Photosynthetic organisms harvest light for energy. Some eukaryotic algae have specialized in harvesting far-red light by tuning chlorophyll a absorption through a mechanism still to be elucidated. Here, we combined optically detected magnetic resonance and pulsed electron paramagnetic resonance measurements on red-adapted light-harvesting complexes, rVCP, isolated from the freshwater eustigmatophyte alga Trachydiscus minutus to identify the location of the pigments responsible for this remarkable adaptation. The pigments have been found to belong to an excitonic cluster of chlorophylls a at the core of the complex, close to the central carotenoids in L1/L2 sites. A pair of structural features of the Chl a403/a603 binding site, namely the histidine-to-asparagine substitution in the magnesium-ligation residue and the small size of the amino acid at the i-4 position, resulting in a [A/G]xxxN motif, are proposed to be the origin of this trait. Phylogenetic analysis of various eukaryotic red antennae identified several potential LHCs that could share this tuning mechanism. This knowledge of the red light acclimation mechanism in algae is a step towards rational design of algal strains in order to enhance light capture and efficiency in large-scale biotechnology applications.

Czech Academy of Sciences Biology Centre Institute of Plant Molecular Biology Branišovská 31 370 05 České Budějovice Czech Republic

Department of Biology and Ecology Faculty of Science University of Ostrava Chittussiho 10 710 00 Ostrava Czech Republic

Department of Chemical Sciences University of Padova via Marzolo 1 35131 Padova Italy

Institute of Chemistry Faculty of Science University of South Bohemia Branišovská 1760 370 05 České Budějovice Czech Republic

Zobrazit více v PubMed

Green, B. R. & Kühlbrandt, W. Sequence conservation of light-harvesting and stress-response proteins in relation to the three-dimensional molecular structure of LHCII. PubMed DOI

Liu, Z. et al. Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. PubMed DOI

Renger, T., Madjet, M. E., Knorr, A. & Müh, F. How the molecular structure determines the flow of excitation energy in plant light-harvesting complex II. PubMed DOI

Novoderezhkin, V., Marin, A. & van Grondelle, R. Intra- and inter-monomeric transfers in the light harvesting LHCII complex: the Redfield–Förster picture. PubMed DOI

Carbonera, D. et al. Photoprotective sites in the violaxanthin–chlorophyll PubMed DOI

Di Valentin, M., Biasibetti, F., Ceola, S. & Carbonera, D. Identification of the sites of chlorophyll triplet quenching in relation to the structure of LHC-II from higher plants. Evidence from EPR spectroscopy. PubMed DOI

Lampoura, S. S., Barzda, V., Owen, G. M., Hoff, A. J. & Van Amerongen, H. Aggregation of LHCII leads to a redistribution of the triplets over the central xanthophylls in LHCII. PubMed DOI

Mozzo, M., Dall’Osto, L., Hienerwadel, R., Bassi, R. & Croce, R. Photoprotection in the antenna complexes of photosystem II: Role of individual xanthophylls in chlorophyll triplet quenching. PubMed DOI

Agostini, A. et al. Altering the exciton landscape by removal of specific chlorophylls in monomeric LHCII provides information on the sites of triplet formation and quenching by means of ODMR and EPR spectroscopies. PubMed DOI

Wang, W. et al. Structural basis for blue-green light harvesting and energy dissipation in diatoms. PubMed DOI

Su, X. et al. Antenna arrangement and energy transfer pathways of a green algal photosystem-I–LHCI supercomplex. PubMed DOI

Pi, X. et al. Unique organization of photosystem I–light-harvesting supercomplex revealed by cryo-EM from a red alga. PubMed DOI PMC

Papagiannakis, E., H.M. van Stokkum, I., Fey, H., Büchel, C. & van Grondelle, R. Spectroscopic Characterization of the Excitation Energy Transfer in the Fucoxanthin–Chlorophyll Protein of Diatoms. PubMed DOI

Gundlach, K., Werwie, M., Wiegand, S. & Paulsen, H. Filling the “green gap” of the major light-harvesting chlorophyll PubMed DOI

Hancock, A. M. et al. Enhancing the spectral range of plant and bacterial light-harvesting pigment-protein complexes with various synthetic chromophores incorporated into lipid vesicles. PubMed DOI

Miyashita, H. et al. Chlorophyll DOI

Chen, M. et al. A Red-Shifted Chlorophyll. PubMed DOI

Elias, E., Liguori, N., Saga, Y., Schäfers, J. & Croce, R. Harvesting Far-Red Light with Plant Antenna Complexes Incorporating Chlorophyll PubMed DOI PMC

Ort, D. R. et al. Redesigning photosynthesis to sustainably meet global food and bioenergy demand. PubMed DOI PMC

Walter, J. & Kromdijk, J. Here comes the sun: How optimization of photosynthetic light reactions can boost crop yields. PubMed DOI PMC

Wolf, B. M. & Blankenship, R. E. Far-red light acclimation in diverse oxygenic photosynthetic organisms. PubMed DOI

Kotabová, E. et al. Novel type of red-shifted chlorophyll a antenna complex from PubMed DOI

Bína, D. et al. Novel type of red-shifted chlorophyll PubMed DOI

Litvín, R. et al. Red-shifted light-harvesting system of freshwater eukaryotic alga PubMed DOI

Wolf, B. M. et al. Characterization of a newly isolated freshwater Eustigmatophyte alga capable of utilizing far-red light as its sole light source. PubMed DOI

Niedzwiedzki, D. M., Wolf, B. M. & Blankenship, R. E. Excitation energy transfer in the far-red absorbing violaxanthin/vaucheriaxanthin chlorophyll PubMed DOI

Morosinotto, T., Breton, J., Bassi, R. & Croce, R. The Nature of a Chlorophyll Ligand in Lhca Proteins Determines the Far Red Fluorescence Emission Typical of Photosystem I. PubMed DOI

Romero, E. et al. The Origin of the Low-Energy Form of Photosystem I Light-Harvesting Complex Lhca4: Mixing of the Lowest Exciton with a Charge-Transfer State. PubMed DOI PMC

Passarini, F., Wientjes, E., van Amerongen, H. & Croce, R. Photosystem I light-harvesting complex Lhca4 adopts multiple conformations: Red forms and excited-state quenching are mutually exclusive. PubMed DOI

Basso, S. et al. Characterization of the photosynthetic apparatus of the Eustigmatophycean Nannochloropsis gaditana: Evidence of convergent evolution in the supramolecular organization of photosystem I. PubMed DOI

Keşan, G. et al. Efficient light-harvesting using non-carbonyl carotenoids: Energy transfer dynamics in the VCP complex from PubMed DOI

Sukenik, A., Livne, A., Apt, K. E. & Grossman, A. R. Characterization of a gene encoding the light-harvesting violaxanthin-chlorophyll protein of PubMed DOI

Litvín, R., Bína, D., Herbstová, M. & Gardian, Z. Architecture of the light-harvesting apparatus of the eustigmatophyte alga PubMed DOI

Přibyl, P., Eliáš, M., Cepák, V., Lukavský, J. & Kaštánek, P. Zoosporogenesis, morphology, ultrastructure, pigment composition, and phylogenetic position of PubMed DOI

Bína, D. et al. Energy transfer dynamics in a red-shifted violaxanthin-chlorophyll PubMed DOI

Gundermann, K., Schmidt, M., Weisheit, W., Mittag, M. & Büchel, C. Identification of several sub-populations in the pool of light harvesting proteins in the pennate diatom PubMed DOI

Lepetit, B. et al. Spectroscopic and Molecular Characterization of the Oligomeric Antenna of the Diatom PubMed DOI

Herbstová, M. et al. Molecular basis of chromatic adaptation in pennate diatom PubMed DOI

Wang, L. et al. LHCF15 facilitates the absorption of longer wavelength light and promotes growth of DOI

Wientjes, E., Roest, G. & Croce, R. From red to blue to far-red in Lhca4: How does the protein modulate the spectral properties of the pigments? PubMed DOI

Sláma, V. et al. Origin of Low-Lying Red States in the Lhca4 Light-Harvesting Complex of Photosystem I. PubMed DOI PMC

Agostini, A., Bína, D., Carbonera, D. & Litvín, R. Conservation of triplet-triplet energy transfer photoprotective pathways in fucoxanthin chlorophyll-binding proteins across algal lineages. PubMed DOI

Agostini, A., Büchel, C., Di Valentin, M. & Carbonera, D. A distinctive pathway for triplet-triplet energy transfer photoprotection in fucoxanthin chlorophyll-binding proteins from PubMed DOI

Paulsen, H., Rümler, U. & Rüdiger, W. Reconstitution of pigment-containing complexes from light-harvesting chlorophyll PubMed DOI

Carbonera, D., Giacometti, G. & Agostini, G. FDMR of Carotenoid and Chlorophyll triplets in light-harvesting complex LHCII of spinach. DOI

Khoroshyy, P. et al. Quenching of chlorophyll triplet states by carotenoids in algal light-harvesting complexes related to fucoxanthin-chlorophyll protein. PubMed DOI

Di Valentin, M. et al. Triplet-triplet energy transfer in Peridinin-Chlorophyll a-protein reconstituted with Chl a and Chl d as revealed by optically detected magnetic resonance and pulse EPR: Comparison with the native PCP complex from PubMed DOI

Di Valentin, M. et al. Triplet–triplet energy transfer in the major intrinsic light-harvesting complex of PubMed DOI

Migliore, A., Corni, S., Agostini, A. & Carbonera, D. Unraveling the electronic origin of a special feature in the triplet-minus-singlet spectra of carotenoids in natural photosystems. PubMed DOI

Carbonera, D., Agostini, G., Morosinotto, T. & Bassi, R. Quenching of chlorophyll triplet states by carotenoids in reconstituted Lhca4 subunit of peripheral light-harvesting complex of photosystem I. PubMed DOI

Di Valentin, M. et al. Triplet–triplet energy transfer in fucoxanthin-chlorophyll protein from diatom PubMed DOI

Di Valentin, M., Ceola, S., Salvadori, E., Agostini, G. & Carbonera, D. Identification by time-resolved EPR of the peridinins directly involved in chlorophyll triplet quenching in the peridinin–chlorophyll PubMed DOI

Carbonera, D. et al. Energy transfer and spin polarization of the carotenoid triplet state in synthetic carotenoporphyrin dyads and in natural antenna complexes. DOI

Bittl, R., Schlodder, E., Geisenheimer, I., Lubitz, W. & Cogdell, R. J. Transient EPR and Absorption Studies of Carotenoid Triplet Formation in Purple Bacterial Antenna Complexes. DOI

Kay, C., Elger, G. & Mobius, K. The photoexcited triplet state of free-base porphycene: a time-resolved EPR and electron spin echo investigation. DOI

Tichy, J. et al. Light harvesting complexes of PubMed DOI

Harpaz, Y., Gerstein, M. & Chothia, C. Volume changes on protein folding. PubMed DOI

Remelli, R., Varotto, C., Sandonà, D., Croce, R. & Bassi, R. Chlorophyll binding to monomeric light-harvesting complex. A mutation analysis of chromophore-binding residues. PubMed DOI

Herbstová, M., Bína, D., Kaňa, R., Vácha, F. & Litvín, R. Red-light phenotype in a marine diatom involves a specialized oligomeric red-shifted antenna and altered cell morphology. PubMed DOI PMC

Guillard, R. R. L. & Lorenzen, C. J. Yellow-green algae with chlorophyllide

Bischoff, H. W. & Bold, H. C. Phycological studies IV. Some soil algae from Enchanted Rock and related algal species.

Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. PubMed DOI PMC

Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. PubMed DOI PMC

Haas, B. J. https://github.com/TransDecoder/TransDecoder.

Premvardhan, L., Robert, B., Beer, A. & Büchel, C. Pigment organization in fucoxanthin chlorophyll PubMed DOI

Bowler, C. et al. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. PubMed DOI

Katoh, K. & Standley, D. M. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. PubMed DOI PMC

Eddy, S. R. Accelerated Profile HMM Searches. PubMed DOI PMC

Yurchenko, T. et al. A gene transfer event suggests a long-term partnership between eustigmatophyte algae and a novel lineage of endosymbiotic bacteria. PubMed DOI PMC

Alboresi, A. et al. Conservation of core complex subunits shaped the structure and function of photosystem I in the secondary endosymbiont alga PubMed DOI PMC

Kumazawa, M. et al. Molecular phylogeny of fucoxanthin‐chlorophyll PubMed DOI

Huerta-Cepas, J., Serra, F. & Bork, P. ETE 3: Reconstruction, Analysis, and Visualization of Phylogenomic Data. PubMed DOI PMC

Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. PubMed DOI PMC

Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies. PubMed DOI PMC

Letunic, I. & Bork, P. Interactive Tree of Life (iTOL) v6: recent updates to the phylogenetic tree display and annotation tool. PubMed DOI PMC

Agostini, A., Palm, D. M., Paulsen, H. & Carbonera, D. Optically Detected Magnetic Resonance of Chlorophyll Triplet States in Water-Soluble Chlorophyll Proteins from PubMed DOI

Stoll, S. & Schweiger, A. EasySpin, a comprehensive software package for spectral simulation and analysis in EPR. PubMed DOI

Vrieze, J. & Hoff, A. J. The orientation of the triplet axes with respect to the optical transition moments in (bacterio) chlorophylls. DOI

Madjet, M. E., Abdurahman, A. & Renger, T. Intermolecular coulomb couplings from ab initio electrostatic potentials: Application to optical transitions of strongly coupled pigments in photosynthetic antennae and reaction centers. PubMed DOI

Wang, J. et al. Structure of plant photosystem I−light harvesting complex I supercomplex at 2.4 Å resolution. PubMed DOI

Exciton Delocalization Promotes Far-Red Absorption in a Tetrameric Chlorophyll a Light-Harvesting Complex from Trachydiscus minutus