Quantum chemical elucidation of a sevenfold symmetric bacterial antenna complex
Jazyk angličtina Země Nizozemsko Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
ERC-AdG-786714
HORIZON EUROPE European Research Council
BB/N016734/1
Biotechnology and Biological Sciences Research Council - United Kingdom
PubMed
35672557
PubMed Central
PMC10070313
DOI
10.1007/s11120-022-00925-8
PII: 10.1007/s11120-022-00925-8
Knihovny.cz E-zdroje
- Klíčová slova
- Excitons, Light-harvesting, Molecular dynamics, Pigment-protein complex, QM/MM, Quantum chemistry,
- MeSH
- bakteriochlorofyly chemie MeSH
- elektronová kryomikroskopie MeSH
- fotosyntetická reakční centra (proteinové komplexy) * chemie MeSH
- Proteobacteria metabolismus MeSH
- simulace molekulární dynamiky MeSH
- světlosběrné proteinové komplexy * metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- bakteriochlorofyly MeSH
- fotosyntetická reakční centra (proteinové komplexy) * MeSH
- světlosběrné proteinové komplexy * MeSH
The light-harvesting complex 2 (LH2) of purple bacteria is one of the most studied photosynthetic antenna complexes. Its symmetric structure and ring-like bacteriochlorophyll arrangement make it an ideal system for theoreticians and spectroscopists. LH2 complexes from most bacterial species are thought to have eightfold or ninefold symmetry, but recently a sevenfold symmetric LH2 structure from the bacterium Mch. purpuratum was solved by Cryo-Electron microscopy. This LH2 also possesses unique near-infrared absorption and circular dichroism (CD) spectral properties. Here we use an atomistic strategy to elucidate the spectral properties of Mch. purpuratum LH2 and understand the differences with the most commonly studied LH2 from Rbl. acidophilus. Our strategy exploits a combination of molecular dynamics simulations, multiscale polarizable quantum mechanics/molecular mechanics calculations, and lineshape simulations. Our calculations reveal that the spectral properties of LH2 complexes are tuned by site energies and exciton couplings, which in turn depend on the structural fluctuations of the bacteriochlorophylls. Our strategy proves effective in reproducing the absorption and CD spectra of the two LH2 complexes, and in uncovering the origin of their differences. This work proves that it is possible to obtain insight into the spectral tuning strategies of purple bacteria by quantitatively simulating the spectral properties of their antenna complexes.
Department of Chemistry and Industrial Chemistry University of Pisa 56124 Pisa Italy
Institute of Molecular Cell and Systems Biology University of Glasgow Glasgow G12 8QQ UK
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Bondanza M, Nottoli M, Cupellini L, Lipparini F, Mennucci B. Polarizable embedding QM/MM: the future gold standard for complex (bio)systems? Phys Chem Chem Phys. 2020;22(26):14433. doi: 10.1039/D0CP02119A. PubMed DOI
Cardoso Ramos F, Nottoli M, Cupellini L, Mennucci B. The molecular mechanisms of light adaption in light-harvesting complexes of purple bacteria revealed by a multiscale modeling. Chem Sci. 2019;2(42):9650. doi: 10.1039/C9SC02886B. PubMed DOI PMC
Caricato M, Mennucci B, Tomasi J, Ingrosso F, Cammi R, Corni S, Scalmani G. Formation and relaxation of excited states in solution: a new time dependent polarizable continuum model based on time dependent density functional theory. J Chem Phys. 2006;124(12):124520. doi: 10.1063/1.2183309. PubMed DOI
Case DA, Ben-Shalom IY, Brozell SR, Cerutti DS, Cheatham TE, III, Cruzeiro VWD, Darden TA, Duke R, Ghoreishi D, Gilson MK, Gohlke H, Goetz AW, Greene D, Harris R, Homeyer N, Izadi S, Kovalenko A, Kurtzman T, Lee TS, LeGrand S, Li P, Lin C, Liu J, Luchko T, Luo R, Mermelstein DJ, Merz KM, Miao Y, Monard G, Nguyen C, Nguyen H, Omelyan I, Onufriev A, Pan F, Qi R, Roe DR, Roitberg A, Sagui C, Schott-Verdugo S, Shen J, Simmerling CL, Smith J, Salomon-Ferrer R, Swails J, Walker RC, Wang J, Wei H, Wolf RM, Wu X, Xiao L, York DM, Kollman PA Amber 2018 (2018) AMBER 2018 University of California, San Francisco
Ceccarelli M, Procacci P, Marchi M. An ab initio force field for the cofactors of bacterial photosynthesis. J Comput Chem. 2003;24(2):129. doi: 10.1002/jcc.10198. PubMed DOI
Cignoni E, Slama V, Cupellini L, Mennucci B. The atomistic modeling of light-harvesting complexes from the physical models to the computational protocol. J Chem Phys. 2022;156:120901. doi: 10.1063/5.0086275. PubMed DOI
Cogdell RJ, Hawthornthwaite AM, Evans MB, Ferguson LA, Kerfeld C, Thornber J, van Mourik F, van Grondelle R. Isolation and characterisation of an unusual antenna complex from the marine purple sulphur photosynthetic bacterium Chromatium Purpuratum BN5500. BBA. 1990;1019(3):239. doi: 10.1016/0005-2728(90)90199-e. DOI
Cogdell RJ, 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(03):227. doi: 10.1017/S0033583506004434. PubMed DOI
Cp Hsu, You ZQ, Chen HC. Characterization of the short-range couplings in excitation energy transfer. J Phys Chem C. 2008;112(4):1204. doi: 10.1021/jp076512i. DOI
Cupellini L, Jurinovich S, Campetella M, Caprasecca S, Guido CA, Kelly SM, Gardiner AT, Cogdell R, Mennucci B. An ab initio description of the excitonic properties of lh2 and their temperature dependence. J Phys Chem B. 2016;120(44):11348. doi: 10.1021/acs.jpcb.6b06585. PubMed DOI
Cupellini L, Caprasecca S, Guido CA, Müh F, Renger T, Mennucci B. Coupling to charge transfer states is the key to modulate the optical bands for efficient light harvesting in purple bacteria. J Phys Chem Lett. 2018;9(23):6892. doi: 10.1021/acs.jpclett.8b03233. PubMed DOI
Cupellini L, Corbella M, Mennucci B, Curutchet C. Electronic energy transfer in biomacromolecules. WIREs Comput Mol Sci. 2019;9(2):e1392. doi: 10.1002/wcms.1392. DOI
Cupellini L, Bondanza M, Nottoli M, Mennucci B. Successes & challenges in the atomistic modeling of light-harvesting and its photoregulation. Biochim Biophys Acta. 2020;4:148049. doi: 10.1016/j.bbabio.2019.07.004. PubMed DOI
Cupellini L, Lipparini F, Cao J. Successes & challenges in the atomistic modeling of light-harvesting and its photoregulation. J Phys Chem B. 2020;124(39):8610. doi: 10.1021/acs.jpcb.0c05180. PubMed DOI PMC
Curutchet C, Mennucci B. Quantum chemical studies of light harvesting. Chem Rev. 2017;117(2):294. doi: 10.1021/acs.chemrev.5b00700. PubMed DOI
Curutchet C, Muñoz-Losa A, Monti S, Kongsted J, Scholes GD, Mennucci B. Electronic energy transfer in condensed phase studied by a polarizable QM/MM model. J Chem Theory Comput. 2009;5(7):1838. doi: 10.1021/ct9001366. PubMed DOI
De Vico L, Anda A, Osipov VA, Madsen AØ, Hansen T. Macrocycle ring deformation as the secondary design principle for light-harvesting complexes. Proc Natl Acad Sci USA. 2018;115(39):E9051. doi: 10.1073/pnas.1719355115. PubMed DOI PMC
Dickson CJ, Madej BD, Skjevik ÅA, Betz RM, Teigen K, Gould IR, Walker RC. Lipid14: the amber lipid force field. J Chem Theory Comput. 2014;10(2):865. doi: 10.1021/ct4010307. PubMed DOI PMC
Dinh TC, Renger T. Towards an exact theory of linear absorbance and circular dichroism of pigment-protein complexes: importance of non-secular contributions. J Chem Phys. 2015;142(3):034104. doi: 10.1063/1.4904928. PubMed DOI
Dinh TC, Renger T. Lineshape theory of pigment-protein complexes: how the finite relaxation time of nuclei influences the exciton relaxation-induced lifetime broadening. J Chem Phys. 2016;145(3):034105. doi: 10.1063/1.4958322. PubMed DOI
Ferretti M, Hendrikx R, Romero E, Southall J, Cogdell RJ, Novoderezhkin VI, Scholes GD, van Grondelle R. Dark states in the light-harvesting complex 2 revealed by two-dimensional electronic spectroscopy. Sci Rep. 2016;6(1):20834. doi: 10.1038/srep20834. PubMed DOI PMC
Gardiner AT, Naydenova K, Castro-Hartmann P, Nguyen-Phan TC, Russo CJ, Sader K, Hunter CN, Cogdell RJ, Qian P. The 2.4 Å cryo-EM structure of a heptameric light-harvesting 2 complex reveals two carotenoid energy transfer pathways. Sci Adv. 2021;7(7):1. doi: 10.1126/sciadv.abe4650. PubMed DOI PMC
Gellings E, Cogdell RJ, van Hulst NF. Room-temperature excitation-emission spectra of single LH2 complexes show remarkably little variation. J Phys Chem Lett. 2020;11(7):2430. doi: 10.1021/acs.jpclett.0c00375. PubMed DOI
Gelzinis A, Abramavicius D, Valkunas L. Absorption lineshapes of molecular aggregates revisited. J Chem Phys. 2015;142(15):154107. doi: 10.1063/1.4918343. PubMed DOI
Georgakopoulou S, Frese RN, Johnson E, Koolhaas C, Cogdell RJ, van Grondelle R, van der Zwan G. Absorption and CD spectroscopy and modeling of various LH2 complexes from purple bacteria. Biophys J. 2002;82(4):2184. doi: 10.1016/S0006-3495(02)75565-3. PubMed DOI PMC
Gudowska-Nowak E, Newton MD, Fajer J. Conformational and environmental effects on bacteriochlorophyll optical spectra: correlations of calculated spectra with structural results. J Phys Chem. 1990;94(15):5795. doi: 10.1021/j100378a036. DOI
Higashi M, Kosugi T, Hayashi S, Saito S. Theoretical study on excited states of bacteriochlorophyll a in solutions with density functional assessment. J Phys Chem B. 2014;118(37):10906. doi: 10.1021/jp507259g. PubMed DOI
Iozzi M, Mennucci B, Tomasi J, Cammi R. Excitation energy transfer (EET) between molecules in condensed matter: a novel application of the polarizable continuum model (PCM) J Chem Phys. 2004;120:7029. doi: 10.1063/1.1669389. PubMed DOI
Jang SJ, Mennucci B. Delocalized excitons in natural light-harvesting complexes. Rev Mod Phys. 2018;90(3):035003. doi: 10.1103/revmodphys.90.035003. DOI
Jang S, Rivera E, Montemayor D. Molecular level design principle behind optimal sizes of photosynthetic LH2 complex: taming disorder through cooperation of hydrogen bonding and quantum delocalization. J Phys Chem Lett. 2015;6(6):928. doi: 10.1021/acs.jpclett.5b00078. PubMed DOI
Jurinovich S, Cupellini L, Guido CA, Mennucci B. EXAT: excitonic analysis tool. J Comput Chem. 2018;39(5):279. doi: 10.1002/jcc.25118. PubMed DOI
Kim J, Nguyen-Phan TC, Gardiner AT, Yoon TH, Cogdell RJ, Cho M, Scholes GD. Vibrational modes promoting exciton relaxation in the B850 band of LH2. J Phys Chem Lett. 2022;13(4):1099. doi: 10.1021/acs.jpclett.1c03868. PubMed DOI
Koepke J, Hu X, Muenke C, Schulten K, Michel H. The crystal structure of the light-harvesting complex II (B800–850) from Rhodospirillum molischianum. Structure. 1996;4(5):581. doi: 10.1016/s0969-2126(96)00063-9. PubMed DOI
Kunz R, Timpmann K, Southall J, Cogdell RJ, 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(40):12020. doi: 10.1021/jp4073697. PubMed DOI
Kunz R, Timpmann K, Southall J, Cogdell RJ, Freiberg A, Köhler J. Single-molecule spectroscopy unmasks the lowest exciton state of the B850 Assembly in LH2 from Rps. Acidophila Biophys J. 2014;106(9):2008. doi: 10.1016/j.bpj.2014.03.023. PubMed DOI PMC
Leiger K, Linnanto JM, Rätsep M, Timpmann K, Ashikhmin AA, Moskalenko AA, Fufina TY, Gabdulkhakov AG, Freiberg A. Controlling photosynthetic excitons by selective pigment photooxidation. J Phys Chem B. 2019;123(1):29. doi: 10.1021/acs.jpcb.8b08083. PubMed DOI
Lipparini F, Mennucci B. Hybrid QM/classical models: methodological advances and new applications. Chem Phys Rev. 2021;2(4):041303. doi: 10.1063/5.0064075. DOI
Loco D, Polack É, Caprasecca S, Lagardère L, Lipparini F, Piquemal JP, Mennucci B. A QM/MM approach using the AMOEBA polarizable embedding: from ground state energies to electronic excitations. J Chem Theory Comput. 2016;12(8):3654. doi: 10.1021/acs.jctc.6b00385. PubMed DOI
Ma J, Cao J. Forster resonance energy transfer, absorption and emission spectra in multichromophoric systems. I. Full cumulant expansions and system-bath entanglement. J Chem Phys. 2015;142(9):094106. doi: 10.1063/1.4908599. PubMed DOI
Macpherson AN, Arellano JB, Fraser NJ, Cogdell RJ, Gillbro T. Efficient energy transfer from the carotenoid S2 state in a photosynthetic light-harvesting complex. Biophys J. 2001;80(2):923. doi: 10.1016/s0006-3495(01)76071-7. PubMed DOI PMC
Maier JA, Martinez C, Kasavajhala K, Wickstrom L, Hauser KE, Simmerling C. ff14SB: improving the accuracy of protein side chain and backbone parameters from ff99SB. J Chem Theory Comput. 2015;11(8):3696. doi: 10.1021/acs.jctc.5b00255. PubMed DOI PMC
McLuskey K, Prince SM, Cogdell RJ, Isaacs NW. The crystallographic structure of the B800–820 LH3 light-harvesting complex from the purple bacteria Rhodopseudomonas acidophila strain 7050. Biochemistry. 2001;40(30):8783. doi: 10.1021/bi010309a. PubMed DOI
Mirkovic T, Ostroumov EE, Anna JM, van Grondelle R, Scholes SD. Light absorption and energy transfer in the antenna complexes of photosynthetic organisms. Chem Rev. 2017;117(2):249. doi: 10.1021/acs.chemrev.6b00002. PubMed DOI
Montemayor D, Rivera E, Jang SJ. Computational modeling of exciton-bath hamiltonians for light harvesting 2 and light harvesting 3 complexes of purple photosynthetic bacteria at room temperature. J Phys Chem B. 2018;122(14):3815. doi: 10.1021/acs.jpcb.8b00358. PubMed DOI
Niedzwiedzki DM, Swainsbury DJK, Canniffe DP, Hunter CN, Hitchcock A. A photosynthetic antenna complex foregoes unity carotenoid-to-bacteriochlorophyll energy transfer efficiency to ensure photoprotection. Proc Natl Acad Sci USA. 2020;117(12):6502. doi: 10.1073/pnas.1920923117. PubMed DOI PMC
Nottoli M, Jurinovich S, Cupellini L, Gardiner AT, Cogdell R, Mennucci B. The role of charge-transfer states in the spectral tuning of antenna complexes of purple bacteria. Photosynth Res. 2018;137(2):215. doi: 10.1007/s11120-018-0492-1. PubMed DOI
Novoderezhkin VI, van Grondelle R. Spectra and dynamics in the B800 antenna: comparing hierarchical equations, redfield and Förster theories. J Phys Chem B. 2013;117(38):11076. doi: 10.1021/jp400957t. PubMed DOI
Olbrich C, Kleinekathöfer U. Time-dependent atomistic view on the electronic relaxation in light-harvesting system II. J Phys Chem B. 2010;114(38):12427. doi: 10.1021/jp106542v. PubMed DOI
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. Chem Phys Chem. 2011;12(3):634. doi: 10.1002/cphc.201000913. PubMed DOI
Papiz MZ, Prince SM, Howard T, Cogdell RJ, Isaacs NW. The structure and thermal motion of the B800–850 LH2 complex from Rps.acidophila at 2.0Å resolution and 100K: new structural features and functionally relevant motions. J Mol Biol. 2003;326(5):1523. doi: 10.1016/S0022-2836(03)00024-X. PubMed DOI
Polli D, Cerullo G, Lanzani G, Silvestri SD, Hashimoto H, Cogdell RJ. Carotenoid-bacteriochlorophyll energy transfer in LH2 complexes studied with 10-fs time resolution. Biophys J. 2006;90(7):2486. doi: 10.1529/biophysj.105.069286. PubMed DOI PMC
Prandi IG, Viani L, Andreussi O, Mennucci B. Combining classical molecular dynamics and quantum mechanical methods for the description of electronic excitations: the case of carotenoids. J Comput Chem. 2016 doi: 10.1002/jcc.24286. PubMed DOI
Qian P, Swainsbury DJK, Croll TI, Castro-Hartmann P, Divitini G, Sader K, Hunter CN. Cryo-EM structure of the Rhodobacter sphaeroides light-harvesting 2 complex at 2.1 Å. Biochemistry. 2021;60(44):3302. doi: 10.1021/acs.biochem.1c00576. PubMed DOI PMC
Renger T, Müh F. Understanding photosynthetic light-harvesting: a bottom up theoretical approach. Phys Chem Chem Phys. 2013;15(10):3348. doi: 10.1039/c3cp43439g. PubMed DOI
Robert B, Cogdell RJ, van Grondelle R. The light-harvesting system of purple bacteria. Dordrecht: Springer; 2003. pp. 169–194.
Schlau-Cohen GS, Wang Q, Southall J, Cogdell RJ, Moerner WE. Single-molecule spectroscopy reveals photosynthetic LH2 complexes switch between emissive states. Proc Natl Acad Sci USA. 2013;110(27):10899. doi: 10.1073/pnas.1310222110. PubMed DOI PMC
Segatta F, Cupellini L, Jurinovich S, Mukamel S, Dapor M, Taioli S, Garavelli M, Mennucci B. A quantum chemical interpretation of two-dimensional electronic spectroscopy of light-harvesting complexes. J Am Chem Soc. 2017;139(22):7558. doi: 10.1021/jacs.7b02130. PubMed DOI
Sláma V, Cupellini L, Mennucci B. Exciton properties and optical spectra of light harvesting complex II from a fully atomistic description. Phys Chem Chem Phys. 2020;22(29):16783. doi: 10.1039/D0CP02492A. PubMed DOI
Voityuk AA, Rösch N. Fragment charge difference method for estimating donor-acceptor electronic coupling: application to DNA DOI
Wang J, Wolf RM, Caldwell JW, Kollman PA, Case DA. Development and testing of a general amber force field. J Comput Chem. 2004;25(9):1157. doi: 10.1002/jcc.20035. PubMed DOI
Wang J, Cieplak P, Li J, Hou T, Luo R, Duan Y. Development of polarizable models for molecular mechanical calculations I: parameterization of atomic polarizability. J Phys Chem B. 2011;115(12):3091. doi: 10.1021/jp112133g. PubMed DOI PMC
Yang CH, Hsu CP. A multi-state fragment charge difference approach for diabatic states in electron transfer: extension and automation. J Chem Phys. 2013;139(15):154104. doi: 10.1063/1.4824906. PubMed DOI