Ultrafast Dynamics of Manganese(III), Manganese(II), and Free-Base

Article pubs.acs.org/IC

Ultrafast Dynamics of Manganese(III), Manganese(II), and Free-Base Bacteriochlorin: Is There Time for Photochemistry? Fabio A. Schaberle,†,‡ Artur R. Abreu,† Nuno P. F. Gonçalves,† Gonçalo F. F. Sá,§ Mariette M. Pereira,‡ and Luís G. Arnaut*,‡ †

Luzitin SA, Ed. Bluepharma, S. Martinho do Bispo, 3045-016 Coimbra, Portugal Chemistry Department, University of Coimbra, 3004-535 Coimbra, Portugal § LaserLeap SA, IPN, R. Pedro Nunes, 3030-199 Coimbra, Portugal ‡

S Supporting Information *

ABSTRACT: Manganese(III) and manganese(II) complexes of halogenated sulfonamide tetraphenylbacteriochlorins were prepared for the first time via a transmetalation reaction and shown to be stable at room temperature. The behavior of the electronic states of the paramagnetic complexes is remarkably different from those of the metal-free bacteriochlorins or diamagnetic metallobacteriochlorins. The Mn3+ complex exhibits eight electronic transitions between different states from 300 to 1100 nm, with a very prominent band (molar absorption coefficient of ca. 50000 M−1 cm−1) at 829 nm. Ultrafast transient absorption showed the formation of an excited singquintet state that decays to a tripquintet state with a femtosecond lifetime. The tripquintet state decays in 5 ps, yielding a tripseptet state with a 570 ps lifetime. The electronic absorption of the Mn2+ complex more closely resembles those of diamagnetic metallobacteriochlorins, but the longest decay lifetime is only ca. 8 ps. The intense photoacoustic waves generated with near-infrared excitation suggest the use of these complexes in photoacoustic tomography.

I. INTRODUCTION Photomedicine, solar energy conversion, and photocatalysis have driven the search for dyes with strong near-infrared (NIR) absorption over the past decade. The steep increase in the transparency of human tissues from the visible to the NIR,1 the absence of endogenous NIR fluorescence,2 the peak of the spectral solar photon flux in the NIR,3 and photocatalytic H2 production under NIR light4 are a few observations that suggest important applications of NIR-absorbing dyes. Although remarkable advances have been made in tailoring NIRabsorbing dyes, namely, free-base bacteriochlorins and freebase and metalated phthalocyanines for various applications, only a few studies on metallobacteriochlorins have been published.5,6 On the basis of the properties of p-type hyperporphyrins,7 it can be expected that p-type hyperbacteriochlorins have red-shifted absorption bands as well as extra charge-transfer (CT) bands with respect to their free-base analogues. Manganese(III) porphyrins are representative of ptype hyperporphyrins, revealed enhanced two-photon absorption,8 photocatalytic reactivity,9 photoreduction to manganese(II),10 and useful behavior as photoacoustic (PA) references,11,12 and are employed in the fabrication of efficient piezophotonic materials.13 The exceptional spectroscopic and photochemical properties of manganese(III) porphyrins motivated the synthesis of the first manganese(III) and © XXXX American Chemical Society

manganese(II) bacteriochlorins, reported in this work, together with the study of their spectroscopy and excited-state dynamics. Bacteriochlorins are derived from porphyrins by the reduction of two diagonally opposite double bonds of the pyrrole rings. This reduction preserves the basic chromophore of these macrocycles but introduces a skeletal distortion that destabilizes the highest occupied molecular orbital (HOMO; labeled au in D2h symmetry) and lifts the degeneracy of the lowest unoccupied molecular orbital LUMO (labeled b2g and b3g in D2h symmetry). Thus, bacteriochlorins show an intense (Qy) absorption band in the NIR, another band (Qx) in the green, and a split Soret band (Bx and By bands) in the UV, whereas the corresponding Q bands of porphyrins are observed in the green and red with much weaker intensities, and one intense Soret is observed ca. 420 nm.14 The advantage of the intense NIR absorption is exploited by bacteriochlorophyll e of green sulfur bacteria to survive under conditions where one bacterium receives 1012 less photons per second than the leaf of a plant on the Earth’s surface.15 The ability of bacteriochlorins to harvest photons at wavelengths where the solar photon flux is higher inspired the development of bacteriochlorins for dyesensitized solar cells.16 NIR light also has the ability to Received: November 26, 2016

A

DOI: 10.1021/acs.inorgchem.6b02871 Inorg. Chem. XXXX, XXX, XXX−XXX

Article

Inorganic Chemistry Chart 1. Alternative Synthetic Routes for Bacteriochlorins

Chart 2. Representative Porphyrin, Bacteriochlorin, and Manganese(III) Complexes Studied in This Worka

a

The manganese(II) complex analogous to (Cl)MnCl2BMet2 was also studied. The wavelength of the lowest-energy band is also shown for each compound.

B


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Inorganic Chemistry

Figure 1. Energy ordering of molecular orbitals (in D4h symmetry for a simpler comparison) of tetraphenylporphyrins, bacteriochlorins, and their manganese(III) complexes.

Cd(OAc)2. Then, cadmium bacteriochlorophyll was transformed in the desired metal complexes by the addition of excesses of its metal chloride. Later, Scherz and co-workers described the synthesis of several metal complexes including the manganese(III) complex of a water-soluble bacteriochlorophyll for application in vascular-target PDT.38 Pandey and coworkers also used the transmetalation approach to prepare the palladium(II) complex of bacteriopurpurin,39 which is a bacteriochlorin containing a fused six- or five-membered diketo or imide ring. Lindsey and co-workers described the synthesis of β-alkyl-substituted stable metallobacteriochlorins using a slight modification of this transmetalation method, involving the use of a strong base in tetrahydrofuran to promote deprotonation of the bacteriochlorin NH, followed by the addition of the desired metal salt.6 Using this approach, Lindsey and co-workers prepared zinc(II), palladium(II), copper(II), and indium(III) complexes with yields of around 80%. In this work, the synthesis of stable halogenated sulfonamide manganese(II) and manganese(III) bacteriochlorins, shown in Chart 2, was achieved with synthetic modifications of the transmetalation approach. The metalation of porphyrins is accompanied by deprotonation of the central NH bonds and increases the symmetry of the macrocycle, from D2h to D4h symmetry. In “regular” metalloporphyrins, the electrons in metal d orbitals perturb only weakly the π electron of the porphyrin ring and absorption spectra resemble that of free-base porphyrins. In hypsopophyrins, the filled eg(dxz,dyz) orbital mixes with the empty eg(π*) of the ring, raises its energy, and produces a blue shift of the absorption bands with respect to the free-base porphyrin. On

penetrate deeply in human tissues, and bacteriochlorins have also been used in the photodynamic therapy (PDT) of cancer.17 For example, padeliporfin is being used in the PDT of prostate cancer18 and redaporfin in head and neck cancer.19−22 The possible use of bacteriochlorins in multiple NIR applications motivated many research groups to develop synthetic processes. The approaches published can be divided into three main groups: (i) derivatization from natural or synthetic β-substituted porphyrins,23−26 (ii) derivatization of synthetic meso-arylporphyrins,27−29 and (iii) the total synthesis of dimethylbacteriochlorins.30 Although natural metallobacteriochlorins play a key role in bacterial photosynthetic processes and it is widely recognized that metalation may modulate the oxidation potential and stabilize the bacteriochlorins against oxidation, the synthesis of metallobacteriochlorophylls remains a challenge. Three methodologies, shown in Chart 1, were published for the synthesis of metallobacteriochlorins: (i) direct metalation and metal-ion templating,31−34 (ii) postmodification,35 and (iii) transmetalation.36 Although the direct metal salt method is the most attractive, its application in the synthesis of bacteriochlorins often leads to a complex mixture of compounds due to isomer formation. The transmetalation process, introduced by Scheer and co-workers in 1998,36 is an interesting alternative. In his pioneering work, Scheer isolated the natural magnesium bacteriochlorophylls from Rhodobacter sphaeroides,37 followed by demetalation of the magnesium with the addition of glacial acetic acid, dissolution of the free base in dimethylformamide (DMF), under a rigorous argon atmosphere, and reflux in the presence of excess anhydrous C


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Inorganic Chemistry Chart 3. Synthesis of (Cl)MnCl2BMet2

the conditions required for transmetalation reactions, and this bacteriochlorin was used to obtain manganese(III) complexes. In a typical experiment, the bacteriochlorin was dissolved in dry DMF, and the solution was added to a suspension of calcium hydride in DMF. Then the reaction was heated at 100 °C for 1 h under an argon atmosphere. After cooling, an excess of manganese chloride was added, and the reaction was heated at 100 °C for 2 h. After cooling, the crude material was dissolved in dichloromethane and subsequently washed with water (three times). The organic layer was dried over anhydrous sodium sulfate and filtered, and the solvent was removed. The mixture of manganese(II) and manganese(III) bacteriochlorins thus obtained was completely transformed into the corresponding manganese(III) bacteriochlorin by the slow addition of H2O2 at room temperature (Chart 3), monitoring the extension of the reaction by the disappearance of the UV/ vis band at ∼750 nm. After a solvent−solvent extraction with water (three times), the organic layer was dried over anhydrous sodium sulfate and filtered. Evaporation of solvent and recrystallization using dichloromethane/pentane gave the respective manganese(III) bacteriochlorin. II.B. Spectroscopy. Figure 2 presents absorption spectra of representative free-base and manganese porphyrins and bacteriochlorins studied in this work. The features of freebase porphyrins and bacteriochlorins are straightforwardly interpreted by the four-orbital model developed by Gouterman.51 Configuration interaction causes the excitations from

the other hand, p-type hyperporphyrins have vacancies in the eg(dxz,dyz) orbitals that lead to extra absorption features in the visible or NIR. Figure 1 shows the molecular orbital relative energies of tetraphenylporphyrin (H2TPP), Mn3+TPP, tetraphenylbacteriochlorin (H2TPB), and Mn3+TPB, adapted from various sources,7,8,14,40,41 which are representative of the molecules presented in Chart 2 and studied in this work. Manganese(III) and manganese(II) porphyrin complexes are very weakly luminescent,42 and their electronically excited states have subnanosecond lifetimes.43−45 Hence, the excitedstate dynamics of the molecules in Chart 2 were studied using ultrafast transient absorption and time-resolved PA methods.

II. RESULTS AND DISCUSSION II.A. Manganese Bacteriochlorin Synthesis. Bacteriochlorins are prone to oxidation. Access to stable bacteriochlorins, which can be manipulated at room temperature and in the presence of light and oxygen, was enabled by the introduction of electron-withdrawing substituents in the phenyl rings of tetraphenylbacteriochlorins28,46−48 and by the introduction of a germinal dimethyl group in each reduced pyrroline ring.30,49,50 This work took advantage of the synthetic methodology developed for halogenated sulfonamide bacteriochlorins to obtain manganese(III) chelates. It was found that 5,10,15,20-tetrakis[2,6-dichloro-3-(N-dimethylsulfamoyl)phenyl]bacteriochlorin (Cl2BMet2) was particularly resistant to D


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Inorganic Chemistry

Figure 2. Absorption spectra in ethanol: (A) F2PMet; (B) F2BMet (also named LUZ11 or redaporfin); (C) Mn(Cl)TPP; (D) Mn(Cl)Cl2BMet2.

Table 1. Assignments of Main Electronic Transitions Observed from 300 to 1100 nm in Ethanol F2PMet

III, 638 nm, 15674 cm−1 IIIa, 582 nm, 17182 cm−1

V, 505 nm, 19802 cm−1

VII, 410 nm, 24390 cm−1

a

ClMnTPP

Qx(0,0) Qx(0,1)

I, 809 nm, 12361 cm−1 II, 709 nm, 14104 cm−1 III, 599 nm, 16694 cm−1 IIIa, 565 nm, 17699 cm−1 IV, 516 nm, 19380 cm−1

I, 1100 nm, 9100 cm−1 tripmultiplet

tripmultiplet

II, 985 nm, 10154 cm−1 III, 829 nm, 12063 cm−1 IIIa, 763 nm, 13106 cm−1 IV, 652 nm, 15337 cm−1 V, 585.5 nm, 17079 cm−1 VI, 477.5 nm, 20942 cm−1 VII, 373.5 nm, 26774 cm−1 VIII, 328 nm, 30488 cm−1

Q(0,0) Q(0,1)

III, 743.5 nm, 13450 cm−1 IIIa, 680 nm, 14706 cm−1

Qy(0,0) Qy(0,1)

(a1u, a2u) → (dxz, dyz) V, 505 nm, 19802 cm−1

V, 467 nm, 21413 cm−1 VI, 399 nm, 25063 cm−1 VII, 399 nm, 25063 cm−1

ClMnCl2BMet2

tripmultiplet

Qy(0,0)

B(0,0)

F2BMet

Qx(0,0)

B(0,0) B(0,0) a1u, a2u) → (dxz, dyz)

VII, 372.5 nm, 26846 cm−1 VIII, 345 nm, 28986 cm−1

Bx(0,0) By(0,0)

tripmultiplet Qy(0,0) Qy(0,1)a (a1u, a2u) → (dxz, dyz) Qx(0,0) (a1u, a2u) → (dxz, dyz) Bx(0,0) By(0,0)

There may also be a contribution from a manganese(II) bacteriochlorin impurity.

the two HOMOs to the two LUMOs to mix and split into a pair of low-energy and low-intensity (Qx and Qy) transitions and a pair of high-energy and high-intensity (Bx and By) transitions. In porphyrins, the two HOMOs (a1u and a2u in D4h symmetry) lie close in energy and the two LUMO (egx and egy in D4h symmetry) are even closer in energy, which make the Bx and By transitions merge into one single (Soret) band. The

reduction of the pyrrole positions in bacteriochlorins raises the energies of the egx and a1u orbitals as a result of a shortening of their π conjugation, while approximately maintaining the energies of the egy and a2u orbitals.52 Destabilization of the a1u orbital associated with the energy insensitivity of the egy orbital to the reduction of the pyrroles lowers the energy of the HOMO → LUMO transition in bacteriochlorins and is at the E


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Inorganic Chemistry

Figure 3. Mn2+Cl2BMet2 absorption and decay in acetonitrile. (A) Absorption spectrum, (B) EADS spectra (from Glotaran) obtained by global analysis with lifetimes of 0.9 and 7.6 ps, and (C) experimental spectra (Surface Explorer), both after excitation at 772 nm.

In view of the strong interaction between eg(dπ) and eg*(π) orbitals and of the variety of electronic transitions possible, it is not surprising that different assignments have been proposed for the bands observed in the absorption spectra of manganese(III) porphyrins. According to Boucher,40 the low-energy bands I and II are (a1u, a2u) → (dxz, dyz) transitions (near 780 nm) and a2u → dz2 transitions (near 680 nm), respectively.8,44 However, Gouterman questioned the CT character of these bands and ascribed them to tripmultiplets.7 The CT transition of the type (a1u, a2u) → (dxz, dyz) was believed to be at an energy higher than that of the Soret band. Band V was assigned to B(0,0) and band VII to a CT transition.7,52 Consequently, Gouterman assigned bands III and IIIa to Q(0,0) and Q(0,1), respectively, whereas Boucher assigned band III to the Q transition and band IIIa to the (a1u, a2u) → (dxz, dyz) transition. We assign the (a1u, a2u) → (dxz, dyz) transition to band IV. The remaining assignments of manganese(III) porphyrins agree with those proposed by Gouterman and are presented in Table 1. The energies of the d orbitals are not expected to change from high-spin manganese(III) porphyrins to manganese(III) chlorins to manganese(III) bacteriochlorins, but the (a1u, a2u) levels are no longer degenerate, the e*gx orbital rises in energy, and the energy of the a1u(π) orbital is much increased in the bacteriochlorin. Hence, we expect two (a1u, a2u) → (dxz, dyz) bands of lower energy than those in the manganese(III) porphyrin and also of lower intensity. If IV and VI are ligandto-metal CT bands, then band V must be the Qx band. According to this assignment, the (a1u, a2u) → (dxz, dyz) and lowest-energy Q transitions have a 4000 cm−1 bathochromic shift related to a 10 kcal mol−1 increase in the energy of the a1u(π) orbital of the bacteriochlorin relative to the porphyrin. The absorption spectrum of the corresponding manganese(II) bacteriochlorin, shown in Figure 3, resembles those of divalent metallobacteriochlorins,6 with the Qy(0,0) band at 760

origin of the red shift with respect to the porphyrin shown in Figure 2. The split of the eg orbitals into two nondegenerate orbitals contributes to the splitting of the Q and Soret (B) bands. The Q bands exhibit clear vibronic progressions. The presence of substituents in the phenyl groups has little effect in the spectra. The wavelengths and wavenumbers of the most prominent bands are presented in Table 1. Manganese(III) forms high-spin d4 complexes with porphyrins40 and chlorins.41 We assume that the same happens with the bacteriochlorins studied in this work. The lower-energy d orbitals, dxy (b2g in D4h symmetry), dxz and dyz (eg symmetry), and dz2 (a1g symmetry), have energies between those of the π and π* systems of the porphyrin and are half-filled. The dx2−y2 orbital (b1g symmetry), whose lobes are directed toward the four porphyrinato nitrogen atoms, is essentially antibonding, has an energy higher than that of the eg*(π) orbitals, and is unoccupied. The energetic proximity and proper symmetry favor mixing between the metal eg(dπ) orbitals and porphyrin eg*(π) orbitals. This mixing should depress the energy of the eg(dπ) orbitals, increase that of the eg*(π) orbitals, and enable the observation of porphyrin-to-metal CT bands.40 Moreover, the partially filled d orbitals of the metal interact with the porphyrin singlet and triplet states to generate sing- and tripmultiplets. The ground state is a quintet (5S0), the (π, π*) excitation of the porphyrin ring originates a quintet excited state, 5S1(π,π*), but the intersystem crossing enhanced by heavy-atom and paramagnetic effects gives access to the tripmultiplet manifold (3T1, 5T1, and 7T1). Furthermore, in addition to CT, singlet, and triplet states, there is the possibility of ligand-field (d, d) transitions. These transitions are of low intensity and are unlikely to be observed in the absorption spectra of manganese(III) porphyrins dominated by (π, π*), (π, d), and (d, π*) transitions, but low-energy (d, d) states may contribute to deactivate the observed higher-energy states. F


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Inorganic Chemistry

Figure 4. F2BMet absorption and decay in ethanol. (A) Absorption spectrum of F2BMet, (B) EADS spectra (from Glotaran) after excitation at 743 nm obtained by global analysis and associated with a lifetime of 2.2 ns and exceeding the 10 ns time window, (C) nanosecond transient absorption measured at 63 ns after excitation of the dye at the Qy band adapted from ref 19, and (D) decays of F2BMet at 607 and 664 nm.

nm and the Qx band at 560 nm. The small peak at 700 nm is assigned to the Qy(0,1) vibronic feature. The strongly antibonding dx2−y2 orbital is singly occupied in high-spin manganese(II) bacteriochlorins. This is likely to cause a large out-of-plane displacement of the Mn2+ ion and weaken CT transitions between the macrocycle π system and the metal d electrons. Metal bacteriochlorin π mixing is weak in manganese(II) bacteriochlorin, as in manganese(II) chlorin.41 Hence, the manganese(II) bacteriochlorin absorption spectrum is pseudonormal, i.e., similar to that of diamagnetic metallobacteriochlorins but with weak underlying CT bands. The assignment of the Q bands is supported by the energetic order of the Qy and Qx bands in bacteriochlorins: free-base > manganese(II) > manganese(III). Concomitant with the red shift of the Qy band, we observe a blue shift of the By band in manganese(III) bacteriochlorin. Finally, it is interesting to note that the minimum-energy splitting between the Q band and tripmultiplets in manganese(III) porphyrins and bacteriochlorins is ca. 6 kcal mol−1, not unrealistically different from the singlet−triplet energy splitting of ca. 10 kcal mol−1 observed in the corresponding free bases.53 Table 1 presents our assignment of the electronic transitions based on these considerations. A visual comparison between the spectra of manganese(III) porphyrin and metal(III) bacteriochlorin in Figure 2 (panels B and D) reveals that the assignments of the III, IIIa, VII, and VIII bands in Table 1 are also supported by their relative intensities, shapes, and energies. II.C. Transient Absorption. The effect of manganese(III) in the transient absorption of bacteriochlorins is placed in an enlightening perspective when the transient absorption of freebase bacteriochlorin is analyzed first under the same experimental conditions. The transient absorption in the

nanosecond−microsecond time scale revealed the presence of a long-lived triplet state that is strongly quenched by molecular oxygen.19 Parts A and B of Figure 4 show the transient absorption spectra of F2BMet in ethanol obtained with femtosecond and nanosecond excitations at 743 and 355 nm, respectively. Global fitting of the transient differential absorption spectra from the femtosecond to the 6 ns time range using Surface Explorer, version 4.1.0 (Ultrafast Systems), and Glotaran54 revealed a 2.2 ns lifetime decay and a species that does not decay in this time range. The persistent species does not absorb at 664 nm, and the fitting of the transient absorption at this wavelength gave an exponential decay with a 3.0 ns lifetime. The singlet lifetime of F2BMet measured by single-photon counting was 3.0 ns.19 Hence, this decay corresponds to S1(π,π*) and is characterized by bands at 450, 515, and 640 nm. As the S1(π,π*) singlet state decays, a new band appears at 607 nm, which is assigned to the T1(π,π*) triplet state. The transient absorption at this wavelength has a 3 ns rise time and does not decrease significantly in the time window of this experiment. The triplet of F2BMet was previously measured by nanosecond transient absorption and exhibits the same prominent band at 607 nm. In the absence of oxygen, this triplet has a lifetime of tens of microseconds.19 Figure 3 shows evolution-associated difference spectrometry (EADS) spectra obtained after femtosecond excitation of Mn2+Cl2BMet2 at 766 nm, selected to minimize the excitation of the free base possibly present in the sample due to demetalation of manganese(II) bacteriochlorin. EADS with a 0.9 ps lifetime exhibits bands at 450, 525, and 650 nm that resemble that observed for the S1(π,π*) of F2BMet (EADS with a 63 fs lifetime is not shown because it is believed to include instrumental artifacts). The 6S1(π,π*) state decays very rapidly G


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Inorganic Chemistry Table 2. Amplitudes and Lifetimes of the Transient Species Found after Excitation of (Cl)MnCl2BMet2 at 830 nm λ/nm

amplitude/10−3

lifetime/ps

476 558a 637a

18 ± 1 5.4 ± 0.2 −4.6 ± 0.4

0.26 ± 0.01 1.0 ± 0.1 0.3 ± 0.2

amplitude/10−3

2.3 ± 0.1

lifetime/ps

amplitude/10−3

lifetime/ns

3.3 ± 0.1

0.58 ± 0.02

11.7 ± 0.2

A decay with a lifetime shorter than 70 fs was also included in the fitting but was too close to the instrumental time resolution to be considered reliable. a

Figure 5. (Cl)MnCl2BMet2 absorption and decay in acetonitrile. (A) Absorption spectrum, (B) EADS spectra (from Glotaran) obtained by global analysis and associated with lifetimes of 507 fs and 6.3 and 581 ps, (C) experimental spectra (Surface Explorer) both after excitation at 830 nm, and (D) decays at 476, 558, and 637 nm in the picosecond time scale. Contamination from the corresponding porphyrin in this sample may contribute to the peak/bleaching at 477 nm.

manganese(III) bacteriochlorin 5S1(π,π*) state are also present in the spectrum of the free-base bacteriochlorin S1(π,π*) state, suggesting that Mn3+ has a limited impact on the nature of this state. Global fitting indicates that the longer-lived component does not absorb at 637 nm. The decay at this wavelength shows that, subsequent to the ultrafast generation of the 5S1(π,π*) state, a new transient is formed and decays with a 11.7 ps lifetime (Figure 5B). Lifetimes of 5−30 ps were observed in decays of manganese(III) porphyrins and assigned to tripquintet 5 T1(π,π*) states.43,44 The fast intersystem crossing observed in manganese(III) porphyrins should also be possible in manganese(III) bacteriochlorins, and we assign this 6−12 ps transient to the 5T1(π,π*) state. Formation of the 5T1(π,π*) state is accompanied by a partial recovery of the ground-state bleaching at 610 nm. The 5S1(π,π*) state decays to the ground state competitively with formation of the 5T1(π,π*) state. On the basis of bleaching recovery in manganese(III) porphyrins, it was estimated that at least 60% of the 5T1(π,π*) decay repopulates the 5S0(π,π*) state.44 Only half of the ground-state bleaching at 610 nm recovers during the decay of the 5T1(π,π*) state of (Cl)MnCl2BMet2. A longer-lived transient, with absorption at 476 nm and a lifetime of ca. 0.6 ns, is still present in the system after the complete decay of the 5T1(π,π*) state at 476 nm. When the analogy with manganese(III) porphyrins is extended to manganese(III) bacteriochlorins,9,44 the long decay may be assigned to the tripseptet 7T1(π,π*) state. Again, on the basis of the recovery of the ground-state

to another transient with a prominent band at 775 nm. This band decays in ca. 8 ps, leaving only weak absorption and bleaching peaks that can be assigned to residual demetalated Mn2+Cl2BMet2 present in the system. The very fast decay of the 6 S1(π,π*) state reflects a combined heavy-atom and paramagnetic enhanced intersystem crossing caused by the central manganese ion, as observed in manganese(II) porphyrins.42 The resulting tripmultiplet state lives for ca. 8 ps, possibly due to deactivation via CT ligand → metal states [a1u, a2u → eg(dπ)]. The dominant mechanism for the decay of this state is the radiationless transition to the ground state. A very similar lifetime was observed in the decay of manganese(II) porphyrin.43 The transient absorption of (Cl)MnCl2BMet2 was studied by exciting the Qy band at 830 nm and probing the transients in the 430−770 nm range from the femtosecond through the nanosecond time ranges (Table 2). Global fitting of the transient differential absorption spectra with a four-exponential model using Surface Explorer and Glotaran yielded the three reliable components shown in Figure 5. A first component with a less than 70 fs lifetime has instrumental artifacts and is not shown. According to the global fitting, a transient with a 507 fs lifetime decays to the baseline at 558 nm. The fit of the decay at 558 nm indeed shows ultrafast generation of a transient that decays to the baseline with a 1 ps lifetime (Figure 5B). This kinetic trace is consistent with the formation and decay of the 5 S1(π,π*) state in the femtosecond time window, which agrees with estimates for the 5S1(π,π*) state lifetime of manganese(III) porphyrins.43,44 The most salient absorption bands of the H


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Inorganic Chemistry bleaching, we estimate that the 7T1(π,π*) state of (Cl)MnCl2BMet2 is formed with a quantum yield of ca. 20%. Interestingly, the lifetimes of manganese(III) porphyrins with 7 T1(π,π*) states with Cl− as the axial ligand are relatively short (80−140 ps),44 whereas those of manganese(III) porphyrins with OH− and CH3COO− axial ligands are in the nanosecond range.9 Such long lifetimes offer the opportunity for photochemical reactions with oxygen, namely, electron transfer to generate the superoxo complex [(O2•−)MnIV(porphyrin)], which can act as a photocatalyst.9,55 The decrease of the 7 T1(π,π*) → 5S0(π,π*) intersystem crossing rate with a change from Cl− to RO− ligands is unexpected in view of the heavyatom effect of spin−orbit coupling.56 The dependence of the lifetime of the long-lived transient on the nature of the ligand would be more consistent with its assignment as a deligated state rather than the 7T1(π,π*) state. Photodissociative states of metalloporphyrins are expected to be the low-lying (π, dz2) CT or (d, dz2) ligand excited states because increasing the electron density in the dz2 orbital weakens the axial bond.57 We investigated the hypothesis of increasing the lifetime of the long decay in manganese(III) bacteriochlorins by replacing the chloride ion by an acetate ion as the axial ligand. We did not find an increase in the lifetime of the longest decays at 476 nm when the axial ligand was changed to acetate, which is consistent with the assignment of the transient species to the 7 T1(π,π*) state. The excitation of manganese(III) porphyrins populates a 5 S1(π,π*) state that lives less than 0.5 ps.58 Part of this singquintet decays by internal conversion to the ground state, but a significant part follows fast intersystem crossing to the 5 T1(π,π*) state. This state was found to have a lifetime between 5 and 30 ps. There is a close analogy between manganese(III) porphyrins and manganese(III) bacteriochlorins. In both complexes, part of the 5T1(π,π*) state returns to the ground state via (π, d) or (d, π*) CT or (d, d) ligand states, and the other part evolves to the 7T1(π,π*) state. Interestingly, 7 T1(π,π*) state lifetimes of manganese(III) porphyrins are between 80 and 140 ps when Cl− is the axial ligand,58 but the 7 T1(π,π*) state lifetime of manganese(III) bacteriochlorins with the same axial ligand is ca. 570 ps. This long lifetime is unexpected because the smaller energy gap between the 7 T1(π,π*) and 5S0(π,π*) states in manganese(III) bacteriochlorins relative to manganese(III) porphyrins would suggest a shorter-lived 7T1(π,π*) state. However, the longer lifetime can be rationalized assuming that CT or ligand states are energetically close and strongly mixed with the 5,7T1(π,π*) states of porphyrins, but the lower energy of the 5,7T1(π,π*) states of bacteriochlorins reduces the mixing with CT or ligand states and allows the lowest 7T1(π,π*) state to have a relatively long lifetime. Admittedly, the nanosecond lifetimes reported for manganese(III) porphyrins with an CH3COO− axial ligand9 do not fit easily into this picture. Tripquintet lifetimes of up to 1 ns were found in manganese(III) porphyrins with different ligands incorporated in the poly(vinyl chloride) polymer films and related to the bulkiness of the axial ligand.59 This motivated a further experiment to test the hypothesis that deligation of the axial ligand could be involved in a decay mechanism. II.D. Time-Resolved Photoacoustic Calorimetry (PAC). Manganese(III) porphyrins and bacteriochlorins in solution are virtually nonluminescent, and all of the excitation energy is lost by a radiationless process. Such processes release heat in the

solution and produce a thermoelastic expansion. If the solution is rigidly confined, the thermoelastic expansion is frustrated and gives rise to a pressure increase in the medium. PAC takes advantage of pulsed-light irradiation of a solution containing a dye confined in a rigid PAC cell to measure the PA waves generated by the radiationless processes subsequent to light absorption.60 These PA waves have frequencies that are conveniently detected by ultrasonic transducers.61,62 When a chromophore absorbs a short pulse of light and converts all of the light energy into heat in a time shorter than the time resolution of the transducer, this chromophore is called a PA reference. This is the case, for example, of azulene excited at 585 nm.19 If the excited state finds a dissociative channel, then a structural volume change can occur concomitant with the thermoelastic expansion and contributes to the observed PA wave. The ratio of energy-normalized signals for the sample (Hs) and reference (Href) is63 Φ ΔV ⎛ Cpρ ⎞ Hs = ϕ + R R⎜ ⎟ ref Eλ ⎝ β ⎠ H

(1)

where Eλ is the energy of 1 mol of photons at the excitation wavelength, ϕ is the fraction of absorbed energy released as heat in the time window of the experiment, ΦR is the quantum yield of the dissociative reaction with ΔVR structural volume change, Cp is the isobaric mass heat capacity, ρ is the density, and β is the thermal expansion coefficient of the solution. Using data for ethanol, we calculate (Cpρ/NAβ) ≈ 2.579 kJ cm−3, and excitation at 585 nm gives Eλ = 205 kJ mol−1. ΔVR should have a contribution from the decrease in the volume of (Cl)MnCl2BMet2 when it loses the axial ligand and a contribution from the partial molar volume of Cl− in ethanol (VCl−0). The contribution to ΔVR from the decreased structural volume of (Cl)MnCl2BMet2 should be negligible. The experimental value of VCl−0 in ethanol is 12 cm3 mol−1.64 If it is assumed that no other processes occur (i.e., ϕ + ΦR = 1), Cl− photodeligation of (Cl)MnCl2BMet2 in ethanol should lead to a ratio of intensities in eq 1 of 1 − 0.85ΦR. This means that photodeligation of (Cl)MnCl2BMet2 in ethanol should give a lower PA wave than that of azulene. We currently employ a time-resolved version of PAC that discriminates heat decays or volume changes taking place in the nanosecond to microsecond time window. However, all of the decays expected for (Cl)MnCl2BMet2 are faster than our current time resolution, and their contributions to the PA wave are expected to appear as “prompt” PA waves. We excited both (Cl)MnCl2BMet2 and azulene at 585 nm in ethanol solutions of matched absorbance at this wavelength. The laser pulse intensity was varied by interposing filters with transmittance down to 25% to assess the presence of biphotonic effects. The data obtained were analyzed with a deconvolution software,65 confirming that (Cl)MnCl2BMet2 decays in a lifetime shorter than the nanosecond time resolution of the experiment. This means that only one transient species was detected. At the lowest laser energy employed, we did not find any statistically significant difference between the PA generated by azulene or by (Cl)MnCl2BMet2. All of the energy absorbed by (Cl)MnCl2BMet2 was deposited as heat in the time window of the experiment, and no evidence was found for transient volume changes associated with the formation of a deligated state. If deligation occurs, the quantum yield of the process must be ΦR < 0.1. Figure 6 shows the PA waves of azulene, (Cl)MnCl2BMet2, and F2BMet obtained under the same conditions. The smaller PA wave of F2BMet is I


Article

Inorganic Chemistry

transient species, with the longest lifetime of ca. 8 ps due to low-energy CT states. Figure 7 also presents a possible decay mechanism for this complex. The ca. 570 ps lifetime of the 7T1(π,π*) state of (Cl)MnCl2BMet2 is relatively long for a paramagnetic metal porphyrin derivative, and this state is reached with a substantial quantum yield, ca. 0.2. No evidence was found for a dissociative mechanism involving the axial ligand, and this dye was quite photostable upon irradiation at 829 nm. Hence, it is possible to use (Cl)MnCl2BMet2 in applications of IR photochemistry, such as photocatalysis or the injection of electrons in the conduction bands of solar cells. However, the efficient radiationless transitions in this manganese(III) bacteriochlorin and its very strong absorption at a wavelength where human tissues are most transparent (ε829 ≈ 50000 M−1 cm−1) suggest that this class of compounds may be more useful for applications such as photothermal therapy or as a contrast agent for PA tomography. The 8 ps lifetime of the longest-lived transient observed for the analogous manganese(II) bacteriochlorin complex precludes the photochemical use of this complex but not photothermal applications.

Figure 6. Representative PAC waves of PA references azulene (black line), (Cl)MnCl2BMet2 (red line), and F2BMet (blue line).

related to the efficient formation of a long-lived triplet state that does not release its energy in the time window of the experiment and to the significant fluorescence quantum yield of this photosensitizer.

IV. EXPERIMENTAL SECTION III. CONCLUSIONS Halogenated manganese(III) tetraphenylbacteriochlorins can be prepared via transmetalation reactions and are sufficiently stable to be purified and characterized at room temperature using standard techniques. These manganese(III) bacteriochlorins exhibit a remarkable electronic absorption spectrum with electronic transitions up to 1100 nm. Eight distinct electronic transitions were assigned, involving both (π, π*) bacteriochlorin and ligand-to-metal transitions. The lowestenergy transitions involve direct excitation from the singlet to triplet manifold, e.g., 5S0(π,π*) → 5T1(π,π*) transitions. However, the mixing of metal (d, d) orbitals with the macrocycle (π, π*) orbitals is smaller than that in manganese(III) porphyrins, which weakens the intensity of the CT transitions and lengthens the lifetime of the lowest-energy electronic state detected and assigned to a 7T1(π,π*) state. Figure 7 presents the deactivation mechanism of manganese(III) bacteriochlorins. The analogous manganese(II) bacteriochlorin has a pseudonormal absorption spectrum, suggestive of little metal porphyrin π mixing, but remarkably short-lived

IV.A. Synthesis. The synthesis of 5,10,15,20-tetrakis[2,6-difluoro3-(N-methylsulfamoyl)phenyl]bacteriochlorin (F2BMet), also named LUZ11 or redaporfin, was described elsewhere. 5,10,15,20-Tetrakis[2,6-dichloro-3-(N-dimethylsulfamoyl)phenyl]bacteriochlorin (Cl2BMet2). Following a literature method,28 a mixture of 5,10,15,20-tetrakis[2,6-dichloro-3-(N-dimethylsulfamoyl)phenyl]porphyrin (500 mg, 0.38 mmol) and p-toluenesulfonyl hydrazide (2.8 g, 15 mmol) was evacuated to 0.1 bar for 1 h. Next, the reactor was heated to 140 °C for 50 min and then brought back to room temperature. After the workup was performed as described, Cl2BMet2 was obtained (380 mg, 76%). 1H NMR (400 MHz, CD3Cl): δ 8.40−8.37 (m, 4H), 7.85−7.82 (m, 8H), 3.90 (m, 8H), 2.99−2.98 (m, 24H), −1.28 (s, 2H). MS (ESI-FIA-TOF). Calcd for C52H47Cl8N8O8S4 ([M + H]+): m/z 1318.9902. Found: m/z 1318.9899. Manganese(III) 5,10,15,20-Tetrakis[2,6-dichloro-3-(Ndimethylsulfamoyl)phenyl]bacteriochlorin [(Cl)MnCl2BMet2]. Initially, a solution of Cl2BMet2 (100 mg, 7.5 × 10−2 mmol) in dry DMF was added to a suspension of calcium hydride (100 mg) in dry DMF. Following the reaction procedure described above, MnCl2 (270 mg, 21.4 mmol) was added. After a similar workup, a mixture of manganese(II) 5,10,15,20-tetrakis[2,6-dichloro-3-(Ndimethylsulfamoyl)phenyl]bacteriochlorin and manganese(III) 5,10,15,20-tetrakis[2,6-dichloro-3-(N-dimethylsulfamoyl)phenyl]bacteriochlorin was dissolved in dichloromethane/methanol (1:1, v/ v), and 4 drops of H2O2 was added dropwise at room temperature. The reaction was monitored by UV/vis until complete oxidation to the corresponding manganese(III) bacteriochlorin (monitored at 829 nm). After recrystallization, manganese(III) 5,10,15,20-tetrakis[2,6dichloro-3-(N-dimethylsulfamoyl)phenyl]bacteriochlorin was obtained (75 mg, 72%). MS (ESI-FIA-TOF). Calcd for C52H42Cl8MnN8O8S4 ([M − Cl]+: m/z 1368.8892. Found: m/z 1368.8878, Manganese(III) 5,10,15,20-Tetrakis[2,6-difluoro-3-(Nmethylsulfamoyl)phenyl]bacteriochlorin [(Cl)MnF2BMet]. Initially, a solution of 5,10,15,20-tetrakis[2,6-difluoro-3-(N-methylsulfamoyl)phenyl]bacteriochlorin (100 mg, 8.8 × 10−2 mmol) in dry DMF was added to a suspension of calcium hydride (100 mg) in dry DMF. Following the reaction procedure described above, MnCl2 (330 mg, 2.64 mmol) was added. After a similar workup, a mixture of manganese(II) 5,10,15,20-tetrakis[2,6-difluoro-3-(Nmethylsulfamoyl)phenyl]bacteriochlorin and manganese(III) 5,10,15,20-tetrakis[2,6-difluoro-3-(N-methylsulfamoyl)phenyl]bacteriochlorin was dissolved in dichloromethane/methanol (1:1, v/ v), and 3 drops of H2O2 was added dropwise at room temperature.

Figure 7. Mechanism of deactivation of the electronically excited states of manganese(II) and manganese(III) bacteriochlorins. J


Article

Inorganic Chemistry Notes

The reaction was monitored by UV/vis until complete oxidation to the corresponding manganese(III) bacteriochlorin. After recrystallization, manganese(III) 5,10,15,20-tetrakis[2,6-difluoro-3-(Nmethylsulfamoyl)phenyl]bacteriochlorin was obtained (78 mg, 75%). MS (MALDI-TOF). Calcd for C48H36F8MnN8O8S4 ([M − Cl]+): m/z 1187.08. Found: m/z 1187.13, IV.B. General Methods. 1H NMR spectra were obtained using a Bruker Avance III 400 MHz spectrometer. The matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) data were acquired using a Bruker Daltonics Flex Analysis apparatus. Absorption spectra were recorded with a Cary 5000 UV/ vis/NIR spectrophotometer in the range 300−1200 nm. The molar absorption coefficients were determined in ethanol PA supplied by Fisher Chemicals. IV.C. Transient Absorption. Time-resolved spectra were collected using a broad-band (350−1600 nm) HELIOS pump−probe femtosecond transient absorption spectrometer from Ultrafast Systems, equipped with an amplified femtosecond Spectra-Physics Solstice100F laser (displaying a pulse width of 128 fs and a 1 kHz repetition rate) coupled with a Spectra-Physics TOPAS Prime F optical parametric amplifier (195−22000 nm) for pulse pump generation. Probe light in the visible range was generated by passing a small portion of the 795 nm light from the Solstice-100F laser through a computerized optical delay (with a time window of 7.6 ns) and focusing on a sapphire plate to generate a white-light continuum (440−800 nm). The samples were prepared in acetonitrile (Fisher Chemicals). All measurements were obtained in a 1 mm quartz cuvette with an absorption of 0.5 at the pump excitation wavelength of 830 nm. To avoid photodegradation, the cuvette was moved using a motorized translating sample holder. Transient absorption data were analyzed using the Surface Xplorer PRO program from Ultrafast Systems and Glotaran. Nanosecond transient absorption employed an Applied Photophysics LKS.60 laser flash photolysis spectrometer, with a Spectra-Physics Quanta-Ray GCR-130 Nd:YAG laser and a Tektronix TDS3052B oscilloscope (500 MHz, 5GS/s); the samples were irradiated with the third harmonic of the laser (355 nm), the monitoring white light was produced by a 150 W pulsed xenon lamp, and detection of the transient spectra in the 300−900 nm range was made with Hamamatsu 1P28 and R928 photomultipliers. IV.D. Time-Resolved PAC. Our PAC equipment follows the frontface irradiation design of Arnaut et al.60 and was recently described in detail elsewhere.62 The PA waves were analyzed with the software developed by Schaberle et al.61 and freely available online.65 The PA reference employed was azulene. Briefly, the sample and reference solution in ethanol (Fisher), with an optical absorption of ca. 0.1 at 585 nm, were flown through the PAC cell and excited at 585 nm using an OPO EKSPLA model PG/122/SH pumped by a Nd:YAG laser EKSPLA model NL301G at 355 nm with a pulse width of 6 ns. A Panametrics contact transducer with a central frequency at 2.25 MHz was used to detect the PA waves. All signals were preamplified through a Panametrics model 5676 amplifier. The data were collected in a Tektronix DPO7254 oscilloscope (2.5 GHz, 40GS/s) and transferred to a computer for deconvolution with the software mentioned above.

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The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was financially supported by the Portuguese Science Foundation (Grants 007630UID/QUI/00313/2013, PTDC/ QUI-QUI/120182/2010, and PTDC/QEQ-MED/3521/ 2014). NMR data were collected at the UC-NMR facility supported by FCT (Grant RECI/QEF-QFI/0168/2012).

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ASSOCIATED CONTENT

* Supporting Information S

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.inorgchem.6b02871. Mass spectra (PDF)

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REFERENCES

AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Phone: (+)351 239 852 808. Fax: (+)351 239 827 703. ORCID

Fabio A. Schaberle: 0000-0002-9339-7259 K


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Ultrafast Dynamics of Manganese(III), Manganese(II), and Free-Base

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