Plants and algae have developed various regulatory mechanisms for optimal delivery of excitation energy to the photosystems even during fluctuating light conditions; these include state transitions as well as non-photochemical quenching. The former process maintains the balance by redistributing antennae excitation between the photosystems, meanwhile the latter by dissipating excessive excitation inside the antennae. In the present study, these mechanisms have been analysed in the cryptophyte alga Guillardia theta. Photoprotective non-photochemical quenching was observed in cultures only after they had entered the stationary growth phase. These cells displayed a diminished overall photosynthetic efficiency, measured as CO2 assimilation rate and electron transport rate. However, in the logarithmic growth phase G. theta cells redistributed excitation energy via a mechanism similar to state transitions. These state transitions were triggered by blue light absorbed by the membrane integrated chlorophyll a/c antennae, and green light absorbed by the lumenal biliproteins was ineffective. It is proposed that state transitions in G. theta are induced by small re-arrangements of the intrinsic antennae proteins, resulting in their coupling/uncoupling to the photosystems in state 1 or state 2, respectively. G. theta therefore represents a chromalveolate algae able to perform state transitions.

Department of Chemistry Umeå University SE 90187 Umeå Sweden

Institute of Microbiology Centre Algatech Laboratory of Photosynthesis Opatovický Mlýn Třeboň 379 81 Czech Republic

Zobrazit více v PubMed

Bailey S, Melis A, Mackey KRM, Cardol P, Finazzi G, van Dijken G, Berg GM, Arrigo K, Shrager J, Grossman A. 2008. Alternative photosynthetic electron flow to oxygen in marine Synechococcus . Biochimica et Biophysica Acta (BBA) - Bioenergetics 1777, 269–276. PubMed

Biggins J, Bruce D. 1989. Regulation of excitation energy transfer in organisms containing phycobilins. Photosynthesis Research 20, 1–34. PubMed

Broughton MJ, Howe CJ, Hiller RG. 2006. Distinctive organization of genes for light-harvesting proteins in the cryptophyte alga Rhodomonas . Gene 369, 72–79. PubMed

Bruyant F, Babin M, Genty B, et al. 2005. Diel variations in the photosynthetic parameters of Prochlorococcus strain PCC 9511: Combined effects of light and cell cycle. Limnology and Oceanography 50, 850–863.

Butler NB. 1982. Carbon dioxide equilibria and their applications . New York: Addison-Wesley Publishing Company Inc.

Campbell D, Hurry V, Clarke AK, Gustafsson P, Öquist G. 1998. Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiology and Molecular Biology Reviews 62, 667–683. PubMed PMC

Collini E, Wong CY, Wilk KE, Curmi PMG, Brumer P, Scholes GD. 2010. Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature. Nature 463, 644–647. PubMed

Dall’Osto L, Bressan M, Bassi R. 2015. Biogenesis of light harvesting proteins. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1847, 861–871. PubMed

de Bianchi S, Ballottari M, Dall’Osto L, Bassi R. 2010. Regulation of plant light harvesting by thermal dissipation of excess energy. Biochemical Society Transactions 38, 651–660. PubMed

Delphin E, Duval J-C, Kirilovsky D. 1995. Comparison of state 1-state 2 transitions in the green alga Chlamydomonas reinhardtii and in the red alga Rhodella violacea: effect of kinase and phosphatase inhibitors. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1232, 91–95.

Delphin E, Duval J-C, Etienne A-L, Kirilovsky D. 1996. State transitions or ΔpH-dependent quenching of photosystem II fluorescence in red algae. Biochemistry 35, 9435–9445. PubMed

Dietzel L, Pfannschmidt T. 2008. Photosynthetic acclimation to light gradients in plant stands comes out of shade. Plant Signaling & Behavior 3, 1116–1118. PubMed PMC

Drop B, Yadav K.N S, Boekema EJ, Croce R. 2014. Consequences of state transitions on the structural and functional organization of Photosystem I in the green alga Chlamydomonas reinhardtii . The Plant Journal 78, 181–191. PubMed

Durnford DG, Deane JA, Tan S, McFadden GI, Gantt E, Green BR. 1999. A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins, with implications for plastid evolution. Journal of Molecular Evolution 48, 59–68. PubMed

Finazzi G, Barbagallo RP, Bergo E, Barbato R, Forti G. 2001. Photoinhibition of Chlamydomonas reinhardtii in State 1 and State 2: damages to the photosynthetic apparatus under linear and cyclic electron flow. Journal of Biological Chemistry 276, 22251–22257. PubMed

Funk C, Alami M, Tibiletti T, Green BR. 2011. High light stress and the one-helix LHC-like proteins of the cryptophyte Guillardia theta . Biochimica et Biophysica Acta (BBA) - Bioenergetics 1807, 841–846. PubMed

Gibbs P, Biggins J. 1989. Regulation of the distribution of excitation energy in Ochromonas danica, an organism containing a chlorophyll-A/C/carotenoid light harvesting antenna. Photosynthesis Research 21, 81–91. PubMed

Gibbs SP. 1981. The chloroplast of some algal groups may have evolved from endosymbiotic eukaryotic algae. Annals of the New York Academy of Sciences 361, 193–208. PubMed

Goss R, Lepetit B. 2015. Biodiversity of NPQ. Journal of Plant Physiology 172, 13–32. PubMed

Green BR, Durnford DG. 1996. The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 47, 685–714. PubMed

Guillard RL. 1975. Culture of phytoplankton for feeding marine invertebrates. In: Smith W, Chanley M, eds. Culture of Marine Invertebrate Animals . New York: Springer US, 29–60.

Hammer A, Schumann R, Schubert H. 2002. Light and temperature acclimation of Rhodomonas salina (Cryptophyceae): photosynthetic performance. Aquatic Microbial Ecology 29, 287–296.

Harrop SJ, Wilk KE, Dinshaw R, et al. 2014. Single-residue insertion switches the quaternary structure and exciton states of cryptophyte light-harvesting proteins. Proceedings of the National Academy of Sciences 111, E2666–E2675. PubMed PMC

Hoef-Emden K. 2008. Molecular phylogeny of phycocyanin-containing cryptophytes: evolution of biliproteins and geographical distribution. Journal of Phycology 44, 985–993. PubMed

Janssen J, Rhiel E. 2008. Evidence of monomeric photosystem I complexes and phosphorylation of chlorophyll a/c-binding polypeptides in Chroomonas sp strain LT (Cryptophyceae). International Microbiology 11, 171–178. PubMed

Jansson S. 1999. A guide to the Lhc genes and their relatives in Arabidopsis . Trends in Plant Science 4, 236–240. PubMed

Jeffrey SW, Humphrey GF. 1975. New spectrophotometric equations for determining chlorophyll a, b, c 1 and c 2 in higher plants, algae and natural phytoplankton. Biochemie und Physiologie der Pflanzen 167, 191–194.

Joshua S, Mullineaux CW. 2004. Phycobilisome diffusion is required for light-state transitions in cyanobacteria. Plant Physiology 135, 2112–2119. PubMed PMC

Kaňa R, Vass I. 2008. Thermoimaging as a tool for studying light-induced heating of leaves Correlation of heat dissipation with the efficiency of photosystem II photochemistry and non-photochemical quenching. Environmental and Experimental Botany 64, 90–96.

Kaňa R, Prášil O, Mullineaux CW. 2009. Immobility of phycobilins in the thylakoid lumen of a cryptophyte suggests that protein diffusion in the lumen is very restricted. FEBS Letters 583, 670–674. PubMed

Kaňa R, Kotabová E, Komárek O, Šedivá B, Papageorgiou GC, Govindjee, Prášil O. 2012a. The slow S to M fluorescence rise in cyanobacteria is due to a state 2 to state 1 transition. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1817, 1237–1247. PubMed

Kaňa R, Kotabová E, Sobotka R, Prášil O. 2012b. Non-photochemical quenching in cryptophyte alga Rhodomonas salina is located in chlorophyll a/c antennae. PLoS ONE 7, e29700. PubMed PMC

Kaňa R, Kotabová E, Lukeš M, Papáček Š, Matonoha C, Liu L-N, Prášil O, Mullineaux CW. 2014. Phycobilisome mobility and its role in the regulation of light harvesting in red algae. Plant Physiology 165, 1618–1631. PubMed PMC

Kirilovsky D, Kaňa R, Prášil O. 2014. Mechanisms modulating energy arriving at reaction centers in cyanobacteria. In: Demmig-Adams B AW, Garab G, Govindjee ed. Non-Photochemical Quenching and Thermal Energy Dissipation In Plants, Algae and Cyanobacteria , Vol. 40 (in press). Dordrecht: Springer Netherlands.

Kolber ZS, Prášil O, Falkowski PG. 1998. Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1367, 88–106. PubMed

Kopečná J, Komenda J, Bučinská L, Sobotka R. 2012. Long-term acclimation of the cyanobacterium Synechocystis sp. PCC 6803 to high light is accompanied by an enhanced production of chlorophyll that is preferentially channeled to trimeric photosystem I. Plant Physiology 160, 2239–2250. PubMed PMC

Kotabová E, Jarešová J, Kaňa R, Sobotka R, Bína D, Prášil O. 2014. Novel type of red-shifted chlorophyll a antenna complex from Chromera velia. I. Physiological relevance and functional connection to photosystems. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1837, 734–743. PubMed

Kouřil R, Wientjes E, Bultema JB, Croce R, Boekema EJ. 2013. High-light vs. low-light: Effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana . Biochimica et Biophysica Acta (BBA) - Bioenergetics 1827, 411–419. PubMed

Lavaud J, Lepetit B. 2013. An explanation for the inter-species variability of the photoprotective non-photochemical chlorophyll fluorescence quenching in diatoms. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1827, 294–302. PubMed

Lavaud J, Strzepek RF, Kroth PG. 2007. Photoprotection capacity differs among diatoms: Possible consequences on the spatial distribution of diatoms related to fluctuations in the underwater light climate. Limnology and Oceanography 52, 1188–1194.

Lewis MR, Smith JC. 1983. A small volume, short-incubation-time method for measurement of photosynthesis as a function of incident irradiance. Marine Ecology Progress Series 13, 99–102.

Lewitus AJ, Caron, David A. 1990. Relative effects of nitrogen or phosphorus depletion and light intensity on the pigmentation, chemical composition, and volume of Pyrenomonas salina (Cryptophyceae). Marine Ecology Progress Series 61, 171–181.

Li X-P, Bjorkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK. 2000. A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403, 391–395. PubMed

Li Z, Wakao S, Fischer BB, Niyogi KK. 2009. Sensing and responding to excess light. Annual Review of Plant Biology 60, 239–260. PubMed

Lunde C, Jensen PE, Rosgaard L, Haldrup A, Gilpin MJ, Scheller HV. 2003. Plants impaired in state transitions can to a large degree compensate for their defect. Plant and Cell Physiology 44, 44–54. PubMed

MacColl R, Eisele LE, Dhar M, Ecuyer J-P, Hopkins S, Marrone J, Barnard R, Malak H, Lewitus AJ. 1999a. Bilin organization in cryptomonad biliproteins. Biochemistry 38, 4097–4105. PubMed

MacColl R, Eisele LE, Marrone J. 1999b. Fluorescence polarization studies on four biliproteins and a bilin model for phycoerythrin 545. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1412, 230–239. PubMed

Minagawa J. 2011. State transitions—The molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1807, 897–905. PubMed

Mullineaux C, Allen J. 1990. State 1-State 2 transitions in the cyanobacterium Synechococcus 6301 are controlled by the redox state of electron carriers between Photosystems I and II. Photosynthesis Research 23, 297–311. PubMed

Mullineaux CW, Emlyn-Jones D. 2005. State transitions: an example of acclimation to low-light stress. Journal of Experimental Botany 56, 389–393. PubMed

Murata N. 1969. Control of excitation transfer in photosynthesis I. Light-induced change of chlorophyll a fluoresence in Porphyridium cruentum . Biochimica et Biophysica Acta (BBA) - Bioenergetics 172, 242–251. PubMed

Neilson JAD, Durnford DG. 2009. Evolutionary distribution of light-harvesting complex-like proteins in photosynthetic eukaryotes. Genome 53, 68–78. PubMed

Niyogi KK, Truong TB. 2013. Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Current Opinion in Plant Biology 16, 307–314. PubMed

Owens TG. 1986. Light-harvesting function in the diatom Phaeodactylum tricornutum: II. Distribution of excitation energy between the photosystems. Plant Physiology 80, 739–746. PubMed PMC

Papageorgiou G, Tsimilli-Michael M, Stamatakis K. 2007. The fast and slow kinetics of chlorophyll a fluorescence induction in plants, algae and cyanobacteria: a viewpoint. Photosynthesis Research 94, 275–290. PubMed

Rappé MS, Suzuki MT, Vergin KL, Giovannoni SJ. 1998. Phylogenetic diversity of ultraplankton plastid small-subunit rRNA genes recovered in environmental nucleic acid samples from the Pacific and Atlantic coasts of the United States. Applied and Environmental Microbiology 64, 294–303. PubMed PMC

Ruban AV, Johnson MP, Duffy CDP. 2012. The photoprotective molecular switch in the photosystem II antenna. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1817, 167–181. PubMed

Snyder UK, Biggins J. 1987. Excitation-energy redistribution in the cryptomonad alga Cryptomonas ovata . Biochimica et Biophysica Acta (BBA) - Bioenergetics 892, 48–55.

Spear-Bernstein L, Miller KR. 1989. Unique location of the phycobiliprotein light-harvesting pigment in the Cryptophyceae. Journal of Phycology 25, 412–419.

Strzepek RF, Harrison PJ. 2004. Photosynthetic architecture differs in coastal and oceanic diatoms. Nature 431, 689–692. PubMed

Suggett DJ, Moore MC, Geider RJ. 2010. Estimating aquatic productivity from active fluorescence measurement. In: Suggett DJ PO, Borowitzka M.A, ed. Chlorophyll a Fluorescence in Aquatic Sciences: Methods and Applications . Dordrecht: Springer, 103–127.

Ünlü C, Drop B, Croce R, van Amerongen H. 2014. State transitions in Chlamydomonas reinhardtii strongly modulate the functional size of photosystem II but not of photosystem I. Proceedings of the National Academy of Sciences 111, 3460–3465. PubMed PMC

Photoprotective strategies in the motile cryptophyte alga Rhodomonas salina-role of non-photochemical quenching, ions, photoinhibition, and cell motility

Role of Ions in the Regulation of Light-Harvesting