Electronic Interactions in the Bacterial Reaction Center Revealed by

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Spectroscopy and Photochemistry; General Theory

Electronic Interactions in the Bacterial Reaction Center Revealed by Two-Color 2D Electronic Spectroscopy Arkaprabha Konar, Riley Sechrist, Yin Song, Veronica R. Policht, Philip D. Laible, David F Bocian, Dewey Holten, Christine R Kirmaier, and Jennifer P. Ogilvie J. Phys. Chem. Lett., Just Accepted Manuscript • DOI: 10.1021/acs.jpclett.8b02394 • Publication Date (Web): 23 Aug 2018 Downloaded from http://pubs.acs.org on August 23, 2018

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The Journal of Physical Chemistry Letters

Electronic Interactions in the Bacterial Reaction Center Revealed by Two-Color 2D Electronic Spectroscopy Arkaprabha Konar †, Riley Sechrist†, Yin Song†, Veronica R. Policht†, Philip D. Laible ‡, David F. Bocian §, Dewey Holten ¶, Christine Kirmaier ¶ and Jennifer P. Ogilvie†,* †

Department of Physics, University of Michigan, Ann Arbor, Michigan, 49109-1040, USA ‡

§

Biosciences Division, Argonne National Laboratory, Argonne, IL 60439;

Department of Chemistry, University of California, Riverside, CA 92521, USA

¶

Department of Chemistry, Washington University, St. Louis, MO 63130, USA

ACS Paragon Plus Environment

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The Journal of Physical Chemistry Letters 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

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Abstract

The bacterial reaction center (BRC) serves as an important model system for understanding the charge separation processes in photosynthesis. Knowledge of the electronic structure of the BRC is critical for understanding its charge separation mechanism. While it is well-accepted that the “special pair” pigments are strongly coupled, the degree of coupling among other BRC pigments has been thought to be relatively weak. Here we study the W(M250)V mutant BRC by two-color two-dimensional electronic spectroscopy to correlate changes in the Qx region with excitation of the Qy transitions. The resulting Qy - Qx cross-peaks provide a sensitive measure of the electronic interactions throughout the BRC pigment network and complement one-color 2D studies in which such interactions are often obscured by energy transfer and excited state absorption signals. Our observations should motivate the refinement of electronic structure models of the BRC to facilitate improved understanding of the charge separation mechanism.

TOC GRAPHICS

Photosynthesis is the process by which energy from sunlight is converted into chemical energy via a series of complex biochemical steps.1 In photosynthesis, light is harvested by an elaborate


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system of antenna complexes that funnel energy to reaction centers (RCs) where an initial charge separation process drives downhill electron transfer that fuels the pumping of protons and leads to a transmembrane potential gradient used for ATP production.1 Remarkably, the primary photosynthetic charge separation processes occur with near unity quantum efficiency. While the light-harvesting antenna protein complexes show great diversity across different species, the reaction center structure is well-conserved. The BRC from purple bacteria has been very wellcharacterized both structurally2 and spectroscopically3 and therefore serves as an ideal model system for investigating the structure function relationship responsible for efficient photosynthetic energy transfer and charge separation. Despite decades of studies characterizing the structure, photoexcitation dynamics and the role of the protein environment, many open questions remain regarding the relationship between the excitonic structure of reaction centers and the functionality of the system as a whole3,4-6,7. The BRC possesses a pseudo two-fold-symmetric (C2v) hexameric core of light-harvesting pigments arranged into two branches (Fig. 1a). These include a strongly coupled “special pair” (collectively P) of bacteriochlorophyll a (BChl), as well as two accessory BChl (BA and BB) and bacteriopheophytin (BPheo) molecules (HA and HB), labeled for their respective location on the A and B branches. Both branches, being structurally similar, act as efficient energy transfer pathways where energy flows from the B and H bands to the P band3. Upon charge separation at the special pair the electron transfer takes place predominantly along the A branch1. The monomer pigment absorption profile is usually described using the Gouterman model of porphyrin transitions8 which proposes the presence of two independent transitions, labelled Qx and Qy for their polarization with respect to the bacteriochlorin macrocycle plane.


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Two-dimensional electronic spectroscopy (2DES) has emerged as a powerful method for investigating chemical and biochemical processes spanning UV, visible and near-IR frequencies.9-12 In 2DES, a sequence of three pulses is used to interrogate the sample and the resulting third order polarization is typically detected in the frequency domain. The time-domain signal measured as a function of the delay between the pump pulse pairs is Fourier transformed to construct the excitation frequency axis. The resulting excitation frequency resolution provides the additional dimension in 2DES when compared to the more traditional transient absorption spectroscopy. The frequency correlation along the excitation and detection axes is an ideal tool for resolving congested linear absorption spectra and provides ultrafast structural and dynamical information such as inter-chromophore electronic couplings in the off-diagonal peaks of the 2D spectrum. The shape of the diagonal peaks at early times carries useful information about the inhomogeneous and homogenous broadening and spectral diffusion10. Most 2DES studies to date have been one-color measurements, employing the same spectral range for excitation and detection frequencies. In studies of photosynthetic systems, one-color 2DES has been used to interrogate and unravel excitonic structure and ultrafast processes.9, 12-15


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Figure 1. (a) Structure of the BRC from R. sphaeroides16 (PDB: 1A1J) in wireframe representation showing the spatial arrangement of the cofactors in the protein scaffold (not shown). Pigments are labelled according to the respective A and B branches, PA and PB are the strongly coupled special pair BChl (red), BA and BB are the accessory BChl (yellow), HA and HB are BPheo (blue) and QA and QB are ubiquinones (gray). The carotenoid is shown in orange. The W(M250)V mutant strain lacks the QA and samples are treated to displace QB. (b) 77 K absorption spectrum of the W(M250)V mutant (black) showing the Qy and Qx absorption bands corresponding to the different excited states along with the broadband pump (red) and the white


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light continuum probe (blue) spectra. The Qx17 and Qy12 transitions are labelled in green and black respectively. In this letter we present results of two-color 2DES on a neutral BRC mutant, W(M250)V from R. capsulatus, aimed at better understanding the electronic structure of the BRC by examining the detection frequency dependence of the Qx transitions upon photoexciting across the Qy region. The W(M250)V mutant is similar in structure and function to the wild-type RC except for its lack of QA, which prohibits the accumulation of the long-lived P+QA− species, enabling higher repetition rate experiments18. The two-color 2D approach allows access to information far from the diagonal region that is accessed in one-color 2D measurements, enabling the investigation of intra-chromophore coupling and energy transfer between distinct electronic states that are widely separated in energy. In principle such information could be obtained using one-color 2DES with sufficiently broadband pulses to span the required energy range, but such bandwidth can pose experimental challenges such as pulse compression and shaping. Figure 1b shows the 77 K absorption spectrum (black) of W(M250)V along with the broadband pump (red) and probe spectrum (blue) centered around 800 nm and 600 nm respectively (further experimental details are given in the Supporting Information). The absorption bands are labeled according to the absorption positions of the most prominent constituent chromophores in the Qy and Qx regions. The BRC features a structured linear absorption spectrum in the Qy region with three main peaks that can be identified with excitonic transitions involving primarily the lower special pair exciton P∗ , and transitions largely localized on the B and H pigments. Using one-color 2DES we recently studied energy transfer and charge separation processes in the BRC and proposed assignments for the Qy excited states based on global analysis of the 2D data.12 In Figure 1b we indicate the locations of these states, including the lower and upper excitonic states of the special pair (P∗


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and P∗ respectively), as well as the B∗ , B∗ , H∗ and H∗ transitions which are named for the pigments on which the excitation is primarily localized. Also indicated are the Qx assignments proposed by Huang et al.17 The structured linear absorption spectrum of the BRC is in contrast to the Photosystem I and II reaction centers in which the constituent pigment absorptions are highly spectrally overlapped.19-20 This makes the BRC a simpler system for studying energy and charge transfer dynamics on the ultrafast timescale. The absorption bands in the Qx region are not as well separated, with the P* and B* band absorptions overlapping significantly around 600 nm while the H∗ and H∗ transitions are slightly better separated at 543 nm and 530 nm17,

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respectively (Figure 1b). While the majority of 2DES studies have been “one-color” experiments employing similar spectra for the excitation and detection pulses, several two-color 2DES experiments have been used to excite and probe different regions in studies of laser dyes22, chlorophyll a23 and colloidal quantum dots.24 An extreme version of two-color 2D spectroscopy is the recent demonstration of 2D electronic-vibrational spectroscopy25-26, with excitation in the visible and detection in the mid-infrared, as well as the reverse excitation-detection sequence27. Here we detect at higher frequencies in the Qx region following excitation of the Qy band in the near infrared. The resulting two-color 2D spectra reveal a rich network of cross-peaks that reflect the electronic structure of the system and report on energy transfer and charge separation processes. Our measurements are closely related to transient absorption experiments that have been performed over the last decade on the BRC using broadband probes to detect transient changes in the Qx region upon selective excitation in the Qy region.28-29 Several mechanisms and timescales pertaining to charge separation and energy transfer have been proposed based on those studies17, 30

.


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For the two-color 2DES experiment, we employ the pump-probe geometry22,

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31-32

, taking

advantage of the relative ease of implementing a supercontinuum probe while using a pulse shaper to partially compress and generate the phase stable pump pulse pairs.33 Broadband probing using white light supercontinua generated in bulk crystals has proven to be a versatile tool in the ultrafast community and has been implemented more recently in multidimensional spectroscopic experiments in combination with broadband visible,33-36,37 and UV38 pulses. These pulses are linearly chirped owing to the large frequency content. We previously showed that a post processing chirp-correction can be made to retrieve the temporally aligned (along detection axis) 2D spectrum.39 All the data presented here have been chirp-corrected and the accuracy was checked by comparing the rise of signal around time zero for different detection frequencies. In Figure 2 we present the two-color 2DES data of the BRC at 77 K at several waiting times following Qy excitation. The T=20 fs 2D spectrum shown in Figure 2a is dominated by the broad excited state absorption (ESA) from the Qy excited states which extends over the Qx region and has been characterized previously in transient absorption studies.3, 30 In order to highlight the cross-peaks in the two-color 2D data we subtract the ESA background corresponding to each excitation frequency for a given delay time as detailed in the SI. We note that a similar ESA subtraction approach has previously been used in transient absorption experiments on the photosystem II RC.40 Background subtracted real absorptive 2DES for several waiting times (20, 60 and 100 fs) are shown in Figure 2b. A representative 2D spectrum along with the BRC absorption regions and pump and probe spectra is shown in Fig. S2. Raw 2D spectra corresponding to additional T values are shown in Fig. S3 along with the ESA subtracted spectra (Fig. S4) and the fits to the broad ESA (Fig. S5). In accordance with other 2DES studies and in contrast to transient absorption spectroscopy, the ground state bleach (GSB) and stimulated


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emission (SE) contributions are positive while the ESA is negative. Given that the transitions of interest are in the Qx region, we truncate the detection frequency axis to ~15,500 cm-1 – 19,300 cm-1. On the 2D spectra we indicate with a dotted line the location of Qy states previously determined via global fitting of our one-color Qy 2DES data.12 Also indicated are proposed locations of the Qx states from the literature.17 Significant cross-peak amplitude is detected at the H* Qx frequencies corresponding to excitation of the H*, B* and P* Qy transitions. We note that alignment of the signal peak maxima with P-* is poor as a result of the pump laser spectrum which has considerably reduced amplitude at frequencies below ~11,100 cm-1.


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Figure 2. a) Two-color 2D absorptive spectrum of BRC at 77 K at T = 20 fs recorded using a broadband pump centered around 800 nm covering the Qy transitions and a white light continuum probe covering the Qx transitions. Positive contours are plotted at 5%, 7.5%, 10% and 15% and in increments of 10% starting from 20% while the negative contours are plotted in increments of 10% starting from 10%. The broad negative Qy ESA overlapping with the weak positive Qx GSB features is apparent in this raw spectrum. b) ESA subtracted 2D absorptive spectra for T = 20, 60 and 100 fs showing the cross-peaks between different states. Positive contours are plotted at 5%, 7.5%, 10% and 15% and in increments of 10% starting from 20%. The spectra for each T value are individually normalized to the maximum amplitude to highlight relative amplitude changes among the different cross-peaks. Dashed lines indicate the positions of the Qy12 and Qx17 transitions. c) Wave-mixing diagrams showing a representative GSB pathway giving rise to a peak at H∗ (Qx) upon exciting P∗ (Qy) (depicted by the green circle in the T = 20 fs spectrum). Also shown are double-sided Feynman diagrams depicting characteristic GSB and ESA pathways. The GSB pathway on the top corresponds to the wave-mixing diagram, while the GSB pathway on the bottom leads to the generation of the signal marked by the blue square. In Figure 2c we depict representative Feynman diagrams for several major pathways that give rise to the observed spectral features in the two-color 2D spectra. These include the broadband ESA that produces the negative background signal throughout this spectral region. More interesting are the positive GSB signals that indicate a common ground state between the Qy and Qx transitions, consistent with the energy level structure shown in Figure 2c. The idea of a common ground state does not necessarily imply strong electronic interactions of the chromophores associated with the transitions. The spectral overlap in the Qx band of the P* and


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B* transitions prohibits clear resolution of the GSB cross-peaks involving Qy excitation of an arbitrary state and detection of the P* or B* Qx transitions. However, the better separation of the H∗ and H∗ Qx transitions enable resolution of the cross-peak amplitudes between the H* Qx and all the Qy states of the BRC (Fig. 2b). Previous studies focused on the Qy region have documented ultrafast energy transfer between the P*, B* and H* states29, 41-44 and more recently 2DES studies have revealed H* → B*,14, 45 B* → P*,46,12 BA* → BB*47 and P+* → P-* 12 energy transfer as a direct observable in below diagonal cross peaks in one-color 2D spectra. Energy transfer processes are also apparent in the two-color 2D spectra and account for the rapid decay within the first ~100 fs of many of the cross-peak features, particularly those involving excitation of H∗ (Qy) and H∗ (Qy). The waiting time kinetics of the different cross-peaks at the relatively well-resolved H∗ (Qx) and H∗ (Qx) detection frequencies are shown in Figure 3a) and b) respectively. The corresponding subtracted ESA contributions at these locations are shown in Figure S7. To understand the kinetics of the Qy-Qx cross-peaks, an additional Feynman diagram to account for excitation energy transfer (EET) is needed. Representative EET diagrams for the H∗ (Qy)/ H∗ (Qx) and P∗ (Qy)/ H∗ (Qx) cross-peaks are shown in Figure 3c along with the overlapping GSB contributions. The initial decay of the positive cross-peak amplitude, most evident in the H∗ (Qy)/ H∗ (Qx) and H∗ (Qy)/ H∗ (Qx) peaks, can be understood as arising from the decay in the positive GSB signal as energy is rapidly transferred away from the H*(Qy) states. The crosspeaks involving P*(Qy) excitations also show small energy transfer signals that can be understood from the GSB and excitation energy transfer (EET) diagrams depicted in Figure 3c. The positive GSB signal that arises from the common ground state between H*(Qx) and P*(Qy) is reduced when excited state population transfers out of the P*(Qy) states.


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The two-color 2D cross-peaks also clearly show the charge separation process as shown in the 2D plots corresponding to the longer time delay (Fig. S8). Contrasting the kinetics for detection at H∗ (Qx) and H∗ (Qx) (Figures 3(a) and (b) respectively), most of the cross-peak signals for H∗ (Qx) remain relatively flat after the initial decay, while the H∗ (Qx) cross-peaks exhibit a rise on the ~ 2 picosecond timescale. This timescale has been attributed to the formation of the charge separated state P H .

3, 12, 48

The rise of the H∗ (Qx) cross-peaks can be understood as an

increase in the positive GSB signal due to depletion of the H∗ (Qx) state which is no longer accessible after charge separation occurs. In contrast, only a slight rise is seen in some of the H∗ (Qx) cross-peaks. Since the HB pigment is not involved in the charge separation process, no comparable increase in GSB signal is expected. It may be that the small rise is due in part to Bside electron transfer49, as well as Stark shifts of H∗ (Qx) following charge separation.50 In addition to clear cross-peaks between the H*(Qx) and the P*(Qy) and B*(Qy) states, the early waiting time 2D spectra show evidence for a cross-peak between H∗ (Qy) and H∗ (Qx), indicating a common ground state. Given the weak coupling between HA and HB pigments, this is perhaps surprising44. We note that the H∗ (Qx) cross-peaks are higher in amplitude than the H∗ (Qx) ones, which may reflect stronger coupling of HA than HB to the other BRC pigments. In addition, we note that the distinct cross-peaks in the T=20 fs two-color 2D spectrum shown in Figure 2b support our previous assignment of P∗ to 11,900 cm-1 (840.3 nm) in the Qy region12. The 2D spectra at later times show reduced cross-peak amplitude at P∗ excitation due to the rapid (~25 fs) energy transfer to P∗ 12. Previous theoretical and experimental studies have placed P∗ at a variety of different frequencies to the blue of our assignment. Specifically, experiments on R. sphaeroides at room temperature assign the value to 12,121 cm-1 (825 nm)42 using pump-probe spectroscopy while low temperature experiments (1.5 – 10 K) assign the P∗ position to between


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12,225 and 12,821 cm-1 (818 - 780 nm).51-54 Theoretical work has predicted the P∗ frequency to be located at 12,346 cm-1 (810 nm) and 12,285 cm-1 (814 nm) at 77 K and room temperature respectively.44 The low oscillator strength of P∗ , its coupling and proximity to other exciton states, and its rapid internal conversion have made it historically difficult to detect. The difference between our assignment and the previous values may be due to the different bacterial species being studied or because the higher dimensionality of our method enables detection and assignment of weak transitions.

Figure 3. Kinetic plots corresponding to excitation at each of the six Qy states and detection of (a) H∗ (QX) or (b) H∗ (Qx) transitions for the ESA subtracted data. (c) Double-sided Feynman


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diagrams depicting the different rephasing contributions of the light-matter interactions involved in generation of the GSB signal. The diagram on the left shows the waiting time dependence of the excited state population decaying to ground state following energy transfer leading to a net negative signal. The diagram on the right is a typical sequence leading to GSB due to a common ground state and has a net positive contribution. Since the earliest studies of the BRC, the strength of coupling and accompanying excitation delocalization among the BRC hexamer has been central to proposed energy transfer and charge separation mechanisms

41,3, 44, 55

. The couplings that have been reported for the BRC range from

~400-750 cm-1 for the special pair, to several cm-1 between H and P and HA and HB 44, 51, 55. The fact that we clearly resolve Qy/Qx cross-peaks even among the most weakly-coupled BRC transitions indicates that either the couplings are stronger than previously thought, or that twocolor 2D spectroscopy is highly sensitive to coupling through a common ground state. The latter explanation seems the most likely. The presence of cross-peaks in one-color 2D spectroscopy at T=0 indicates electronic coupling10, and is typically interpreted as revealing strong (excitonic) coupling56. However, cross-peaks in 2D spectra may have several components with different signs, including positively signed GSB and stimulated emission, as well as negatively-signed ESA. In some cases a lack of cross-peaks at T=0 can be attributed to a cancelation of GSB and ESA components rather than to a lack of coupling. Such signal cancelations in 2DES are becoming more apparent with the increased use of fluorescence-detected 2DES,57 for which GSB and ESA cross-peak components combine in a different manner58 (K. J. Karki et al.(unpublished results), V. Tiwari et al. (unpublished results)). We note that our one-color 2D data12 in the Qy region at T=11 fs shows little indication of any below diagonal H-P cross-peaks, and the abovediagonal region is overwhelmed by ESA (see Figure S9 in the SI). Although overlapping ESA


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signals are present in our two-color 2D data, the broad nature of the signals far from the excitation frequency allowed their subtraction to reveal the underlying GSB cross-peaks. This likely makes the two-color approach sensitive to weak coupling that is not readily apparent in one-color 2D spectra. The considerable structure of the ESA signals in the Qy region would complicate an ESA subtraction approach. In one-color 2D measurements the detection of weak cross-peaks can be facilitated by polarization-dependent studies 59-60. In both one-color and twocolor 2D spectroscopy, extracting the absolute electronic coupling strength from cross-peaks in 2D data will require careful modeling and proper weighting of the different signal contributions. We note that GSB signals arising from a common ground state have been reported in pumpprobe studies, where competing ESA signals have partially obscured the GSB contributions61. Compared to pump-probe spectroscopy, 2D spectroscopy resolves the excitation frequency, enabling resolution of individual GSB cross-peaks. Resolving individual GSB cross-peaks could be achieved with tunable narrowband excitation in a series of pump-probe experiments, but at the expense of time resolution, which could prove limiting in systems like the BRC with overlapping transitions and rapid

Electronic Interactions in the Bacterial Reaction Center Revealed by

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