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Singlet oxygen photogeneration by ethanolic extract of Syzygium cumini fruits: Theoretical elucidation through excited states computations
Accepted Manuscript Research paper Singlet oxygen photogeneration by ethanolic extract of Syzygium cumini fruits: Theoretical elucidation through excited states computations Carlos Díaz-Uribe, Angela Rodriguez-Serrano, Maria López, Eduardo Schott, Amner Muñoz, Ximena Zarate PII: DOI: Reference:
S0009-2614(18)30936-9 https://doi.org/10.1016/j.cplett.2018.11.016 CPLETT 36087
To appear in:
Chemical Physics Letters
Received Date: Accepted Date:
31 October 2018 7 November 2018
Please cite this article as: C. Díaz-Uribe, A. Rodriguez-Serrano, M. López, E. Schott, A. Muñoz, X. Zarate, Singlet oxygen photogeneration by ethanolic extract of Syzygium cumini fruits: Theoretical elucidation through excited states computations, Chemical Physics Letters (2018), doi: https://doi.org/10.1016/j.cplett.2018.11.016
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Singlet oxygen photogeneration by ethanolic extract of Syzygium cumini fruits: Theoretical elucidation through excited states computations Carlos Díaz-Uribe,*a Angela Rodriguez-Serrano,b Maria López,a Eduardo Schott,c Amner Muñozd and Ximena Zarate*e a
Grupo de Fotoquímica y Fotobiología. Universidad del Atlántico. 081007 Puerto Colombia. Colombia. E-mail: carlosdí[email protected] b
Department of Computational Biochemistry, Universität Duisburg-Essen, 45117 Essen. Germany
c
Departamento de Química Inorgánica, Facultad de Química, Pontificia Universidad Católica de Chile. Chile d
e
Grupo de Investigación en Química y Biología, Universidad del Norte. Puerto Colombia. Colombia
Instituto de Ciencias Químicas Aplicadas, Facultad de Ingeniería, Universidad Autónoma de Chile. Chile. Email:[email protected]
The ethanolic extract of Syzygium cumini fruits was characterized and evaluated in the photogeneration of singlet 1 oxygen ( O2) under visible light radiation. This process was studied from a theoretical approach by the survey of the generated electronic excited states, after photoexcitation of the most abundant anthocyanin of the extract, i.e. delphinidin-3,5-diglucoside. It was determinated that the adiabatic energy of the optimized T1(πH-1→πL*) state was 1.55 eV and that the overall energy transfer releases ~0.58 eV in an exothermic process. Therefore, this state is the responsible of promoting electron transfer reactions and subsequent formation of 1O2 through illumination.
Keywords: TDDFT, singlet oxigen, anthocyanin, Syzygium cumin.
1 Introduction Reactive oxygen species (ROS) are molecules involved in a variety of chemical, biological and environmental processes.1–3 Their generation is promising in antimicrobial photodynamic therapy, as these species induce damage or degradation on the microbial membrane or proteins.4 Also, potential applications in advanced oxidation processes rely on ROS generation as these
chemical species can mineralize almost any 5 recalcitrant organic pollutant. The process of ROS generation can be carried out through chemical reactions, both in the absence and under electromagnetic radiation. For the latter (so-called photochemical pathways), in addition to the presence of light, there are molecular oxygen (O 2) and a photosensitizer.6,7 Dyes typically act as photosensitizers as these compounds absorb light and, after photoexcitation, they can subsequently
transfer their energy excess to other molecules present in their surrounding environment or undergo redox reactions. Among the most widely used synthetic photosensitizers are ionic dyes (e.g. rose bengal, methylene blue, eosin Y and rhodamine B),8,9 porphyrins and 10,11 phthalocyanines. Porphyrins and phthalocyanines are the most common sensitizers used in the fields of medicine and environmental chemistry due to their high stability and ability to 12 generate ROS. Nevertheless, the synthesis of these compounds is expensive and sometimes harmful for the humans and/or the environment. In this sense, natural sensitizers have become a more viable alternative than synthetic organic compounds due to their relatively large abundance, easy availability, low cost and because they are friendly to the environment.13 In this case, nature is the main factory of these types of compounds, such as pigments (e.g. carotenoids, flavonoids, anthocyanins, betalains), which are responsible of the different observed colors (from yellow/orange to red/purple) in some plant parts (e.g. fruits, flowers and leaves), and are produced from the secondary metabolism of certain plants. These natural pigments have been isolated and employed as sensitizers in dye-sensitized solar cells,14–16 antimicrobial photodynamic chemotherapy and for the photodegradation of 17,18 One of these organic contaminants in water. plants is Syzygium cumini (Synonymous. Eugenia jambolana L.; common names: Jambu, Java Plum, Jambolan, Jaamun), which belongs to Myrtaceae family. This plant is a perennial tree native from India and is also found distributed in other countries of Asia, Eastern Africa and South America.19 The different parts of Jambu, such as fruits, seeds, bark and leaves, have interesting uses in Ayurvedic and traditional medicines, carminative, diuretic, antidiarrheal, hypoglycemic and antibacterial, among others.20 The violet juice obtained from the fruits shows intense and broad absorption bands in the visible region of the electromagnetic spectrum (attributed to the high content of anthocyanins), which constitutes an advantage in their application not only in the design of photoelectrochemical solar cells but also 21 as sensitizers.
The aim of the herein work is to evaluate the use of an ethanolic extract from S. cumini fruits (an inexpensive and abundant natural resource at Colombian Caribbean region) as a new photosensitizer mixture for the generation (under visible light irradiation) of singlet oxygen. To get further insights on the ROS photogeneration, the electronic structures of the low-lying singlet and triplet excited states of the anthocyanins present in the extract have been explored by means of the Time-Dependent Density Functional Theory (TDDFT). Their excited states interplay after photoexcitation has been examined concentrating the attention on the production of singlet oxygen.
2 Materials and methods The procedure of extraction, qualitative and quantitative characterization of by HPLC of the anthocyanins of the vegetal material (Syzygium cumini) are described in detail in a previous report carried out by our group.22 2.1 Singlet oxygen determination Singlet oxygen was detected by means of chemical trapping based on the rubrene method described 23 by Nardello et al. A mixture of 10 mL of rubrene solution (500 ppm) with 100 µL of crude extract (50 ppm) was prepared and placed inside a batch photo-reactor with enriched-oxygen atmosphere under visible radiation (100 W OSRAM halogen immersion lamp). From the light source, the wavelengths < 500 nm were filtered and removed by using a 1.0 M potassium dichromate solution. The incident photon flow per unit volume (I o= 5.8×10-5 Einstein L-1 s-1) was determined according to chemical actinometry using a 0.0100 M Reinecke salt (K[Cr(NH 3 )2(CNS)]4 ) solution. The rubrene oxidation was monitored by visible spectrophotometry at 522 nm. 2.2 Quantum chemical calculations Density Functional Theory (DFT) in combination with its Time-Dependent approach (TDDFT) were used to analyze the electronic structure of the anthocyanins and the excited states interplay. This with the aim of elucidating the possible decay route that the dye might trigger upon photoexcitation, to finally successfully photogenerate one of the most important ROS, as singlet oxygen (1 O2). Geometry optimizations of the ground states were performed employing the Becke-3-parameter-Lee-Yang–Parr (B3LYP) 24–26 in conjunction with the 6-31+G(d,p) functional basis set.27 According to our experience this combination yields reliable geometries for the
study of the electronic properties of these dyes.28,29 The optimization of the S1 states has been carried out using TDDFT, with the same functional and basis set. The T 1 states were optimized using unrestricted DFT (UDFT) also at the same level of theory. A TDDFT calculation was performed at the optimized minima for obtaining the electronic properties and the corresponding adiabatic excitation energies. Harmonic vibrational frequencies were computed to guarantee the converged structures are minima in the corresponding potential energy surfaces. For the vertical excitations, TDDFT calculations were performed using the long-range corrected version of the B3LYP hybrid exchange-correlation functional, the Coulomb-attenuating method30 B3LYP (CAM-B3LYP). which have been reported 31,32 to provide accurate excitation energies. Solvent effects were included implicitly in all our computations using the polarizable continuum model (PCM) with a dielectric constant ε=24.55 which represents ethanol, all calculations were performed using the Gaussian09. 33,34
Figure. 1. UV-Vis spectrum of Syzygium cumini extract in ethanol (inside; three main anthocyanins found in the extract. Finally, for these anthocyanins, absorption maxima wavelengths of 534, 520 and 540 nm have been reported respectively.28
2 Results and discussions 3.1 UV-VIS Characterization of the extract Studies have shown that the fruit-pulp from Syzygium cumini contains anthocyanins, which are responsible for its bright purple color.35,36 Based on the structures, the anthocyanins have displayed maximum absorption bands ranged between 520 nm and 540 nm, which are the wavelengths commonly used by spectrophotometric assays for 28 their characterization. Figure 1 shows the UV/Vis absorption spectrum of the ethanol extract from Syzygium cumini fruit-pulp, the broadband located at visible range suggests that the extract may contain more than one type of anthocyanin, furthermore, the absorption maximum is located at 526 nm, this band can be assigned to the cinamoyl group and corresponds to the aromatic ring of the flavonoid structure, this band is characteristic for flavonoids of the anthocyanins group. In a recent report, three main anthocyanins were identified in Syzygium cumini fruit, being the delphinidin-3,5-diglucoside dye the most abundant with a relative amount of 44 % in the sample, followed by malvidin-3-5-diglucoside (28 %) and petunidin-3-5-diglucoside (9 %). (inside Figure 1, are shown the chemical structures of the three main anthocyanin).22
3.2 Determination of singlet oxygen The generation of singlet oxygen (1 O2) from the S. cumini extract was monitored through trapping reaction of the singlet species with rubrene (orange compound), which once is selectively oxidized by 1O2 , it is transformed into cycloendoperoxide derivative (colorless 37 compound). The lost in color (from orange to colorless) of rubrene in the reaction was measured by visible spectroscopy at wavelength 488 nm, and the monitoring of oxidation, in function of the irradiation time, is showed in Figure 2. A decrease in the maximum absorption band (488 nm) of rubrene spectrum was observed as the irradiation time increased, due to the formation of rubrene endoperoxide due to a [4+2]-cycloaddition mechanism.23 These results confirmed that rubrene oxidation was carried out by singlet oxygen under visible irradiation.
wavelength of delphinidine-3,5-glucoside appears at ~2.9 eV. The experimental absorption band is 28 reported at 2.32 eV and the obtained here in the ethanolic extract is 2.36 eV. This band is composed by two optically active and isoenergetic electronic states: the S2 state arising due to a πH-1 →πL* transition with a more prominent oscillator strength (f(L)=0.39) and the S1 state characterized by the πH→πL* transition with a lower oscillator strength (f(L)=0.17). a)
Figure 2. Absorption spectra in visible region (l:400600 nm) for rubrene oxidation produced by 1O2 photo-generated by irradiation, as a function time, of ethanol extract from S. cumini fruit-pulp (inside: Rubrene oxidation chemical reaction). S0
S1
3.3 Quantum chemical results
Herein, the results obtained in the framework of DFT calculations are presented. Due to the resemblance on the electronic structure of the three dyes, the present analysis of the results will focus in the delphinidine-3,5-diglucoside, which is the most abundant compound found in the extract. First, the electronic properties of the calculated ground states (S0 ) are discussed. The ground-state geometries used in this work have been selected according to previous studies, where ground state geometries, UV–vis spectra and 22,28 In those photovoltaic properties are reported. reports, the interaction of the anthocyanin dyes with the glucoside motifs are described in detail. Therefore, to get insights on the ROS photogeneration, here we focus the attention on the routes of energy dissipation after photoexcitation, we discuss possible pathways of ISC that may conduce to an efficient population of the triplet state in a qualitative manner. To aid the discussion about the production of singlet oxygen through energy transfer from the triplet states of the anthocyanins, the electronic properties computed at the adiabatic T 1 state minima are presented. Selected geometrical parameters of the computed geometries of the electronic states minima are presented in Figure 3. The corresponding frontier molecular orbitals (MOs) of delphinidine-3,5-diglucoside involved in the low-lying energy singlet and triplet states are displayed in Figure 4. The excited-state vertical excitation energies and their leading electronic configurations at the ground state geometry are shown in Table 1. The TDDFT maximum absorption
T1
b)
c)
S0
T1
S0
T1
Figure 3. Optimized ground and excited state minima of a) delphinidine-3,5-diglucoside, b) malvidin-3,5-diglucoside and c) petunidin-3,5diglucoside. The labelling of these two states was chosen for simplicity. This vertical excitation is represented as an orange arrow in the Jablonsky diagram of the delphinidine-3,5-diglucoside (see Figure 5). The S3 state corresponding to a πH-2 →πL* transition presents also a minor absorption (f(L)=0.16). The molecular orbitals corresponding to the associated
transitions are localized mainly in the anthocyanin rather than on the glycoside moiety. While the S2 and S3 states correspond to valence transitions, the S1 state shows up as a charge transfer state (CT) with the πH MO amplitudes localized in the pyrogallol part of the anthocyanin and the πL over the whole anthocyanin part. Consequently, our results indicate that this state may be responsible of promoting electron transfer reactions and subsequent formation of singlet oxygen through illumination of anthocyanins. After geometry relaxation, the system would populate an adiabatic S1 state characterized with the same electronic transition as vertically, and show an energetic stabilization by 0.31 eV respect to the vertical energy.
Figure 4. Frontier molecular orbitals (MOs) of delphinidine-3,5-diglucoside calculated at the ground state minimum at the B3LYP-D3/TZVP + PCM (ε=24.852) level of theory. This fact is in concordance with the small variations observed in the geometrical parameters computed for these states (S0 and S1, see Figure 5). In this adiabatic minimum, the excitation energy of the S2(πH-1 →πL*) state is separated by 0.23 eV from the S1 state, which indicates that this state can be thermally populated from the adiabatic S1 state. Here, the TDDFT adiabatic energies for the optimized S1 and T1 states are presented in Table 1. It is known from the experiments that a part of the singlet population undergoes intersystem crossing to the triplet states where the efficiency of this process is crucial for the production of the singlet oxygen. In the triplet manifold, vertically, three states (T1-T3) are energetically located below the S1(πH→πL*) state. If the S1 state is sufficiently longlived, it might show intersystem crossing (ISC) to
those triplet (π→π*) states. The lowest energy triplet state (T1) is characterized by a πH-1 →πL* transition and the T 2 and T3 states arise from πH→πL* and πH-2 →πL* electronic excitations, respectively. After relaxation to the minimum of the S1(πH→πL*) state, as presented in Figure 5, these excited triplet states preserve their energetic ordering as in the Franck-Condon region. The T 3(πH2→πL*) state is slightly destabilized and becomes closer in energy to the adiabatic S1(πH→πL*) state. Here, ISC processes are expected to be efficient if the singlet and triplet states involved are close in energy, their spin–orbit coupling (SOC) is reasonably strong and the density of vibrational levels is high in the accepting state. For this reason, this T3(πH-2 →πL*) state may constitute the main target for ISC from the S1 (πH→πL*) state. According to El-Sayed's rule, the SOC between π→π* states can be considered weak in the Condon approximation. Nevertheless, many reports have evidenced that the ISC processes between close lying singlet and triplet states of π→π* character can be enhanced due to vibronic SOC in the context of the Herzberg-Teller approximation.38 After the system undergo efficient ISC to the triplet state, a fast internal conversion (IC) process will lead to the population of the adiabatic T 1(πH-1 →πL*) state, see Figure 5. This process is accompanied by smooth changes in the molecular geometry and an energy stabilization of 0.28 eV (for delphinidine-3,5diglucoside) with respect to the corresponding vertical energy. Table 1. Vertical excitation energies [eV] of the low-lying energy singlet and triplet states of delphinidine-3,5-diglucoside calculated at the TDB3LYP-D3/TZVP + PCM (ε=24.852) level of theory samples ΔEvet a b State Electronic structure [eV] S1 (85.3)πHπL 2.88(0.17) S2 (77.2)πH-1 πL 2.89(0.39) S3 (76.1)πH-2 πL 3.48(0.16) T1 (83.7)πH-1 πL 1.83 T2 (87.1)πHπL 2.04 T3 (69.6)πH-2 πL 2.56 (55.3)πH-3 πL (13.0)πHT4 3.17 1πL+7 a
Percentage of dominant contributions of the calculated
transitions at delphynidine-3,5-digludoside in parenthesis. Only contributions larger than the 10% are listed. strengths in parenthesis.
b
Oscillator
Conclusions
Figure 5. Representation of the proposed nonradiative decay of the delphinidin-3,5-diglucoside to generate singlet oxygen through energy transfer process. 3
1
Excitation energy transfer to O2 to form O2 may occur from this state. The efficiency of this process will depend on many aspects, such as electronic coupling (e.g. short- and long-range interactions) vibronic interactions, entropic aspects, and diffusion processes.39 But, among these factors, it is crucial that the energy available in the donor of the energy transfer process is higher than that 1 required to populate the O2 acceptor state to undergo an exothermic reaction. We therefore analyze these energy differences in order to keep the description of this process as simple as possible. Considering adiabatic energy of the optimized T1 (πH-1→πL*) state as 1.55 eV (Table 2) and the reported experimental energy of 1O2 (1Δg) of 0.97 eV, the overall energy transfer would release an amount of ~0.58 eV in an exothermic process. As all three anthocyanins have similar adiabatic excitation energies for the T 1 state, then the same conclusions can be extrapolated to malvidin- and petunidin-3,5-diglucoside. Table 2. TDDFT adiabatic excitation energies (eV) calculated at the optimized lowest-lying singlet and triplet excited states of the anthocyanins. Delphinidin Petunidin Malvinidin -3,5-3,5-3,5a State diglucoside diglucoside diglucoside S0 0.00 0.00 0.00 S1 (97.3)πHπL 2.57 T1 (83.7)π H-1πL 1.55 1.60 1.57 a Percentage of dominant contributions of the calculated transitions in parenthesis
The energetic route for the singlet oxygen generation, constituted by the interplay of the electronic excited states after photoexcitation, was elucidated for delphinidine-3,5-diglucoside, which represents 44% of the anthocyanins present in the extract of the fruit Syzygium cumini. On the other hand, the experimental photogeneration of singlet oxygen under visible light was performed using the ethanolic extract as photosensitizer and was monitored using a chemical trapping method, specifically the rubrene method. Thus, theoretically, it was determined that the adiabatic energy of the optimized T 1(πH-1→πL*) state was 1.55 eV and that the overall energy transfer would release an amount of ~0.58 eV in an exothermic process. Those results relate this state with the promotion electron transfer 1 reactions and subsequent formation of O2 through irradiation of the dyes. Therefore, it was possible to confirm that computational tools are valuable tools to get insights on the photogeneration mechanism of ROS.
Conflicts of interest There are no conflicts to declare.
Acknowledgements The authors would like to thank Universidad del Norte and Departamento del Atlántico (Sistema General de Regalías - Fondo de Ciencia, Tecnología e Innovación) for the financial support through of the Strategic Area “Biodiversidad, Servicios Ecosistémicos y Bienestar Humano” (Code Project 2013-DI0024) and “Programa Agroindustrial Bioenergético del Atlántico (componente Extractos de plantas)”. FONDECYT 1161416 and FONDECYT 1180565.
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Graphical abstract
Highlights ·
An ethanolic extract of S. cumini was used as sensitizers for photogeneration of ROS.
·
The extract demonstrated its potential as antioxidant agent.
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The interplay of the excited states and photogeneration mechanism of 1O2 were studied by DFT methods.
S0009-2614(18)30936-9 https://doi.org/10.1016/j.cplett.2018.11.016 CPLETT 36087
To appear in:
Chemical Physics Letters
Received Date: Accepted Date:
31 October 2018 7 November 2018
Please cite this article as: C. Díaz-Uribe, A. Rodriguez-Serrano, M. López, E. Schott, A. Muñoz, X. Zarate, Singlet oxygen photogeneration by ethanolic extract of Syzygium cumini fruits: Theoretical elucidation through excited states computations, Chemical Physics Letters (2018), doi: https://doi.org/10.1016/j.cplett.2018.11.016
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Singlet oxygen photogeneration by ethanolic extract of Syzygium cumini fruits: Theoretical elucidation through excited states computations Carlos Díaz-Uribe,*a Angela Rodriguez-Serrano,b Maria López,a Eduardo Schott,c Amner Muñozd and Ximena Zarate*e a
Grupo de Fotoquímica y Fotobiología. Universidad del Atlántico. 081007 Puerto Colombia. Colombia. E-mail: carlosdí[email protected] b
Department of Computational Biochemistry, Universität Duisburg-Essen, 45117 Essen. Germany
c
Departamento de Química Inorgánica, Facultad de Química, Pontificia Universidad Católica de Chile. Chile d
e
Grupo de Investigación en Química y Biología, Universidad del Norte. Puerto Colombia. Colombia
Instituto de Ciencias Químicas Aplicadas, Facultad de Ingeniería, Universidad Autónoma de Chile. Chile. Email:[email protected]
The ethanolic extract of Syzygium cumini fruits was characterized and evaluated in the photogeneration of singlet 1 oxygen ( O2) under visible light radiation. This process was studied from a theoretical approach by the survey of the generated electronic excited states, after photoexcitation of the most abundant anthocyanin of the extract, i.e. delphinidin-3,5-diglucoside. It was determinated that the adiabatic energy of the optimized T1(πH-1→πL*) state was 1.55 eV and that the overall energy transfer releases ~0.58 eV in an exothermic process. Therefore, this state is the responsible of promoting electron transfer reactions and subsequent formation of 1O2 through illumination.
Keywords: TDDFT, singlet oxigen, anthocyanin, Syzygium cumin.
1 Introduction Reactive oxygen species (ROS) are molecules involved in a variety of chemical, biological and environmental processes.1–3 Their generation is promising in antimicrobial photodynamic therapy, as these species induce damage or degradation on the microbial membrane or proteins.4 Also, potential applications in advanced oxidation processes rely on ROS generation as these
chemical species can mineralize almost any 5 recalcitrant organic pollutant. The process of ROS generation can be carried out through chemical reactions, both in the absence and under electromagnetic radiation. For the latter (so-called photochemical pathways), in addition to the presence of light, there are molecular oxygen (O 2) and a photosensitizer.6,7 Dyes typically act as photosensitizers as these compounds absorb light and, after photoexcitation, they can subsequently
transfer their energy excess to other molecules present in their surrounding environment or undergo redox reactions. Among the most widely used synthetic photosensitizers are ionic dyes (e.g. rose bengal, methylene blue, eosin Y and rhodamine B),8,9 porphyrins and 10,11 phthalocyanines. Porphyrins and phthalocyanines are the most common sensitizers used in the fields of medicine and environmental chemistry due to their high stability and ability to 12 generate ROS. Nevertheless, the synthesis of these compounds is expensive and sometimes harmful for the humans and/or the environment. In this sense, natural sensitizers have become a more viable alternative than synthetic organic compounds due to their relatively large abundance, easy availability, low cost and because they are friendly to the environment.13 In this case, nature is the main factory of these types of compounds, such as pigments (e.g. carotenoids, flavonoids, anthocyanins, betalains), which are responsible of the different observed colors (from yellow/orange to red/purple) in some plant parts (e.g. fruits, flowers and leaves), and are produced from the secondary metabolism of certain plants. These natural pigments have been isolated and employed as sensitizers in dye-sensitized solar cells,14–16 antimicrobial photodynamic chemotherapy and for the photodegradation of 17,18 One of these organic contaminants in water. plants is Syzygium cumini (Synonymous. Eugenia jambolana L.; common names: Jambu, Java Plum, Jambolan, Jaamun), which belongs to Myrtaceae family. This plant is a perennial tree native from India and is also found distributed in other countries of Asia, Eastern Africa and South America.19 The different parts of Jambu, such as fruits, seeds, bark and leaves, have interesting uses in Ayurvedic and traditional medicines, carminative, diuretic, antidiarrheal, hypoglycemic and antibacterial, among others.20 The violet juice obtained from the fruits shows intense and broad absorption bands in the visible region of the electromagnetic spectrum (attributed to the high content of anthocyanins), which constitutes an advantage in their application not only in the design of photoelectrochemical solar cells but also 21 as sensitizers.
The aim of the herein work is to evaluate the use of an ethanolic extract from S. cumini fruits (an inexpensive and abundant natural resource at Colombian Caribbean region) as a new photosensitizer mixture for the generation (under visible light irradiation) of singlet oxygen. To get further insights on the ROS photogeneration, the electronic structures of the low-lying singlet and triplet excited states of the anthocyanins present in the extract have been explored by means of the Time-Dependent Density Functional Theory (TDDFT). Their excited states interplay after photoexcitation has been examined concentrating the attention on the production of singlet oxygen.
2 Materials and methods The procedure of extraction, qualitative and quantitative characterization of by HPLC of the anthocyanins of the vegetal material (Syzygium cumini) are described in detail in a previous report carried out by our group.22 2.1 Singlet oxygen determination Singlet oxygen was detected by means of chemical trapping based on the rubrene method described 23 by Nardello et al. A mixture of 10 mL of rubrene solution (500 ppm) with 100 µL of crude extract (50 ppm) was prepared and placed inside a batch photo-reactor with enriched-oxygen atmosphere under visible radiation (100 W OSRAM halogen immersion lamp). From the light source, the wavelengths < 500 nm were filtered and removed by using a 1.0 M potassium dichromate solution. The incident photon flow per unit volume (I o= 5.8×10-5 Einstein L-1 s-1) was determined according to chemical actinometry using a 0.0100 M Reinecke salt (K[Cr(NH 3 )2(CNS)]4 ) solution. The rubrene oxidation was monitored by visible spectrophotometry at 522 nm. 2.2 Quantum chemical calculations Density Functional Theory (DFT) in combination with its Time-Dependent approach (TDDFT) were used to analyze the electronic structure of the anthocyanins and the excited states interplay. This with the aim of elucidating the possible decay route that the dye might trigger upon photoexcitation, to finally successfully photogenerate one of the most important ROS, as singlet oxygen (1 O2). Geometry optimizations of the ground states were performed employing the Becke-3-parameter-Lee-Yang–Parr (B3LYP) 24–26 in conjunction with the 6-31+G(d,p) functional basis set.27 According to our experience this combination yields reliable geometries for the
study of the electronic properties of these dyes.28,29 The optimization of the S1 states has been carried out using TDDFT, with the same functional and basis set. The T 1 states were optimized using unrestricted DFT (UDFT) also at the same level of theory. A TDDFT calculation was performed at the optimized minima for obtaining the electronic properties and the corresponding adiabatic excitation energies. Harmonic vibrational frequencies were computed to guarantee the converged structures are minima in the corresponding potential energy surfaces. For the vertical excitations, TDDFT calculations were performed using the long-range corrected version of the B3LYP hybrid exchange-correlation functional, the Coulomb-attenuating method30 B3LYP (CAM-B3LYP). which have been reported 31,32 to provide accurate excitation energies. Solvent effects were included implicitly in all our computations using the polarizable continuum model (PCM) with a dielectric constant ε=24.55 which represents ethanol, all calculations were performed using the Gaussian09. 33,34
Figure. 1. UV-Vis spectrum of Syzygium cumini extract in ethanol (inside; three main anthocyanins found in the extract. Finally, for these anthocyanins, absorption maxima wavelengths of 534, 520 and 540 nm have been reported respectively.28
2 Results and discussions 3.1 UV-VIS Characterization of the extract Studies have shown that the fruit-pulp from Syzygium cumini contains anthocyanins, which are responsible for its bright purple color.35,36 Based on the structures, the anthocyanins have displayed maximum absorption bands ranged between 520 nm and 540 nm, which are the wavelengths commonly used by spectrophotometric assays for 28 their characterization. Figure 1 shows the UV/Vis absorption spectrum of the ethanol extract from Syzygium cumini fruit-pulp, the broadband located at visible range suggests that the extract may contain more than one type of anthocyanin, furthermore, the absorption maximum is located at 526 nm, this band can be assigned to the cinamoyl group and corresponds to the aromatic ring of the flavonoid structure, this band is characteristic for flavonoids of the anthocyanins group. In a recent report, three main anthocyanins were identified in Syzygium cumini fruit, being the delphinidin-3,5-diglucoside dye the most abundant with a relative amount of 44 % in the sample, followed by malvidin-3-5-diglucoside (28 %) and petunidin-3-5-diglucoside (9 %). (inside Figure 1, are shown the chemical structures of the three main anthocyanin).22
3.2 Determination of singlet oxygen The generation of singlet oxygen (1 O2) from the S. cumini extract was monitored through trapping reaction of the singlet species with rubrene (orange compound), which once is selectively oxidized by 1O2 , it is transformed into cycloendoperoxide derivative (colorless 37 compound). The lost in color (from orange to colorless) of rubrene in the reaction was measured by visible spectroscopy at wavelength 488 nm, and the monitoring of oxidation, in function of the irradiation time, is showed in Figure 2. A decrease in the maximum absorption band (488 nm) of rubrene spectrum was observed as the irradiation time increased, due to the formation of rubrene endoperoxide due to a [4+2]-cycloaddition mechanism.23 These results confirmed that rubrene oxidation was carried out by singlet oxygen under visible irradiation.
wavelength of delphinidine-3,5-glucoside appears at ~2.9 eV. The experimental absorption band is 28 reported at 2.32 eV and the obtained here in the ethanolic extract is 2.36 eV. This band is composed by two optically active and isoenergetic electronic states: the S2 state arising due to a πH-1 →πL* transition with a more prominent oscillator strength (f(L)=0.39) and the S1 state characterized by the πH→πL* transition with a lower oscillator strength (f(L)=0.17). a)
Figure 2. Absorption spectra in visible region (l:400600 nm) for rubrene oxidation produced by 1O2 photo-generated by irradiation, as a function time, of ethanol extract from S. cumini fruit-pulp (inside: Rubrene oxidation chemical reaction). S0
S1
3.3 Quantum chemical results
Herein, the results obtained in the framework of DFT calculations are presented. Due to the resemblance on the electronic structure of the three dyes, the present analysis of the results will focus in the delphinidine-3,5-diglucoside, which is the most abundant compound found in the extract. First, the electronic properties of the calculated ground states (S0 ) are discussed. The ground-state geometries used in this work have been selected according to previous studies, where ground state geometries, UV–vis spectra and 22,28 In those photovoltaic properties are reported. reports, the interaction of the anthocyanin dyes with the glucoside motifs are described in detail. Therefore, to get insights on the ROS photogeneration, here we focus the attention on the routes of energy dissipation after photoexcitation, we discuss possible pathways of ISC that may conduce to an efficient population of the triplet state in a qualitative manner. To aid the discussion about the production of singlet oxygen through energy transfer from the triplet states of the anthocyanins, the electronic properties computed at the adiabatic T 1 state minima are presented. Selected geometrical parameters of the computed geometries of the electronic states minima are presented in Figure 3. The corresponding frontier molecular orbitals (MOs) of delphinidine-3,5-diglucoside involved in the low-lying energy singlet and triplet states are displayed in Figure 4. The excited-state vertical excitation energies and their leading electronic configurations at the ground state geometry are shown in Table 1. The TDDFT maximum absorption
T1
b)
c)
S0
T1
S0
T1
Figure 3. Optimized ground and excited state minima of a) delphinidine-3,5-diglucoside, b) malvidin-3,5-diglucoside and c) petunidin-3,5diglucoside. The labelling of these two states was chosen for simplicity. This vertical excitation is represented as an orange arrow in the Jablonsky diagram of the delphinidine-3,5-diglucoside (see Figure 5). The S3 state corresponding to a πH-2 →πL* transition presents also a minor absorption (f(L)=0.16). The molecular orbitals corresponding to the associated
transitions are localized mainly in the anthocyanin rather than on the glycoside moiety. While the S2 and S3 states correspond to valence transitions, the S1 state shows up as a charge transfer state (CT) with the πH MO amplitudes localized in the pyrogallol part of the anthocyanin and the πL over the whole anthocyanin part. Consequently, our results indicate that this state may be responsible of promoting electron transfer reactions and subsequent formation of singlet oxygen through illumination of anthocyanins. After geometry relaxation, the system would populate an adiabatic S1 state characterized with the same electronic transition as vertically, and show an energetic stabilization by 0.31 eV respect to the vertical energy.
Figure 4. Frontier molecular orbitals (MOs) of delphinidine-3,5-diglucoside calculated at the ground state minimum at the B3LYP-D3/TZVP + PCM (ε=24.852) level of theory. This fact is in concordance with the small variations observed in the geometrical parameters computed for these states (S0 and S1, see Figure 5). In this adiabatic minimum, the excitation energy of the S2(πH-1 →πL*) state is separated by 0.23 eV from the S1 state, which indicates that this state can be thermally populated from the adiabatic S1 state. Here, the TDDFT adiabatic energies for the optimized S1 and T1 states are presented in Table 1. It is known from the experiments that a part of the singlet population undergoes intersystem crossing to the triplet states where the efficiency of this process is crucial for the production of the singlet oxygen. In the triplet manifold, vertically, three states (T1-T3) are energetically located below the S1(πH→πL*) state. If the S1 state is sufficiently longlived, it might show intersystem crossing (ISC) to
those triplet (π→π*) states. The lowest energy triplet state (T1) is characterized by a πH-1 →πL* transition and the T 2 and T3 states arise from πH→πL* and πH-2 →πL* electronic excitations, respectively. After relaxation to the minimum of the S1(πH→πL*) state, as presented in Figure 5, these excited triplet states preserve their energetic ordering as in the Franck-Condon region. The T 3(πH2→πL*) state is slightly destabilized and becomes closer in energy to the adiabatic S1(πH→πL*) state. Here, ISC processes are expected to be efficient if the singlet and triplet states involved are close in energy, their spin–orbit coupling (SOC) is reasonably strong and the density of vibrational levels is high in the accepting state. For this reason, this T3(πH-2 →πL*) state may constitute the main target for ISC from the S1 (πH→πL*) state. According to El-Sayed's rule, the SOC between π→π* states can be considered weak in the Condon approximation. Nevertheless, many reports have evidenced that the ISC processes between close lying singlet and triplet states of π→π* character can be enhanced due to vibronic SOC in the context of the Herzberg-Teller approximation.38 After the system undergo efficient ISC to the triplet state, a fast internal conversion (IC) process will lead to the population of the adiabatic T 1(πH-1 →πL*) state, see Figure 5. This process is accompanied by smooth changes in the molecular geometry and an energy stabilization of 0.28 eV (for delphinidine-3,5diglucoside) with respect to the corresponding vertical energy. Table 1. Vertical excitation energies [eV] of the low-lying energy singlet and triplet states of delphinidine-3,5-diglucoside calculated at the TDB3LYP-D3/TZVP + PCM (ε=24.852) level of theory samples ΔEvet a b State Electronic structure [eV] S1 (85.3)πHπL 2.88(0.17) S2 (77.2)πH-1 πL 2.89(0.39) S3 (76.1)πH-2 πL 3.48(0.16) T1 (83.7)πH-1 πL 1.83 T2 (87.1)πHπL 2.04 T3 (69.6)πH-2 πL 2.56 (55.3)πH-3 πL (13.0)πHT4 3.17 1πL+7 a
Percentage of dominant contributions of the calculated
transitions at delphynidine-3,5-digludoside in parenthesis. Only contributions larger than the 10% are listed. strengths in parenthesis.
b
Oscillator
Conclusions
Figure 5. Representation of the proposed nonradiative decay of the delphinidin-3,5-diglucoside to generate singlet oxygen through energy transfer process. 3
1
Excitation energy transfer to O2 to form O2 may occur from this state. The efficiency of this process will depend on many aspects, such as electronic coupling (e.g. short- and long-range interactions) vibronic interactions, entropic aspects, and diffusion processes.39 But, among these factors, it is crucial that the energy available in the donor of the energy transfer process is higher than that 1 required to populate the O2 acceptor state to undergo an exothermic reaction. We therefore analyze these energy differences in order to keep the description of this process as simple as possible. Considering adiabatic energy of the optimized T1 (πH-1→πL*) state as 1.55 eV (Table 2) and the reported experimental energy of 1O2 (1Δg) of 0.97 eV, the overall energy transfer would release an amount of ~0.58 eV in an exothermic process. As all three anthocyanins have similar adiabatic excitation energies for the T 1 state, then the same conclusions can be extrapolated to malvidin- and petunidin-3,5-diglucoside. Table 2. TDDFT adiabatic excitation energies (eV) calculated at the optimized lowest-lying singlet and triplet excited states of the anthocyanins. Delphinidin Petunidin Malvinidin -3,5-3,5-3,5a State diglucoside diglucoside diglucoside S0 0.00 0.00 0.00 S1 (97.3)πHπL 2.57 T1 (83.7)π H-1πL 1.55 1.60 1.57 a Percentage of dominant contributions of the calculated transitions in parenthesis
The energetic route for the singlet oxygen generation, constituted by the interplay of the electronic excited states after photoexcitation, was elucidated for delphinidine-3,5-diglucoside, which represents 44% of the anthocyanins present in the extract of the fruit Syzygium cumini. On the other hand, the experimental photogeneration of singlet oxygen under visible light was performed using the ethanolic extract as photosensitizer and was monitored using a chemical trapping method, specifically the rubrene method. Thus, theoretically, it was determined that the adiabatic energy of the optimized T 1(πH-1→πL*) state was 1.55 eV and that the overall energy transfer would release an amount of ~0.58 eV in an exothermic process. Those results relate this state with the promotion electron transfer 1 reactions and subsequent formation of O2 through irradiation of the dyes. Therefore, it was possible to confirm that computational tools are valuable tools to get insights on the photogeneration mechanism of ROS.
Conflicts of interest There are no conflicts to declare.
Acknowledgements The authors would like to thank Universidad del Norte and Departamento del Atlántico (Sistema General de Regalías - Fondo de Ciencia, Tecnología e Innovación) for the financial support through of the Strategic Area “Biodiversidad, Servicios Ecosistémicos y Bienestar Humano” (Code Project 2013-DI0024) and “Programa Agroindustrial Bioenergético del Atlántico (componente Extractos de plantas)”. FONDECYT 1161416 and FONDECYT 1180565.
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Graphical abstract
Highlights ·
An ethanolic extract of S. cumini was used as sensitizers for photogeneration of ROS.
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The extract demonstrated its potential as antioxidant agent.
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The interplay of the excited states and photogeneration mechanism of 1O2 were studied by DFT methods.