1), (5)

where k„T =

ET Vn

f t) theor \6

R0

R

V ADA /

(6)

and mean value for tryptophan (D) emission decay <td0>=2.5 ns was taken from.[56]

1

Quantitative Description of Photoinduced Electron Transfer Processes to Covalently Linked Quinone

With respect to the dyad Dp-Q and triad Trp-Dp-Q, the corresponding analysis gives the following. Since the absorption spectra for alone Dp and Dp in the dyad Dp-Q and triad Trp-Dp-Q do not differ practically, we will analyze PET processes in these complexes in terms of the semi-classical Marcus theory[5758] developed for charge-transfer reactions in the "normal" region. At high temperatures, the semi-classical Marcus theory of ender-gonic or moderately exergonic non-adiabatic ET occurring within the "normal" region predicts the following expressions for the rate constant k •

ks = — .

PET -

V2

' 1 1

• exp

AG

h (4nXkBT )"2 ^ kBT (AG0 +X)2

with activation energy AG* =

4X

(7)

(8)

Here kB is Boltzman's constant, T is the temperature, h = h / 2n, h is Plank's constant, V12 is the electronic coupling term between the electronic wave functions of the reactant and product states, 1=1in+1ext is the Gibbs reorganisation energy determined by the nuclear 1in and solvent 1ext reorganisation energies, AG0 is the Gibbs free energy of the PET reaction, AG* is the Marcus Gibbs activation energy. For porphyrin macrocycles, the term, l involving vibrational energy changes between the reactant and product states was estimated to be l «0.3 eV.[5960]

in

The solvent-dependent term l „ (l , ) or for

A ext v solv'

the surrounding medium treated as a dielectric continuum, is expressed as:[57-60]

^ solv

4 nen

1 1 1

-+-+ —

2rD 2rA rDA

1 1

(9)

where e =n2 is the optical dielectric constant, n is the refrac-

op 1 7

tion index and e . is the static dielectric constant of the sol-

vent (n=1.49693, e =2.38 for toluene; n=1.43047, e =36.7 for

v ' st ' ' st

dimethylformamide); rD=5 A (for porphyrin macrocycle), rA=3.3 A (for quinone);[1037] rDA is an intercenter Dp-Q distance in the dyad Dp-Q and triad Trp-Dp-Q. These values have been used for the calculation of PET parameters listed in Table 3.

According to Marcus theory,[5758] adiabatic PET in a "normal" region becomes possible if the Gibbs free energy of the process AG0<0. With respect to our complexes, Gibbs free energy of PET reaction may be calculated according to[61]

AG0 = E(CT) - E(S^) = e(EDOX - EARED) + AGS - E(S^). (10)

The oxidation potential for porphyrin (EDOX=0.63 V in dimethylformamide vs. SCE) and reduction potential for quinone EARED=-0.45 V (in dimethylformamide vs. SCE) were taken from literature.[62-64] The correction term AGS accounts for the Coulomb interaction between D and A of the radical ion pair, and was estimated to be AGS<0.21 eV.[3765] All calculated energetic parameters describing PET processes for the dyad Dp-Q are presented in Table 3, thus permitting to quantitatively describe the photoinduced electron transfer events in the systems under study.

Comparative analysis of experimental data being obtained for the dyad Dp-Q and triad Trp-Dp-Q (see Table 1) shows that the efficiencies of Dp fluorescence quenching due PET do not differ significantly for these two complexes (being a little bit smaller for the triad Trp-Dp-Q compared to the dyad Dp-Q). It may be explained by the fact that possible steric interactions between covalently linked Trp and Q subunits in the triad do not significantly change the arrangement of Q molecule with respect to a porphyrin macrocycle compared to the dyad Dp-Q. Nevertheless, it is seen from Table 1 that transition from non-polar toluene to polar dimethylformamide manifests itself for both complexes in the strengthening of Dp fluorescence quenching as well as an existence of bi-exponential emission decay. According to PET theory,[57-59] the increase of quenching effects upon the solvent polarity increase is typically explained by the stabilization

Table 3. Energies of the donor localized S1 state, E(S1), radical ion pair state, E(CT), and PET parameters for the dyad Dp-Q in dimethylformamide at ambient temperature (n=1.43047, e =36.71).

£(Sj),a eV r b  rDA, A l , ,c eV solv' 1,d eV E(CT), eV AG°,e eV AG*,f eV k g s-i PET' " V12,h meV

1.99 19 0.77 1.03 1.86 -0.13 0.197 2.7-108 0.42

Notes: Evaluation of redox potential values for Dp (EDOX) and Q (EARED) as well as D and A radii (rD and rA) is described in the text with the corresponding references.

aThe energy level of Dp locally excited S1 state was determined on the basis of the corresponding fluorescence and absorption Q(0,0) bands. bIntercenter distances rDA were estimated on the basis of Draiding structural models and molecular modeling taking into account possible steric interactions and are in the range ~ 19 A. cThe solvent-dependent term l lv was estimated using Eq. (9).

dThe Gibbs reorganization energy was estimated to be 1=1 +1 » 1.03, where l was taken to ~ 0.3 eV.[59,60] eThe Gibbs free energy of the PET reaction AG0 was calculated using Eq. (10). The activation energy AGS was estimated according to Eq. (8).

Calculations of experimental rate constants, kPET for PET with participation of Sj states of the donor molecule (Dp) were done according to well-known expression:

kpET= 1/T - 1/1», (11)

where t0 and t are fluorescence decays of unquenched and quenched Dp, correspondingly; taking into account two-exponential decay of Dp emission in the dyad, kPET was found for the shorter component t1=3.6 ns of Dp fluorescence decay in the dyad (see Table 1). hThe electronic coupling term was calculated on the basis of Eq. (7).

2

of the energy of the radical ion pair state, E(CT). In its turn, we apt to believe that non-exponential emission decay for Dp in this case may reflect some changes of conformational mobility of the complexes when going to dimethylfor-mamide. Correspondingly, Table 3 collects the estimated PET parameters upon taking into account experimental data for the shorter component of Dp emission decay in the dyad.

Thus, assuming realistic errors for l and AG0 estimations one may conclude that for the dyad Dp-Q in dimeth-ylformamide at 293 K, the Dp fluorescence quenching is appropriately described by Marcus theory of PET in a "normal" region (i.e. -AG0<1). In addition, as far as the electronic coupling term V12 is smaller than kT=25.7 meV at room temperature, the pEt reaction is non-adiabatic in this case. It was mentioned above that steric interactions between covalently linked Trp and Q subunits in the triad Trp-Dp-Q do not significantly change the arrangement of Q molecule with respect to a porphyrin macrocycle compared to the dyad Dp-Q. Thus, the main peculiarities of PET reaction in dimethylformamide for the triad seem to be the same. It is known also[57-60] that the medium between D and A strongly influences the rate constant of PET process (through solvent coupling). Correspondingly, when going from polar dimethylformamide to the non-polar toluene, PET efficiency and rate constant decrease significantly and Dp fluorescence quenching is not so pronounced (see Table 1).

Finally, we like to address the question why are PET processes in the dyad Dp-Q less pronounced compared to other D-A complexes containing porphyrins and electron acceptors. For instance, in benzene at 293 K, for covalently linked ZnP-Q complexes with smaller D-A distance rDA=13 A (compared to our case) PET is essentially stronger: kpET=(6.0 -9.5)-1010 s-1 (AG0=-0.46+ -0.39 eV).[66] On the other hand, for the Q-substituted dimer (ZnOEP)2Ph-Q having the same rDA distance and similar Gibbs free energy AG0, in toluene at 293 K the PET rate constant kET=2.86-1010 s-1 [1137] is smaller as compared to the above complex with monomeric porphyrin ZnP-Q. This may be explained by taking into account the competition between the non-radiative S-S energy transfer among monomeric subunits in the dimer (ZnOEP)2Ph and charge separation.[3537] According to experimental findings and theoretical estimations[11,37] in Zn-porphyrin chemical dimers with intercenter distances of d«11 - 13 rate constants of the non-radiative S-S energy migration are close to kET«(3-7)-1010 s-1. Correspondingly, as far as for the Q-substituted dimer (ZnOEP)2Ph-Q kEM<kET, a slower energy transfer process limits the fast PET leading to the relative decrease of the experimental kpET values in the dimers[11,37] with respect to those found for Q-substituted monomers.[66]

Thus, the above comparison and considerations allow us to do some additional conclusions concerning the realization of PET events in the dyad Dp-Q and triad Trp-Dp-Q. Low PET efficiency in these systems compared to ZnP-Q complexes[66] or Q-substituted dimer (ZnOEP)2Ph-Q[1137] are explained mainly by larger D-A distances in our case. Moreover, our experimental low kpET values show again that the formation of folded geometries may be excluded

for the dyad Trp-Dp and triad Trp-Dp-Q in dimethylfor-mamide and toluene at ambient temperature. In addition, high flexibility of a covalent spacer -CH2-CH2-COO- followed by a rotation of interacting electron D and A moieties excludes practically the realization of through-bond cou-pling[59,65] which may strengthen PET efficiency.

Conclusions

From the basic point of view, upon study of properties and possible functionalities of artificial multicomponent organic complexes the basic task seems to be the analysis of spectral-structural correlations as well the mechanisms of interchromophoric interaction depending on the morphology of the given nanostructures.

In this contribution, on the basis steady-state and time-resolved spectral-fluorescent measurements carried out in solutions of various polarity at 295 K for covalently linked dyads and triads (consisting of deuteroporphyrin being attached via b-positions to naphthoquinone or to one or two tryptophan residues), the comparative analysis of regularities and mechanisms of the non-radiative deacti-vation of excited singlet states for tryptophan and porphyrin counterparts has been carried out (including energy transfer and photoinduced electron transfer), and the main parameters determining the efficiency of the processes under consideration have been estimated.

In the case of the dyad Trp-Dp experimental and theoretical values of ET efficiency are in a reasonable agreement. It indicates that the Foerster theory of inductive resonance is still applicable to weakly interacting porphyrin and tryptophan n-conjugated systems at intercenter distances RDA«19+25 A. The application of Foerster theory relies on the approximation that the distance RDA between interacting D and A dipoles is larger than the length |l| of the transition dipoles themselves. The necessary estimations may be derived using well-known expressions[67] for oscillator strength f and transition dipole moment ||| of the corresponding low-energy electronic transitions of interacting porphyrin and tryptophan molecules:

f = 4.33x10-9(v)Avl

mi

A, f = (8n2 me v||2 )/3he2

(12)

(13)

where e (v) is the molar decimal extinction coefficient at

maxv ^

the maximum of the absorption band and Àv1/2 the corresponding spectral width. Making use of the experimental data known for porphyrins and tryptophan related compounds (having sizes of ~10 A) we obtain that the effective length of the transition dipoles |l|<1-2.0 A for these n-conjugated systems. Consequently, |l| << RDA, and it means that in this case the point dipole-dipole approximation is still valid. It should be mentioned in this respect, that the same principal conclusion concerning the application of the weak coupling inductive-resonant model has been done in our early publications for porphyrin chemical dimers[68,69] as well as for self-assembled multiporphyrin complexes.[11,70]

We have shown that for the dyad Dp-Q in dimethylformamide at 293 K the Dp fluorescence quenching is due the photoinduced electron transfer Dp^quinone. In the triad Trp-Dp-Q, steric interactions between covalently linked Trp and Q subunits do not significantly change the arrangement of Q residues with respect to a porphyrin macrocycle compared to the dyad Dp-Q. In these complexes, the Gibbs free energy of PET is AG0=-0.13 eV<0, while the Gibbs reorganisation energy is estimated to be 1=1.03 eV, that is -AG0<1. Correspondingly, the photoinduced electron transfer process in the given dyad may be appropriately described by the semi-classical Marcus theory as an endergonic or moderately exergonic PET occurring within the "normal" region. Moreover, as far as the electronic coupling term V12=0.42 meV is smaller than kT=25.7 meV at room temperature, the PET reaction is non-adiabatic in this case. It is known also,[50] that PET reaction is non-adiabatic by Landau-Zener criteria if it satisfies the following relationship

4n2 V/hro (21kBT)1/2 < 1,

(14)

where ra~100 cm-1 for typical low-frequency solvent motions at 300 K. It follows from above presented data that for the dyad Dp-Q and the triad Trp-Dp-Q this criterion is operative in both solvents. Thus, assuming realistic errors for 1 and AG0 estimations one may conclude that at ambient temperature the porphyrin Sj-state quenching is due to the non-adiabatic PET. Such conclusions with respect to PET mechanisms have been done by us earlier for multiporphyrin complexes containing covalently linked quinone derivatives.[11,37] It should be mentioned also that high flexibility of a covalent spacer -CH2-CH2-COO- followed by a rotation of interacting electron D and A moieties excludes practically the realization of through-bond couplings9,6^ which may strengthen PET efficiency.

Finally, taken together, the quantitative experimental and theoretical analysis of both energy and photoinduced electron transfer processes for the systems under study leads to the conclusion that the formation of folded geometries (types B, C, see Figure 2) is hardly realized for the dyads Trp-Dp, Dp-Q and triads Trp-Dp-Trp, Trp-Dp-Q in liquid solvents at ambient temperature.

Acknowledgements. Financial support from the program BSPSR "Convergence-2020 3.03" and BRFBR Grant №>®18P-314.

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Received 10.01.2019 Accepted 29.01.2019