The Eighth Bacteriochlorophyll Completes the Excitation Energy

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The Eighth Bacteriochlorophyll Completes the Excitation Energy Funnel in the FMO Protein €h,‡ Mohamed El-Amine Madjet,‡ and Thomas Renger*,† Marcel Schmidt am Busch,† Frank Mu †

Institut f€ ur Theoretische Physik, Johannes Kepler Universit€ at Linz, Altenberger Strasse 69, 4040 Linz, Austria, and ‡Institut f€ ur Chemie und Biochemie, Freie Universit€ at Berlin, Fabeckstrasse 36a, D-14195 Berlin, Germany

ABSTRACT The Fenna-Matthews-Olson (FMO) light-harvesting protein connects the outer antenna system (chlorosome/baseplate) with the reaction center complex in green sulfur bacteria. Since its first structure determination in the mid70s, this pigment-protein complex has become an important model system to study excitation energy transfer. Recently, an additional bacteriochlorophyll a (the eighth) pigment was discovered in each subunit of this homotrimer. Our structurebased calculations of the optical properties of the FMO protein demonstrate that the eighth pigment is the linker to the baseplate, confirming recent suggestions from crystallographic studies. SECTION Biophysical Chemistry

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ight-harvesting pigment-protein complexes in the neighborhood of photosynthetic reaction center (RC) complexes serve to increase the absorption cross section of the RC by absorbing sunlight and transferring the excitation energy with almost 100% quantum efficiency to the RC. For this purpose, nature has created excitation energy funnels, as in the LH2 complex of purple bacteria1,2 and in the special pairs of purple bacteria and of photosystem I, which are realized through long-range and short-range Coulomb couplings, respectively.2,3 Here, we provide evidence for another type of excitation energy funnel. In the FennaMatthews-Olson (FMO) protein, a funnel is created by the pigment-protein coupling, which tunes the optical properties of the complex in a specific way, such that pigments facing the outer antenna are blue-shifted with respect to those that serve as linkers to the RC. The FMO protein of green sulfur bacteria is a homotrimer that transfers excitation energy between the outer antenna systems and the RC complex (Figure 1).4 Until recently, crystallographic studies reported the presence of seven bacteriochlorophyll a (BChl) pigments per monomeric subunit.5,6 Fitting of optical spectra7,8 and direct structure-based calculations9,10 revealed the location of the energy sink in the FMO protein at BChl 3. On the basis of this fact and the calculation of the energy flow, it was concluded that this pigment represents the linker to the RC complex,8 a prediction that was recently confirmed experimentally in a combined approach of chemical labeling and mass spectrometry-based footprinting.11 Recent crystallographic studies reported the presence of an additional BChl pigment per subunit.12,13 Results presented here are based on the 1.30 Å resolution structural data from Prosthecochloris aestuarii by Tronrud et al.13 Therein, the binding site of the new pigment (BChl 8) shows an occupancy of only about 35%, i.e., most likely this pigment is lost in the

r 2010 American Chemical Society

majority of the complexes during the isolation procedure. BChl 8 is located in a cleft at the surface of the complex, which points toward the chlorosome/baseplate. Therefore, it is tempting to assume that this pigment acts as the linker pigment between the FMO protein and the baseplate.13 Here, we show that the optical properties of BChl 8 strongly support this hypothesis. We performed structure-based calculations of the site energies and optical spectra of the FMO protein using the apo (seven BChl per monomer) and holo (eight BChl per monomer) form of the new crystal structure13 and our theoretical approach developed9 and simplified10,14 previously. Briefly, the approach combines quantum chemistry on BChl ground and excited states with electrostatic calculations, including the whole protein in atomic detail considering all possible nonstandard protonation patterns of the titratable residues in the protein. The titration calculation has been refined recently14,15 by taking into account that the protonation pattern is expected to freeze at 210 K.16 Therefore, the protonation probabilities of all titratable residues at the experimental conditions of 4 K were calculated at 210 K (Supporting Information (SI), Tables 6-9). We titrated the FMO protein at pH 12 taking into account the pH temperature dependence of the water/glycerol mixture7 buffered with Tris-HCl, resulting in an increase from pH 8.3 at room temperature (sample preparation) to pH ∼12 at 210 K.17 As in previous studies,9,14,15 the protonation pattern of the titratable residues was obtained performing Poisson-Boltzmann-type electrostatic calculations,18,19 where the polarizability of the protein and the solvent environment are approximated by that of homogeneous Received Date: November 12, 2010 Accepted Date: December 15, 2010 Published on Web Date: December 23, 2010

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DOI: 10.1021/jz101541b |J. Phys. Chem. Lett. 2011, 2, 93–98

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Figure 2. The left panel shows BChl 8 (in green) with those parts of its protein environment that have a large influence on its site energy. The three acidic side chains ASP 157 and 160 and GLU 163 are part of an R-helix (shown in purple). The protein backbone part shown in gray is connected with the acidic residue ASP 127 and the basic residue ARG 125. The right panel places the net charges of the residues shown in the left panel relative to the difference in electrostatic potentials between the charge densities of the excited and the ground state of BChl 8. The potentials were calculated by using time-dependent density functional theory with the B3LYP exchange correlation functional.22 A negative difference potential is colored in red and a positive difference potential is shown in blue.

Figure 1. Spatial arrangement of the trimeric FMO protein between the chlorosome (outer antenna) and the cytoplasmic membrane with the RC complex. The protein is depicted as a ribbon diagram, and the BChls are colored from blue to red, according to the computed site energy shifts, on a linear scale. The right side contains an enlarged view on the eight BChls of a monomeric subunit. Table 1. Site Energies Ei in Units of cm-1 Obtained at T = 210 K for the apo and holo Forms of the New Crystal Structure Data (pdb code: 3eoj) in Comparison to Site Energies Obtained for the Previous Structural Data (pdb code: 4bcl) Using the PBQC Approach,9 the CDC Method Assuming a Standard Protonation Pattern,10 and by Fitting Optical Spectra Using a Genetic Algorithm (fit)10 a present work BChl

previous work b

fit

PBQCc

CDCb

apo

holo

1

12490

12505

12470

12410

12545

2

12445

12425

12450

12500

12360

3

12205

12195

12190

12195

12160

4

12380

12375

12380

12395

12455

5 6

12570 12535

12600 12515

12570 12565

12620 12510

12590 12470

7

12495

12465

12475

12460

12405

8

contribute only weakly to calculated site energy shifts (SI Table 10). The site energies calculated for the new crystal structure containing the additional BChl 8 demonstrate that this pigment is the blue-most pigment in the FMO protein (Table 1). Analysis of the pigment-protein couplings reveals that two side chains of monomer C (ARG 125 and ASP 127) and three side chains of monomer A (ASP 157, ASP 160 and GLU 163) have a strong influence on the site energy of BChl 8 (SI Table 2). As seen in Figure 2, the negative net charges of the ASPand the GLU residues are located in the negative difference potential of BChl 8, thereby causing the blue shift. In contrast to the strong blue shift of the four acidic residues, the electric field of nearby helices (SI Figure 3) induces a minor red shift (SI Table 3). The site energies obtained for the seven previously known BChls are very similar to our earlier results that were based on a fit of optical spectra,8,10 a CDC calculation, assuming a standard protonation pattern10 and a Poisson-Boltzmann/ quantum chemical approach (PBQC) taking into account nonstandard protonation patterns9 (Table 1). In the latter work, it was assumed that the protons can equilibrate at all temperatures. The present more realistic calculations of protonation probabilities in which the protonation states are assumed to be frozen in at 210 K,16 reveal a considerably lower amount of nonstandard protonation states at the experimental condition of 4 K (SI Table 6-9). However, the calculated site energies are barely affected by this change in protonation states, with the largest deviation being 90 cm-1 for BChl 1 between the present study and our earlier PBQC approach.9 The small deviations show that the detailed protonation pattern is of minor importance for the FMO protein, supporting our earlier CDC calculations10 that were performed for the standard protonation pattern. The reason for this effect is probably the relatively large spatial separation between the titratable groups located on the outside and

12700

εeff -1

Eo/cm

3.0

3.0

2.8

1.8/10d

2.5

12570

12570

12560

12560

12540

Eo and εeff are determined from a comparison of calculated and experimental spectra. The present site energies were refined within the error range of (60 cm-1 of the CDC method. The unrefined values are given in SI Table 1. b From ref 10. c From ref 9. d These values refer to the dielectric constants for the protein and the solvent, respectively. a

dielectrica with dielectric constants εprotein = 4 and εsolvent = 80, respectively. The site energies are obtained using the charge density coupling (CDC) method10,14 as Ei = E0 þ ΔEi, where E0 is a reference energy, and the site energy shift ΔEi is obtained from the CDC between the pigments and the protein using an effective dielectric constant εeff to describe screening and local field effects. E0 and εeff are two fit parameters determined by comparing the experimental with the calculated spectra. Incomplete amino acid residues of the crystal structure data were modeled as discussed in the SI, but


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recently13 that the varying binding mode of BChl 8 in different species is responsible for the differences in optical spectra, which are strongest around 12300 cm-1. The present finding that BChl 8 contributes strongest at 12700 cm-1 to the spectra, therefore, suggests that other pigments than BChl 8 are responsible for the spectral differences. Since BChl 8 is located at the surface of the protein and its site energy shift is dominated by titratable residues (Figure 2), a modified environment provided by the neighboring baseplate in vivo could change its site energy. Unfortunately, at present no detailed structural information is available about the interaction between the FMO protein and the baseplate. Cross-linking studies suggested that the FMO complex is in contact with a 17 amino acid long tail of the CsmA protein, but that solvent molecules can also access space between the FMO and the baseplate.11,20,21 To investigate the influence of such an environment qualitatively, we modeled the baseplate and the RC complex by two layers with dielectric constant εborder using the high dielectric constant of the solvent only between these layers (Figure 4). We note that varying the value of εsolvent within the physiologically relevant range (75-80) has practically no influence on the calculated site energies. The value of εborder was varied between 4 and 20 (SI Table 4) in order to take into account the more frequent occurrence of polar side chains at the surface of proteins. Depending on these variations, ASP 160 has a tendency to become deprotonated, whereas all other residues in the vicinity of the pigments do not alter their protonation pattern (SI Table 8). At neutral pH and εborder = 4, this effect lowers the site energy of BChl 8 by ∼80 cm-1 (Figure 4, SI Table 4), which brings the excited states of BChl 8, BChl 1, and the baseplate BChl closer together in energy (Figure 4). BChl 1 is excitonically coupled to BChl 8 by a coupling strength of 40 cm-1 (SI Table 5). The smaller energy gap between these two BChls obtained for εborder = 4 allows for a better delocalization of the excitonic wave functions and thereby opens a second entrance channel for the excitation energy from the baseplate (see below). In addition, the red shift of BChl 8 increases the overlap with the baseplate fluorescence (Figure 4) and thereby the efficiency of the energy transfer, which is studied in the following. We simulated the excitation energy flow through the FMO protein under physiological conditions (T = 300 K). Exciton relaxation was described with modified Redfield theory,24-26 as explained in detail before.8,9 The initial condition was determined using generalized F€ orster theory27-29 for the transfer between the baseplate and the FMO protein.9 Within the latter theory, the rate constant and thereby the initial population of exciton state M in the FMO protein is determined by P M (0) ∼ |V Mb | 2 SOL(M,b), where V Mb = P mcm(M)Vmb with the exciton coefficient cm(M) of pigment m in exciton state M and the excitonic coupling Vmb between m and the baseplate BChl. SOL(M,b) is the spectral overlap between the homogeneous fluorescence line shape function of the baseplate BChl and the absorbance line shape function of exciton state M of the FMO protein. The homogeneous fluorescence line shape function of the baseplate BChl was extracted from the absorbance and fluorescence spectra before.9 Taking into account that BChl 8, as a result of its

Figure 3. Simulated absorbance (OD), linear dichroism (LD), and circular dichroism (CD) spectra at 4 K (solid lines) in comparison to experimental data7 (dashed black lines). The left side contains simulations based on the apo form containing 7 BChls per monomer, and the right side shows simulations of the holo form with all eight BChls (red lines) as well as a superposition of apo and holo simulations (green lines) according to the 35% occupation of the binding site of BChl 8 observed in the crystal structure.13 The structure-based calculated site energies were refined by variations within (60 cm-1 corresponding to the estimated error of the CDC method resulting in the values given in Table 1.10 A comparison with spectra calculated for unrefined site energies is shown in SI Figures 1 and 2.

the pigments located inside the FMO protein. We will show below that the site energy of BChl 8, which is located at the surface of the protein, is indeed strongly influenced by titratable residues. A second example for such an influence is given by photosystem I, where a nonstandard protonation state of a titratable residue was found to be responsible for a 500 cm-1 blue-shift of a site energy.14 Finally, we conclude that the more elaborate treatment of the polarizabilitiy in our earlier PBQC calculations9 is well approximated by an effective dielectric constant, as in the present CDC approach. Using the above site energies and the excitonic couplings given in SI Table 5, optical spectra were calculated as described in detail before.8-10 Spectra obtained for the apo form and a superposition of the apo and holo form taking into account the 35% occupation of the eighth binding site, agree well with experimental data (Figure 3). The differences between these two calculations are too small to decide whether BChl 8 was present in the experiment. However, 100% occupancy of the eighth site seems unlikely, as this is predicted to result in a more pronounced peak in OD and LD at 12700 cm-1 (Figure 3, right panel). It was suggested


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Figure 4. The left panel shows the fluorescence spectrum of the baseplate BChl at T = 300 K23 and the site energies (horizontal lines) of the BChls (numbers) for two different values of εborder used in the calculation of protonation probabilities of titratable residues. εborder = 4 represents the protein environment of the FMO protein in vivo, and εborder = 80 is the solvent environment of the FMO trimers in vitro, as illustrated in the right panel. Numerical values of the site energies for εborder = 4 are given in Table 1, those for εborder = 80 are shown in SI Table 4, including εborder = 10, 20. The two arrows in the left panel are positioned at the energies of the two exciton levels of the FMO protein, obtained for εborder = 4, that function as entrance channels for the excitation energy from the baseplate. The thickness of the arrows is proportional to the respective rate constant.

location at the top of the FMO complex, most likely has the strongest excitonic coupling to the baseplate BChl, that is, VMb ≈ c8(M)V8b; the initial population of an exciton state in the FMO protein is approximated by PM(0) ∼ |c8(M)|2SOL(M,b). We note that, in addition to the distance, the mutual orientation between the BChl a in the baseplate and the BChl a pigments in the FMO determines the excitonic couplings. From linear dichroism ensemble measurements on squeezed gels, an orientation of the transition dipole moment perpendicular to the membrane plane was inferred for the baseplate BChl a.30,31 Since the macrocycle of BChl 8 of the FMO is rather oriented in plane than perpendicular to it (Figure 1), one could expect that this orientation is unfavorable for accepting excitation energy from the baseplate. However, recent single molecule studies32 infer, instead, that there is an angle of β = 47° between the transition dipole moment of the baseplate BChl a and the normal of the membrane. Furthermore, it is suggested,32 that the random orientation with fixed angle β around the axis of the normal, realized in different complexes, leads to a cancelation of the anisotropy signals in the other directions in ensemble measurements. For an angle of 47° between the membrane normal and the transition dipole moment of the baseplate BChl a, the orientation does not seem to be the limiting factor for the excitonic couplings. Therefore, at the present level of structural knowledge, it is most realistic to assume that BChl 8, because of its closest distance, is coupled more strongly than the other BChls of the FMO to the baseplate BChl a. Due to the excitonic coupling (SI Table 5) between BChl 8 and 1, these two pigments are initially excited (Figure 5). The main entrance route for the excitation energy is via the highest exciton state of FMO (upper arrow in Figure 4), which has the largest contribution from the excited BChl 8, but a somewhat smaller spectral overlap with the baseplate fluorescence than the third highest exciton state. The latter, which


is dominated by BChl 1, functions as a second entrance route (lower arrow in Figure 4). The excitation energy relaxes to BChl 3 along the branches formed by BChl 2 and by BChl 4 to 7. Whereas relaxation/equilibration via the latter is completed within 500 fs, BChl 2 forms a bottleneck that limits the overall relaxation/equilibration time to about 1.5 ps. This time can be expected to be shorter than the time scale of energy transfer between the baseplate and FMO and between the latter and the RC complex. The fast equilibration and the large energy gap of 400 cm-1 between the entrance BChl 8 and the energy sink at BChl 3, which is about twice the thermal energy at room temperature, prevents the excitation energy from leaking out of the FMO protein back into the chlorosome and thus leads to efficient unidirectional excitation energy transfer between the baseplate and the RC complex (Figure 5). The site energy of BChl 8 seems to be optimized to achieve a large energy gap to BChl 3 without loosing significant spectral overlap with the baseplate fluorescence. More detailed structural information about the baseplate and RC environment of the FMO protein would be desirable in order to determine the relative time scales of excitation energy transfer into, within and out of the FMO protein and the overall efficiency of light-harvesting. Interestingly, electronic quantum beats first measured33,34 and calculated35 at low temperatures were recently predicted36 and measured37 at physiological temperatures. Two-dimensional (2D) electronic spectroscopy pioneered by the Fleming group38 has become a promising tool to gain deeper insight into the elementary interactions responsible for energy transfer. At present, it is not clear whether the coherent signatures found in the exciton relaxation in the FMO protein are significant for the physiological function of the complex. Most likely, it is rather the intercomplex than the intracomplex exciton transfer that is critical for the overall efficiency, since the latter transfer can be assumed to be fast compared to the former. Therefore, it

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thank Gernot Kieseritzky and Prof. E. W. Knapp for advice in performing the electrostatic calculations.

REFERENCES (1)

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(8) Figure 5. Flow of excitation energy through the FMO protein. At time zero, it is assumed that the excitation energy enters from the baseplate as explained in the text. The lower panel contains the occupation probabilities of the local excited states of the pigments, and in the upper panel these probabilities are illustrated. The macrocycles of the BChl are colored according to their population at the given time, on a linear scale.

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would be important to investigate whether the quantum mechanical coherences found36,37 within isolated FMO proteins at physiological temperatures prevail also in the transfer steps in and off the FMO protein.

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SUPPORTING

INFORMATION AVAILABLE Numerical values of site energies and individual influence on site energy shifts of important amino acids, the backbone of R-helices, the dielectric constant εborder; excitonic couplings, protonation probabilities, optical spectra obtained for unrefined site energies, and details on the treatment of the crystal structure data. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION Corresponding Author: *To whom correspondence should be addressed. E-mail: [email protected].

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ACKNOWLEDGMENT We thank D. E. Tronrud and R. E.

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Blankenship for sending the latest structural data of the FMO protein prior to publication and for helpful discussions. We also


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The Eighth Bacteriochlorophyll Completes the Excitation Energy

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