Abstract
To be able to survive, marine macroalgae in shallow coastal waters need mechanisms for short-term acclimation to fast changes in their environment. Of major importance are mechanisms that regulate the efficiency of photosynthesis by protecting PS II from photo-oxidative damage. Carotenoids, xanthophyll cycles and non-photochemical quenching (NPQ) are central constituents of such protection mechanisms. Red algae as a group do not have a universal carotenoid composition. We screened ten red algal species and selected two species, originating from similar ecological conditions but with different carotenoid compositions, for use in irradiance-acclimation experiments. We selected the tropical intertidal species Gracilaria domingensis and Kappaphycus alvarezii with antheraxanthin and lutein as major xanthophylls, respectively. Simultaneous in vivo fluorescence and O2 evolution experiments were performed at different irradiance levels, which allowed a direct comparison of overall photosynthetic performance with NPQ. Interconversions of xanthophylls (violaxanthin, zeaxanthin, β-cryptoxanthin and one unidentified carotenoid) did occur in G. domingensis, but not in response to sudden exposure to light. Thus, NPQ was not correlated with any xanthophyll cycle during short-term acclimation to light. G. domingensis had five times higher weight-specific photosynthetic rates than K. alvarezii, which can be explained by the thicker thallus of K. alvarezii. Chlorophyll-specific gross photosynthetic rates were higher in K. alvarezii, but net rates were the same for both species. G. domingensis showed an immediate strong onset of NPQ upon exposure to irradiance, followed by downregulation to the NPQ level required. In K. alvarezii NPQ increased slowly until the required NPQ level was reached. At high irradiance G. domingensis downregulated photosynthesis while K. alvarezii continued to produce O2 even at 2,000 μmol photons m−2 s−1 without NPQ increase. The strategy of K. alvarezii may provide short-term gains but with the risk of oxidative damage. The fast onset of NPQ in G. domingensis even at subsaturating irradiance as well as downregulation of photosynthesis when NPQ is saturated might provide this species with a competitive advantage under conditions of changing irradiance in the field.
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References
Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Ann Rev Plant Physiol Plant Mol Biol 50:601–639
Britton G (1993) Biosynthesis of carotenoids. In: Young A, Britton G (eds) Carotenoids in photosynthesis. Chapman & Hall, London, pp 96–126
Brown LM, McLachlan J (1982) Atypical carotenoids for the Rhodophyceae in the genus Gracilaria (Gigartinales). Phycologia 21:9–16
Bungard RA, Ruban AV, Hibbered JM, Press MC, Horton P, Scholes JD (1999) Unusual carotenoid composition and a new type of xanthophyll cycle in plants. Proc Natl Acad Sci USA 96:1135–1139
Carnicas E, Jiménez C, Niell FX (1999) Effects of changes of irradiance on the pigment composition of Gracilaria tenuistipitata var. liui Zhang et Xia. J Photochem Photobiol B Biol 50:149–158
Choo KS, Nilsson J, Pedersén M, Snoeijs P (2005) Photosynthesis, carbon uptake and antioxidant defence in two coexisting filamentous green algae under different stress conditions. Mar Ecol Prog Ser 292:127–138
Consalvey M, Perkins RG, Paterson DM, Underwood GJC (2005) PAM fluorescence: a beginners guide for benthic diatomists. Diatom Res 20:1–22
Demmig-Adams B (1990) Carotenoids and photoprotection in plants: a role of the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24
Demmig-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626
Demmig-Adams B, Adams WW (1993) The xanthophyll cycle. In: Young A, Britton G (eds) Carotenoids in photosynthesis. Chapman & Hall, London, pp 206–251
Ekman P, Yu S, Pedersén M (1991) Effects of altered salinity, darkness and algal nutrient status on floridoside and starch content, α-galactosidase activity and agar yield of cultivated Gracilaria sordida. Br Phycol J 26:123–131
Falkowski PG, Raven JA (1997) Aquatic photosynthesis. Blackwell Science, Oxford, p 375
Frank HA, Cogdell RJ (1993) The photochemistry and function of carotenoids in photosynthesis. In: Young A, Britton G (eds) Carotenoids in photosynthesis. Chapman & Hall, London, pp 252–326
García-Plazoala JI, Hernández A, Errasti, Becerril JM (2002) Occurrence and operation of the lutein epoxide cycle in Quercus species. Funct Plant Biol 29:1075–1080
García-Plazoala JI, Hernández A, Olano JM, Becerril JM (2003) The operation of the lutein epoxide cycle correlates with energy dissipation. Funct Plant Biol 30:319–324
Gilmore AM, Yamamoto Y (1993) Linear models relating xanthophylls and lumen acidity to non-photochemical fluorescence quenching. Evidence that antheraxanthin explains zeaxanthin-independent quenching. Photosynth Res 35:67–78
Goss R, Böhme K, Wilhelm C (1998) The xanthophyll cycle of Mantoniella squamata converts violaxanthin into antheraxanthin but not to zeaxanthin: consequences for the mechanism of enhanced non-photochemical quenching. Planta 205:613–621
Granbom M (2001) Circadian rhythms and carbon acquisition in the red algae Kappaphycus alvarezii and Eucheuma denticulatum. Doctoral Thesis, Department of Botany, Stockholm University
Hager A (1980) The reversible, light-induced conversions of xanthophylls in the chloroplast. In: Czygan F-C (ed) Pigments in Plants. Gustav Fischer, Stuttgart, pp 57–79
Hanelt D, Nultsch W (1991) The role of chromatophore arrangement in protecting the chromatophores of the brown alga Dictyota dichotoma against photodamage. J Plant Physiol 138:470–475
Henley WJ (1993) Measurement and interpretation of photosynthetic light-response curves in algae in the context of photoinhibition and diel changes. J Phycol 29:729–739
Holt NE, Fleming GR, Niyogi KK (2004) Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry 43:8281–8289
Horton P, Hague A (1988) Studies on the induction of chlorophyll fluorescence in isolated barley protoplasts. IV. Resolution of non-photochemical quenching. Biochim Biophys Acta 932:107–115
Jassby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547
Johansson G, Snoeijs P (2002) Macroalgal photosynthetic responses to light in relation to morphology and depth zonation. Mar Ecol Progr Ser 244:63–72
Kromkamp JC, Forster RM (2003) The use of variable fluorescence measurements in aquatic ecosystems: differences between multiple and single turnover measuring protocols and suggested terminology. Eur J Phycol 38:103–112
Kroon B, Prézelin BB, Schofield O (1993). Chromatic regulation of quantum yields for photosystem II charge separation, oxygen evolution and carbon fixation in Heterocapsa pygmaea (Pyrrophyta). J Phycol 29:453–462
Marquardt J, Hanelt D (2004) Carotenoid composition of Delesseria lancifolia and other marine red algae from polar and temperate habitats. Eur J Phycol 39:285–292
Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566
Niyogi KK, Björkman O, Grossman AR (1997) The roles of specific xanthophylls in photoprotection. Proc Natl Acad Sci USA 94:14162–14167
Pedersén M, Collén J, Abrahamsson K, Mtolera M, Semesi AK, Garcia Reina G (1996) The ice-ice disease and oxidative stress of marine algae. In: Björk M, Semesi AK, Pedersén M, Bergman B (eds) Current trends in marine botanical research in the East African region. Gotab AB, Sweden, pp 11–24
Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Watanabe A, Hattori A (eds) Cultures and collections of algae. Proceedings of the United States – Japan Conference Hakone, Japan Society Plant Physiologica, pp 63–75
Redfield AC, Ketchum BH, Richards FA (1963) The influence of organisms on the composition of seawater. In: Hill MN (ed) The sea, vol 2. Interscience Publishers, NY, pp26–77
Rmiki N-E, Brunet C, Cabioch J, Lemoine Y (1996) Xanthophyll-cycle and photosynthetic adaptation to environment in macro- and microalgae. Hydrobiologia 326/327:407–413
Sagert S, Schubert H (2000) Acclimation of Palmaria palmata (Rhodophyta) to light intensity: Comparison between artificial and natural light fields. J Phycol 36:1119–1128
Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze ED, Caldwell M (eds) Ecophysiology of photosynthesis. Springer-Verlag, Berlin, pp 49–70
Schubert H, Gerbersdorf S, Titlyanov E, Titlyanova T, Granbom M, Pape C, Lüning K (2004) Circadian rhythm of photosynthesis in Kappaphycus alvarezii (Rhodophyta): independence of the cell cycle and possible photosynthetic clock targets. Eur J Phycol 39:423–430
Shen YK, Chow WS, Park YI, Anderson JM (1996) Photoinactivation of photosystem II by cumulative exposure to short light pulses during the induction period of photosynthesis. Photosynth Res 47:51–59
Shimidzu N, Goto M, Miki W (1996) Carotenoids as singlet oxygen quenchers in marine organisms. Fish Sci 62:134–137
Uhrmacher S, Hanelt D, Nultsch W (1995) Zeaxanthin content and the degree of photoinhibition are linearly correlated in the brown alga Dictyota dichotoma. Mar Biol 123:159–165
Ursi S, Pedersén M, Plastino E, Snoeijs P (2003) Intraspecific variation of photosynthesis, respiration and photoprotective carotenoids in Gracilaria birdiae (Gracilariales: Rhodophyta). Mar Biol 142:997–1007
Wright SW, Jeffrey SW (1997) High-resolution HPLC system for chlorophylls and carotenoids of marine phytoplankton. In: Jeffrey SW, Mantoura RFC, Wright SW (eds) Phytoplankton pigments in oceanography: guidelines to modern methods. Unesco, Paris, pp 327–341
Young AJ, Frank HA (1996) Energy transfer reactions involving carotenoids: quenching of chlorophyll fluorescence. J Photochem Photobiol B Biol 36:3–15
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Financial support from the Sernanders Stiftelse, Uppsala University and the Stockholm Marine Research Centre is gratefully acknowledged. We thank two anonymous reviewers for valuable comments to an earlier draft of this paper.
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Communicated by M. Kühl, Helsingør
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Andersson, M., Schubert, H., Pedersén, M. et al. Different patterns of carotenoid composition and photosynthesis acclimation in two tropical red algae. Mar Biol 149, 653–665 (2006). https://doi.org/10.1007/s00227-005-0174-3
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DOI: https://doi.org/10.1007/s00227-005-0174-3