References

Biogeosciences

1726-4189

Copernicus Publications

Göttingen, Germany

10.5194/bg-8-1441-2011

Photosynthetic responses of Emiliania huxleyi to UV radiation and elevated temperature: roles of calcified coccoliths

¹ Gao

¹ Villafañe

V. E.

² Helbling

E. W.

State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, 361005, China

Estación de Fotobiología Playa Unión and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Casilla de Correos No. 15, 9103 Rawson, Chubut, Argentina

06 06 2011

8 6 1441 1452

2011

This work is licensed under the Creative Commons Attribution 3.0 Unported License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/3.0/

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Changes in calcification of coccolithophores may affect their photosynthetic responses to both, ultraviolet radiation (UVR, 280–400 nm) and temperature. We operated semi-continuous cultures of Emiliania huxleyi (strain CS-369) at reduced (0.1 mM, LCa) and ambient (10 mM, HCa) Ca2+ concentrations and, after 148 generations, we exposed cells to six radiation treatments (>280, >295, >305, >320, >350 and >395 nm by using Schott filters) and two temperatures (20 and 25 °C) to examine photosynthesis and calcification responses. Overall, our study demonstrated that: (1) decreased calcification resulted in a down regulation of photoprotective mechanisms (i.e., as estimated via non-photochemical quenching, NPQ), pigments contents and photosynthetic carbon fixation; (2) calcification (C) and photosynthesis (P) (as well as their ratio) have different responses related to UVR with cells grown under the high Ca2+ concentration being more resistant to UVR than those grown under the low Ca2+ level; (3) elevated temperature increased photosynthesis and calcification of E. huxleyi grown at high Ca2+ concentrations whereas decreased both processes in low Ca2+ grown cells. Therefore, a decrease in calcification rates in E. huxleyi is expected to decrease photosynthesis rates, resulting in a negative feedback that further reduces calcification.

References 1

Adams III., W. W. and Demmig-Adams, B.: Chlorophyll fluorescence as a tool to monitor plant response to the environment, in: Chlorophyll a Fluorescence: A Signature of Photosynthesis, edited by: Papageorgiou, G. C. and Govindjee, Springer, Berlin, Germany, 583–604, 2004.

Anning, T., Nimer, N., Merrett, M. J., and Brownlee, C.: Costs and benefits of calcification in coccolithophorids, J. Marine Syst., 9, 45–56, 1996.

Beardall, J., Sobrino, C., and Stojkovic, S.: Interactions between the impacts of ultraviolet radiation, elevated CO2, and nutrient limitation on marine primary producers, Photochem. Photobio. S., 8, 1257–1265, <a href="http://dx.doi.org/10.1039/b9pp00034h">https://doi.org/10.1039/b9pp00034h</a>, 2009.

Bornman, J. F., Reuber, S., Cen, Y., and Weissenböck, G.: Ultraviolet radiation as a stress factor and the role of protective pigments, in: Plants and UV-B: Responses to Environmental Change, edited by: Lumsden, P. J., Cambridge University Press, Cambridge, NY, 157–168, 1997.

Brownlee, C. and Taylor, A.: Calcification in coccolithophores: a cellular perspective, in: Coccolithophores: From Molecular Biology to Global Impact, edited by: Thierstein, H. R. and Young, J. R., Springer, Berlin, Germany, 31–49, 2004.

Brownlee, C., Davies, M., Nimer, N., Dong, L., and Merrett, M.: Calcification, photosynthesis and intracellular regulation in Emiliania huxleyi, B. Inst. Oceanogr. Monaco, 14, 19–35, 1995.

Buma, A. G. J., Van Oijen, T., Van de Poll, W., Veldhuis, M. J. W., and Gieskes, W. W. C.: The sensitivity of Emiliania huxleyi (Prymnesiophyceae) to ultraviolet-B radiation, J. Phycol., 36, 296–303, 2000.

Cokacar, T., Kubilay, N., and Oguz, T.: Structure of Emiliania huxleyi blooms in the Black Sea surface waters as detected by SeaWIFS imagery, Geophys. Res. Lett., 28, 4607–4610, 2001.

De Bodt, C., Van Oostende, N., Harlay, J., Sabbe, K., and Chou, L.: Individual and interacting effects of pCO2 and temperature on Emiliania huxleyi calcification: study of the calcite production, the coccolith morphology and the coccosphere size, Biogeosciences, 7, 1401–1412, <a href="http://dx.doi.org/10.5194/bg-7-1401-2010">https://doi.org/10.5194/bg-7-1401-2010</a>, 2010.

Demmig-Adams, B.: Carotenoids and photoprotection in plants: a role for the xanthophylls zeaxanthin, Biochim. Biophys. Acta, 1020, 1–24, 1990.

Dickson, A. G. and Millero, F. J.: A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media, Deep-Sea Res., 34, 1733–1743, 1987.

Falkowski, P. G. and Raven, J. A.: Aquatic Photosynthesis, Blackwell Scientific, Oxford, UK, 1997.

Feng, Y., Warner, M. E., Zhang, Y., Sun, J., Fu, F., Rose, J. M., and Hutchins, D. A.: Interactive effects of increased pCO2, temperature and irradiance on the marine coccolithophore Emiliania huxleyi (Prymnesiophyceae), Eur. J. Phycol., 43, 87–98, 2008.

Gao, K., Ruan, Z., Villafañe, V. E., Gattuso, J. P., and Helbling, E. W.: Ocean acidification exacerbates the effect of UV radiation on the calcifying phytoplankter Emiliania huxleyi, Limnol. Oceanogr., 54, 1855–1862, 2009.

Genty, B. E., Briantais, J. M., and Baker, N. R.: Relative quantum efficiencies of the two photosystems of leaves in photorespiratory and non-photorespiratory conditions, Plant Physiol. Bioch., 28, 1–10, 1989.

Guan, W. and Gao, K.: Impacts of UV radiation on photosynthesis and growth of the coccolithophore Emiliania huxleyi (Haptophyceae), Environ. Exp. Bot., 67, 502–508, 2010.

Gattuso, J. P., Gao, K., Lee, K., Rost, B., and Schulz, K. G.: Approaches and tools to manipulate the carbonate chemistry, in: Guide to best practices for ocean acidification research and data reporting, edited by: Riebesell, U., Fabry, V. J., Hansson, L., and Gattuso, J.-P., Publications office of the European Union, Luxembourg, 41–52, 2010.

Häder, D. P., Helbling, E. W., Williamson, C. E., and Worrest, R. C.: Effects of UV radiation on aquatic ecosystems and interactions with climate change, Photochem. Photobiol. Sci., 10, 242–260, 2011.

He, Y. and Häder, D. P.: Reactive oxygen species and UV-B: effects on cyanobacteria, Photochem. Photobio. S., 1, 729–736, 2002.

Helbling, E. W., Villafañe, V. E., Ferrario, M. E., and Holm-Hansen, O.: Impact of natural ultraviolet radiation on rates of photosynthesis and on specific marine phytoplankton species, Mar. Ecol.-Prog. Ser., 80, 89–100, 1992.

Herfort, L., Thake, B., and Roberts, R. J.: Acquisition and use of bicarbonate by Emiliania huxleyi, New Phytol., 156, 427–436, 2002.

Herfort, L., Loste, E., Meldrum, F., and Thake, B.: Structural and physiological effects of calcium and magnesium in Emiliania huxleyi (Lohmann) Hay and Mohler, J. Struct. Biol., 148, 307–314, 2004.

Ho, T. Y., Chou, W. C., Wei, C. L., Lin, F. J., Wong, G. T. F., and Lin, H. L.: Trace metal cycling in the surface water of the South China Sea: vertical fluxes, composition, and sources, Limnol. Oceanogr., 55, 1807–1820, 2010.

Iglesias-Rodriguez, M. D., Halloran, P. R., Rickaby, R. E. M., Hall, I. R., Colmenero-Hidalgo, E., Gittins, J. R., Green, D. R. H., Tyrrell, T., Gibbs, S. J., von Dassow, P., Rehm, E., Armbrust, E. V., and Boessenkool, K. P.: Phytoplankton calcification in a high-CO2 world, Science, 320, 336–340, 2008.

Leonardos, N., Read, B., Thake, B., and Young, J. R.: No mechanistic dependence of photosynthesis on calcification in the coccolithophorid Emiliania huxleyi (Haptophyta), J. Phycol., 45, 1046–1051, 2009.

Lewis, E. and Wallace, D. W. R.: Program Developed for CO2 System Calculations, ORNL/CDIAC-105, Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, Tennessee, 1998.

Li, G., Gao, K., and Gao, G.: Differential impacts of solar UV radiation on photosynthetic carbon fixation from the coastal to offshore surface waters in South China Sea, Photochem. Photobiol., 87, 329–334, 2011.

Mehrbach, C., Culberson, C. H., Hawley, J. E., and Pytkowicz, R. N.: Measurement of the appearent dissociation constants of carbonic acid in seawater at atmospheric pressure, Limnol. Oceanogr., 18, 897–907, 1973.

Mikaelyan, A. S., Pautova, L. A., Pogosyan, S. I., and Sukhanova, I. N.: Summer bloom of coccolithophorids in the northeastern Black Sea, Oceanology, 45 (Suppl. 1), S127–S138, 2005.

Milliman, J. D.: Production and accumulation of calcium carbonate in the ocean: Budget of a nonsteady state, Global Biogeochem. Cy., 7, 927–957, 1993.

Neale, P. J. and Kieber, D. J.: Assessing biological and chemical effects of UV in the marine environment: spectral weighting functions, in: Causes and Environmental Implications of Increased UV-B Radiation, edited by: Hester, R. E. and Harrison, R. M., The Royal Society of Chemistry, Cambridge, 61–83, 2000.

Nanninga, H. J. and Tyrrell, T.: Importance of light for the formation of algal blooms by Emiliania huxleyi, Mar. Ecol.-Progr. Ser., 136, 195–203, 1996.

Nimer, N. A., Merrett, M. J., and Brownlee, C.: Inorganic carbon transport in relation to culture age and inorganic carbon concentration in a high calcifying strain of Emiliania huxleyi, J. Phycol., 32, 813–818, 1996.

Paasche, E.: Action spectrum of coccolith formation, Physiol. Plant., 19, 770–779, 1966.

Paasche, E.: A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae), with particular reference to growth, coccolith formation, and calcification photosynthesis interactions, Phycologia, 40, 503–529, 2002.

Pitsyk, G. K.: O kachestvennom sostave fytoplanktona Azovkogo moray (On the qualitiative compostion of phytoplankton in the Sea of Azov), Sevastopol' Biol. Sta. Trudy, 16, 71–89, 1963.

Porra, R. J.: The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b, Photosynth. Res., 73, 149–156, 2002.

Price, N. M., Harrison, G. I., Hering, J. G., Hudson, R. J., Nirel, P. M. V., Palenik, B., and Morel, F. M. M.: Preparation and chemistry of the artificial algal culture medium Aquil, Biol. Oceanogr., 6, 443–461, 1988/89.

Riebesell, U., Zondervan, I., Rost, B., Tortell, P. D., Zeebe, R. E., and Morel, F. M. M.: Reduced calcification of marine plankton in response to increased atmospheric CO2, Nature, 407, 364–367, 2000.

Rost, B. and Riebesell, U.: Coccolithophores and the biological pump: responses to environmental changes, in: Coccolithophores: From Molecular Biology to Global Impact, edited by: Thierstein, H. R. and Young, J. R., Springer, Berlin, Germany, 76–99, 2004.

Shaked, Y., Xu, Y., Leblanc, K., and Morel, F. M. M.: Zinc availability and alkaline phosphatase activity in Emiliania huxleyi: implications for Zn-P co-limitation in the ocean, Limnol. Oceanogr., 51, 299–309, 2006.

Shiraiwa, Y.: Physiological regulation of carbon fixation in the photosynthesis and calcification of coccolithophorids, Comp. Biochem. Phys. B., 136, 775–783, 2003.

Sikes, C. S. and Wilbur, K. M.: Function of coccolith formation, Limnol. Oceanogr., 27, 18–26, 1982.

Sikes, C. S., Roer, R. D., and Wilbur, K. M.: Photosynthesis and coccolith formation: inorganic carbon sources and net inorganic reaction of deposition, Limnol. Oceanogr., 25, 248–261, 1980.

Strickland, J. D. H. and Parsons, T. R.: A practical handbook of seawater analysis, B. Fish. Res. Board Can., 167, 49–80, 1972.

Trimborn, S., Langer, G., and Rost, B.: Effect of varying calcium concentrations and light intensities on calcification and photosynthesis in Emiliania huxleyi, Limnol. Oceanogr., 52, 2285–2293, 2007.

Van de Poll, H. W. and Buma, A. G. J.: Does ultraviolet radiation affect the xanthophyll cycle in marine phytoplankton?, Photochem. Photobio. S., 8, 1295–1301, 2009.

Villafañe, V. E., Sundbäck, K., Figueroa, F. L., and Helbling, E. W.: Photosynthesis in the aquatic environment as affected by UVR, in: UV Effects in Aquatic Organisms and Ecosystems, edited by: Helbling, E. W. and Zagarese, H. E., The Royal Society of Chemistry, Cambridge, 357–397, 2003.

Zondervan, I.: The effects of light, macronutrients, trace metals and CO2 on the production of calcium carbonate and organic carbon in coccolithophores – A review, Deep-Sea Res. Pt. II, 54, 521–537, 2007.