Dimerization Behavior of Methyl Chlorophyllide a as the Model of

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Dimerization Behavior of Methyl Chlorophyllide a as the Model of Chlorophyll a in Presence of Water Molecules - Theoretical Study Micha# Chojecki, Dorota Rutkowska-Zbik, and Tatiana Korona J. Chem. Inf. Model., Just Accepted Manuscript • DOI: 10.1021/acs.jcim.8b00984 • Publication Date (Web): 18 Apr 2019 Downloaded from http://pubs.acs.org on April 21, 2019

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Journal of Chemical Information and Modeling

Dimerization Behavior of Methyl Chlorophyllide a as the Model of Chlorophyll a in Presence of Water Molecules – Theoretical Study Michal Chojecki,† Dorota Rutkowska-Zbik,‡ and Tatiana Korona∗,† †Faculty of Chemistry, University of Warsaw, ul. Pasteura 1, 02-093 Warsaw, Poland ‡Jerzy Haber Institute of Catalysis and Surface Chemistry, Polish Academy of Sciences, ul. Niezapominajek 8, 30-239 Cracow, Poland * E-mail: [email protected]

Abstract A dimerization of methyl chlorophyllide a molecules and a role of water in stabilization and properties of methyl chlorophyllide a dimers were studied by means of symmetry-adapted perturbation theory (SAPT), functional-group SAPT (F-SAPT), density-functional theory (DFT), and time-dependent DFT approaches. The quantification of various types of interactions, such as π-π stacking, coordinative, and hydrogen bonding by applying the F-SAPT energy decomposition scheme shows the major role of the magnesium atom and the pheophytin macrocycle in the stability of the complex. The examination of interaction energy components with respect to a mutual orientation of monomers and in the presence or absence of water molecules reveals that the dispersion energy is the main binding factor of the interaction, while water molecules tend to weaken the attraction between methyl chlorophyllide a species. The dimerization can be seen in computed UV-Vis spectra, and results in a doubling of the lowest peaks, as compared to the monomer spectrum, and in an intensity rise of the lowest 1.8 eV and 2.4 eV peaks at a cost of the 3.5 eV peaks for the majority of dimer configurations. The complexation of water has little effect on the peaks’ position, however it affects the overall shape of simulated spectra through changes in peak intensities, which is strongly ACS Paragon Plus Environment

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dependent on the structure of the complex. The VCD spectra for the dimers show several characteristic features attributed to the interaction of substituting groups and/or water ligand attached to macrocycle groups belonging to different monomers. VCD is sensitive to the type of the formed dimer, but not to the number of water molecules it contains. This and several other features, as well as the differential UV-Vis spectra, may serve as the indicator of the presence of a given dimer structure in the experiment.

Introduction Chlorophylls and bacteriochlorophylls, which serve as green pigments in plants, algae, and phototropic bacteria, constitute the key components of their photosynthetic apparatuses. In vivo not only individual molecules, but also the complexes of several monomers (also called aggregates), are widely present, therefore the aggregation of these molecules has become a widely studied phenomenon. The interest in aggregates is especially due to their participation in the energy-transfer process during photosynthesis. It should be noted that already the monomers themselves possess a rich absorption spectrum, which is attributed to the presence of macrocyclic tetrapyrrolic ligands: chlorin and bacteriochlorin in chlorophylls and bacteriochlorophylls, respectively. Aggregates contribute to the light-harvesting mostly through the excitonic coupling resulting from the interactions of these light-absorbing species, what makes the photo-physical properties of dimers and higher oligomers differ from the properties of monomers. Recently, one observes a renewed interest in the process of tetrapyrrole aggregation, as such aggregates are tested as candidates for artificial solar-light harvesting systems. 1–6 The aggregation of chlorophylls is a result of the coordination properties of the central magnesium ion and of the ability of the tetrapyrrolic moiety to interact one with another. The first step of chlorophyll aggregation is a formation of smaller aggregates, probably dimers, followed by an induction time, after which larger aggregates are formed. 7 Since chlorophylls are widespread in Nature, the underlying physics of the interactions between tetrapyrroles and in particular between chlorophyll entities became subject of many theoretical and experimental studies with various techniques, see e.g. Refs. 4,8,9 and references therein. Experimental studies concern among others interactions of pigments with environment (protein, solvent) and possible interactions among pigACS Paragon Plus Environment

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ment molecules. Theoretical studies focus on their properties relevant for photosynthesis, such as ionization potentials and charge distribution, 10,11 as well as on the modification of these properties by protein environment. 12 It has been postulated that the aggregation process is driven by a number of factors: the ring-ring interactions (π-π stacking), as confirmed by resonance light scattering spectroscopy and crystallographic studies; 13 the coordinative bonding formed by the central magnesium atom; 14 hydrogen bonding between tetrapyrrole substituents which pins together the interacting moieties; 14,15 and – last but not least – the involvement of solvent molecules as co-aggregating species, such as water 16 or molecules possessing aromatic functionalities in organic solvents, like e.g. azulenes. 17 Dimers of chlorophylls ligated by histidine, as found in photosystem II of the cyanobacterium thermosynechococcus elongatus, were studied by B3LYP-DCP/6-31+G(d,p), 18 where DCP stands for dispersion-correcting atom-centered potentials. The authors predicted the dimerization energy to amount to −70 kJ/mol and −79 kJ/mol at M06-2X/6-31+G(d,p) and B3LYP-DCP/631+G(d,p), respectively. The comparison of dimerization energies computed at B3LYP-DCP/631+G(d,p) and B3LYP/6-31+G(d,p) allowed them to estimate the contribution of the dispersion energy to the overall binding at −126 kJ/mol. For the case of bacteriochlorophyll c aggregates the relative importance of each interaction type was studied by means of Møller-Plesset (MP), density-functional theory (DFT), and semiempirical methods by Burda et al. 19 They concluded that the aggregation is governed mostly by the π-π interaction of macrocycles (the interaction strength amounts to 168 kJ/mol for the most favorable orientation of bacteriochlorophyll macrocycles), followed by the coordinative bond between the magnesium ion with the OH group of the neighboring substituent (about 84 kJ/mol), while the hydrogen bonds contribute with only 34 kJ/mol on average. Similarly, the importance of the π-π interaction between two macrocycles was stressed in Ref., 20 where the intermolecular interaction energy of −90 kJ/mol between two bacteriochlorophylls a forming a dimer was computed at MP2/6-31G*(0.25) level. Due to the size of pigments, the formation of dimers and higher aggregates was studied also with semi-empirical quantum chemistry, Molecular Dynamics (MD) or Quantum Mechanics/Molecular Mechanics (QM/MM) methods. Such an approach is justified, as QM methods would be computationally too expensive to sufficiently probe the conformational space. It seems that the primary ACS Paragon Plus Environment

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interest of these studies lies in the photophysical properties of chlorophylls, either isolated or their aggregates, in proteins and in solution. Dynamical behavior of chlorophyllide a was e.g. studied in water, methanol, and benzene. 21 The study yielded rotational time constants, ligand-exchange time rates, as well as indicated which groups of chlorophyllide a might interact with solvent molecules. Often MD and QM/MM are used to generate multiple geometry structures which serve as input for higher level computations. Canuto et al. 22 employed Monte Carlo approach to probe the Mg coordination in chlorophyll c2 in methanol in order to study spectral properties of the solvated pigment with PCM-B3LYP/6-31G(d,p). Zheng et al. 23 studied energy transfers in chlorophyllide a dimers of different geometries using semi-empirical Austin Model 1 (AM1) derived structures with the CIS method. They found that dimerization-induced energy level splittings lead to narrowing of energy gaps between the excited states. Such an effect leads to a faster relaxation rate as compared to a single chlorophyllide a species. Since the least explored field in the aggregate formation is the involvement of solvent molecules, we will focus the present study on this topic and will model the methyl chlorophyllide a (Chla) dimers which may be formed in the aqueous solution. The aim of our studies is the quantification of various types of interactions (the π-π stacking, coordinative and hydrogen bonds, as well as involvement of water) and investigation of how the interaction energy between two Chla reflects: (i) changes in the mutual orientation of monomers and (ii) the number of added water molecules. Different geometries and different pigment-tosolvent ratios (2:0, 1:1, 2:1) are considered, when a relatively high pigment-to-solvent ratio reflects the situation, in which pigment molecules undergo the self-assembly and form thin films. It should be noted that the experimental evidence as to the stoichiometry of chlorophyll – water aggregates is ambiguous. While some reports suggest that the most probable Chla to water ratio is 1:1, 24 some other claim that this ration is equal to 2:1 for samples obtained by electrodeposition of Chla colloid on Au(111) surface. 25 To complete the study, we look at the modification in the UV-Vis spectra induced by the formation of the dimers. According to a recent review paper (Ref. 26 ) the nonplanarity of the Chla ring may enhance the chirality of a single Chla molecule, so since a complexation modifies the ring planarity, the dimer creation and water attachment can affect the chirality as well. Additionally, it is known that the chiral C132 center may undergo enolization and chirality inversion, creating ACS Paragon Plus Environment

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Chla’, and such an inverted form has been suggested to exist in Ref. 27 Therefore, we examine the influence of Chla chirality on the strength of the interaction by considering an artificial dimer with one Chla replaced by its mirror image, i.e. by comparing two diastereoisomers of (Chla)2 . Finally, by simulating VCD experiments, we check how the chirality of Chla is manifested in the resulting spectra. It should be noted parenthetically that in a recent publication of one of the present authors (T.K.) several interesting differences were encountered when investigating RR and RS diastereomers of a chiral C82 with CHFClBr, especially for the VCD spectra, while the UV-Vis spectra remained largely unaffected, 28 so it is interesting to check whether these differences will be distributed in a similar way among both types of spectra in the present case. The studies presented in this work will help to understand the role of water in modulating the strength of the interaction between Chla monomers and in changing the absorption properties of Chla aggregates, what is of a crucial importance in view of their potential applications as organic light-emitting diodes.

Methodology As a theoretical model of chlorophyll a we employed the methyl chlorophyllide a molecule, as depicted in Figure 1a. All the peripheral groups of native chlorophyll a were taken into account with the exception of the phytyl chain, which is replaced by a methyl group. Such a procedure of replacement of the long nonessential aliphatic back-chain with a simpler group is a standard technique in studies of chlorophylls and porphyrins. It has been applied, for instance, in a study of an electronic spectrum of one chlorophyll a molecule reported in Ref. 29 , where this group has been replaced by a single hydrogen atom. In Figure 1a the main parts of the molecule, such as pyrrole rings, an isocyclic ring, and all remaining peripheral groups relevant for a further discussion are shown, like methyl acetate and propanoate groups. Additionally, we will denote the whole set of all four pyrroles, one isocyclic ring and the magnesium ion as a macrocycle ring. If the Mg ion is removed from the macrocycle, the remaining moiety will be denoted as pheophytin, following the popular name setting. Large molecules, like methyl chlorophyllide a, have several rotatable bonds, which can twist differently in a monomer and a dimer. Therefore our search for the most plausible stacking dimers started from the generation of approximate geometries with the AutoDock Vina program 30 and ACS Paragon Plus Environment

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the elimination of high-energy structures. The remaining structures served as starting points for the geometry optimization. Such a protocol, in which the structures were generated in vacuum, has the limitation resulting from the neglect of environment, as the mechanism of dimerisation depends also on the solute – solvent interactions. Therefore, the conformational sampling in solvent would yield the results which would be closer to reality. The accounting for this fact is beyond our capabilities now, but we are aware that the improved approach may be crucial to explain the aggregation pathways. The geometry optimization was done at the DFT level with the B97-D3 functional 31 with the resolution-of-identity (RI) (denoted also as density-fitting – DF) method used to accelerate the computations. 32 Geometry optimizations were carried out using the def2-SVP basis set 33,34 (the application of larger basis sets has been hampered by too high computational costs) and performed with the turbomole suite of codes 35 . The corresponding default auxiliary basis sets 36 were utilized for the RI. After the initial visual examination of the obtained geometries with zero, one, and two water molecules we additionally selected several structures which are higher in energy, but which represent a “missing” link in the series for (Chla)2 · · · (H2 O)n , (n = 0, 1, 2), for a given arrangement of the Chla molecules (for n = 2) (see below). Cartesian coordinates of the optimized structures are listed in the Supporting Information. The harmonic frequencies’ analysis was performed to confirm that the obtained stationary points are local minima on the potential energy hypersurface. The optimized dimer structures were utilized to obtain the interaction and stabilization energies. These single-point calculations were performed with the def2-TZVP basis set 34 (with exception of one small component, see below). The interaction energies together with their decomposition into physically interpretable components were calculated by symmetry-adapted perturbation theory (SAPT), 37,38 with monomers described on the DFT/TD-DFT level (the so-called SAPT(DFT) model 39,40 ). The asymptotically corrected PBE0 functional 41,42 with the asymptotic correction defined by Gr¨ uning 43 was utilized. The DF technique was applied for the calculation of the electron repulsion integrals. 44 In the SAPT method, the interaction energy is obtained perturbationally, where the zeroth-order Hamiltonian is composed from the sum of Hamiltonians of interacting molecules (monomers). Therefore, the remaining (perturbation) operator describes the intermolecular interaction. In the first order, such a perturbational theory describes the Coulomb interaction between unmodified electron clouds of monomers (electrostatic interaction), while in the second order – the polarization of one monomer ACS Paragon Plus Environment

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by another and vice versa (induction) and the attraction of instantaneous multipoles (dispersion). The symmetry adaptation of the approximate wave function, which enforces the correct symmetry with respect to permutations of electrons between the interacting molecules, results in an appearance of the so-called exchange corrections to the first-order electrostatic and the second-order induction and dispersion components. Additionally, higher-order effects are estimated through the so-called delta Hartree-Fock correction, which approximately accounts for third- and higher order induction and exchange-induction terms. 45 Summarizing, the SAPT interaction energy is calculated as the sum, (1)

(2)

(2)

(1)

(2)

(2)

Eint = Eelst + Eind + Edisp + Eexch + Eexch−ind + Eexch−disp + δEHF ,

(1)

(10) (10) (20) (20) δEHF = EHF − E + E + E + E int elst exch ind,resp exch−ind,resp ,

(2)

with

where EHF int denotes the supermolecular HF interaction energy and the SAPT components were obtained with monomers described on the HF level. In practice, the exact solutions of the zerothorder Hamiltonian are not known and they are approximated by e.g. density-functional theory (DFT), resulting in the SAPT(DFT) model. The SAPT(DFT) method has been utilized with success for numerous studies of large intermolecular complexes, see e.g. Refs. 46–50 Since the SAPT method provides the interaction energy between two closed-shell fragments, it was necessary to treat a complex of Chla and water as one molecule. Note that such treatment is justified taking into account the strength of the coordination bonding between water and Chla, which is stronger than an average noncovalent bonding (e.g. it amounts to −54 kJ/mol for the Mg-porphyrin· · · water complex, see Ref. 48 ). Although the SAPT energy decomposition into electrostatic, induction, dispersion, and their exchange counterparts is very useful for analysis of the nature of the Chla–Chla interaction, it is not detailed enough to provide a comprehensive interpretation of the interaction of large molecules. To this end, we enhanced our study by utilizing the Functional-group SAPT (F-SAPT) method, 51,52 which enables an approximate partition of the SAPT components into terms corresponding to the interaction of various monomer fragments. The full set of data containing the F-SAPT partition have been moved to the Supporting Information because of their volume. Here we will only discuss ACS Paragon Plus Environment

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main conclusions obtained from the F-SAPT analysis. Additionally, we will analyze some features of monomers and dimers, which can be obtained from quantum-theory of atoms-in-molecule (QTAIM). 53 The influence of dimerization and water complexation on the UV-Vis spectra was studied by performing TD-DFT calculations with the CAM-B3LYP functional 54 with coefficients switching between short- and long-range exchange modified as proposed in the work of Koopen et al. 55 This functional has been especially designed for the calculations of electronic spectra of large molecules and has been used very recently to obtain UV-Vis spectra of similar chlorophyll species. 56 Since the environment can cause significant changes in the electronic spectra, these calculations were performed in vacuum, as well as in water and in methanol solvents (for the two latter cases within the polarizable continuum model (PCM). 57 Several basis sets (def2-SVP, def2-TZVP, and augcc-pVDZ 58 ) were tested for the TD-DFT calculations on a single Chla-like molecule (with the hydrogen atom replacing the phytyl group as in Ref. 29 ) and finally, the def2-TZVP basis has been applied for the production calculations. The def2-TZVP basis was selected as a compromise between hardware requirements and the accuracy: for the smallest def2-SVP basis two first excited states have energies quite close to these from the aug-cc-pVDZ (−0.05 and 0.14 eV difference, respectively), but the differences rise to 0.2-0.3 eV for four next states and more than 0.4 eV for the seventh excited state and beyond. For the larger def2-TZVP basis, on the contrary, the discrepancies in comparison to the aug-cc-pVDZ basis are smaller also for higher states. Additionally, some tests of based on the comparison of dipole polarizabilities calculated in length and mixed lengthvelocity gauges 59,60 has been performed for def2-SVP, def2-TZVP and several other basis sets in order to confirm the sufficient quality of the def2-TZVP basis for this property (the results of these calculations are also placed in the Supporting Information). The excitation energies for one Chla molecule with different basis sets can be found in the Supporting Information. The character of the electronic excitations (local or charge-transfer) was measured by an analysis of transition density matrices with the method of Plasser and Lischka. 61 Finally, the VCD spectra were obtained with the B97-D3/def2-SVP model – they were plotted with using Lorentzian widening of half-width 20 cm−1 . Supermolecular calculations were performed with turbomole, 35 while the SAPT calculations – with molpro. 62 Additionally, the F-SAPT decomposition were performed with Psi4, 63 and the TD-DFT and VCD calculations – with Gaussian. 64 The transition-density analysis was ACS Paragon Plus Environment

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obtained with help of the THEODORE program, 65 and the QTAIM and electrostatic potential calculations – with AIMAll 66 (the M06-2X 67 densities were utilized for the latter purposes).

Results and discussion The geometries of the Chla molecule (unhydrated and hydrated) optimized at the same level as the dimer are presented in Figures 1a and 1b, respectively. The figure on the left presents a planar macrocycle ring, to which the peripheral groups are attached. If one water molecule enters this system, it preferably binds to the central Mg atom. A side effect of this process is making the macrocycle ring nonplanar (with the dihedral angle between two Mg-N-N planes of 15◦ and a Mg-O distance of 2.15 ˚ A). The position of the OH groups of water is optimized so that one of the hydrogens points towards the the oxygen of the O – CH3 group (from the phytyl attachment site). It should be noted that the whole methyl propanoate group bends significantly towards the new ligand in order to allow for a hydrogen bond creation, which with its the O-H· · · O bond length of 1.79 ˚ A and the angle of 161◦ represents a typical H-bond. The hydrogen bond interactions between carbonyl groups of Chla and protic solvents (here: water molecules) are in line with the experimental findings on photosynthetic pigments in different solvents . 26 The interaction of water molecules with different functional groups of Chla was also evoked based on the MD study. 21 This geometry undergoes some changes upon complexation with another Chla, which will be analyzed below. The unhydrated and hydrated Chla molecule will be denoted as Chla0 and Chla1 in the following.

Analysis of dimer stacked structures For the Chla dimer one expects that the interaction between two Chla moieties can be maximized through various intermolecular binding types available in this case, namely: (i) coordination interactions involving central Mg ions, (ii) a hydrogen bonding including water and/or Chla peripheral groups, and (iii) dispersion forces between pheophytin-pheophytin macrocycles. Based on the analysis of geometry optimization of the structures, eight mutual orientations of two Chla molecules with zero, one, or two H2 O molecules have been proposed. In all the structures two macrocycles are parallel (or almost parallel) and shifted with respect to each other, in agreement with previACS Paragon Plus Environment

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ous theoretical and experimental findings for photosynthetic pigments and their analogs. 14,24,68,69 The resulting geometries of the Chla dimers’ structures are presented in Figure 2. One dimer configuration composed of the Chla and its enantiomer (abbreviated as iChla in the following) is also shown at the bottom in this figure. The order of structures in Figure 2 allows us to examine changes caused by the presence of one or two water molecules while retaining the relative position of the macrocycle rings. The columns of this figure can be regarded as series, where within each series the main difference is the number of H2 O molecules ligated to Chla. If the side of the pheophytin ring shown in Figure 1a is called “back” (note that the pyrrole rings in this figure are numbered counterclockwise) and another side the “face” (the notation already used in the literature, where the “face” side of chlorophyll macrocycle is the one with the phytyl chain protruding, see e.g. Ref. 70 ), then the left series represents the stacked and parallelly shifted (by about one bond-length) back-to-back macrocycle rings, which differ in the degree of rotation of one macrocycle ring with respect to another and will be denoted as BB. The right series represents back-to-face (BF) placed macrocycle rings, which are additionally rotated by about 180◦ and parallelly shifted by several bond lengths with respect to each other.

The number in the notation

indicates the number of water molecules present in the complex. We start a detailed investigation of the geometry features of the obtained structures from unhydrated dimers, i.e. from the structures BF0 and BB0. The BF0 structure is stabilized by two coordination bonds between the central metal atom in the first Chla and the ester carbonyl group, which is in turn connected to the isocyclic ring of the second entity. Both monomers are placed symmetrically with respect to each other and the O· · · Mg bonding equals to 2.11 ˚ A for both coordination bonds. Such a bond length usually corresponds to a quite strong binding.

For the

remaining BB0 aggregate the macrocycle rings are twisted so that distances between the Mg and the nearest N atom of the second Chla are equal to 2.78 and 3.19 ˚ A, indicating a much weaker coordination bonding for the second case. As a result of the close contact between various side groups of both monomers, these groups rearrange themselves so that methyl propanoate groups point outside the complex. In all these cases the magnesium atoms are pushed inside the macrocycle plane (the dihedral angle between two planes defined by the Mg-N-N triangle amounts up to 17◦ ), what may result in a new significant perturbation of the monomer electronic spectra for the excitations spreading on the ACS Paragon Plus Environment

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system of conjugated bonds. Such a geometry change may induce the additional permanent dipole moment for the macrocycle ring, and – as a consequence – a larger induction component resulting from the polarization by this field, which can be indeed detected in some induction components. The next two structures comprise of a Chla dimer with one water molecule, which in all the cases is ligated to the central magnesium atom through its oxygen atom, so it becomes the second axial ligand, where the first axial ligand is either one nitrogen atom from the pheophytin inner ring (BB1) or the carbonyl ester group (BF1) of another Chla. For the BF1 structure, which resembles the BF0 structure with one H2 O added, the six-coordination of Mg causes an elongation of the Mg· · · O=C bonding from 2.11 to 2.21 ˚ A and a planarization of the center of the macrocycle (the largest dihedral angle between two Mg-N-N planes amounts to 7◦ only, which should be compared with 15◦ for Chla1). It should be noted that the planarization is observed also for another complex with one water.

In the BB1 case the influence of the H2 O ligand is so large that it causes the Mg

atom to be placed a bit above the inner circle plane. Additionally the H-bond with a very similar characteristics as in the hydrated monomer (1.83 ˚ A and 159◦ ) can be found in this case. The four remaining structures contain two water molecules ligated from the opposite sides either to the magnesium atoms of both Chla (BB2 and BF2) or to magnesium atom of one Chla and to the carbonyl group of another Chla (BBC and BFC). Also in these cases the addition of the second axial ligand partially restores the planarity of the macrocycle ring. For the BB2 structure the second water causes a further elongation of the Mg-N distances (between Mg and the closest nitrogen atom of the second Chla) from 3.15 ˚ A and 3.27 ˚ A for BB1 to 3.22 ˚ A and 3.44 ˚ A in the present case. Similarly as in the BB1 case, one water molecule creates an additional “frustrated” H-bond with the methyl propanoate group for the same Chla, to which this water is ligated with the H-bond parameters: 1.84 ˚ A and 158◦ . The second BB structure type has one H2 O molecule ligated to Mg and additionally connected through the H-bond to the propanoate group, as in the BB1 case, while the second water molecule makes two H-bonds (each time serving as a hydrogen donor!) with both peripheral groups of another Chla, from with one can be classified as almost “regular” (1.94 ˚ A and 169◦ ), while another one as “frustrated” (2.08 ˚ A and 157◦ ). Since the second water does not affect the Mg-N binding, the smallest distances between Mg and the closest N of another Chla are smaller than for the BB2aggregate and are equal to 3.12 and 3.17 ˚ A. It should be noted that the ability of the substituents of the macrocycle to form hydrogen bonds with solvent ACS Paragon Plus Environment

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molecules was already evoked in the literature. 21,26 Two structures of the BF type show the same trends, regarding the planarization of the inner ring with magnesium, i.e. the complexation of water to magnesium causes this structure to become more planar than for the Chla1 monomer. For the BF2 case both Mg-O coordination bonds become longer by 0.1 ˚ A than for the unhydrated case, indicating that the bond between both planes becomes weaker. Both water molecules are placed parallelly to the pheophytin moities. Finally, the BFC structure has Mg-O bonds of different lengths (2.21 ˚ A if H2 O is ligated on the other side, and 2.11 ˚ A otherwise, just like in the case of BF1), while its second water molecule is primarily bound to the carboxyl group of the methyl propanoate (with the H· · · O distance of 1.99 ˚ A and the H· · · O-H angle of 168◦ ). However, this water is also to some extent bound to the oxygen atom for the ester group, although this connection is much less effective than in the BBC case (2.16 ˚ A and 137◦ ). Since the broad goal of the present study is to examine possible artificial light-harvesting structures and since in many cases the excitation yield of a monomer in a complex depends on fine matching details, which differ among two diastereomeric complexes (e.g. RR and RS), we also considered a hypothetical case, where one Chla has been exchanged by its mirror image. For the structure INV, which is the most similar to the “normal” BB0 structure, the inversion of Chla does not affect the length of the Mg-N coordination bonds.

However, because the iChla has its

methyl propanoate group is a different direction, it cannot be bent toward the Mg like in the BB0 case. It will be therefore interesting to observe how this fact influences the stability and spectral properties of this complex in comparison to the BB0 and the monomer case.

Interactions First of all, let us consider the predictions which follow the total electrostatic potential (ESP) values of the Chla monomer. The map of the ESP on the charge density isosurface of the monomer (see Figure 3) shows that the most negative part of the potential occurs in the region of the oxygen atoms connected to the isocyclic ring or belonging to the carboxyl group of the ester unit, while the most negative pheophytin parts are placed in the region of nitrogens connected to the rings I-III. The most positive part of the pheophytin is the region of the magnesium atom. Therefore based ACS Paragon Plus Environment

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on the ESP analysis it is expected that the connections: Mg· · · O=C and Mg· · · N (rings I-III) are likely to occur. It should be also noted that for the hydrated monomer the former way of attaching the second Chla is blocked by the water ligand (H2 O is ligated to exactly the same site), therefore water is expected to serve as an inhibitor of the creation of structures like BF.

SAPT interaction energies The interaction energies for the studied complexes calculated with SAPT(DFT) and the SAPT energy components are listed in Table 1. The stabilization energy, obtained from adding the deformation energies and zero-point vibrational energy (ZPVE) corrections to the interaction energy, are listed in the same table. The deformation and ZPVE energies were calculated at the same level as utilized in geometry optimization. Because of the size of the system and the limitations of the available computational resources the SAPT(DFT) calculations could be successfully performed for the def2-SVP and def2-TZVP (with exception of δEHF term which was computed, as the most expensive term, solely in the def2-SVP) basis sets. The SAPT calculations for systems of comparable sizes show that basis sets of a similar quality reproduce trustfully enough all the SAPT terms with the exception of the second-order dispersion, for which a larger basis is required 46 in order to reach the complete basis set (CBS) limit. Therefore we performed the CBS estimation for this term in the same way as in Ref. 48 (see also Ref. 71 ). The order of the dimers in the table is such that the three consecutive structures correspond to the same pheophytin groups arrangement and an increasing (from 0 to 2) number of water molecules for an easier comparison of the energetics of these species, and the fourth structure corresponds to the two water molecule in the complex as well, but one of these H2 O is bound to the peripheral groups. As mentioned in the previous section, the ligated water is treated as a part of the monomer in SAPT calculations. This approach can be justified by comparing the H2 O· · · Chla interaction energy, which amounts to −85 kJ/mol (DFT+D3/def2-TZVP), i.e. is much stronger than typical noncovalent interaction between molecules of these sizes. The table shows that the deformation energies range from 32 kJ/mol to 149 kJ/mol, depending on the dimer type. Such a large energy span results in several cases in a change of energetic order based on either the interaction energy, or the stabilization energy is considered. To this end, the energetic order of the interaction energies between two Chla (hydrated and unhydrated)grows ACS Paragon Plus Environment

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in the sequence: BF0< BF1< BFC< BF2< BB0< BBC< BB1< BB2, while for the stabilization energies the order changes to: BF0< BB0< BB1< BB2< BF1< BBC< BF2< BFC. The INV complex, which we do not include in the same list, as it requires the existence of the iChla, resembles the BB0 structure, as far as the interaction energy and stabilization energy are concerned. Since it is known that interaction energies and the resulting energetic order of complexes of Chla can undergo potentially significant changes if the polar environment, like water or methanol solvents, comes into effect, we performed additional calculations of the DFT+D3 interaction energies within the PCM model (the geometry was not relaxed under the influence of the solvent). The results, available in the Supporting Information, show that in this case the modification of interaction energies does not change the energetic order of complexes, and differences between the energies in solvent and in vacuum do not exceed 10-15%. Therefore, we can assume that in this case the role of the solvent is secondary and as the first approximation it can be neglected in further calculations. Let us go back to the energetic sequence of Chla aggregates. The most stable is the BF0 dimer, for which two coordination bonds between the magnesium atom and the methyl acetate groups can be found. It is followed by the BB0 dimer bound by another type of coordination bonds, i.e. between the magnesium atom and the nitrogen atom of another monomer. In the case of these two structures stabilization energies

are very similar (–121 and –118 kJ/mol), although

the interaction and deformation energies themselves are quite different. It is also interesting to compare the SAPT partition of the interaction energy for both structures. It turns out that the BF0 structure has the highest attractive contribution from the electrostatics and induction terms and the smallest attractive contribution from the dispersion energy. The latter finding is in line with the geometrical features of this dimer, where the Chla monomers are relatively far from each other as compared to other cases. On the other hand, since the Chla monomers are positioned such that the polar peripheral groups are on the opposite sides, the negatively/positively charged Chla fragments of the first monomer are placed over the positive/negative parts of the second monomer, what is expressed in the SAPT partition as a large electrostatic contribution. For the BB0 case the highest attractive contribution from the dispersion is observed among all the structures under study, but the attraction caused by electrostatics and induction forces is much smaller than for ACS Paragon Plus Environment

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the BF0 structure. Finally, the INV structure resembles the BB0 one as far as the magnitude of the individual SAPT components is concerned. An examination of the interaction and stabilization energy order in Table 1 shows that an addition of a water molecule makes the interaction energy smaller in absolute value. For instance, all the structures, which are the least attractive (BF2 BB2), have two water molecules, each connected to one Chla through the magnesium atom. On the other side, the two strongest attraction cases (BF0 and BB0) are exerted by two Chla molecules not complexated by water. If the relative position of Chla monomers is the same (up to some geometry relaxation), the structures with zero, one, and two water molecules show a decreasing stability. For the strongest stabilization the Chla moieties are bound through two coordination bonds of the Mg· · · O – C type. From two pairs of structures with two water molecules (the BB2, BBC pair and BF2, BFC pair) the structure with both H2 O connected to Mg have the smallest absolute value of the interaction energy, while the structures with one H2 O attached to Mg and the second one – to the peripheral groups are characterized with the interaction energies close to the corresponding structures with one water molecule. Let us examine the SAPT components of the interaction energy in more detail. If pairs: electrostatics and first-order exchange, induction and exchange-induction plus delta HF, dispersion and exchange-dispersion, are treated together, it turns out that the major negative (attractive) contribution comes from the effective dispersion term, but since this term has a similar value for complexes within the same series, other components play the major role in establishing the stability order. In particular, for the BB series the difference between dispersion terms do not exceed 1 kJ/mol, while for the BF series, it is somewhat larger, but anyway the stability order deduced from the dispersion term is opposite to this resulting from the total interaction energies. If just the complexes with the same number of water ligands are compared, one can see that the decisive role is played by the induction (attraction) and first-order term (repulsion) in a larger stabilization of BF with respect do BB series. A more detailed account of the interactions cannot be revealed without switching to a more scrupulous partitioning of the SAPT terms, as possible with F-SAPT.

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F-SAPT analysis The F-SAPT partitioning of the interaction energy of the complexes reveals that the major contributions arise (which is understandable) from the neighboring groups with overlapping electron densities. Therefore, in addition to negative contributions there is always a large repulsive exchange contribution for such functional pairs. A large overlap also means that the short-range SAPT contributions play a role here, so conclusions driven from the asymptotic SAPT behavior can be found false in some cases. For this reason, it is not possible to name a single SAPT component as mainly responsible for the attraction between the two functional groups. For most of the cases a major attractive contribution stems either from the interaction of two macrocycle rings (the BB series), or from the interaction of the macrocycle ring with peripheral methyl acetate group (the BF series). The ring-ring attraction is predominantly of the dispersion type, while the net first-order contribution is highly repulsive due to a very high first-order exchange term. However, the net induction is also nonnegligible in this case. For the BF series the first-order repulsion between rings becomes smaller, first because of a larger distance between these two planes, and second, because of a parallel shift of two rings with respect to each other. The dispersion contribution becomes smaller in absolute value, too, so the overall contribution from this pair of functional groups is smaller than for BB series. Therefore, the interaction of two macrocycle rings contributes 86–117kJ/mol to the stabilization for the BB series and only about half of it for the BF series. On the other hand, the ring-methyl acetate attraction starts to be the major stabilizing term in the interaction energy for the latter series, since the parallel shift of the rings enables the methyl acetate groups to interact with another ring. This contribution, which is of the order of −100 kJ/mol, is the major reason of the greatest stability of the BF0 complex. Before we analyze the influence of water molecules on the stability of structures, let us consider the role of the central magnesium atom. Since the Mg atom is closed-shell and apparently it has a weaker tendency to create coordinative bonds than transition metals, it would be interesting to check how the presence of magnesium changes the strength of the macrocycle rings’ attraction. To this end, we performed an additional F-SAPT calculation for the unhydrated BF0 case with the Mg ion replaced by two hydrogen atoms (which is a standard “capping” technique in the molecular ACS Paragon Plus Environment

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fragmentation models, see e.g. Ref. 72 ) without a re-optimization of the geometry (unfortunately, the current F-SAPT technique did not allow to separate the contribution from Mg directly). Contrary to the known lower capability of Mg to form coordination bonds it turns out that the presence of the Mg atom is crucial for the stability of the system. The Chla molecules deprived of the magnesium atom stick together about three times weaker, which is mostly due to the switching-off the electrostatic attraction between macrocycle rings and methyl acetate groups and between both macrocycle rings. These electrostatic components are equal to 5, 3, and −18 kJ/mol, respectively, while two former contribute significantly to the overall attraction between Chla’s, if the metal atom is present in the center of the macrocycle ring (then their electrostatic F-SAPT contributions are equal to: −125, −123, and 0 kJ/mol). The induction contributions from the macrocycle ring· · · acetyl group also play a role if the Mg atom is present, while they are virtually negligible without Mg in the macrocycle ring center. The attraction remaining after the removal of Mg mostly comes from the dispersion term, which is of similar value regardless of the presence or absence of Mg. It is therefore evident that denoting the Chla dimer bond as the coordination Mg· · · O=C bond is fully supported by the F-SAPT analysis. Since the complexes with two Mg-ligated water molecules are less stable than their one-water counterparts, and these are in turn less stable than the unhydrated complexes, it is interesting to look for the F-SAPT interpretation of this phenomenon. First of all, an examination of the electrostatic term, possible with the F-SAPT method, defies the intuitive explanation that it is the dipole-dipole repulsion of two water molecules which destabilizes these complexes: the electrostatic, as well as the total H2 O· · · H2 O contributions, are close to zero in all the cases. The interaction energy between water and another monomer without water are usually effectively nonzero, but their range is −1 to +6 kJ/mol only, so their values are not sufficient to explain differences in the interaction energies found in Table 1. The addition of one water molecule to the BF0 weakens the bonding, but the direct interaction of water with another Chla, although it is weakly repulsive (+4 kJ/mol), does not cover the whole discrepancy between both interaction energies. It turns out that the attraction between the ring of the water-containing Chla with the peripheral methyl acetate group becomes weaker by about 27 kJ/mol for the water-containing structure, and that electrostatic and induction contributions are significantly smaller in absolute value in this case. This behavior can be explained by the increased planarity of the ring under the influence of the ACS Paragon Plus Environment

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water ligand, what reduces the polarity of the ligated monomer. The further weakening of the BF2 structure (with two ligated waters) can be explained in a completely analogous way. Finally, within the BB series, the F-SAPT analysis points to the ring-ring interaction as the main stabilization factor for the complex. Other significant energy components

are at least

one order of magnitude less important, e.g. the interaction of the ring with the – COOCH3 group contributes about −19 kJ/mol (almost exclusively as electrostatics), however, the same group is placed so that it exhibits a strong first-order repulsion from the – CH2 CH3 group, what makes the total contribution from this group much smaller than expected. It should be noted that this behavior of the – COOCH3 group is almost independent of the number or water molecules. The ring-ring interaction energy becomes smaller in absolute value for the hydrated complexes. This trend stems from a smaller electrostatic and induction attraction, which can be in turn explained through the planarization of the hydrated Chla and the loss of its dipole moment. It should be noted that delta Hartree-Fock terms contribute substantially to the total interaction energy, too. The magnitude of this contribution is in agreement with the quite substantial second-order effective induction term, which is the third largest in the whole table. At the end, it is interesting to look for similarities and differences in the interaction of the unhydrated complexes within one series containing the INV complex, i.e. to compare either a composition of two Chla monomers, or one Chla monomer and one iChla. From the pair:

BB0

and INV the “normal” complex is more strongly bound in terms of the interaction energy, while the stabilization energy prefers the INV complex because of a smaller deformation energy in this case. The macrocycle rings’ mutual attraction is the largest contribution to the interaction energy and it is by 17 kJ/mol more attractive for INV, however, the total F-SAPT (and SAPT(DFT) as well) interaction energy is more binding for the BB0 case, what indicates that other interactions play a role in this complex.

A more detailed comparison of the interaction between various

functional groups shows that it is the increased attraction involving some peripheral groups which reduces the difference in the interaction energies of these structures. In this case no single secondary interaction can be named, which is finally responsible for the lesser absolute value of the interaction energy for the INV case. It turns out that there are several interacting groups with the interaction energy of order of 10 kJ/mol and the placement of the iChla instead of the second Chla makes some of these groups to be moved from “optimal” interacting positions. For instance, ACS Paragon Plus Environment

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the already mentioned ring· · · COOCH3 interaction is smaller by about 8 kJ/mol for the INV case. The larger value of the dispersion energy suggests that in principle the creation of complexes composed of Chla and iChla could lead to more strongly bound dimers. Such dimers are expected to have similar properties, as far as the electronic excitations are concerned (see below).

QTAIM analysis Another popular way of examination of the intra- and intermolecular interactions consists in a topological analysis of the one-electron density within the QTAIM method. In our case it is especially interesting whether bond paths (BPs) and values of the total density ρ in the bond critical points (BCPs) correspond to the assumed stronger of weaker interaction between pairs of atoms. In particular, the BPs starting from the magnesium atom can tell us whether the QTAIM interaction picture agrees with results from other models, like F-SAPT, and – last but not least – with chemical intuition. Let us examine the intermolecular BPs in more detail. It can be found that for unhydrated dimers the expected coordination BPs: Mg· · · O (for the BF series) and Mg· · · N (for the BB series) are indeed present among intermolecular BPs of the dimers and that the larger ρBCP values correspond to the increasing stability of the unhydrated dimers (ρBCP have values of about 0.009 and 0.027 a.u. for BB0 and BF0, respectively). For the dimers with one ligated water a more complex picture occurs. First of all, for the BF1 case both Mg· · · O BPs are still present, but the water molecule creates an additional BP between Mg and oxygen from H2 O, what results in weakening of the coordination BP on the opposite side of the magnesium atom. While the ρBCP for the unhydrated Mg atom does not change in comparison to the BF0 case, the ligation of H2 O to the second Mg causes this value to become significantly smaller (0.021). For the doublyhydrated dimer the same mechanism causes the weakening of both coordination bonds (their ρBCP are equal to 0.021 a.u.) at cost of the creation of the Mg· · · OH2 bond, for which the BCP ρ value is only insignificantly smaller (it equals to 0.020 a.u.). For the BB series the values of ρ’s in the coordination BCPs are already quite small for the unhydrated case. As a result, the ligation of water causes a disappearance of the corresponding Mg· · · N BP. Therefore, according to the QTAIM analysis there is no coordination bond between a hydrated Mg and the nitrogen from another pheophytin ring. On the other hand, the Mg· · · OH2 bond is stronger than in the BF ACS Paragon Plus Environment

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series: its ρBCP value amounts to about 0.026. Summarizing, the analysis of the Mg-originating BPs is in agreement with SAPT and F-SAPT findings. However, it should be noted that apart from these BPs the QTAIM analysis shows several other noncovalent BPs with ρBCP of order of a few thousandths of a.u. (i.e. several times smaller than for the coordination bonds). Although one or two such BPs are not enough to bind two Chla molecules, ten or more of them can tackle this task. In particular, the strong interactions between both macrocycle rings correlate quite well with the existence of numerous BPs between various atoms belonging to these rings.

Spectral properties The excitation energies and oscillator strengths for several lowest excited states of all the Chla dimers and for the Chla molecule with and without one water are presented in Table 2. Additionally, simulated absorption spectra for monomers and dimers are presented in Figures 4 and 5, while the spatial extent of the lowest excitations obtained from the analysis of transition densities is presented in Figure 6 for several selected cases and in the Supporting Information for all the aggregates. As can be seen from these data, both the complexation with water and the complexation of two Chla molecules causes significant changes in the UV-Vis spectra, which will be discussed in the following chapters. Analogous spectra obtained for two popular solvents (water and methanol) within the PCM model are presented in the Supporting Information.

Monomers Let us start the discussion of the Chla spectra from a comparison of the results for the unhydrated Chla case. Table 2 and Figure 4 show that this molecule has its two lowest excitations within the visible range, among which the first one is of a higher intensity. This excitation, which amounts to 1.84 eV, is denoted in the literature as QY band. The second excitation of about 2.45 eV is known as the QX band. The values of the excitation energies presented here are in a good agreement with other recent theoretical and experimental studies, 29,73 what assures us that the more complex calculations of the dimer will be similarly accurate. The analysis of the character of these two states, as well as of third and fifth states, denoted in the literature as Soret, or B states, reveals that they are all described as various combinations of four possible promotions ACS Paragon Plus Environment

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from HOMO and HOMO − 1 to LUMO and LUMO + 1, in line with the popular Gouterman four-orbital model. 74 These four states are dominated by the excitations within the pheophytin macrocycle, while the fourth excited state is the first excitation with a fractional charge-transfer (CT) character, namely, the electron density changes not only within the macrocycle ring, but also from the ethene peripheral group to the pheophytin macrocycle (see the CT coefficients’ figures presented in the Supporting Information). Its major promotion is from HOMO − 2, which is localized mostly on the ethene peripheral group and a neighboring double bond, to LUMO. The latter three states have much higher intensity than the states corresponding to the Q band. An examination of the orbitals describing the major character of the lowest excitations reveals that these orbitals do not have any significant part close to the Mg atom. Since the water ligand is attached to magnesium, it can be expected that its influence on the spectrum is modest, especially if we take into account the fact that the lowest excitation of water (which amounts to about 7 eV) lies much higher than all the excitations from Table 2, so no resonant interaction with water is possible. Therefore we expect an indirect influence of H2 O only, either resulting from geometry modifications under complexation, or from the redistribution of the electron density caused by the ligand. An examination of the Chla1 case shows that this is indeed the case. The lowest excitation remains virtually untouched by the complexation of water (with a small blueshift of 0.01 eV), while from the next four states these described by the four-orbital model are redshifted by several hundredths of eV, while the fourth state is blueshifted by 0.03 eV. Intensity changes within the states third to fifth are much more pronounced than the energy changes. It appears that the fourth state borrows the intensity from both lower and higher states, thus changing the excitation spectrum considerably. As already mentioned, an interesting feature of the spectrum is a high intensity of excitations in the near-UV region (about 3.5 eV) in comparison to the Vis excitations. The overall intensity of the three states (from third to fifth) is about five times higher than for the two lowest states. This means that the Chla monomer (hydrated and unhydrated) is more effective in absorbing the UV radiation than the visible light.

Dimers Table 2 and Figure 5 show that for the complexes formed by two Chla molecules two closelying excitations below 1.9 eV appear in the spectrum with the energy difference between them ACS Paragon Plus Environment

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ranging from 0.07 to 0.20 eV, so the energetic effect of the dimerization is moderately weak. The obvious explanation of this quasi-degeneracy is the interaction of the first excited states of both monomers (either unhydrated or hydrated, depending on the structure type). In an ideal two-state mixing one expects that one of these two states lies lower, and the second one – higher than the original monomer states, and this is exactly the case of all dimer structures included in this study. However, only for the BF0 case the monomer energy (1.84 eV) lies precisely in the middle between the doubled line, while for all the other cases the lowering of the first excited state is much more pronounced than the raising the second state, therefore the explanation of the line doubling by the two-state interaction has a qualitative value only. The two-state mixing described above may manifest itself in the broadening of QY peak, which is exactly the effect observed experimentally. 75 It should be also noted that the total oscillator strength of these two states of the dimer is larger than the monomer value with the exception of the artificial INV complex, and that this increase is more pronounced for the BF series. It is also interesting to note that the higher state from this doublet has always a higher intensity and that the intensity ratio can be used to distinguish between the BF and BB series. The calculated redshift of the first dimer excitation is in line with experimental UV-Vis spectra recorded after the dimerization of Chla in different solvents. For instance, the QY peak in ethanol is displaced by 35 nm towards longer wavelengths, 76 while in an aqueous solution of DMF – by 40 nm, 77 what is within the lowering range resulting from a dimerization observed by us (from 0.05 to 0.17 eV). The redshift was also reported in other theoretical studies on Chla dimers. 69,73 Joint theoretical and experimental studies indicate that the size of the shift depends on the mutual orientation of both macrocycle rings. It has been found that it is larger in stacked molecules 69 in an agreement with the present study, where the shift is equal to 0.15–0.17 eV for the BB series and only 0.04–0.07 eV for the BF series. It is interesting that the INV complex resembles in this aspect the BF behavior, although in terms of geometry it is more similar to the BB0 complex. Further, it is known that the redshift depends on the type of solvent in which the dimer is formed. 22 For our case, however, we observed only small (of order of one or two hundredths of eV) shifts in both sides, if a solvent like water or methanol were accounted for. Also, the second pair of excited states, which is still within the visible region, is close energetically, too (the energy gap ranging from 0.01 to 0.12 eV only), what can be at first approximation ACS Paragon Plus Environment

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explained by the two-state mixing of the monomers’ QX excitations. Much larger changes can be seen in the intensity pattern (note a different intensity scale for different complexes in Figure 5). Here, depending on the dimer structure, either both lines have a similar intensity – this is the case of the complexes BF1, BF2, and BFC, or the lower of these lines is almost forbidden (BB0, BB2, BBC), or – for the remaining structures – the intensity of both lines is quite low. For all the dimer cases the monomer orbitals: HOMO − 1, HOMO, LUMO, and LUMO + 1 have a (spatial) possibility to effectively overlap with each other, what gives new sets of dimer orbitals, which visually resemble a combination of orbitals of both monomers (see Figures in the Supporting Information for the visualisation of selected monomer and dimer orbitals). The mixing ratio strongly depends on the structure type and hydration. For instance, for the BF0 and BB0 structures the orbitals from HOMO − 3 to LUMO + 1 are visually evenly distributed over both macrocycle rings, while LUMO + 2 and LUMO + 3 are mostly localized on first or second monomer, respectively. Also the orbitals HOMO−4 and HOMO−5 are localized on one monomer, and they closely resemble the corresponding HOMO − 2 of the single Chla molecule, i.e. they are mostly localized on the ring I and the ethene group.

For the BF1 complex the above pattern

holds for orbitals from HOMO − 5 to HOMO − 2 only, while the orbitals from HOMO − 1 to LUMO + 3 are localized alternately either on one or on second Chla starting from the hydrated Chla for HOMO − 1. An addition of one water in the BB series (the BB1 complex) causes an even larger disruption of intermolecular orbital mixing: here all the orbitals from HOMO − 5 to LUMO + 3 are localized mostly on one Chla. A similar situation occurs e.g. for the BBC case, where additionally the character of the HOMO − 4 orbital is changed. This orbital is localized on the ring I only, since the ethene group is rotated outside the macrocycle plane for this structure. A general rule from the inspection of orbital shapes is that their delocalization is supported by the approximate symmetry of the system: the unhydrated complexes (including the INV one) and fully Mg-hydrated complexes have more delocalized orbitals than the complexes with only one water attached to magnesium. None of these orbitals has an appreciable share on Mg, but some of them have a nonzero contribution at nitrogen atoms, which are bound to magnesium. It can be expected that the excitations where such orbitals are involved are more prone to larger changes after complexation. However, the perusal at the list of major configurations for most dimer excitations, with a possible exception of two lowest states, shows no clear leader among ACS Paragon Plus Environment

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electron promotions, therefore, one cannot deduce clear interpretations of energy and intensity changes based on orbital shapes only. Luckily, the analysis of CT coefficients is more useful in this aspect (see Figure 6 for the BF0 case and figures in the Supporting Information for the remaining structures). For all the cases the lowest two excitations turn out to be of the Frenkel (i.e. local) type, what means that although the dimer orbitals involved in these two lowest excitations are delocalized over both macrocycle rings for the majority of the structures, these excitations are composed of two local: macrocycle ring(monomer 1)→macrocycle ring(monomer 1) and macrocycle ring(monomer 2)→macrocycle ring(monomer 2) parts. According to the transition-density analysis, the next pair of states (third and fourth one) is strictly localized on either one, or the second monomer (and within the monomer – in the macrocycle ring). The cross (CT) excitations, i.e. macrocycle ring(monomer 2)→macrocycle ring(monomer 1) and vice versa are absent for the lowest states, and one should go as far as to the fifth and sixth excited state to find such type of excitations for the BB0 complex, but even then they contribute only partially to the total excitation pattern, while the major excitations have still a local character (see Figure 6). It should be noted that a clear correspondence between the monomer and dimer states breaks down after the second pair of states for the BB series. The third monomer excitation amounts to 3.4 eV, while for all the dimers the fifth state is much lower in energy (it has the excitation energy of 2.6 eV). As the result, much more states with nonzero oscillator strengths appear in the visible range for BB. Therefore, the dimerization – with or without water ligands – appears to increase the possibility of visible light harvesting in these cases. This increase is moderate because of rather small oscillator strengths of these excitations. The intensity pattern for hydrated and unhydrated complexes within the same series shows significant differences. As can be seen from the figure, the spectra of complexes with two, one, or zero water molecules should be distinguishable based on changes in intensities of various peaks, especially in the UV region. On the other hand, the comparison of excitation energies of spectra of the unhydrated complex from the series and the corresponding Chla· · · iChla complex shows that for some states (e.g. first and third) the “normal” (BB0) complex is more redshifted than INV, while changes in the oscillator strengths are smaller. All the states under study do not reveal any significant contribution from water molecules. Therefore, the influence of hydration on the electronic excitations has a rather indirect character ACS Paragon Plus Environment

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and can be attributed to geometry modifications and fluctuations of the electron density in the ground state. However, this influence is more than enough to modify the spectrum through changes in oscillator strengths. If spectra for the same series are compared, such differences can be seen more clearly, especially if one focuses on higher excitations. An indirect influence of water environment has been additionally tested by performing additional TD-DFT calculations.

The resulting

spectra (see the Supporting Information) show that in the present case the influence of the water solvent does not lead to significant changes in the spectra of the dimers. The shift of the lowest four lines (usually, but not always a redshift) does not exceed 0.03 eV. Also the intensity changes are not large for the lowest states. A more significant difference is observed for the third excited state of the monomer: here the redshift of about 0.1 eV is observed. An important observation is that the intensity of lower lines becomes significantly higher, what may be vital for visual light harvesting.

VCD spectra The VCD spectra for monomers (both unhydrated and with one water ligand) and for all the studied dimers are presented in Figures 7 and 8. A comparison of simulated spectrum for the unhydrated monomer reveals that it has two major regions: (i) wide and signal-rich profile for wave numbers up to about 1800 cm−1 , which can be further divided into those corresponding to the deformation of the macrocycle ring (usually up to 1000 cm−1 ) and those attributed to the side-chain vibrations (usually showing up in a higher wave number region), (ii) the stretching and bending of the C – H bond at about 3000 cm−1 . For the un-ligated chlorophyll, the VCD signals in the range 1000÷1200 cm−1 correspond to the vibrations involving chiral carbon atoms of the pyrrole rings I and II and the substituents of these rings. A strong positive and negative signals at 1770-1776 cm−1 correspond to the vibrations at the C-132 carbon atom from the III pyrrole ring (mostly involving the – COOCH3 group) and the – COOCH3 phytyl attachement site, which serve as chiral centers of the molecule. A smaller peak at about 3000 cm−1 can be attributed to the stretching of the C – H bonds from alkyl groups substituting the Chla macrocycle. A similar spectrum was obtained for the Chla1 system, with an additional small negative peak emerging at about 3500 cm−1 , which corresponds to the O – H ACS Paragon Plus Environment

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vibrations of the water ligand. Let us now move to the analysis of the dimers’ VCD spectra, which are depicted in Figure 8. There are several common features in the VCD spectra in all considered groups of dimers: BB, BF, INV and monomers. The spectra of the BB2, BB1, BB0, and BBC structures are characterized by the intensive negative and positive peaks at about 1200 cm−1 , emerging from a plethora of lowerintensity peaks for wave numbers up to about 1800 cm−1 .

They correspond to the vibrations

involving chiral carbon atoms of the pyrrole rings III and IV and isocyclic ring as well as their substituents. This broad band ends with the pair of very intensive positive and negative peaks at about 1750 cm−1 arising from the vibrations of the carbonyl groups of the isocyclic ring and macrocycles’ substituents.

Additionally, the spectra contain the small, broad peak at about

3000 cm−1 , which should be attributed to the stretching of the alkyl C – H bonds. The small peak at about 3500 cm−1 results from the presence of the O – H vibrations of water molecules in the BB2 and BB1 complexes. A pair comprising one negative and one positive peak at circa 1700 cm−1 is the characteristic feature of the simulated spectra for the BF2, BF1, and BF0 dimers. This feature arises of the coupled motions of the isocyclic rings of both Chla molecules. The peaks of the highest intensity refer to the vibrations of the substituents of the III and IV pyrrolic rings. The peak at about 3500 cm−1 resulting from the O – H vibrations in water is much weaker than the respective BB dimers. In BFC the water peak is very weak. In the spectrum of the BBC aggregate additional very intensive and broad negative and positive peaks at about 3600 cm−1 , arising from water vibrations, appear and they are the characteristic feature of this structure. Finally, a comparison of the VCD spectrum of the INV dimer with other simulated spectra allows to find some unique features for this case. Namely, although the broad band till about 1700 cm−1 with the strong peaks at about 1200 cm−1 is similar to the ones computed for BB and BF structures, the end of this band is quite characteristic in its shape – it ends with the doublet of a low intensity, which results from carbonyl vibrations. Summarizing, we can thus conclude that the VCD spectroscopy may be used to distinguish which type of the dimer (BB, BF, INV) is created, but not to tell how many water molecules it contains, since the features corresponding to water molecules are too weak and too similar ACS Paragon Plus Environment

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among the aggregates. The comparison of the presented VCD spectra with experimental ones is not possible, because up to our best knowledge, VCD spectra of Chla dimers with water are not available in the literature. Therefore our theoretical results might serve as a prediction, to be verified by experimentalists in the future.

Summary Our theoretical studies on different dimers of Chla, which may be formed in the presence of water, reveal that the unhydrated dimer has the highest stability, since the magnesium ion forms the strongest coordination bond with the carbonyl group of another monomer or with its pheophytin group. However, the structures with the water ligand attached to magnesium are also possible, although somewhat less stable. The stability of the hydrated Chla could prohibit a creation of the most stable form of the dimer because of its involvement in a magnesium coordination. The presence of Mg ion is crucial for the stabilization of dimers, as revealed by the F-SAPT energy decomposition scheme. It was shown that Chla molecules without central magnesium ions interact one with another about three times weaker. This points to the importance of a central metal atom in chlorophylls and bacteriochlorophylls via facilitating the formation of their dimers or aggregates. Our finding supplements earlier studies indicating that the presence of the light Mg atom does not influence much the spectral properties of the macrocyclic ligands (i.e. chlorin or bacteriochlorin, respectively), 78 but it enables the attachment of Chla to the protein environment due to its coordinative properties, 48 and maybe partly responsible for their stability because of its central position in the macrocycle. 79 The π-π stacking (identified in F-SAPT as the interaction of macrocycle rings) is the most significant attractive contribution of the interaction energy for backto-back structures, but it is only of a secondary importance for the most stable dimer structure, for which the coordination bond plays the major role. The mostly destructive role of water ligands in creating a bonding between Chla’s can be seen not only in the F-SAPT decomposition, but also from the QTAIM analysis of the bond paths. Both UV-Vis and VCD spectra of the dimers show many interesting features, which may be used to differentiate between the dimer structures, as well as recognize whether the spectrum has been recorded from the dimer or monomer, hydrated or unhydrated. The influence of water on ACS Paragon Plus Environment

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the electronic spectrum is of an indirect type and can be attributed to geometry changes under complexation, while the dimerization of two Chla monomers results in doubling of the monomer peaks and, in many cases, in intensity borrowing between these peaks. This second feature is strongly structure-dependent and can be proposed as a fingerprint of a given dimer structure. Finally, in literature one observes an increasing interest for devising an accurate description of the interaction between chlorophylls (and related molecules) and with solvent molecules both with MM/MD 80–82 as well as coarse-grain methods. 83 We hope that the presented SAPT and DFT results can serve as a benchmark for the development of force fields suitable for the description of the photosynthetic pigments, as it is believed that only advanced parametrization techniques might yield input to computational methods, which would correctly predict the properties of chlorophylls and bacteriochlorophylls. 84

Acknowledgments The support from the National Science Centre of Poland through grant 2015/19/B/ST4/01812 is gratefully acknowledged. This research was supported in part by PL-Grid Infrastructure.

Supporting Information UV-Vis spectra: Figures S1,S3 (in water), Figures S2,S4 (in methanol); molecular orbitals: Figures S5-S15; spatial intensities of excited states: Figures S16-S26; SAPT interaction energies: Table S1; DFT supermolecular interaction energies: Table S2; excitation energies: Table S3 (in water), Table S4 (in methanol); characters of the excitations: Table S5 (monomer), Table S7 (complexes); static polarizability: Table S6; optimized geometries: Tables S8-S16; F-SAPT partitioning: Tables S17-S26.

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Tables and Figures Table 1: Components of the SAPT interaction energy1 and the stabilization energies for the complexes under study in the CBS limit (see the text). Structure

(1)

(2)

Eexch

(2)

Eind

(2)

Eexch−ind

(2)

Edisp

Eexch−disp

ESAPT int

∆ZPE

Edef

Estab

−158.4 −138.8 −133.2 −139.7

327.6 314.1 315.0 315.3

−162.1 −133.1 −125.6 −134.8

139.4 118.1 113.4 119.5

−330.7 −328.2 −330.4 −329.2

48.1 46.5 46.4 46.6

−22.7 −22.9 −22.4 −23.0

−158.8 −144.3 −136.8 −145.2

5.8 4.7 −1.6 4.7

41.3 32.2 39.3 67.2

−117.5 −112.1 −97.6 −78.0

BF0 BF1 BF2 BFC

−268.3 −249.5 −228.6 −247.1

348.8 344.9 342.3 344.2

−294.0 −265.8 −235.3 −263.0

230.9 210.8 189.4 209.2

−247.1 −253.4 −261.5 −254.4

34.4 35.3 36.5 35.3

−19.8 −19.6 −19.6 −19.5

−215.0 −197.4 −176.7 −195.2

3.9 −0.5 −3.0 0.3

93.6 103.7 119.1 148.8

−121.4 −93.7 −57.6 −46.4

INV

−154.5

329.9

−157.7

135.9

−336.2

48.2

−23.3

−157.6

5.6

38.1

−119.6

1

Eelst

(1)

BB0 BB1 BB2 BBC

δEHF

Energies are in kJ/mol.

Table 2: CAM-B3LYP/def2-TZVP excitation energies1 (in vacuum) followed by oscillator strengths in parenthesis for the lowest ten excited states of the considered systems. BB0 1.69 1.87 2.33 2.41 2.56 2.71 3.05 3.14 3.27 3.30

1

(0.04) (0.22) (0.01) (0.04) (0.02) (0.02) (0.01) (0.02) (0.04) (0.34)

BB1 1.67 1.87 2.32 2.40 2.43 2.86 2.97 3.10 3.28 3.37

(0.04) (0.23) (0.01) (0.02) (0.06) (0.02) (0.01) (0.03) (0.27) (0.02)

BB2 1.67 1.86 2.28 2.40 2.49 2.76 2.98 3.09 3.27 3.29

(0.04) (0.23) (0.01) (0.06) (0.02) (0.02) (0.01) (0.02) (0.23) (0.13)

BBC 1.67 1.87 2.32 2.41 2.43 2.85 2.98 3.10 3.29 3.36

(0.04) (0.23) (0.01) (0.02) (0.06) (0.02) (0.01) (0.03) (0.29) (0.01)

BF0 1.80 1.88 2.45 2.46 3.28 3.33 3.38 3.40 3.58 3.64

(0.13) (0.22) (0.01) (0.08) (0.12) (1.10) (0.28) (0.08) (0.80) (0.09)

BF1 1.78 1.87 2.36 2.44 3.24 3.27 3.34 3.44 3.54 3.65

(0.12) (0.21) (0.04) (0.05) (0.09) (0.59) (0.81) (0.03) (0.72) (0.22)

BF2 1.77 1.85 2.35 2.39 3.24 3.28 3.35 3.37 3.51 3.66

(0.12) (0.21) (0.04) (0.05) (0.20) (0.91) (0.29) (0.06) (0.67) (0.38)

BFC 1.79 1.88 2.39 2.43 3.22 3.28 3.33 3.50 3.54 3.61

INV

(0.12) (0.20) (0.05) (0.05) (0.04) (0.47) (0.96) (0.01) (0.74) (0.11)

1.76 1.86 2.39 2.42 2.60 2.68 3.06 3.09 3.21 3.40

(0.04) (0.19) (0.02) (0.02) (0.01) (0.05) (0.03) (0.07) (0.07) (0.27)

Chla0 1.84 2.44 3.41 3.64 3.79 4.02 4.05 4.33 4.61 4.70

(0.23) (0.03) (1.07) (0.33) (0.95) (0.00) (0.00) (0.19) (0.07) (0.13)

Chla1 1.85 2.43 3.38 3.67 3.73 3.99 4.11 4.30 4.52 4.69

(0.21) (0.05) (0.80) (0.43) (0.82) (0.01) (0.01) (0.21) (0.08) (0.15)

Energies are in eV.

(a) Chla0

(b) Chla1

Figure 1: Optimized B97-D/def2-SVP geometries for the studied structures of the methyl chlorophyllide a monomers. The five-membered rings with nitrogen atoms are numbered from I to IV counterclockwise, where number I corresponds to the ring opposite to the isocyclic ring (i.e. the pentagon comprised of carbon atoms only). The phytyl binding site is attached to the ring IV.


39


Page 40 of 46

(a) BB0

(b) BF0

(c) BB1

(d) BF1

(e) BB2

(f) BF2

(g) BBC

(h) BFC

(i) INV

Figure 2: Optimized B97-D/def2-SVP geometries for the studied structures of the methyl chlorophyllide a dimers. ACS Paragon Plus Environment

40

Page 41 of 46

(a)

(b)

Figure 3: The ESP at the electron density isosurface (ρ = 0.001 a.u.) for the methyl chlorophyllide a monomer (back – (a) and face – (b)). The color scale from blue to red corresponds to the positive to negative values of the potential.

1.2

1.2

1

1

0.8

0.8

Intensity

Intensity

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


0.6

0.6

0.4

0.4

0.2

0.2

0

0 1.5

2

2.5

3

3.5

4

4.5

5

1.5

Energy [eV]

2

2.5

3

3.5

4

4.5

5

Energy [eV]

(a) Chla0

(b) Chla1

Figure 4: Simulated CAM-B3LYP/def2-TZVP UV-Vis spectra (in vacuum) for the studied structures of the methyl chlorophyllide a monomers.


41

Journal of Chemical Information and Modeling 0.4

1.4

0.35

1.2

0.3 1

Intensity

Intensity

0.25

0.2

0.8

0.6

0.15 0.4 0.1 0.2

0.05

0

0 2

2.5

3

3.5

1.5

2

2.5

3

Energy [eV]

Energy [eV]

(a) BB0

(b) BF0

0.3

1.2

0.25

1

0.2

0.8

Intensity

Intensity

1.5

0.15

3.5

4

3.5

4

3.5

4

0.6

0.1

0.4

0.05

0.2

0

0 1.5

2

2.5

3

3.5

1.5

2

2.5

3

Energy [eV]

Energy [eV]

(c) BB1

(d) BF1

0.4

1.2

0.35 1 0.3 0.8

Intensity

Intensity

0.25

0.2

0.6

0.15 0.4 0.1 0.2 0.05

0

0 1.5

2

2.5

3

3.5

1.5

2

2.5

Energy [eV]

Energy [eV]

(e) BB2

(f) BF2

0.3

3

1.4

1.2

0.25

1

Intensity

0.2

Intensity

0.15

0.8

0.6

0.1 0.4

0.05

0.2

0

0 1.5

2

2.5

3

3.5

1.5

Energy [eV]

2

2.5

3

3.5

4

Energy [eV]

(g) BBC

(h) BFC 0.3

0.25

0.2

Intensity

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 42 of 46

0.15

0.1

0.05

0 1.5

2

2.5

3

3.5

Energy [eV]

(i) INV

Figure 5: Simulated CAM-B3LYP/def2-TZVP UV-Vis (in vacuum) spectra for the studied structures of the methyl chlorophyllide a dimers. ACS Paragon Plus Environment

42

m-ring(2)

m-ring(2) CO2CH3(2)

CH3-4(2)

CH3-4(2)

CH3-3(2)

CH3-3(2)

CH3-3(2)

CHCH2(2)

CHCH2(2)

CH3-2(2)

CH3-2(2)

CH3-2(2)

CH3-1(2) m-ring(1)

phytyl(1)

CH3-4(1)

CH3-4(1)

CH3-3(1)

CH3-3(1)

CHCH2(1)

CHCH2(1)

(b) Excited state 2

m-ring(2)

CH3-4(2) CH3-3(2)

0.5

CHCH2(2)

CHCH2(2)

CH3-2(2)

CH3-2(2)

CH3-2(2) 0.4

CH2CH3(2) CH3-1(2)

CH3-1(2)

m-ring(1)

m-ring(1) 0.3

CO2CH3(1)

CH3-3(1)

(e) Excited state 5

m-ring(2)

CH3-4(2) CH3-3(2)

0.5

CHCH2(2)

CHCH2(2)

CH3-2(2)

CH3-2(2)

CH3-2(2) 0.4

CH2CH3(2) CH3-1(2)

CH3-1(2)

m-ring(1)

m-ring(1) 0.3

CO2CH3(1) phytyl(1)

0.2

CH3-4(1)

0.2

CH3-4(1)

CH3-3(1)

CH3-3(1)

CH3-3(1)

CHCH2(1)

CHCH2(1)

CHCH2(1)

0.1

CH3-2(1)

0.1

CH3-2(1) CH2CH3(1) CH3-1(1)

(g) Excited state 7

0.1

CH3-2(1)

CH3-1(1)

0.0 CH3-1(1)

m-ring(2)

CO2CH3(2)

CH3-4(2)

phytyl(2)

CH3-3(2)

CHCH2(2)

CH3-2(2)

CH3-1(2)

m-ring(1)

CH2CH3(2)

CH3-4(1)

phytyl(1)

CO2CH3(1)

CH3-3(1)

CH3-2(1)

0.0 CH3-1(1)

m-ring(2)

CO2CH3(2)

CH3-4(2)

phytyl(2)

CH3-3(2)

CHCH2(2)

CH3-2(2)

CH3-1(2)

m-ring(1)

CH2CH3(2)

CH3-4(1)

phytyl(1)

CO2CH3(1)

CH3-3(1)

CH3-2(1)

CH3-1(1)

CHCH2(1)

0.0

CHCH2(1)

CH3-1(1)

0.2

CH2CH3(1)

CH2CH3(1)

CH2CH3(1)

m-ring(2)

phytyl(1)

(h) Excited state 8

m-ring(2)

CH3-4(1)

0.3

CO2CH3(1)

CO2CH3(2)

0.3

phytyl(1)

0.4

CH2CH3(2)

CH3-1(2) m-ring(1) CO2CH3(1)

0.5

CH3-4(2)

0.4

m-ring(2)

CH3-3(2)

CHCH2(2)

CH2CH3(2)

CH3-4(2)

CH3-4(2)

phytyl(2)

0.5

0.6

phytyl(2)

CH3-3(2)

CH3-3(2)

CO2CH3(2)

CO2CH3(2) 0.6

phytyl(2)

CHCH2(2)

CH3-4(2)

CH3-4(2)

m-ring(2)

CO2CH3(2) 0.6

phytyl(2)

(f) Excited state 6

CH3-2(2)

m-ring(2) CO2CH3(2) phytyl(2)

0.0 CH3-1(1)

m-ring(2)

CO2CH3(2)

CH3-4(2)

phytyl(2)

CH3-3(2)

CHCH2(2)

CH3-2(2)

CH3-1(2)

m-ring(1)

CH2CH3(2)

CH3-4(1)

phytyl(1)

CO2CH3(1)

CH3-3(1)

CH3-2(1)

CH3-1(1)

(d) Excited state 4

CHCH2(1)

CH2CH3(1)

m-ring(2)

CO2CH3(2)

CH3-4(2)

phytyl(2)

CH3-3(2)

CHCH2(2)

CH3-2(2)

CH3-1(2)

m-ring(1)

CH2CH3(2)

CH3-4(1)

phytyl(1)

CO2CH3(1)

CH3-3(1)

CH3-2(1)

CH3-1(1)

CHCH2(1)

CH2CH3(1)

0.0

CH3-3(2)

CH3-1(1) CHCH2(2)

CH2CH3(1)

CH3-1(1)

CH3-2(2)

CH2CH3(1)

CH3-1(1)

0.0

0.1

CH3-2(1)

CH2CH3(1)

CH3-1(2)

0.1

CH3-2(1)

0.2

CH3-1(2)

0.1

CH3-2(1)

CO2CH3(2)

CH3-4(1)

CHCH2(1)

m-ring(1)

0.2

CH3-3(1) CHCH2(1)

CH2CH3(2)

CH3-4(1)

CH3-3(1) CHCH2(1)

m-ring(1)

0.2

phytyl(1)

CH2CH3(2)

CH3-4(1)

0.3

CO2CH3(1)

CH3-4(1)

phytyl(1)

phytyl(1)

0.3

phytyl(1)

0.4

CH2CH3(2)

CH3-1(2) m-ring(1) CO2CH3(1)

0.5

CO2CH3(1)

0.4

CH3-3(2)

CH3-3(2)

CHCH2(2)

CH2CH3(2)

phytyl(2)

CH3-4(2)

CH3-4(1)

0.5

0.6

phytyl(2)

phytyl(1)

CH3-3(2)

CH3-2(2)

CO2CH3(2) 0.6

phytyl(2)

CO2CH3(1)

CH3-4(2)

CHCH2(2)

m-ring(2)

CO2CH3(2) 0.6

CH3-1(2)

(c) Excited state 3

CH2CH3(1)

m-ring(2) CO2CH3(2) phytyl(2)

0.0 CH3-1(1)

m-ring(2)

CH3-4(2)

CO2CH3(2)

CH3-3(2)

phytyl(2)

CH3-2(2)

CHCH2(2)

CH3-1(2)

m-ring(1)

CH2CH3(2)

CH3-4(1)

CH3-3(1)

phytyl(1)

CO2CH3(1)

CH3-2(1)

CH3-1(1)

(a) Excited state 1

CHCH2(1)

CH2CH3(1)

m-ring(2)

CH3-4(2)

CO2CH3(2)

CH3-3(2)

phytyl(2)

CH3-2(2)

CHCH2(2)

CH3-1(2)

m-ring(1)

CH2CH3(2)

CH3-4(1)

CH3-3(1)

phytyl(1)

CO2CH3(1)

CH3-2(1)

CH3-1(1)

CHCH2(1)

CH2CH3(1)

0.0

m-ring(1)

CH3-1(1) CH2CH3(2)

CH2CH3(1)

CH3-1(1)

0.0

0.1

CH3-2(1)

CH2CH3(1)

CH3-1(1)

CH3-4(1)

0.1

CH3-2(1)

CH2CH3(1)

CH3-3(1)

0.1

CH3-2(1)

0.2

CH3-3(1)

0.2

CH3-3(1) CHCH2(1)

CH3-3(1)

0.2

0.3

CO2CH3(1)

phytyl(1)

CH3-4(1)

phytyl(1)

0.3

CO2CH3(1)

phytyl(1)

CH3-2(1)

0.3

CO2CH3(1)

0.4

CH2CH3(2)

CH3-1(2) m-ring(1)

CO2CH3(1)

0.4

CH2CH3(2)

CH3-1(2) m-ring(1)

CHCH2(1)

0.4

CH2CH3(2)

0.5

CH3-2(1)

0.5

CHCH2(2)

CH3-2(1)

0.5

0.6

phytyl(2)

CH3-4(2)

CHCH2(1)

0.6

phytyl(2)

CH2CH3(1)

CO2CH3(2) 0.6

phytyl(2)

CHCH2(1)

m-ring(2) CO2CH3(2)

CH2CH3(1)

(i) Excited state 9

m-ring(2) CO2CH3(2) 0.6

phytyl(2) CH3-4(2) CH3-3(2)

0.5

CHCH2(2) CH3-2(2) 0.4

CH2CH3(2) CH3-1(2) m-ring(1)

0.3

CO2CH3(1) phytyl(1) CH3-4(1)

0.2

CH3-3(1) CHCH2(1) 0.1

CH3-2(1) CH2CH3(1) CH3-1(1) m-ring(2)

CO2CH3(2)

CH3-4(2)

phytyl(2)

CH3-3(2)

CHCH2(2)

CH3-2(2)

CH3-1(2)

m-ring(1)

CH2CH3(2)

CH3-4(1)

phytyl(1)

CO2CH3(1)

CH3-3(1)

CH3-2(1)

CH3-1(1)

CHCH2(1)

0.0 CH2CH3(1)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


CH2CH3(1)

Page 43 of 46

(j) Excited state 10

Figure 6: The classification of the spatial intensities of the first ten excited states for BF0. ACS Paragon Plus Environment

43


200

100

150 0

100

-100

Intensity

50

Intensity

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 44 of 46

0

-200

-50 -300

-100

-400 -150

-200

-500 0

500

1000

1500

2000

2500

3000

3500

4000

0

500

Wave number

1000

1500

2000

2500

3000

3500

4000

Wave number

(a) Chla0

(b) Chla1

Figure 7: Simulated B97-D/def2-SVP VCD spectra for the studied structures of the methyl chlorophyllide a monomers.


44

Page 45 of 46 600

800

400

600

200 400

Intensity

Intensity

0 200

-200

0

-400

-200 -600

-400

-800

-1000

-600 500

1000

1500

2000

2500

3000

3500

4000

0

500

1000

1500

2000

Wave number

Wave number

(a) BB0

(b) BF0

600

1000

400

800

200

600

0

400

Intensity

Intensity

0

-200

2500

3000

3500

4000

2500

3000

3500

4000

2500

3000

3500

4000

2500

3000

3500

4000

200

-400

0

-600

-200

-800

-400

-1000

-600 0

500

1000

1500

2000

2500

3000

3500

4000

0

500

1000

1500

2000

Wave number

Wave number

(c) BB1

(d) BF1

600

800

600

400

400 200

Intensity

Intensity

200 0

-200

0

-200

-400 -400

-600

-600

-800

-800 0

500

1000

1500

2000

2500

3000

3500

4000

0

500

1000

1500

2000

Wave number

Wave number

(e) BB2

(f) BF2

600

1000

800

400

600 200

Intensity

400

Intensity

0

-200

200

0

-400 -200

-600

-400

-800

-600 0

500

1000

1500

2000

2500

3000

3500

4000

0

500

1000

1500

2000

Wave number

Wave number

(g) BBC

(h) BFC 400

300

200

Intensity

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


100

0

-100

-200 0

500

1000

1500

2000

2500

3000

3500

4000

Wave number

(i) INV

Figure 8: Simulated B97-D/def2-SVP VCD spectra for the studied structures of the methyl chlorophyllide a dimers. ACS Paragon Plus Environment

45


Graphical TOC


46

Page 46 of 46

Dimerization Behavior of Methyl Chlorophyllide a as the Model of

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