Thermal Adaptability of the Light-Harvesting Complex 2 from

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Thermal Adaptability of the Light-Harvesting Complex 2 from Thermochromatium tepidum: Temperature-Dependent Excitation Transfer Dynamics Ying Shi,† Ning-Jiu Zhao,† Peng Wang,† Li-Min Fu,† Long-Jiang Yu,‡,§ Jian-Ping Zhang,*,† and Zheng-Yu Wang-Otomo*,‡ †

Department of Chemistry, Renmin University of China, Beijing 1000872, P. R. China Faculty of Science, Ibaraki University, Mito 310-8512, Japan

‡

S Supporting Information *

ABSTRACT: The photosynthetic purple bacterium Thermochromatium (Tch.) tepidum is a thermophile that grows at an optimal temperature of ∼50 °C. We have investigated, by means of steady-state and time-resolved optical spectroscopies, the effects of temperature on the near-infrared light absorption and the excitation energy transfer (EET) dynamics of its light-harvesting complex 2 (LH2), for which the mesophilic counterpart of Rhodobacter (Rba.) sphaeroides 2.4.1 (∼30 °C) was examined in comparison. In a limited range around the physiological temperature (10−55 °C), the B800-to-B850 EET process of the Tch. tepidum LH2, but not the Rba. sphaeroides LH2, was found to be characteristically temperature-dependent, mainly because of a temperature-tunable spectral overlap. At 55 °C, the LH2 complex from Tch. tepidum maintained efficient near-infrared light harvesting and B800-to-B850 EET dynamics, whereas this EET process was disrupted in the case of Rba. sphaeroides 2.4.1 owing to the structural distortion of the LH2 complex. Our results reveal a remarkable thermal adaptability of the light-harvesting function of Tch. tepidum, which could enhance our understanding of the survival strategy of this thermophile in response to environmental challenges.

1. INTRODUCTION The primary reaction of bacterial photosynthesis involves light harvesting by the antennae and subsequent excitation energy transfer (EET) to the reaction centers (RCs) where chargeseparation reactions are initiated. There are two major types of antennae, namely, the RC-associated, core light-harvesting complex 1 (LH1) and the peripheral light-harvesting complex 2 (LH2).1−3 Depending on species or light conditions, photosynthetic bacteria can also develop various spectral variants of LH2 such as LH3 and LH4 with different spectra of nearinfrared absorption.4−7 Overall, the peripheral antennae convert light into electronic excitation that is further transferred to LH1 and eventually to the RC, and these downhill EET processes take place in a cascading manner with extremely high efficiency.8−11 The atomic-resolution crystallographic structures of the LH2s of the purple bacteria Rhodopseudomonas (Rps.) acidophila12,13 and Rhodospirilum (Rs.) molischianum14 have stimulated extensive experimental and theoretical investigations. It is known that, for Rs. molischianum and Rps. acidophila, the LH2 assemblies consist of eight and nine repeating subunits, respectively. Each subunit is a heterodimer of α and β transmembrane polypeptide helices that binds three bacteriochlorophyll a (BChl) molecules, giving rise to intense near-infrared light absorption, and one all-trans carotenoid molecule absorbing in blue-green spectral region. In the LH2 © 2015 American Chemical Society

complex of Rs. molischianum, for instance, 16 BChls lying perpendicularly to the membrane plane form a tightly coupled circular aggregate, whereas 8 BChls parallel to the membrane are weakly coupled and hence monomeric-like. The former and latter groups of BChls are termed B850 and B800, respectively, according to their characteristic Qy absorption wavelengths. In a subunit, the carotenoid molecule bypassing the B800 unit is sandwiched by the pair of B850s. For bacterial LH2 complexes, especially those from the aforementioned species, the electronic structures and excited-state properties of the B850 aggregate, as well as the EET processes among different pigment cofactors, have been examined in considerable detail, and substantial understandings of structure−function relationships have been developed.1,9,15−17 Thermochromatium (Tch.) tepidum is a photosynthetic purple bacterium that grows in the optimal temperature range of 48− 50 °C.18 Its LH2 complex consists of multicompositional polypeptides and carotenoids,19,20 and the crystallographic structure of LH2 remains unknown. Compared to mesophilic counterparts such as Rhodobacter (Rba.) sphaeroides 2.4.1 (∼30 °C), the LH1-RC core complex from Tch. tepidum exhibits notably higher thermal stability and longer-wavelength nearReceived: September 16, 2015 Revised: October 26, 2015 Published: October 29, 2015 14871

DOI: 10.1021/acs.jpcb.5b09023 J. Phys. Chem. B 2015, 119, 14871−14879

Article

The Journal of Physical Chemistry B

Figure 1. Temperature-dependent (a,b) near-infrared absorption and (c,d) fluorescence spectra of the LH2 complexes from (a,c) Tch. tepidum and (b,d) Rba. sphaeroides 2.4.1. The fluorescence excitation wavelength was 788 nm, as indicated by the red arrows.

2. MATERIALS AND METHODS 2.1. LH2 Preparations. Tch. tepidum cells were grown anaerobically at 48 °C for 7 days under a light intensity of 2000 lx. The whole cells were disrupted by ultrasonication at 4 °C for 10 min, and the chromatophores were isolated by differential centrifugation. The obtained chromatophores were resuspended in 20 mM tris(hydroxymethyl)aminomethane hydrochloride (Tris-HCl) buffer (pH 8.5) at a concentration such that OD850 nm = 50 cm−1. After solubilization with 0.35% (v/v) lauryldimethylamine oxide (LDAO; Kao Corp.) for 60 min in the dark, the suspension was centrifuged for 100 min (145400g, 4 °C). The supernatant was collected and purified with diethylaminoethyl cellulose (Whatman DE52) column chromatography in the presence of 0.05% n-dodecyl-β-D-maltoside (DDM). The LH2 preparation in 20 mM Tris·HCl buffer (pH 7.5, 0.05% DDM) was used for steady-state and time-resolved spectroscopic measurements. For the LH2 preparation from Rba. sphaeroides 2.4.1, we followed the procedures reported in ref 17, and the LH2 preparation in 20 mM Tris·HCl buffer (pH 7.8) with 0.1% LDAO was used in the experiments. 2.2. Steady-State and Time-Resolved Spectroscopies. Steady-state optical absorption spectra were recorded on a Cary-50 absorption spectrometer (Varian), whereas nearinfrared fluorescence spectra were measured with a FLS 980 fluorescence spectrometer (Edinburgh Instruments). The sample concentration for fluorescence measurements was A850 nm ≈ 0.05. The apparatus for time-resolved absorption with a 160-fs (full width at half-maximum, fwhm) instrumental response function was described in detail in ref 29. Briefly, a modelocked Ti-sapphire laser (Tsunami, Spectra Physics) in conjunction with a regenerative amplifier (SPTF-100F1KHPR, Spectra Physics) was used to generate actinic laser pulses (∼120 fs, fwhm) at 788 nm. A white-light continuum probe was generated from a 3-mm-thick sapphire plate and was detected, after interrogating the excited sample (optical path length, 1 mm), with a liquid-nitrogen-cooled charge-coupled device detector (Spec-10:400B/LN) attached to an imaging

infrared absorption. Such unique structural and spectroscopic properties are ascribed to the binding of calcium ions (Ca2+) with a given stoichiometry21,22 and were further elucidated in the recently reported high-resolution crystallographic structure of the LH1-RC complex.23 In addition, the binding of Ca2+ was recently rationalized by quantum chemical analysis.24 On the other hand, the excitation dynamics of the Tch. tepidum LH2 complex has been investigated by the use of time-resolved optical spectroscopies, which revealed efficient B800-to-B850 EET and a major photoprotective role of carotenoid.25−28 Note that, at room temperature, the B800-to-B850 EET time scale of the LH2 complex from Tch. tepidum (∼1.3 ps) was found to be considerably longer than those of the LH2s from mesophilic purple bacteria (∼0.7 ps).25 Despite the research efforts on the Tch. tepidum LH2, the possible effects of temperature on its structure and function have not been studied in detail. It is interesting for us to examine the effects of temperature variations around the physiological range (rather than at a fixed ambient temperature) on the light-harvesting and EET functionalities of the Tch. tepidum LH2 complex. The present work investigated the light-harvesting and EET functionalities of the Tch. tepidum LH2 in response to temperature variations over the range of 10−55 °C. The B800-to-B850 EET rate was found to be distinctly temperaturedependent in this temperature range, in contrast to the case of Rba. sphaeroides, for which the transfer rate is essentially temperature-independent. At 55 °C, slightly exceeding the optimal physiological temperature, the Tch. tepidum LH2 complex retains its near-infrared light absorptivity and efficient B800-to-B850 EET function, whereas for the Rba. sphaeroides LH2, the EET process is substantially disrupted at 55 °C, that is, 25 °C above its physiological temperature. These results reveal the thermal robustness of the LH2 functions of Tch. tepidum, which might be helpful in understanding the environmental adaptability of Tch. tepidum as a thermophile. The different temperature responses are discussed in terms of the structural variations between the LH2 complexes from the two bacteria. 14872

DOI: 10.1021/acs.jpcb.5b09023 J. Phys. Chem. B 2015, 119, 14871−14879

Article

The Journal of Physical Chemistry B

consisting of both α1 and α2 (or α3) apoproteins.31 In the case of Tch. tepidum, the B800 band showed 2% hypochromicity and a 5% bandwidth increase from 10 to 55 °C, whereas the B850 band exhibited 10% hypochromicity, a ∼6-nm blue shift, and a 6% bandwidth increase (Figure 1a, Table 1), indicating that the interactions of B850 with the chromophore and apoprotein surroundings are susceptible to temperature variations. In the case of Rba. sphaeroides 2.4.1 (Figure 1b, Table 1), the B800 and B850 absorption bands showed little spectral shift with changing temperature. However, when the temperature was increased from 10 to 55 °C, their amplitudes dropped by ∼10−15%, accompanied by 20% and 3% band broadening for B800 and B850, respectively. Comparing the near-infrared absorption of the LH2s from different species, one can see the following conspicuous differences: The B800 and B850 bandwidths of the Tch. tepidum LH2 are ∼40% broader than that of the Rba. sphaeroides LH2, and therefore, the binding site and/or intermolecular interactions among BChls are of substantially higher heterogeneity in the Tch. tepidum LH2. In addition, only the B850 band is sensitive to temperature variations in the case of Tch. tepidum, whereas both B800 and B850 bands are in the case of Rba. sphaeroides 2.4.1. Figure 1 also shows the near-infrared fluorescence spectra of the LH2s. In the case of the Tch. tepidum LH2 (Figure 1c, Table 1), from 10 to 55 °C, the B850 fluorescence intensity decreased monotonically with a ∼9% increase of bandwidth. Meanwhile, the fluorescence band shifted to the blue by ∼11 nm, which resulted in a substantial decrease of Stokes shift (258 → 180 cm−1). In the case of the Rba. sphaeroides LH2 (Figure 1d, Table 1), from 10 to 50 °C, the B850 fluorescence showed a monotonic intensity decrease and a ∼10% bandwidth increase. However, the fluorescence maximum blue-shifted by as little as ∼1 nm, and accordingly, the Stokes shift decreased only slightly (97 → 83 cm−1). At 55 °C, upon B800 photoexcitation, the B850 emission at 830−980 nm from the Rba. sphaeroides LH2 became nearly undetectable (Figure 1d), which is in contrast to the normal B850 fluorescence observed for the Tch. tepidum LH2 at the same temperature (Figure 1c). From the enlarged spectra in the inset of Figure 1b, one can see a slight enhancement around 760 nm in the 55 °C spectrum, indicating that some free BChls were released from the Rba. sphaeroides LH2. However, the same phenomenon was not seen for the Tch. tepidum LH2 (Figure 1a, inset). In addition, in Figure 1d, one can see that, on the shorter-wavelength side ( B850 Energy Transfer Mechanism in Bacterial LH2 Complexes Investigated by B800 Pigment Exchange. Biophys. J. 2000, 78, 2590−2596. (17) Zhang, J. P.; Fujii, R.; Qian, P.; Inaba, T.; Mizoguchi, T.; Koyama, Y.; Onaka, K.; Watanabe, Y.; Nagae, H. Mechanism of the Carotenoid-To-Bacteriochlorophyll Energy Transfer via the S-1 State in the LH2 Complexes from Purple Bacteria. J. Phys. Chem. B 2000, 104, 3683−3691. (18) Madigan, M. T. A Novel Photosynthetic Purple Bacterium Isolated from a Yellowstone Hot Spring. Science 1984, 225, 313−315. (19) Zeng, X.; Choudhary, M.; Kaplan, S. A Second and Unusual Pucba Operon of Rhodobacter sphaeroides 2.4.1: Genetics and Function of the Encoded Polypeptides. J. Bacteriol. 2003, 185, 6171−6184. (20) Sekine, F.; Horiguchi, K.; Kashino, Y.; Shimizu, Y.; Yu, L. J.; Kobayashi, M.; Wang, Z. Y. Gene Sequencing and Characterization of the Light-Harvesting Complex 2 from Thermophilic Purple Sulfur Bacterium Thermochromatium tepidum. Photosynth. Res. 2012, 111, 9− 18. (21) Kimura, Y.; Hirano, Y.; Yu, L. J.; Suzuki, H.; Kobayashi, M.; Wang, Z. Y. Calcium Ions Are Involved in the Unusual Red Shift of the Light-Harvesting 1 Q(y) Transition of the Core Complex in Thermophilic Purple Sulfur Bacterium Thermochromatium tepidum. J. Biol. Chem. 2008, 283, 13867−13873. (22) Kimura, Y.; Inada, Y.; Yu, L. J.; Wang, Z. Y.; Ohno, T. A Spectroscopic Variant of the Light-Harvesting 1 Core Complex from the Thermophilic Purple Sulfur Bacterium Thermochromatium tepidum. Biochemistry 2011, 50, 3638−3648. (23) Niwa, S.; Yu, L. J.; Takeda, K.; Hirano, Y.; Kawakami, T.; WangOtomo, Z. Y.; Miki, K. Structure of the LH1-RC Complex from Thermochromatium tepidum at 3.0 Å. Nature 2014, 508, 228−232. (24) Khrenova, M. G.; Nemukhin, A. V.; Grigorenko, B. L.; Wang, P.; Zhang, J. P. All-Atom Structures and Calcium Binding Sites of the Bacterial Photosynthetic LH1-RC Core Complex from Thermochromatium tepidum. J. Mol. Model. 2014, 20, 2287-1−2287-6. (25) Yang, F.; Yu, L. J.; Wang, P.; Ai, X. C.; Wang, Z. Y.; Zhang, J. P. Effects of Aggregation on the Excitation Dynamics of LH2 from Thermochromatium tepidum in Aqueous Phase and in Chromatophores. J. Phys. Chem. B 2011, 115, 7906−7913. (26) Niedzwiedzki, D. M.; Fuciman, M.; Kobayashi, M.; Frank, H. A.; Blankenship, R. E. Ultrafast Time-Resolved Spectroscopy of the LightHarvesting Complex 2 (LH2) from the Photosynthetic Bacterium Thermochromatium tepidum. Photosynth. Res. 2011, 110, 49−60. (27) Yang, F.; Yu, L. J.; Wang, P.; Ai, X. C.; Wang, Z. Y.; Zhang, J. P. Excitation Dynamics of the Light-Harvesting Complex 2 from Thermochromatium tepidum. Acta Phys.-Chim. Sin. 2010, 26, 2021− 2030. (28) Niedzwiedzki, D. M.; Kobayashi, M.; Blankenship, R. E. Triplet Excited State Spectra and Dynamics of Carotenoids from the Thermophilic Purple Photosynthetic Bacterium Thermochromatium tepidum. Photosynth. Res. 2011, 107, 177−186. (29) Zhang, W.; Hu, R.; Li, D.; Huo, M.-M.; Ai, X.-C.; Zhang, J.-P. Primary Dynamics of Exciton and Charge Photogeneration in Solvent Vapor Annealed P3HT/PCBM Films. J. Phys. Chem. C 2012, 116, 4298−4310. (30) van Dijk, B.; Nozawa, T.; Hoff, A. J. The B800−850 Complex of the Purple Bacterium Chromatium tepidum: Low-Temperature Absorption and Stark Spectra. Spectrochim. Acta, Part A 1998, 54, 1269−1278. (31) Löhner, A.; Carey, A.-M.; Hacking, K.; Picken, N.; Kelly, S.; Cogdell, R.; Köhler, J. The Origin of the Split B800 Absorption Peak in the LH2 Complexes from Allochromatium vinosum. Photosynth. Res. 2015, 123, 23−31.

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Department of Biology, Faculty of Science, Okayama University, Okayama, Japan. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS Grants in Aid (Nos. 21173265 and 21273282) and China− Russia cooperative project (No. 21411130185) from the Natural Science Foundation of China are acknowledged. We are grateful for the support from the Fundamental Research Funds for the Central Universities and the Research Funds of Renmin University of China (No. 10XNI007).

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REFERENCES

(1) Sundström, V.; Pullerits, T.; van Grondelle, R. Photosynthetic Light-Harvesting: Reconciling Dynamics and Structure of Purple Bacterial LH2 Reveals Function of Photosynthetic Unit. J. Phys. Chem. B 1999, 103, 2327−2346. (2) Cogdell, R.; Lindsay, J. G. Tansley Review No. 109. The Structure of Photosynthetic Complexes in Bacteria and Plants: an Illustration of the Importance of Protein Structure To the Future Development of Plant Science. New Phytol. 2000, 145, 167−196. (3) Sturgis, J. N.; Tucker, J. D.; Olsen, J. D.; Hunter, C. N.; Niederman, R. A. Atomic Force Microscopy Studies of Native Photosynthetic Membranes. Biochemistry 2009, 48, 3679−3698. (4) McLuskey, K.; Prince, S.; Cogdell, R.; Isaacs, N. The Crystallographic Structure of the B800−820 LH3 Light-Harvesting Complex from the Purple Bacteria Rhodopseudomonas acidophila strain 7050. Biochemistry 2001, 40, 8783−8789. (5) Cogdell, R. J.; Hawthornthwaite, A. M.; Evans, M. B.; Ferguson, L. A.; Kerfeld, C.; Thornber, J. P.; van Mourik, F.; van Grondelle, R. Isolation and Characterisation of an Unusual Antenna Complex from the Marine Purple Sulphur Photosynthetic Bacterium Chromatium purpuratum BN5500. Biochim. Biophys. Acta, Bioenerg. 1990, 1019, 239−244. (6) Hartigan, N.; Tharia, H. A.; Sweeney, F.; Lawless, A. M.; Papiz, M. Z. The 7.5-Å Electron Density and Spectroscopic Properties of a Novel Low-Light B800 LH2 from Rhodopseudomonas palustris. Biophys. J. 2002, 82, 963−977. (7) Niedzwiedzki, D. M.; Fuciman, M.; Frank, H. A.; Blankenship, R. E. Energy Transfer in an LH4-Like Light Harvesting Complex from the Aerobic Purple Photosynthetic Bacterium Roseobacter denitrif icans. Biochim. Biophys. Acta, Bioenerg. 2011, 1807, 518−528. (8) Hu, X.; Damjanović, A.; Ritz, T.; Schulten, K. Architecture and Mechanism of the Light-Harvesting Apparatus of Purple Bacteria. Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 5935−5941. (9) Linnanto, J.; Korppi-Tommola, J. Modelling Excitonic Energy Transfer in the Photosynthetic Unit of Purple Bacteria. Chem. Phys. 2009, 357, 171−180. (10) Cogdell, R. J.; Gardiner, A. T.; Roszak, A. W.; Law, C. J.; Southall, J.; Isaacs, N. W. Rings, Ellipses and Horseshoes: How Purple Bacteria Harvest Solar Energy. Photosynth. Res. 2004, 81, 207−214. (11) Cogdell, R. J.; Gall, A.; Köhler, J. The Architecture and Function of the Light-Harvesting Apparatus of Purple Bacteria: from Single Molecules To in Vivo Membranes. Q. Rev. Biophys. 2006, 39, 227− 324. ( 1 2 ) M c d e r m o t t , G . ; P r in c e , S . M . ; Fr e e r , A . A .; Hawthornthwaitelawless, A. M.; Papiz, M. Z.; Cogdell, R. J.; Isaacs, N. W. Crystal-Structure of an Integral Membrane Light-Harvesting Complex from Photosynthetic Bacteria. Nature 1995, 374, 517−521. (13) Papiz, M. Z.; Prince, S. M.; Howard, T.; Cogdell, R. J.; Isaacs, N. W. The Structure and Thermal Motion of the B800−850 LH2 Complex from Rps. acidophila at 2.0 Å Resolution and 100K: New Structural Features and Functionally Relevant Motions. J. Mol. Biol. 2003, 326, 1523−1538. 14878

DOI: 10.1021/acs.jpcb.5b09023 J. Phys. Chem. B 2015, 119, 14871−14879

Article

The Journal of Physical Chemistry B (32) Pullerits, T.; Chachisvilis, M.; Sundströ m, V. Exciton Delocalization Length in the B850 Antenna of Rhodobacter sphaeroides. J. Phys. Chem. 1996, 100, 10787−10792. (33) Shreve, A. P.; Trautman, J. K.; Owens, T. G.; Frank, H. A.; Albrecht, A. C. Invivo Energy-Transfer Studies in Photosynthetic Systems by Subpicosecond Timing. Proc. SPIE 1990, 1403, 394−399. (34) Shreve, A. P.; Trautman, J. K.; Frank, H. A.; Owens, T. G.; Albrecht, A. C. Femtosecond Energy-Transfer Processes in the B800− 850 Light-Harvesting Complex of Rhodobacter sphaeroides 2.4.1. Biochim. Biophys. Acta, Bioenerg. 1991, 1058, 280−288. (35) Kennis, J. T. M.; Streltsov, A. M.; Vulto, S. I. E.; Aartsma, T. J.; Nozawa, T.; Amesz, J. Femtosecond Dynamics in Isolated LH2 Complexes of Various Species of Purple Bacteria. J. Phys. Chem. B 1997, 101, 7827−7834. (36) Pullerits, T.; Hess, S.; Herek, J. L.; Sundström, V. Temperature Dependence of Excitation Transfer in LH2 of Rhodobacter sphaeroides. J. Phys. Chem. B 1997, 101, 10560−10567. (37) Pajusalu, M.; Rätsep, M.; Trinkunas, G.; Freiberg, A. Davydov Splitting of Excitons in Cyclic Bacteriochlorophyll a Nanoaggregates of Bacterial Light-Harvesting Complexes between 4.5 and 263 K. ChemPhysChem 2011, 12, 634−644. (38) Trinkunas, G.; Zerlauskiene, O.; Urbonienė, V.; Chmeliov, J.; Gall, A.; Robert, B.; Valkunas, L. Exciton Band Structure in Bacterial Peripheral Light-Harvesting Complexes. J. Phys. Chem. B 2012, 116, 5192−5198. (39) Kunz, R.; Timpmann, K.; Southall, J.; Cogdell, R. J.; Köhler, J.; Freiberg, A. Fluorescence-Excitation and Emission Spectra from LH2 Antenna Complexes of Rhodopseudomonas acidophila as a Function of the Sample Preparation Conditions. J. Phys. Chem. B 2013, 117, 12020−12029. (40) Hess, S.; Åkesson, E.; Cogdell, R. J.; Pullerits, T.; Sundström, V. Energy Transfer in Spectrally Inhomogeneous Light-Harvesting Pigment-Protein Complexes of Purple Bacteria. Biophys. J. 1995, 69, 2211−2225. (41) Hess, S.; Feldchtein, F.; Babin, A.; Nurgaleev, I.; Pullerits, T.; Sergeev, A.; Sundström, V. Femtosecond Energy-Transfer within the LH2 Peripheral Antenna of the Photosynthetic Purple Bacteria Rhodobacter sphaeroides and Rhodopseudomonas palustris Ll. Chem. Phys. Lett. 1993, 216, 247−257. (42) Joo, T. H.; Jia, Y. W.; Yu, J. Y.; Jonas, D. M.; Fleming, G. R. Dynamics in Isolated Bacterial Light Harvesting Antenna (LH2) of Rhodobacter sphaeroides at Room Temperature. J. Phys. Chem. 1996, 100, 2399−2409. (43) Kennis, J. T. M.; Streltsov, A. M.; Permentier, H.; Aartsma, T. J.; Amesz, J. Exciton Coherence and Energy Transfer in the LH2 Antenna Complex of Rhodopseudomonas acidophila at Low Temperature. J. Phys. Chem. B 1997, 101, 8369−8374. (44) Salverda, J. M.; van Mourik, F.; van der Zwan, G.; van Grondelle, R. Energy Transfer in the B800 Rings of the Peripheral Bacterial Light-Harvesting Complexes of Rhodopseudomonas acidophila and Rhodospirillum molischianum Studied with Photon Echo Techniques. J. Phys. Chem. B 2000, 104, 11395−11408. (45) Ma, J.; Cao, J. Förster Resonance Energy Transfer, Absorption and Emission Spectra in Multichromophoric Systems. I. Full Cumulant Expansions and System-Bath Entanglement. J. Chem. Phys. 2015, 142, 094106. (46) Jang, S.; Newton, M. D.; Silbey, R. J. Multichromophoric Forster Resonance Energy Transfer from B800 To B850 in the Light Harvesting Complex 2: Evidence for Subtle Energetic Optimization by Purple Bacteria. J. Phys. Chem. B 2007, 111, 6807−6814. (47) Sumi, H. Theory on Rates of Excitation-Energy Transfer Between Molecular Aggregates Through Distributed Transition Dipoles with Application To the Antenna System in Bacterial Photosynthesis. J. Phys. Chem. B 1999, 103, 252−260. (48) Scholes, G. D. Long-Range Resonance Energy Transfer in Molecular Systems. Annu. Rev. Phys. Chem. 2003, 54, 57−87. (49) Harel, E.; Engel, G. S. Quantum Coherence Spectroscopy Reveals Complex Dynamics in Bacterial Light-Harvesting Complex 2 (LH2). Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 706−711. 14879

DOI: 10.1021/acs.jpcb.5b09023 J. Phys. Chem. B 2015, 119, 14871−14879