Enhanced calcification ameliorates the negative effects of UV radiation on photosynthesis in the calcifying phytoplankter Emiliania huxleyi
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Abstract
The calcifying phytoplankton species, coccolithophores, have their calcified coccoliths around the cells, however, their physiological roles are still unknown. Here, we hypothesized that the coccoliths may play a certain role in reducing solar UV radiation (UVR, 280–400 nm) and protect the cells from being harmed. Cells of Emiliania huxleyi with different thicknesses of the coccoliths were obtained by culturing them at different levels of dissolved inorganic carbon and their photophysiological responses to UVR were investigated. Although increased dissolved inorganic carbon decreased the specific growth rate, the increased coccolith thickness significantly ameliorated the photoinhibition of PSII photochemical efficiency caused by UVR. Increase by 91% in the coccolith thickness led to 35% increase of the PSII yield and 22% decrease of the photoinhibition of the effective quantum yield (ΦPSII) by UVR. The coccolith cover reduced more UVA (320–400 nm) than UVB (280–315 nm), leading to less inhibition per energy at the UV-A band.
Keywords
BWF coccolith dissolved inorganic carbon Emiliania huxleyi photochemical efficiency UVRPreview
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References
- 1.Sabine C L, Feely R A, Gruber N, et al. The oceanic sink for anthropogenic CO2. Science, 2004, 305: 367–371CrossRefGoogle Scholar
- 2.Feely R A, Sabine C L, Lee K, et al. Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science, 2004, 305: 362–366CrossRefGoogle Scholar
- 3.Brewer P G. Ocean chemistry of the fossil fuel CO2 signal: the haline signal of “business as usual”. Geophys Res Lett, 1997, 24: 1367–1369CrossRefGoogle Scholar
- 4.Caldeira K, Wickett M E, Anthropogenic carbon and ocean pH. Nature, 2003, 425: 365CrossRefGoogle Scholar
- 5.Gao K S, Aruga Y, Asada K, et al. Calcification in the articulated coralline alga Corallina pilulifera, with special reference to the effect of elevated CO2 concentration. Mar Biol, 1993, 117: 129–132CrossRefGoogle Scholar
- 6.Riebesell U, Zondervan I, Rost B, et al. Reeeuced calcification of marine plankton in response to increased atmospheric CO2. Nature, 2000, 407: 364–367CrossRefGoogle Scholar
- 7.Paasche E. A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae), with particular reference to growth coccolith formation, and calcification-photosynthesis interactions. Phycologia, 2001, 40: 503–529Google Scholar
- 8.Holligan P M, Fernandez E, Aiken J, et al. A biogeochemical study of the coccolithophore, Emiliania huxleyi, in the North Atlantic. Glob Biogeochem Cycl, 1993, 7: 879–900CrossRefGoogle Scholar
- 9.Nielsen M V. Growth, dark respiration and photosynthetic parameters of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae) acclimated to different day length-irradiance combinations. J Phycol, 1997, 33: 818–822CrossRefGoogle Scholar
- 10.Nanninga H J, Tyrell T. Importance of light for the formation of algal blooms by Emiliania huxleyi. Mar Ecol Prog Ser, 1996, 136: 195–203CrossRefGoogle Scholar
- 11.Harris G N, Scanlan J S, Geider R J. Acclimation of Emiliania huxleyi (Prymnesiophyceae) to photon flux density. J Phycol, 2005, 41: 851–862CrossRefGoogle Scholar
- 12.Trimborn S, Langer G, Rost B. Effect of varying calcium concentrations and light intensities on calcification and photosynthesis in Emiliania huxleyi. Limnol Oceanogr, 2007, 52: 2285–2293Google Scholar
- 13.Häder D P, Kumar H D, Smith R C, et al. Effect of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochem Photobiol, 2007, 6: 267–285CrossRefGoogle Scholar
- 14.Weatherhead E C, Andersen S B. The search of the signs of recovery of ozone layer. Nature, 2006, 441: 39–45CrossRefGoogle Scholar
- 15.Boelen P, De-Boer M K, Kraay G W, et al. UVBR-induced DNA damage in natural marine picoplankton assemblages in the tropical Atlantic Ocean. Mar Ecol Prog Ser, 2000, 193: 1–9CrossRefGoogle Scholar
- 16.Xiong F S. Evidence that UV-B tolerance of the photosynthetic apparatus in microalgae is related to the D1-turnover mediated repair cycle in vivo. J Plant Physiol, 2001, 158: 285–294CrossRefGoogle Scholar
- 17.Wu H Y, Gao K S, Villafañe V E, et al. Effects of solar UV radiation on morphology and photosynthesis of filamentous cyanobacterium Arthrospira platensis. Appl Environ Microb, 2005, 71: 5004–5013CrossRefGoogle Scholar
- 18.Guan W C, Gao K S. Light histories influence the impacts of solar ultraviolet radiation on photosynthesis and growth in a marine diatom, Skeletonema costatum. J Photochem Photobiol B Biol, 2008, 91: 151–156CrossRefGoogle Scholar
- 19.Behrenfeld M J, Hardy J T, Lee H II. Ultraviolet-B radiation effects on inorganic nitrogen uptake by natural assemblages of oceanic phytoplankton. J Phycol, 1995, 31: 25–36CrossRefGoogle Scholar
- 20.Buma A G J, van Oijen T. van de Poll W. The sensitivity of Emiliania huxleyi (Prymnesiophyceae) to ultraviolet-B radiation. J Phycol, 2000, 36: 296–303CrossRefGoogle Scholar
- 21.Van Rijssel M, Buma A G J. UV radiation induced stress does not affect DMSP synthesis in the marine prymnesiophyte Emiliania huxleyi. Aquat Microb Ecol, 2002, 28: 167–174CrossRefGoogle Scholar
- 22.Guan W C, Gao K S. Impacts of UV radiation on photosynthesis and growth of the coccolithophore Emiliania huxleyi (Haptophyceae). Environ Exp Bot, 2010, 67: 502–508CrossRefGoogle Scholar
- 23.Keller M D, Selvin R C, Claus W, et al. Media for the culture of oceanic ultraplankton. J Phycol, 1987, 23: 633–638CrossRefGoogle Scholar
- 24.Takano H, Takei R, Manabe E, et al. Increased coccolith production by Emiliania huxleyi cultures enriched with dissolved inorganic carbon. Appl Microbiol Biotechnol, 1995, 43: 460–465CrossRefGoogle Scholar
- 25.Raven J A, Johnston A M. Mechanisms of inorganic carbon acquisition inmarine phytoplankton and their implications for the use of other resources. Limnol Oceanogr, 1991, 36: 1701–1714Google Scholar
- 26.Nimer N A, Merrett M J. Calcification and utilization of inorganic carbon by the coccolithophorid Emiliania huxleyi Lohmann. New Phytol, 1992, 121: 173–177CrossRefGoogle Scholar
- 27.Häder D P, Lebert M, Marangoni R, et al. ELDONET - European light dosimeter network hardware and software. J Photochem Photobiol B Biol, 1999, 52: 51–58CrossRefGoogle Scholar
- 28.Korbee-Peinado N, Abdala-DÍaz R T, Figueroa F L, et al. Ammonium and UV radiation stimulate the accumulation of mycosporine-like amino acids in Porphyra columbina (Rhodophyta) from patagonia, argentina. J Phycol, 2004, 40: 248–259CrossRefGoogle Scholar
- 29.Zheng Y Q, Gao K S. Impacts of solar UV radiation on the photosynthesis, growth, and UV-absorbing compounds in Gracilaria lemaneiformis (Rhodophyta) grown at different nitrate concentrations J Phycol, 2009, 45: 314–323CrossRefGoogle Scholar
- 30.Steeman N E. The use of radio-active carbon (C14) for measuring organic production in the sea. J Cons Perm Int Explor Mer, 1952, 18: 117–140Google Scholar
- 31.Villafañe V E, Sundbäck K, Figueroa F L, et al. Photosynthesis in the aquatic environment as affected by UVR. In: Helbling E W, Zagarese H E, eds. UV Effects in Aquatic Organisms and Ecosystems. Cambridge: The Royal Society of Chemistry, 2003. 357–397CrossRefGoogle Scholar
- 32.Neale P J, Kieber D J. Assessing biological and chemical effects of UV in the marine environment: Spectral weighting functions. In: Hester R E, Harrison R M, eds. Causes and Environmental Implications of Increased UV-B radiation. Cambridge: The Royal Society of Chemistry, 2000. 61–83CrossRefGoogle Scholar
- 33.Ruggaber A, Dlugi R, Nakajima T. Modelling of radiation quantities and photolysis frequencies in the troposphere. J Atmos Chem, 1994, 18: 171–210CrossRefGoogle Scholar
- 34.Genty B E, Briantais J M, Baker N R. Relative quantum efficiencies of the two photosystems of leaves in photorespiratory and non-photorespiratory conditions. Plant Physiol Biochem, 1989, 28: 1–10Google Scholar
- 35.Gao K S, Ruan Z X, Villafañce V E, et al. Ocean acidification exacerbates the effect of UV radiation on the calcifiying phytoplankter Emiliania huxleyi. Limnol Oceanogr, 2009, 54: 1855–1962Google Scholar
- 36.Gieskes W W C, Buma A G J. UV damage to plant life in a photobiologically dynamic environment: the case of marine phytoplankton. Plant Ecol, 1997, 128: 17–25CrossRefGoogle Scholar
- 37.Garde K, Caroline C. The impact of UV-B radiation and different PAR intensities on growth, uptake of 14C, excretion of DOC, cell volume, and pigmentation in the marine prymnesiophyte, Emiliania huxleyi. J Exp Mar Biol Ecol, 2000, 247: 99–112CrossRefGoogle Scholar
- 38.Suggett D, Le Floc H E, Harris G N, et al. Different strategies of photoacclimation by two strains of Emiliania huxleyi (Haptophyta). J Phycol, 2007, 43: 1209–1222CrossRefGoogle Scholar
- 39.Balch W M, Holligan P M, Ackleson S G, et al. Biological and optical properties of mesoscale coccolithophore blooms in the Gulf of Maine. Limnol. Oceanogr, 1991, 36: 629–643CrossRefGoogle Scholar
- 40.Ziveri P, Thunell R C. Coccolithophore export production in Guaymas Basin, Gulf of California: response to climate forcing. Deep-Sea Res II, 2000, 47: 2073–2100CrossRefGoogle Scholar
- 41.Tyrrell T, Taylor A H. A modelling study of Emiliania huxleyi in the NE Atlantic. J Mar Syst, 1996, 9: 83–112CrossRefGoogle Scholar
- 42.Robertson J E, Robinson C, Turner D R, et al. The impact of a coccolithophore bloom on oceanic carbon uptake in the northeast Atlantic during summer 1991. Deep-Sea Res, 1994, 41: 297–314CrossRefGoogle Scholar
- 43.Boelen P, Obernosterer I, Vink A A, et al. Atenuation of biologically effective UV radiation in tropical Atlantic waters measured with a biochemical DNA dosimeter. Photochem Photobiol, 1999, 69: 34–40CrossRefGoogle Scholar
- 44.Smith R C, Prezelin B B, Baker K S, et al. Ozone depletion: ultraviolet radiation and phytoplankton biology in Antarctic waters. Science, 1992, 255: 952–959CrossRefGoogle Scholar
- 45.Gieskes W W C, Karry G W. Transmission of ultraviolet light in the Weddell Sea: report on the first measurements made in Antarctic. Biomass Newsl, 1990, 12: 12–14Google Scholar