Seasonal photoacclimation patterns in the intertidal macroalga Cystoseira tamariscifolia (Ochrophyta)
DOI:
https://doi.org/10.3989/scimar.04053.05AKeywords:
antioxidant activity, Cystoseira tamariscifolia, phenolic compounds, photoinhibition, photoprotectionAbstract
Cystoseira tamariscifolia thalli collected from rocky shores and rockpools in winter and summer in Southern Spain were incubated for 7 days in UV transparent cylindrical vessels under outdoor conditions. Photosynthetic activity estimated as in vivo chlorophyll α fluorescence of photosystem II, photosynthetic pigments, antioxidant activity (DPPH assay), phenolic compounds and total internal C and N contents were determined after short-term (3 d) and mid-term (7 d) periods. Maximum quantum yield of PSII (Fv/Fm) was significantly higher in field-collected algae and after 7 d incubation in winter than in summer. In rocky shores and rockpools thalli, maximum electron transport rate (ETRmax) and photosynthetic efficiency (αETR) were much higher in summer than in winter. ETR of outdoor-grown thalli (in situ ETR) showed a daily pattern, with a decrease at noon in both winter and summer (3rd and 7th days). We found much higher antioxidant activity in thalli collected in summer than in winter. However, the concentration of internal UV screen substances (polyphenols) was higher in winter than in summer, whereas the release of phenolic compounds was lower. The highest capacity of acclimation in C. tamariscifolia found in summer and RS with emersion periods was explained by the highest dynamic photoinhibition, energy dissipation (non-photochemical quenching) and antioxidant activity (EC50).
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Abdala-Díaz R.T., Cabello-Pasini A., Pérez-Rodríguez E., et al. 2006. Daily and seasonal variations of optimum quantum yield and phenolic compounds in Cystoseira tamariscifolia (Phaeophyta). Mar. Biol. 148: 459-465. http://dx.doi.org/10.1007/s00227-005-0102-6
Amsler C.D., Fairhead V.A. 2006. Defensive and sensory chemical ecology of brown algae. Adv. Bot. Res. 43: 1-91. http://dx.doi.org/10.1016/S0065-2296(05)43001-3
Arévalo R., Pinedo S., Ballesteros E. 2007. Changes in the composition and structure of Mediterranean rocky-shore communities following a gradient of nutrient enrichment: descriptive study and test of proposed methods to assess water quality regarding macroalgae. Mar. Pollut. Bull. 55: 104-113. http://dx.doi.org/10.1016/j.marpolbul.2006.08.023 PMid:17045305
Ballesteros E., Torras X., Pinedo S., et al. 2007. A new methodology based on littoral community cartography dominated by macroalgae for the implementation of the European Water Framework Directive. Mar. Pollut. Bull. 55: 172-180. http://dx.doi.org/10.1016/j.marpolbul.2006.08.038 PMid:17045303
Belshe E.F., Durako M.J., Blum J.E. 2007. Photosynthetic rapid light curves (RLC) of Thalassia testudinum exhibit diurnal variation. J. Exp. Mar. Biol. Ecol. 342: 253-268. http://dx.doi.org/10.1016/j.jembe.2006.10.056
Bischof K., Gómez I., Molis M., et al. 2006. Ultraviolet radiation shapes seaweed communities. Rev. Environ. Sci. Biotechnol. 5: 141-166. http://dx.doi.org/10.1007/s11157-006-0002-3
Blois M.S. 1958. Antioxidant determinations by the use of a stable free radical. Nature 181: 1199-1200. http://dx.doi.org/10.1038/1811199a0
Cabello-Pasini A., Macías-Carranza V., Abdala R., et al. 2011. Effect of nitrate concentration on UVR on photosynthesis, respiration, nitrate reductase activity and phenolic compounds in Ulva rigida (Chlorophyta). J. Appl. Phycol. 23: 363-369. http://dx.doi.org/10.1007/s10811-010-9548-0
Carlson D.J., Carlson M.L. 1984. Reassessment of exudation by fucoid macroalgae. Limnol. Oceanogr. 29: 1077-1084. http://dx.doi.org/10.4319/lo.1984.29.5.1077
Celis-Plá P., Martínez B., Quintano E., et al. 2014. Short-term ecophysiological and biochemical responses of Cystoseira tamariscifolia and Ellisolandia elongata to enviromental changes. Aquat. Biol. In press. http://dx.doi.org/10.3354/ab00573
Connan S., Goulard F., Stiger V., et al. 2004. Interspecific and temporal variation in phlorotannin levels in an assemblage of brown algae. Bot. Mar. 47: 410-416. http://dx.doi.org/10.1515/BOT.2004.057
Connan S., Delisle F., Deslandes E., et al. 2006. Intra-thallus phlorotannin content and antioxidant activity in Phaeophyceae of temperate waters. Bot. Mar. 49: 39-46. http://dx.doi.org/10.1515/BOT.2006.005
Craigie J.S., McLachlan J. 1964. Excretion of coloured ultraviolet absorbing substances by marine algae. Can. J. Bot. 42: 23-33. http://dx.doi.org/10.1139/b64-003
Cruces E., Huovinen P., Gómez I. 2012. Phlorotannin and antioxidant responses upon short-term exposure to UV radiation and elevated temperature in three south Pacific kelps. Photochem. Photobiol. 88: 58-66. http://dx.doi.org/10.1111/j.1751-1097.2011.01013.x PMid:22011039
Demmig-Adams B., Adams W.III. 2006. Photoprotection in an ecological context: the remarkable complexity of thermal dissipation. New. Phytologist 172: 11-21. http://dx.doi.org/10.1111/j.1469-8137.2006.01835.x PMid:16945085
Dring M.J., Brown F.A. 1982. Photosynthesis of intertidal brown algae during and after periods of emersion; a renewed search for physiological case of zonations. Mar. Ecol. Prog. Ser. 8: 301-308. http://dx.doi.org/10.3354/meps008301
Dujmov J., Sucevic P., Antolic B. 1996. Spectrofluorometric applications in studying macroalgal exudates. Mar. Ecol. 17: 501-508. http://dx.doi.org/10.1111/j.1439-0485.1996.tb00523.x
Falkowski P. G. 1997. Evolution of the nitrogen cycle and its influence on the biological sequestration of C02 in the ocean. Nature 382: 272-275. http://dx.doi.org/10.1038/387272a0
Figueroa F.L., Gómez I. 2001. Photoacclimation to solar UV radiation in red macroalgae. J. Appl. Phycology. 13: 235-248. http://dx.doi.org/10.1023/A:1011126007656
Figueroa F.L., Korbee N. 2010. Interactive effects of UV radiation and nutrients on ecophysiology: vulnerability and adaptation to climate change. In: Israel A., Einvav R., Seckbach J. (eds), Seaweeds and their role in globally changing environments. Springer, pp. 157-182. http://dx.doi.org/10.1007/978-90-481-8569-6_10
Figueroa F.L., Vi-egla B. 2001. Effects of solar UV radiation on photosynthesis and enzyme activities (carbonic anhydrase and nitrate reductase) in marine macroalgae from Southern Spain. Rev. Chil. Hist. Nat. 74: 237-249. http://dx.doi.org/10.4067/S0716-078X2001000200003
Figueroa F.L., Salles S., Aguilera J., et al. 1997. Effects of solar radiation on photoinhibition and pigmentation in the red alga Porphyra leucosticta. Mar. Ecol. Prog. Ser. 151: 81-90. http://dx.doi.org/10.3354/meps151081
Figueroa F.L., Conde-Álvarez R., Gómez I. 2003. Relations between electron transport rates determined by pulse amplitude modulated chlorophyll fluorescence and oxygen evolution in macroalgae under different light conditions. Photosynth. Res. 75: 259-275. http://dx.doi.org/10.1023/A:1023936313544 PMid:16228606
Figueroa F.L., Martínez B., Israel A., et al. 2009. Acclimation of Red Sea macroalgae to solar radiation: photosynthesis and thallus absorptance. Aquat. Biol. 7: 159-172. http://dx.doi.org/10.3354/ab00186
Figueroa F.L., Domínguez-González, B. Korbee N. 2014. Vulnerability and acclimation to increased UVB radiation in three intertidal macroalgae of different morpho-funtional groups. Mar. Environ. Res. 97: 30-38. http://dx.doi.org/10.1016/j.marenvres.2014.01.009 PMid:24556033
Flores-Moya A., Gómez I., Vi-egla B., et al. 1998. Effects of solar radiation on the endemic Mediterranean red alga Rissoella verrucosa: photosynthetic performance, pigment content and the activities of enzymes related to nutrient uptake. New. Phytol. 139: 673-683. http://dx.doi.org/10.1046/j.1469-8137.1998.00233.x
Flores-Moya A., Hanelt D., Figueroa F.L., et al. 1999. Involvement of solar UV-B radiation in recovery of inhibited photosynthesis in the brown alga Dictyota dichotoma (Hudson) Lamouroux. J. Photochem. Photobiol. 49: 29-135.
Folin O., Ciocalteu V. 1927. On tyrosine and tryptophane determinations in proteins. J Biol. Chem. 12: 239-243.
Gómez I., Huovinen P. 2010. Induction of phlorotannins during UV exposure mitigates inhibition of photosynthesis and DNA damage in the kelp Lessonia nigrencens. Photochem. Photobiol. 86: 1056-1063. http://dx.doi.org/10.1111/j.1751-1097.2010.00786.x PMid:20670358
Häder D.P., Figueroa F.L. 1997. Photoecophysiology of marine macroalgae. Photochem. Photobiol. 66: 1-14. http://dx.doi.org/10.1111/j.1751-1097.1997.tb03132.x
Häder D.P., Lebert M., Figueroa F.L., et al. 1998. Photoinhibition in Mediterranean macroalgae by solar radiation measured on site by PAM fluorescence. Aquat. Bot. 61: 225-236. http://dx.doi.org/10.1016/S0304-3770(98)00068-0
Hanelt D. 1996. Photoinhibition of photosynthesis in marine macroalgae. Sci. Mar. 60: 243-248.
Hanelt D., Figueroa F.L. 2012. Physiological and photomorphogenic effects of light of marine macrophytes. In: Wienke C., Bischof K. (eds), Seaweed biology. Ecological studies, Springer-Verlag Berlin Heidelberg, pp. 3-23. http://dx.doi.org/10.1007/978-3-642-28451-9_1
Hanelt D., Wiencke C., Bischof K. 2003. Photosynthesis in Marine Macroalgae, Photosynthesis in Algae. In: Larkum W.A., Douglas E., Raven J.A. (eds), Advances in Photosynthesis and Respiration. Kluwer Academic Publisher, pp. 413-435.
Honkanen T., Jormalainen V. 2002. Within-plant integration and compensation: effects of simulated herbivory on growth and reproduction of the brown alga, Fucus vesiculosus. Int. J. Plant. Sci. 163: 815-823. http://dx.doi.org/10.1086/342081
Høiskar B.A.K., Haugen R., Danielsen T., et al. 2003. Multichannel moderate-bandwidth filter instrument for measurement the ozone-column amount, cloud transmittance, and ultraviolet dose rates. Appl. Optics 42: 18-20. http://dx.doi.org/10.1364/AO.42.003472
Huovinen P., Leal P., Gómez I. 2010. Interacting effects of copper, nitrogen and ultraviolet radiation on the physiology of three south Pacific kelps. Mar. Freshwater. Res. 61: 330-341. http://dx.doi.org/10.1071/MF09054
Jassby A.D., Platt T. 1976. Mathematical Formulation of the Relationship between Photosynthesis and Light for Phytoplankton. Limno. Oceanogr. 21: 540-547. http://dx.doi.org/10.4319/lo.1976.21.4.0540
Jennings J. G., Steinberg P. D. 1994. In situ exudation of phlorotannins by the sublittoral kelp Ecklonia radiata. Mar. Biol. 121: 349-354. http://dx.doi.org/10.1007/BF00346744
Karban R., Baldwin I.T. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago, USA, 329 pp. http://dx.doi.org/10.7208/chicago/9780226424972.001.0001
Klughammer C., Schreiber U. 2008. Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the Saturation Pulse method. PAM Applications notes. 1: 27-35.
Koivikko R., Loponen J., Honkanen T., et al. 2005. Contents of soluble, cell-wall-bound and exuded phlorotannins in the brown alga Fucus vesiculosus, with implications on their ecological functions. J. Chem. Ecol. 31: 195-212. http://dx.doi.org/10.1007/s10886-005-0984-2 PMid:15839490
Korbee N., Figueroa F.L., Aguilera J. 2006. Effect of light quality on the accumulation of photosynthetic pigments, proteins and mycosporine-like amino acids in the red alga Porphyra leucosticta (Bangiales, Rhodophyta). J. Photoch. Photobiol. B. 80: 71-78. http://dx.doi.org/10.1016/j.jphotobiol.2005.03.002 PMid:16038805
Lobban C.S., Harrison P.J. 1994. Seaweed Ecology and Physiology. Cambridge University Press, New York, 367 pp. http://dx.doi.org/10.1017/CBO9780511626210 PMCid:PMC1137507
Longstaff B.J., Kildea T., Runcie J.W., et al. 2002. An in situ study of photosynthetic oxygen exchange and electron transport rate in the marine macroalga Ulva lactuca (Chlorophyta). Photosynth. Res. 74: 281-293. http://dx.doi.org/10.1023/A:1021279627409 PMid:16245139
Lüning K. 1990. Seaweeds: Their Environment, Biogeography and Ecophysiology. Wiley, New York, 527 pp. PMCid:PMC1971603
Lüning K., Dring M.J. 1985. Action spectra and spectral quantum yield of photosynthesis in marine macroalgae with thin and thick thalli. Mar. Biol. 87: 119-129. http://dx.doi.org/10.1007/BF00539419
Mercado J. M., Gordillo F.J., Figueroa F.L., et al. 1998. External carbonic anhydrase and affinity to inorganic carbon in intertidal macroalgae. J. Exp. Mar. Biol. Ecol. 221: 209-220. http://dx.doi.org/10.1016/S0022-0981(97)00127-5
Nitschke U., Connan S., Stengel D. 2012. Chlorophyll a fluorescence responses of temperate Phaeophyceae under submersion and emersion regimes: a comparison of a rapid and steady-state light curves. Photosynth. Res. 114: 29-42. http://dx.doi.org/10.1007/s11120-012-9776-z PMid:22915336
Nygard C.A., Dring M.J. 2008. Influence of salinity, temperature and dissolved inorganic carbon and nutrient concentration on the photosynthesis and growth of Fucus vesiculosus form Baltic and Irish Sea. Eur. J. Phycol. 43: 253-262. http://dx.doi.org/10.1080/09670260802172627
Osmond C.B. 1994. What is photoinhibition? Some insights from comparisons of shade and sun plants. In: Baker N.R., Bowyer J.R. (eds) Photoinhibition of photosynthesis, from molecular mechanisms to the field. Bios Scientific Publ Oxford, Oxford, pp. 1-24.
Pavia H., Toth G.B. 2000. Influence of nitrogen on the phlorotannin content of the brown seaweeds Ascophyllum nodosum and Fucus vesiculosus. Hydrobiologia 440: 299-305. http://dx.doi.org/10.1023/A:1004152001370
Pavia H., Cervin G., Lindgren A., et al. 1997. Effects of UVB radiation and simulated herbivory on phlorotannins in the brown alga Ascophylum nodosum. Mar. Ecol. Prog. Ser. 157: 139-146. http://dx.doi.org/10.3354/meps157139
Platt T., Gallegos C.L. 1980. Modelling primary production. In: Falkowski P. (eds) Primary Productivity in the Sea. Plenum Press, New York, pp. 339-362. http://dx.doi.org/10.1007/978-1-4684-3890-1_19
Peckol P., Krane J. M., Yates J.L. 1996. Interactive effects of inducible defense and resource availability on phlorotannins in the North Atlantic brown alga Fucus vesiculosus. Mar. Ecol. Prog. Ser. 138: 209-217. http://dx.doi.org/10.3354/meps138209
Ragan M.A., Graige A. 1980. Quantitative studies on brown algal phenols IV. Ultraviolet spectrophotometry of extracted polyphenols and implications for measuring dissolved organic matter in sea water. J. Exp. Mar. Biol. Ecol. 46: 231-239. http://dx.doi.org/10.1016/0022-0981(80)90033-7
Ragan M.A., Jensen A. 1978. Quantitative studies on brown algal phenols II. Seasonal variation in polyphenol content of Ascophyllum nodosum (L.) Le Jol. and Fucus vesiculosus (L) J. Exp. Mar. Biol. Ecol. 34: 245-258. http://dx.doi.org/10.1016/S0022-0981(78)80006-9
Ramírez T., Cortés D., Mercado J.M., et al. 2005. Seasonal dynamics of inorganic nutrients and phytoplankton biomass in the NW Alboran Sea. Estuar. Coast. Shelf. Sci. 65: 654-670. http://dx.doi.org/10.1016/j.ecss.2005.07.012
Ritchie R.J. 2008. Universal chlorophyll equations for estimating chlorophylls a, b, c and d and total chlorophylls in natural assemblages of photosynthetic organisms using acetone, methanol, or ethanol solvents. Photosynthetica 46: 115-126. http://dx.doi.org/10.1007/s11099-008-0019-7
Roleda M.Y., Clayton M.N., Wiencke C. 2006. Screening capacity of UV-absorbing compounds in spores of Arctic Laminariales. J. Exp. Mar. Biol. Ecol. 338: 123-133. http://dx.doi.org/10.1016/j.jembe.2006.07.004
Sales M., Ballesteros E. 2012. Seasonal dynamics and annual production of Cystoseira crinita (Fucales: Ochrophyta) dominated assemblages from the northwestern Mediterranean. Sci. Mar. 76: 391-401. http://dx.doi.org/10.3989/scimar.03465.16D
Schreiber U., Schliwa U., Bilger W. 1986.Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth. Res. 10: 51-62. http://dx.doi.org/10.1007/BF00024185 PMid:24435276
Schreiber U., Endo T., Mi H., et al. 1995. Quenching analysis of chlorophyll fluorescence by saturation pulse method: particular aspects relating to the study of eukaryotic algae and cyanobacteria. Plant. Cell. Physiol. 36: 873-882.
Swanson A., Druehl L.D. 2002. Induction, exudation and the UV protective role of kelp phlorotannins. Aquat. Bot. 73: 241-253. http://dx.doi.org/10.1016/S0304-3770(02)00035-9
Targett N.M., Coen L.D., Boettcher A.A., et al. 1992. Biogeographic comparisons of marine algal polyphenolics: evidence against a latitudinal trend. Oecologia 89: 464-470.
Thibaut T., Pinedo S., Torras X., et al. 2005. Long-term decline of the populations of Fucales (Cystoseira spp. and Sargassum spp.) in the Albères coast (France), north-western Mediterranean). Mar. Pollut. Bull. 50: 1472-1489. http://dx.doi.org/10.1016/j.marpolbul.2005.06.014 PMid:16026805
Toth G. B., Pavia H. 2000. Water-borne cues induce chemical defense in a marine alga (Ascophyllum nodosum). Proc. Natl. Acad. Sci. USA 97: 14418-14420. http://dx.doi.org/10.1073/pnas.250226997 PMid:11106371 PMCid:PMC18933
Underwood A.J. 1997. Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge, New York, 509 pp.
Zubia M., Payri C., Deslandes E. 2008. Alginate, mannitol, phenolic compounds and biological activities of two range-extending brown algae, Sargassum mangarevense and Turbinaria ornata (Phaeophyta: Fucales), from Tahiti (French Polynesia). J. Appl. Phycol. 20: 1033-1043. http://dx.doi.org/10.1007/s10811-007-9303-3
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