Strong excitonic interactions are a key design strategy in photosynthetic light harvesting, expanding the spectral cross-section for light absorption and creating considerably faster and more robust excitation energy transfer. These molecular excitons are a direct result of exceptionally densely packed pigments in photosynthetic proteins. The main light-harvesting complexes of diatoms, known as fucoxanthin-chlorophyll proteins (FCPs), are an exception, displaying surprisingly weak excitonic coupling between their chlorophyll (Chl) a's, despite a high pigment density. Here, we show, using single-molecule spectroscopy, that the FCP complexes of Cyclotella meneghiniana switch frequently into stable, strongly emissive states shifted 4-10 nm toward the red. A few percent of isolated FCPa complexes and ∼20% of isolated FCPb complexes, on average, were observed to populate these previously unobserved states, percentages that agree with the steady-state fluorescence spectra of FCP ensembles. Thus, the complexes use their enhanced sensitivity to static disorder to increase their light-harvesting capability in a number of ways. A disordered exciton model based on the structure of the main plant light-harvesting complex explains the red-shifted emission by strong localization of the excitation energy on a single Chl a pigment in the terminal emitter domain due to very specific pigment orientations. We suggest that the specific construction of FCP gives the complex a unique strategy to ensure that its light-harvesting function remains robust in the fluctuating protein environment despite limited excitonic interactions.

Department of Physics and Astronomy Vrije Universiteit Amsterdam 1081 HV Amsterdam The Netherlands

Department of Physics University of Pretoria Hatfield 0028 South Africa

Department of Physics University of Pretoria Hatfield 0028 South Africa;

Faculty of Mathematics and Physics Charles University 121 16 Prague 2 Czech Republic

Institute of Molecular Biosciences Department of Biosciences Goethe University Frankfurt 60438 Frankfurt Germany

Zobrazit více v PubMed

Fleming GR, Schlau-Cohen GS, Amarnath K, Zaks J. Design principles of photosynthetic light-harvesting. Faraday Discuss. 2012;155:27–41, discussion 103–114. PubMed

Novoderezhkin VI, van Grondelle R. Physical origins and models of energy transfer in photosynthetic light-harvesting. Phys Chem Chem Phys. 2010;12:7352–7365. PubMed

Scholes GD, Fleming GR, Olaya-Castro A, van Grondelle R. Lessons from nature about solar light harvesting. Nat Chem. 2011;3:763–774. PubMed

van Grondelle R, Novoderezhkin VI. Energy transfer in photosynthesis: Experimental insights and quantitative models. Phys Chem Chem Phys. 2006;8:793–807. PubMed

Van Amerongen H, Valkunas L, Van Grondelle R. Photosynthetic Excitons. World Scientific Publishing; Singapore: 2000.

Mirkovic T, et al. Light absorption and energy transfer in the antenna complexes of photosynthetic organisms. Chem Rev. 2017;117:249–293. PubMed

Ramanan C, et al. The role of exciton delocalization in the major photosynthetic light-harvesting antenna of plants. Biophys J. 2015;108:1047–1056. PubMed PMC

Beer A, Gundermann K, Beckmann J, Büchel C. Subunit composition and pigmentation of fucoxanthin-chlorophyll proteins in diatoms: Evidence for a subunit involved in diadinoxanthin and diatoxanthin binding. Biochemistry. 2006;45:13046–13053. PubMed

Büchel C. Fucoxanthin-chlorophyll proteins in diatoms: 18 and 19 kDa subunits assemble into different oligomeric states. Biochemistry. 2003;42:13027–13034. PubMed

Röding A, Boekema E, Büchel C. The structure of FCPb, a light-harvesting complex in the diatom Cyclotella meneghiniana. Photosynth Res. 2016:1–9. PubMed

Premvardhan L, Robert B, Beer A, Büchel C. Pigment organization in fucoxanthin chlorophyll a/c(2) proteins (FCP) based on resonance Raman spectroscopy and sequence analysis. Biochim Biophys Acta. 2010;1797:1647–1656. PubMed

Butkus V, et al. Coherence and population dynamics of chlorophyll excitations in FCP complex: Two-dimensional spectroscopy study. J Chem Phys. 2015;142:212414. PubMed

Joshi-Deo J, et al. Characterization of a trimeric light-harvesting complex in the diatom Phaeodactylum tricornutum built of FcpA and FcpE proteins. J Exp Bot. 2010;61:3079–3087. PubMed PMC

Szabó M, et al. Structurally flexible macro-organization of the pigment-protein complexes of the diatom Phaeodactylum tricornutum. Photosynth Res. 2008;95:237–245. PubMed

Gundermann K, Büchel C. The fluorescence yield of the trimeric fucoxanthin-chlorophyll-protein FCPa in the diatom Cyclotella meneghiniana is dependent on the amount of bound diatoxanthin. Photosynth Res. 2008;95:229–235. PubMed

Gildenhoff N, et al. Oligomerization and pigmentation dependent excitation energy transfer in fucoxanthin-chlorophyll proteins. Biochim Biophys Acta. 2010;1797:543–549. PubMed

Papagiannakis E, van Stokkum IHM, Fey H, Büchel C, van Grondelle R. Spectroscopic characterization of the excitation energy transfer in the fucoxanthin-chlorophyll protein of diatoms. Photosynth Res. 2005;86:241–250. PubMed

Di Valentin M, Büchel C, Giacometti GM, Carbonera D. Chlorophyll triplet quenching by fucoxanthin in the fucoxanthin-chlorophyll protein from the diatom Cyclotella meneghiniana. Biochem Biophys Res Commun. 2012;427:637–641. PubMed

Di Valentin M, et al. Triplet-triplet energy transfer in fucoxanthin-chlorophyll protein from diatom Cyclotella meneghiniana: Insights into the structure of the complex. Biochim Biophys Acta. 2013;1827:1226–1234. PubMed

Falkowski PG, Barber RT, Smetacek V. Biogeochemical controls and feedbacks on ocean primary production. Science. 1998;281:200–207. PubMed

Field CB, Behrenfeld MJ, Randerson JT, Falkowski P. Primary production of the biosphere: Integrating terrestrial and oceanic components. Science. 1998;281:237–240. PubMed

Green BR, Kühlbrandt W. Sequence conservation of light-harvesting and stress-response proteins in relation to the three-dimensional molecular structure of LHCII. Photosynth Res. 1995;44:139–148. PubMed

Liu Z, et al. Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature. 2004;428:287–292. PubMed

Eppard M, Rhiel E. The genes encoding light-harvesting subunits of Cyclotella cryptica (Bacillariophyceae) constitute a complex and heterogeneous family. Mol Gen Genet. 1998;260:335–345. PubMed

Beer A, Juhas M, Büchel C. Influence of different light intensities and different iron nutrition on the photosynthetic apparatus in the diatom Cyclotella meneghiniana (Bacillariophyceae) J Phycol. 2011;47:1266–1273. PubMed

Novoderezhkin VI, Palacios MA, van Amerongen H, van Grondelle R. Excitation dynamics in the LHCII complex of higher plants: Modeling based on the 2.72 angstrom crystal structure. J Phys Chem B. 2005;109:10493–10504. PubMed

Liguori N, Periole X, Marrink SJ, Croce R. From light-harvesting to photoprotection: Structural basis of the dynamic switch of the major antenna complex of plants (LHCII) Sci Rep. 2015;5:15661. PubMed PMC

Krüger TPJ, Novoderezhkin VI, Romero E, Van Grondelle R. Photosynthetic energy transfer and charge separation in higher plants. In: Golbeck JH, van der Est A, editors. The Biophysics of Photosynthesis. Vol 11. Springer; New York: 2014. pp. 79–118.

Moerner WE. A dozen years of single-molecule spectroscopy in physics, chemistry, and biophysics. J Phys Chem B. 2002;106:910–927.

Premvardhan L, Bordes L, Beer A, Büchel C, Robert B. Carotenoid structures and environments in trimeric and oligomeric fucoxanthin chlorophyll a/c2 proteins from resonance Raman spectroscopy. J Phys Chem B. 2009;113:12565–12574. PubMed

Bopp MA, Jia Y, Li L, Cogdell RJ, Hochstrasser RM. Fluorescence and photobleaching dynamics of single light-harvesting complexes. Proc Natl Acad Sci USA. 1997;94:10630–10635. PubMed PMC

Gwizdala M, Berera R, Kirilovsky D, van Grondelle R, Krüger TPJ. Controlling light harvesting with light. J Am Chem Soc. 2016;138:11616–11622. PubMed

Hofkens J, et al. Triplet states as non-radiative traps in multichromophoric entities: Single molecule spectroscopy of an artificial and natural antenna system. Spectrochim Acta A Mol Biomol Spectrosc. 2001;57:2093–2107. PubMed

Krüger TPJ, et al. The specificity of controlled protein disorder in the photoprotection of plants. Biophys J. 2013;105:1018–1026. PubMed PMC

Novoderezhkin VI, Palacios MA, van Amerongen H, van Grondelle R. Energy-transfer dynamics in the LHCII complex of higher plants: Modified Redfield approach. J Phys Chem B. 2004;108:10363–10375. PubMed

Novoderezhkin V, Marin A, van Grondelle R. Intra- and inter-monomeric transfers in the light harvesting LHCII complex: The Redfield-Förster picture. Phys Chem Chem Phys. 2011;13:17093–17103. PubMed

Songaila E, et al. Ultrafast energy transfer from chlorophyll c2 to chlorophyll a in fucoxanthin-chlorophyll protein complex. J Phys Chem Lett. 2013;4:3590–3595.

Fox KF, Bricker WP, Lo C, Duffy CDP. Distortions of the xanthophylls caused by interactions with neighboring pigments and the LHCII protein are crucial for studying energy transfer pathways within the complex. J Phys Chem B. 2015;119:15550–15560. PubMed

Brecht M, Studier H, Radics V, Nieder JB, Bittl R. Spectral diffusion induced by proton dynamics in pigment-protein complexes. J Am Chem Soc. 2008;130:17487–17493. PubMed

Olsen JD, Sockalingum GD, Robert B, Hunter CN. Modification of a hydrogen bond to a bacteriochlorophyll a molecule in the light-harvesting 1 antenna of Rhodobacter sphaeroides. Proc Natl Acad Sci USA. 1994;91:7124–7128. PubMed PMC

Krüger TPJ, Novoderezhkin VI, Ilioaia C, van Grondelle R. Fluorescence spectral dynamics of single LHCII trimers. Biophys J. 2010;98:3093–3101. PubMed PMC

Krüger TPJ, Wientjes E, Croce R, van Grondelle R. Conformational switching explains the intrinsic multifunctionality of plant light-harvesting complexes. Proc Natl Acad Sci USA. 2011;108:13516–13521. PubMed PMC

Wahadoszamen M, et al. Stark fluorescence spectroscopy reveals two emitting sites in the dissipative state of FCP antennas. Biochim Biophys Acta. 2014;1837:193–200. PubMed

Ghazaryan A, Akhtar P, Garab G, Lambrev PH, Büchel C. Involvement of the Lhcx protein Fcp6 of the diatom Cyclotella meneghiniana in the macro-organisation and structural flexibility of thylakoid membranes. Biochim Biophys Acta. 2016;1857:1373–1379. PubMed

Gundermann K, Büchel C. Factors determining the fluorescence yield of fucoxanthin-chlorophyll complexes (FCP) involved in non-photochemical quenching in diatoms. Biochim Biophys Acta. 2012;1817:1044–1052. PubMed

Krüger TPJ, Ilioaia C, Johnson MP, Ruban AV, van Grondelle R. Disentangling the low-energy states of the major light-harvesting complex of plants and their role in photoprotection. Biochim Biophys Acta. 2014;1837:1027–1038. PubMed

Malý P, Gruber JM, van Grondelle R, Mančal T. Single molecule spectroscopy of monomeric LHCII: Experiment and theory. Sci Rep. 2016;6:26230. PubMed PMC