Abstract
Two-dimensional electronic spectra (2DES) provide unique ways to track the energy transfer dynamics in light-harvesting complexes. The interpretation of the peaks and structures found in experimentally recorded 2DES is often not straightforward, since several processes are imaged simultaneously. The choice of specific pulse polarization sequences helps to disentangle the sometimes convoluted spectra, but brings along other disturbances. We show by detailed theoretical calculations how 2DES of the Fenna–Matthews–Olson complex are affected by rotational and conformational disorder of the chromophores.
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References
Adolphs J, Renger T (2006) How proteins trigger excitation energy transfer in the FMO complex of green sulfur bacteria. Biophys J 91(8):2778–2797. https://doi.org/10.1529/biophysj.105.079483
Adolphs J, Müh F, Madjet MEA, Renger T (2008) Calculation of pigment transition energies in the FMO protein. Photosynth Res 95(2–3):197–209. https://doi.org/10.1007/s11120-007-9248-z
Aghtar M, Strümpfer J, Olbrich C, Schulten K, Kleinekathöfer U (2013) The FMO complex in a glycerol–water mixture. J Phys Chem B 117(24):7157–7163. https://doi.org/10.1021/jp311380k
Avery J, Bay Z, Szent-Gyorgyi A (1961) On the energy transfer in biological systems. Proc Natl Acad Sci USA 47(11):1742–1744
Bína D, Gardian Z, Vácha F, Litvín R (2016) Native FMO-reaction center supercomplex in green sulfur bacteria: an electron microscopy study. Photosynth Res 128(1):93–102. https://doi.org/10.1007/s11120-015-0205-y
Blankenship RE (2014) Molecular mechanisms of photosynthesis, 2nd edn. Wiley, Oxford
Brixner T, Stenger J, Vaswani HM, Cho M, Blankenship RE, Fleming GR (2005) Two-dimensional spectroscopy of electronic couplings in photosynthesis. Nature 434(7033):625–628. https://doi.org/10.1038/nature03429
Chen L, Zheng R, Jing Y, Shi Q (2011) Simulation of the two-dimensional electronic spectra of the Fenna–Matthews–Olson complex using the hierarchical equations of motion method. J Chem Phys 134(19):194508–194508. https://doi.org/10.1063/1.3589982
Cho M (2008) Coherent two-dimensional optical spectroscopy. Chem Rev 108(4):1331–1418. https://doi.org/10.1021/cr078377b
Dostál J, Pšenčík J, Zigmantas D (2016) In situ mapping of the energy flow through the entire photosynthetic apparatus. Nat Chem 8(7):705–710. https://doi.org/10.1038/nchem.2525
Engel GS, Calhoun TR, Read EL, Ahn TK, Mančal T, Cheng YC, Blankenship RE, Fleming GR (2007) Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446(7137):782–786. https://doi.org/10.1038/nature05678
Fenna RE, Matthews BW (1975) Chlorophyll arrangement in a bacteriochlorophyll protein from Chlorobium limicola. Nature 258(5536):573–577. https://doi.org/10.1038/258573a0
Gelin MF, Borrelli R, Domcke W (2017) Efficient orientational averaging of nonlinear optical signals in multi-chromophore systems. J Chem Phys 147(4):044114–044114. https://doi.org/10.1063/1.4996205
Gordon R (1968) Correlation functions for molecular motion, vol 3. Advances in magnetic and optical resonance. Academic press inc., Cambridge, pp 1–42. https://doi.org/10.1016/B978-1-4832-3116-7.50008-4
Hamm P, Zanni MT (2011) Concepts of 2D spectroscopy. Cambridge University Press, Cambridge
Hein B, Kreisbeck C, Kramer T, Rodríguez M (2012) Modelling of oscillations in two-dimensional echo-spectra of the Fenna–Matthews–Olson complex. New J Phys 14(2):023018–023018. https://doi.org/10.1088/1367-2630/14/2/023018
Hochstrasser RM (2001) Two-dimensional IR-spectroscopy: polarization anisotropy effects. Chem Phys 266(2–3):273–284. https://doi.org/10.1016/S0301-0104(01)00232-4
Ishizaki A, Fleming GR (2009) On the adequacy of the Redfield equation and related approaches to the study of quantum dynamics in electronic energy transfer. J Chem Phys 130(23):234110–234110. https://doi.org/10.1063/1.3155214
Kramer T, Kreisbeck C (2014) Modelling excitonic-energy transfer in light-harvesting complexes. AIP Conf Proc 1575:111–135. https://doi.org/10.1063/1.4861701
Kramer T, Rodriguez M (2017) Two-dimensional electronic spectra of the photosynthetic apparatus of green sulfur bacteria. Sci Rep 7:45245–45245. https://doi.org/10.1038/srep45245
Kramer T, Noack M, Reimers JR, Reinefeld A, Rodríguez M, Yin S (2018a) Energy flow in the Photosystem I supercomplex: comparison of approximative theories with DM-HEOM. Chem Phys 515:262–271. https://doi.org/10.1016/j.chemphys.2018.05.028
Kramer T, Noack M, Reinefeld A, Rodríguez M, Zelinskyy Y (2018b) Efficient calculation of open quantum system dynamics and time-resolved spectroscopy with distributed memory HEOM (DM-HEOM). J Comput Chem 39(22):1779. https://doi.org/10.1002/jcc.25354
Kreisbeck C, Kramer T (2012) Long-lived electronic coherence in dissipative exciton dynamics of light-harvesting complexes. J Phys Chem Lett 3(19):2828–2833. https://doi.org/10.1021/jz3012029
Kreisbeck C, Kramer T, Rodríguez M, Hein B (2011) High-performance solution of hierarchical equations of motion for studying energy transfer in light-harvesting complexes. J Chem Theory Comput 7(7):2166–2174. https://doi.org/10.1021/ct200126d
Kreisbeck C, Kramer T, Aspuru-Guzik A (2013) Disentangling electronic and vibronic coherences in two-dimensional echo spectra. J Phys Chem B 117(32):9380–9385. https://doi.org/10.1021/jp405421d
Kreisbeck C, Kramer T, Aspuru-Guzik A (2014) Scalable high-performance algorithm for the simulation of exciton dynamics. Application to the light-harvesting complex II in the presence of resonant vibrational modes. J Chem Theory Comput 10:4045–4054. https://doi.org/10.1021/ct500629s
Lambrev PH, Akhtar P, Tan HS (2019) Insights into the mechanisms and dynamics of energy transfer in plant light-harvesting complexes from two-dimensional electronic spectroscopy. Biochimica et Biophysica Acta (BBA) - Bioenergetics. https://doi.org/10.1016/j.bbabio.2019.07.005
Lindorfer D, Renger T (2018) Theory of anisotropic circular dichroism of excitonically coupled systems: application to the baseplate of green sulfur bacteria. J Phys Chem B 122(10):2747–2756. https://doi.org/10.1021/acs.jpcb.7b12832
May V, Kühn O (2008) Optical field control of charge transmission through a molecular wire I. Generalized master equation description. Phys Rev B 77(11):115439–115439. https://doi.org/10.1103/PhysRevB.77.115439
Mukamel S (1995) Principles of nonlinear optical spectroscopy. Oxford University Press, Oxford
Noack M, Reinefeld A, Kramer T, Steinke T (2018) DM-HEOM: a portable and scalable solver-framework for the hierarchical equations of motion. In: 2018 IEEE international parallel and distributed processing symposium workshops (IPDPSW) p 947. https://doi.org/10.1109/IPDPSW.2018.00149
Novoderezhkin VI, van Grondelle R (2017) Modeling of excitation dynamics in photosynthetic light-harvesting complexes: exact versus perturbative approaches. J Phys B Atomic Mol Opt Phys 50(12):124003–124003. https://doi.org/10.1088/1361-6455/aa6b87
Nuernberger P, Ruetzel S, Brixner T (2015) Multidimensional electronic spectroscopy of photochemical reactions. Angew Chem Int Ed 54(39):11368–11386. https://doi.org/10.1002/anie.201502974
Olbrich C, Jansen TLC, Liebers J, Aghtar M, Strümpfer J, Schulten K, Knoester J, Kleinekathöfer U (2011) From atomistic modeling to excitation transfer and two-dimensional spectra of the FMO light-harvesting complex. J Phys Chem B 115(26):8609–8621. https://doi.org/10.1021/jp202619a
Olson JM, Romano CA (1962) A new chlorophyll from green bacteria. Biochim Biophys Acta 59(3):726–728. https://doi.org/10.1016/0006-3002(62)90659-5
Panitchayangkoon G, Hayes D, a Fransted K, Caram JR, Harel E, Wen J, Blankenship RE, Engel GS, (2010) Long-lived quantum coherence in photosynthetic complexes at physiological temperature. In: Proceedings of the National Academy of Sciences of the United States of America 107(29):12766–70. https://doi.org/10.1073/pnas.1005484107
Rodríguez M, Kramer T (2019) Machine learning of two-dimensional spectroscopic data. Chem Phys 520:52–60. https://doi.org/10.1016/j.chemphys.2019.01.002
Schlau-Cohen GS, Ishizaki A, Calhoun TR, Ginsberg NS, Ballottari M, Bassi R, Fleming GR (2012) Elucidation of the timescales and origins of quantum electronic coherence in LHCII. Nat Chem 4(5):389–395. https://doi.org/10.1038/nchem.1303
Tanimura Y, Kubo R (1989) Time evoultion of a quantum system in contact with a nearly Gaussian–Markoffian noise bath. J Phys Soc Jpn 58(1):101–114. https://doi.org/10.1143/JPSJ.58.101
Thyrhaug E, Žídek K, Dostál J, Bína D, Zigmantas D (2016) Exciton structure and energy transfer in the Fenna–Matthews–Olson complex. J Phys Chem Lett 7(9):1653–1660. https://doi.org/10.1021/acs.jpclett.6b00534
Thyrhaug E, Tempelaar R, Alcocer MJP, Žídek K, Bína D, Knoester J, Jansen TLC, Zigmantas D (2018) Identification and characterization of diverse coherences in the Fenna–Matthews–Olson complex. Nat Chem 10(7):780–786. https://doi.org/10.1038/s41557-018-0060-5
Tiwari V, Peters WK, Jonas DM (2013) Electronic resonance with anticorrelated pigment vibrations drives photosynthetic energy transfer outside the adiabatic framework. Proc Natl Acad Sci 110(4):1203–1208. https://doi.org/10.1073/pnas.1211157110
Tronrud DE, Wen J, Gay L, Blankenship RE (2009) The structural basis for the difference in absorbance spectra for the FMO antenna protein from various green sulfur bacteria. Photosynth Res 100(2):79–87. https://doi.org/10.1007/s11120-009-9430-6
Vulto SIE, de Baat MA, Louwe RJW, Permentier HP, Neef T, Miller M, van Amerongen H, Aartsma TJ (1998) Exciton simulations of optical spectra of the FMO complex from the green sulfur bacterium chlorobium tepidum at 6 K. J Phys Chem B 102(47):9577–9582. https://doi.org/10.1021/jp982095l
Vulto SIE, de Baat MA, Neerken S, Nowak FR, van Amerongen H, Amesz J, Aartsma TJ (1999) Excited state dynamics in FMO antenna complexes from photosynthetic green sulfur bacteria: a kinetic model. J Phys Chem B 103(38):8153–8161. https://doi.org/10.1021/jp984702a
Westenhoff S, Palecek D, Edlund P, Smith P, Zigmantas D (2012) Coherent picosecond exciton dynamics in a photosynthetic reaction center. J Am Chem Soc 134(40):16484–16487. https://doi.org/10.1021/ja3065478
Yuen-Zhou J, Krich JJ, Kassal I, Johnson A, Aspuru-Guzik A (2014) Ultrafast spectroscopy. IOP Publ. https://doi.org/10.1088/978-0-750-31062-8
Zanni MT, Ge NH, Kim YS, Hochstrasser RM (2001) Two-dimensional IR spectroscopy can be designed to eliminate the diagonal peaks and expose only the crosspeaks needed for structure determination. Proc Natl Acad Sci 98(20):11265–11270. https://doi.org/10.1073/pnas.201412998
Acknowledgements
The work was supported by the German Research Foundation (DFG) grants KR 2889 and RE 1389 (“Realistic Simulations of Photoactive Systems on HPC Clusters with Many Core Processors”). We acknowledge compute time allocation by the North German Supercomputing Alliance (HLRN). M.R. has received funding from the European Union’s Horizon 2020 research and innovation program under the Marie Sklodowska-Curie Grant agreement No. 707636.
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Kramer, T., Rodríguez, M. Effect of disorder and polarization sequences on two-dimensional spectra of light-harvesting complexes. Photosynth Res 144, 147–154 (2020). https://doi.org/10.1007/s11120-019-00699-6
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DOI: https://doi.org/10.1007/s11120-019-00699-6