The monomeric photosystem I-light-harvesting antenna complex I (PSI-LHCI) supercomplex from the extremophilic red alga Cyanidioschyzon merolae represents an intermediate evolutionary link between the cyanobacterial PSI reaction center and its green algal/higher plant counterpart. We show that the C. merolae PSI-LHCI supercomplex is characterized by robustness in various extreme conditions. By a combination of biochemical, spectroscopic, mass spectrometry, and electron microscopy/single particle analyses, we dissected three molecular mechanisms underlying the inherent robustness of the C. merolae PSI-LHCI supercomplex: (1) the accumulation of photoprotective zeaxanthin in the LHCI antenna and the PSI reaction center; (2) structural remodeling of the LHCI antenna and adjustment of the effective absorption cross section; and (3) dynamic readjustment of the stoichiometry of the two PSI-LHCI isomers and changes in the oligomeric state of the PSI-LHCI supercomplex, accompanied by dissociation of the PsaK core subunit. We show that the largest low light-treated C. merolae PSI-LHCI supercomplex can bind up to eight Lhcr antenna subunits, which are organized as two rows on the PsaF/PsaJ side of the core complex. Under our experimental conditions, we found no evidence of functional coupling of the phycobilisomes with the PSI-LHCI supercomplex purified from various light conditions, suggesting that the putative association of this antenna with the PSI supercomplex is absent or may be lost during the purification procedure.

Botany Department Faculty of Science Kafrelsheikh University 33516 Kafr El Sheikh Egypt

Centre of the Region Haná for Biotechnological and Agricultural Research Department of Biophysics Faculty of Science Palacký University 783 71 Olomouc Czech Republic

Faculty of Biology University of Warsaw 02 096 Warsaw Poland

Leibniz Institute on Aging Fritz Lipmann Institute 07745 Jena Germany

Plant Biochemistry Faculty of Biology and Biotechnology Ruhr University D 44780 Bochum Germany

Solar Fuels Laboratory Center of New Technologies University of Warsaw 02 097 Warsaw Poland

Zobrazit více v PubMed

Adachi H, Umena Y, Enami I, Henmi T, Kamiya N, Shen JR (2009) Towards structural elucidation of eukaryotic photosystem II: purification, crystallization and preliminary X-ray diffraction analysis of photosystem II from a red alga. Biochim Biophys Acta 1787: 121–128 PubMed

Ago H, Adachi H, Umena Y, Tashiro T, Kawakami K, Kamiya N, Tian L, Han G, Kuang T, Liu Z, et al. (2016) Novel features of eukaryotic photosystem II revealed by its crystal structure analysis from a red alga. J Biol Chem 291: 5676–5687 PubMed PMC

Allakhverdiev SI, Sakamoto A, Nishiyama Y, Inaba M, Murata N (2000) Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiol 123: 1047–1056 PubMed PMC

Amunts A, Toporik H, Borovikova A, Nelson N (2010) Structure determination and improved model of plant photosystem I. J Biol Chem 285: 3478–3486 PubMed PMC

Babcock GT, Barry BA, Debus RJ, Hoganson CW, Atamian M, McIntosh L, Sithole I, Yocum CF (1989) Water oxidation in photosystem II: from radical chemistry to multielectron chemistry. Biochemistry 28: 9557–9565 PubMed

Ballottari M, Alcocer MJP, D’Andrea C, Viola D, Ahn TK, Petrozza A, Polli D, Fleming GR, Cerullo G, Bassi R (2014) Regulation of photosystem I light harvesting by zeaxanthin. Proc Natl Acad Sci USA 111: E2431–E2438 PubMed PMC

Barber J. (2004) Engine of life and big bang of evolution: a personal perspective. Photosynth Res 80: 137–155 PubMed

Boekema EJ, Folea M, Kouřil R (2009) Single particle electron microscopy. Photosynth Res 102: 189–196 PubMed PMC

Busch A, Hippler M (2011) The structure and function of eukaryotic photosystem I. Biochim Biophys Acta 1807: 864–877 PubMed

Busch A, Nield J, Hippler M (2010) The composition and structure of photosystem I-associated antenna from Cyanidioschyzon merolae. Plant J 62: 886–897 PubMed

Castenholz RW. (1988) Culturing methods for cyanobacteria. Methods Enzymol 167: 68–93

Chitnis VP, Chitnis PR (1993) PsaL subunit is required for the formation of photosystem I trimers in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 336: 330–334 PubMed

Cox J, Mann M (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26: 1367–1372 PubMed

Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, Mann M (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res 10: 1794–1805 PubMed

Croce R, Dorra D, Holzwarth AR, Jennings RC (2000) Fluorescence decay and spectral evolution in intact photosystem I of higher plants. Biochemistry 39: 6341–6348 PubMed

Croce R, van Amerongen H (2013) Light-harvesting in photosystem I. Photosynth Res 116: 153–166 PubMed PMC

Croce R, Zucchelli G, Garlaschi FM, Bassi R, Jennings RC (1996) Excited state equilibration in the photosystem I-light-harvesting I complex: P700 is almost isoenergetic with its antenna. Biochemistry 35: 8572–8579 PubMed

Croce R, Zucchelli G, Garlaschi FM, Jennings RC (1998) A thermal broadening study of the antenna chlorophylls in PSI-200, LHCI, and PSI core. Biochemistry 37: 17355–17360 PubMed

Cunningham FX, Dennenberg RJ, Mustardy L, Jursinic PA, Gantt E (1989) Stoichiometry of photosystem I, photosystem II, and phycobilisomes in the red alga Porphyridium cruentum as a function of growth irradiance. Plant Physiol 91: 1179–1187 PubMed PMC

Cunningham FX Jr, Lee H, Gantt E (2007) Carotenoid biosynthesis in the primitive red alga Cyanidioschyzon merolae. Eukaryot Cell 6: 533–545 PubMed PMC

DeLano WL. (2002) The PyMOL Molecular Graphics System. Delano Scientific, San Carlos.

Drop B, Webber-Birungi M, Fusetti F, Kouřil R, Redding KE, Boekema EJ, Croce R (2011) Photosystem I of Chlamydomonas reinhardtii contains nine light-harvesting complexes (Lhca) located on one side of the core. J Biol Chem 286: 44878–44887 PubMed PMC

Elias JE, Gygi SP (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 4: 207–214 PubMed

El-Mohsnawy E, Kopczak MJ, Schlodder E, Nowaczyk M, Meyer HE, Warscheid B, Karapetyan NV, Rögner M (2010) Structure and function of intact photosystem 1 monomers from the cyanobacterium Thermosynechococcus elongatus. Biochemistry 49: 4740–4751 PubMed

Engelmann E, Zucchelli G, Casazza AP, Brogioli D, Garlaschi FM, Jennings RC (2006) Influence of the photosystem I-light harvesting complex I antenna domains on fluorescence decay. Biochemistry 45: 6947–6955 PubMed

Farci D, Kirkpatrick J, Piano D (2017) A new procedure for fast soft staining of BN-PAGEs on photosynthetic complexes. Electrophoresis 38: 441–446 PubMed

Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303: 1831–1838 PubMed

Gardian Z, Bumba L, Schrofel A, Herbstova M, Nebesarova J, Vacha F (2007) Organisation of photosystem I and photosystem II in red alga Cyanidium caldarium: encounter of cyanobacterial and higher plant concepts. Biochim Biophys Acta 1767: 725–731 PubMed

Gibasiewicz K, Szrajner A, Ihalainen JA, Germano M, Dekker JP, van Grondelle R (2005) Characterization of low-energy chlorophylls in the PSI-LHCI supercomplex from Chlamydomonas reinhardtii: a site-selective fluorescence study. J Phys Chem B 109: 21180–21186 PubMed

Gobets B, van Grondelle R (2001) Energy transfer and trapping in photosystem I. Biochim Biophys Acta 1507: 80–99 PubMed

Gordiichuk PI, Wetzelaer GJAH, Rimmerman D, Gruszka A, de Vries JW, Saller M, Gautier DA, Catarci S, Pesce D, Richter S, et al. (2014) Solid-state biophotovoltaic cells containing photosystem I. Adv Mater 26: 4863–4869 PubMed

Gruszecki WI, Strzałka K (2005) Carotenoids as modulators of lipid membrane physical properties. Biochim Biophys Acta 1740: 108–115 PubMed

Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-A resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16: 334–342 PubMed

Havaux M, Dall’osto L, Bassi R (2007) Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol 145: 1506–1520 PubMed PMC

Ihalainen JA, Jensen PE, Haldrup A, van Stokkum IHM, van Grondelle R, Scheller HV, Dekker JP (2002) Pigment organization and energy transfer dynamics in isolated photosystem I (PSI) complexes from Arabidopsis thaliana depleted of the PSI-G, PSI-K, PSI-L, or PSI-N subunit. Biophys J 83: 2190–2201 PubMed PMC

Iwuchukwu IJ, Vaughn M, Myers N, O’Neill H, Frymier P, Bruce BD (2010) Self-organized photosynthetic nanoparticle for cell-free hydrogen production. Nat Nanotechnol 5: 73–79 PubMed

Janna Olmos JD, Kargul J (2015) A quest for the artificial leaf. Int J Biochem Cell Biol 66: 37–44 PubMed

Jennings RC, Zucchelli G, Croce R, Garlaschi FM (2003) The photochemical trapping rate from red spectral states in PSI-LHCI is determined by thermal activation of energy transfer to bulk chlorophylls. Biochim Biophys Acta 1557: 91–98 PubMed

Jensen PE, Bassi R, Boekema EJ, Dekker JP, Jansson S, Leister D, Robinson C, Scheller HV (2007) Structure, function and regulation of plant photosystem I. Biochim Biophys Acta 1767: 335–352 PubMed

Johnson MP, Havaux M, Triantaphylidès C, Ksas B, Pascal AA, Robert B, Davison PA, Ruban AV, Horton P (2007) Elevated zeaxanthin bound to oligomeric LHCII enhances the resistance of Arabidopsis to photooxidative stress by a lipid-protective, antioxidant mechanism. J Biol Chem 282: 22605–22618 PubMed

Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauss N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature 411: 909–917 PubMed

Kamiya N, Shen JR (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. Proc Natl Acad Sci USA 100: 98–103 PubMed PMC

Kargul J, Barber J (2011) Structure and function of photosynthetic reaction centres. In Wydrzynski TJ, Hillier W, eds, Molecular Solar Fuels. Royal Society of Chemistry, Cambridge, UK, pp 107–142

Kargul J, Janna Olmos JD, Krupnik T (2012) Structure and function of photosystem I and its application in biomimetic solar-to-fuel systems. J Plant Physiol 169: 1639–1653 PubMed

Kargul J, Nield J, Barber J (2003) Three-dimensional reconstruction of a light-harvesting complex I-photosystem I (LHCI-PSI) supercomplex from the green alga Chlamydomonas reinhardtii: insights into light harvesting for PSI. J Biol Chem 278: 16135–16141 PubMed

Klukas O, Schubert WD, Jordan P, Krauss N, Fromme P, Witt HT, Saenger W (1999) Photosystem I, an improved model of the stromal subunits PsaC, PsaD, and PsaE. J Biol Chem 274: 7351–7360 PubMed

Krassen H, Schwarze A, Friedrich B, Ataka K, Lenz O, Heberle J (2009) Photosynthetic hydrogen production by a hybrid complex of photosystem I and [NiFe]-hydrogenase. ACS Nano 3: 4055–4061 PubMed

Krupnik T, Kotabová E, van Bezouwen LS, Mazur R, Garstka M, Nixon PJ, Barber J, Kaňa R, Boekema EJ, Kargul J (2013) A reaction center-dependent photoprotection mechanism in a highly robust photosystem II from an extremophilic red alga, Cyanidioschyzon merolae. J Biol Chem 288: 23529–23542 PubMed PMC

Kuhl H, Kruip J, Seidler A, Krieger-Liszkay A, Bunker M, Bald D, Scheidig AJ, Rögner M (2000) Towards structural determination of the water-splitting enzyme: purification, crystallization, and preliminary crystallographic studies of photosystem II from a thermophilic cyanobacterium. J Biol Chem 275: 20652–20659 PubMed

Kuroiwa T. (1998) The primitive red algae Cyanidium caldarium and Cyanidioschyzon merolae as model system for investigating the dividing apparatus of mitochondria and plastids. BioEssays 20: 344–354

Kuroiwa T, Kuroiwa H, Sakai A, Takahashi H, Toda K, Itoh R (1998) The division apparatus of plastids and mitochondria. Int Rev Cytol 181: 1–41 PubMed

León-Bañares R, González-Ballester D, Galván A, Fernández E (2004) Transgenic microalgae as green cell-factories. Trends Biotechnol 22: 45–52 PubMed

Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438: 1040–1044 PubMed

Marquardt J, Lutz B, Wans S, Rhiel E, Krumbein WE (2001) The gene family coding for the light-harvesting polypeptides of photosystem I of the red alga Galdieria sulphuraria. Photosynth Res 68: 121–130 PubMed

Matsuzaki M, Misumi O, Shin-i T, Maruyama S, Takahara M, Miyagishima SY, Mori T, Nishida K, Yagisawa F, Nishida K, et al. (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428: 653–657 PubMed

Mazor Y, Borovikova A, Caspy I, Nelson N (2017) Structure of the plant photosystem I supercomplex at 2.6 Å resolution. Nat Plants 3: 17014. PubMed

Mazor Y, Borovikova A, Nelson N (2015) The structure of plant photosystem I super-complex at 2.8 Å resolution. eLife 4: e07433. PubMed PMC

Melkozernov AN, Kargul J, Lin S, Barber J, Blankenship RE (2004) Energy coupling in the PSI-LHCI supercomplex from the green alga Chlamydomonas reinhardtii. J Phys Chem B 108: 10547–10555

Melkozernov AN, Kargul J, Lin S, Barber J, Blankenship RE (2005) Spectral and kinetic analysis of the energy coupling in the PSI-LHCI supercomplex from the green alga Chlamydomonas reinhardtii at 77 K. Photosynth Res 86: 203–215 PubMed

Mershin A, Matsumoto K, Kaiser L, Yu D, Vaughn M, Nazeeruddin MK, Bruce BD, Graetzel M, Zhang S (2012) Self-assembled photosystem-I biophotovoltaics on nanostructured TiO2 and ZnO. Sci Rep 2: 234. PubMed PMC

Minoda A, Sakagami R, Yagisawa F, Kuroiwa T, Tanaka K (2004) Improvement of culture conditions and evidence for nuclear transformation by homologous recombination in a red alga, Cyanidioschyzon merolae 10D. Plant Cell Physiol 45: 667–671 PubMed

Miyagishima SY, Nishida K, Mori T, Matsuzaki M, Higashiyama T, Kuroiwa H, Kuroiwa T (2003) A plant-specific dynamin-related protein forms a ring at the chloroplast division site. Plant Cell 15: 655–665 PubMed PMC

Morosinotto T, Mozzo M, Bassi R, Croce R (2005) Pigment-pigment interactions in Lhca4 antenna complex of higher plants photosystem I. J Biol Chem 280: 20612–20619 PubMed

Nikolova D, Weber D, Scholz M, Bald T, Scharsack JP, Hippler M (2017) Temperature-induced remodeling of the photosynthetic machinery tunes photosynthesis in the thermophilic alga Cyanidioschyzon merolae. Plant Physiol 174: 35–46 PubMed PMC

Nilsson H, Krupnik T, Kargul J, Messinger J (2014) Substrate water exchange in photosystem II core complexes of the extremophilic red alga Cyanidioschyzon merolae. Biochim Biophys Acta 1837: 1257–1262 PubMed

Nishida K, Takahara M, Miyagishima SY, Kuroiwa H, Matsuzaki M, Kuroiwa T (2003) Dynamic recruitment of dynamin for final mitochondrial severance in a primitive red alga. Proc Natl Acad Sci USA 100: 2146–2151 PubMed PMC

Nozaki H, Matsuzaki M, Takahara M, Misumi O, Kuroiwa H, Hasegawa M, Shin-i T, Kohara Y, Ogasawara N, Kuroiwa T (2003) The phylogenetic position of red algae revealed by multiple nuclear genes from mitochondria-containing eukaryotes and an alternative hypothesis on the origin of plastids. J Mol Evol 56: 485–497 PubMed

Ocakoglu K, Krupnik T, van den Bosch B, Harputlu E, Gullo MP, Olmos JDJ, Yildirimcan S, Gupta RK, Yakuphanoglu F, Barbieri A, et al. (2014) Photosystem I-based biophotovoltaics on nanostructured hematite. Adv Funct Mater 24: 7467–7477

Ohta H, Suzuki T, Ueno M, Okumura A, Yoshihara S, Shen JR, Enami I (2003) Extrinsic proteins of photosystem II: an intermediate member of PsbQ protein family in red algal PS II. Eur J Biochem 270: 4156–4163 PubMed

Olmos JDJ, Becquet P, Gront D, Sar J, Dąbrowski A, Gawlik G, Teodorczyk M, Pawlak D, Kargul J (2017) Biofunctionalisation of p-doped silicon with cytochrome c553 minimises charge recombination and enhances photovoltaic performance of the all-solid-state photosystem I-based biophotoelectrode. RSC Advances 7: 47854–47866

Oren A, Kuhl M, Karsten U (1996) An endoevaporitic microbial mat within a gypsum crust: zonation of phototrophs, photopigments, and light penetration. Oceanogr Lit Rev 6: 593

Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975: 384–394

Qin X, Suga M, Kuang T, Shen JR (2015) Photosynthesis: structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex. Science 348: 989–995 PubMed

Reeb V, Bhattacharya D (2010) The thermo-acidophilic Cyanidiophyceae (Cyanidiales). In Seckbach J, Chapman D, eds, Red Algae in the Genomic Age. Springer, Dordrecht, The Netherlands, pp 409–426

Rivadossi A, Zucchelli G, Garlaschi FM, Jennings RC (1999) The importance of PS I chlorophyll red forms in light-harvesting by leaves. Photosynth Res 60: 209–215

Schägger H, von Jagow G (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 199: 223–231 PubMed

Scheres SHW. (2012) RELION: implementation of a Bayesian approach to cryo-EM structure determination. J Struct Biol 180: 519–530 PubMed PMC

Schlodder E, Shubin VV, El-Mohsnawy E, Roegner M, Karapetyan NV (2007) Steady-state and transient polarized absorption spectroscopy of photosystem I complexes from the cyanobacteria Arthrospira platensis and Thermosynechococcus elongatus. Biochim Biophys Acta 1767: 732–741 PubMed

Schluchter WM, Shen G, Zhao J, Bryant DA (1996) Characterization of psaI and psaL mutants of Synechococcus sp. strain PCC 7002: a new model for state transitions in cyanobacteria. Photochem Photobiol 64: 53–66 PubMed

Snellenburg JJ, Dekker JP, van Grondelle R, van Stokkum IHM (2013) Functional compartmental modeling of the photosystems in the thylakoid membrane at 77 K. J Phys Chem B 117: 11363–11371 PubMed

Suga M, Akita F, Hirata K, Ueno G, Murakami H, Nakajima Y, Shimizu T, Yamashita K, Yamamoto M, Ago H, et al. (2015) Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond x-ray pulses. Nature 517: 99–103 PubMed

Szalkowski M, Janna Olmos JD, Buczyńska D, Maćkowski S, Kowalska D, Kargul J (2017) Plasmon-induced absorption of blind chlorophylls in photosynthetic proteins assembled on silver nanowires. Nanoscale 9: 10475–10486 PubMed

Tan S, Ducret A, Aebersold R, Gantt E (1997) Red algal LHC I genes have similarities with both Chl a/b- and a/c-binding proteins: a 21 kDa polypeptide encoded by LhcaR2 is one of the six LHC I polypeptides. Photosynth Res 53: 129–140

Thangaraj B, Jolley CC, Sarrou I, Bultema JB, Greyslak J, Whitelegge JP, Lin S, Kouřil R, Subramanyam R, Boekema EJ, et al. (2011) Efficient light harvesting in a dark, hot, acidic environment: the structure and function of PSI-LHCI from Galdieria sulphuraria. Biophys J 100: 135–143 PubMed PMC

Tian L, Liu Z, Wang F, Shen L, Chen J, Chang L, Zhao S, Han G, Wang W, Kuang T, et al. (2017a) Isolation and characterization of PSI-LHCI super-complex and their sub-complexes from a red alga Cyanidioschyzon merolae. Photosynth Res 133: 201–214 PubMed

Tian L, Xu P, Chukhutsina VU, Holzwarth AR, Croce R (2017b) Zeaxanthin-dependent nonphotochemical quenching does not occur in photosystem I in the higher plant Arabidopsis thaliana. Proc Natl Acad Sci USA 114: 4828–4832 PubMed PMC

Ueno Y, Aikawa S, Niwa K, Abe T, Murakami A, Kondo A, Akimoto S (2017) Variety in excitation energy transfer processes from phycobilisomes to photosystems I and II. Photosynth Res 133: 235–243 PubMed

Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473: 55–60 PubMed

Utschig LM, Silver SC, Mulfort KL, Tiede DM (2011) Nature-driven photochemistry for catalytic solar hydrogen production: a photosystem I-transition metal catalyst hybrid. J Am Chem Soc 133: 16334–16337 PubMed

Vanselow C, Weber APM, Krause K, Fromme P (2009) Genetic analysis of the photosystem I subunits from the red alga, Galdieria sulphuraria. Biochim Biophys Acta 1787: 46–59 PubMed

Vernon LP, Cardon S (1982) Direct spectrophotometric measurement of photosystem I and photosystem II activities of photosynthetic membrane preparations from Cyanophora paradoxa, Phormidium laminosum, and spinach. Plant Physiol 70: 442–445 PubMed PMC

Werst M, Jia Y, Mets L, Fleming GR (1992) Energy transfer and trapping in the photosystem I core antenna: a temperature study. Biophys J 61: 868–878 PubMed PMC

Wientjes E, Roest G, Croce R (2012) From red to blue to far-red in Lhca4: how does the protein modulate the spectral properties of the pigments? Biochim Biophys Acta 1817: 711–717 PubMed

Wolfe GR, Cunningham FX, Durnfordt D, Green BR, Gantt E (1994a) Evidence for a common origin of chloroplasts with light-harvesting complexes of different pigmentation. Nature 367: 566–568

Wolfe GR, Cunningham FX, Grabowski B, Gantt E (1994b) Isolation and characterization of photosystems I and II from the red alga Porphyridium cruentum. Biochim Biophys Acta 1188: 357–366

Yokono M, Murakami A, Akimoto S (2011) Excitation energy transfer between photosystem II and photosystem I in red algae: larger amounts of phycobilisome enhance spillover. Biochim Biophys Acta 1807: 847–853 PubMed

Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409: 739–743 PubMed

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