Photochemical & Photobiological Sciences

Korean Society of Photoscience (한국광과학회)
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Interactions between the impacts of ultraviolet radiation, elevated $CO_2$, and nutrient limitation on marine primary producers

  • Received : 2009.05.19
  • Accepted : 2009.07.02
  • Published : 2009.09.01
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Abstract

It is well known that UV radiation can cause deleterious effects to the physiological performance, growth and species assemblages of marine primary producers. In this review we describe the range of interactions observed between these impacts of ultraviolet radiation (UVR, 280-400 nm) with other environmental factors such as the availability of photosynthetically active radiation (PAR), nutrient status and levels of dissolved $CO_2$, all of which can, in turn, be influenced by global climate change. Thus, increases in $CO_2$ levels can affect the sensitivity of some species to UV-B radiation (UV-B), while others show no such impact on UV-B susceptibility. Both nitrogen- and phosphorus-limitation can have direct interactive effects on the susceptibility of algal cells and communities to UVR, though such effects are somewhat variable. Nutrient depletion can also potentially lead to a dominance of smaller celled species, which may be less able to screen out and are thus likely to be more susceptible to UVR-induced damage. The variability of responses to such interactions can lead to alterations in the species composition of algal assemblages.

Keywords

References

  1. J. A. Raven and P. G. Falkowski, Oceanic sinks for atmospheric $CO_2$, Plant, Cell Environ., 1999, 22, 741-755. https://doi.org/10.1046/j.1365-3040.1999.00419.x
  2. M. J. Behrenfeld, R. T. O'Malley, D. A. Siegel, C. R. McClain, J. L. Sarmiento, G. C. Feldman, A. J. Milligan, P. G. Falkowski, R. M. Letelier and E. S. Boss, Climate-driven trends in contemporary ocean productivity, Nature, 2006, 444, 752-755. https://doi.org/10.1038/nature05317
  3. S. Doney, The dangers of ocean acidification, Sci. Am., 2006, 294, 58-65. https://doi.org/10.1038/scientificamerican0306-58
  4. D.-P. Hader, H. D. Kumar, R. C. Smith and R. C. Worrest, Effects of solarUV radiation on aquatic ecosystems and interactions with climate change, Photochem. Photobiol. Sci., 2007, 6, 267-285. https://doi.org/10.1039/b700020k
  5. J. Beardall and J. A. Raven, The potential effects of global climate change on microalgal photosynthesis, growth and ecology, Phycologia, 2004, 43, 26-40. https://doi.org/10.2216/i0031-8884-43-1-26.1
  6. J. Beardall and S. Stojkovic, Microalgae under global environmental change: implications for growth and productivity, populations and trophic flow, Science Asia, 2006, 32(s1), 1-10.
  7. J. W. Harrison and R. E. H. Smith, Effects of ultraviolet radiation on the productivity and composition of freshwater phytoplankton communities, Photochem. Photobiol. Sci., 2009, DOI: 10.1039/b902604e.
  8. S. Burkhardt and U. Riebesell, $CO_2$ availability affects elemental composition (C:N:P) of themarine diatom Skeletonema costatum, Mar. Ecol. Prog. Ser., 1997, 155, 67-76.
  9. S. Burkhardt, I. Zondervan I and U. Riebesell, Effect of $CO_2$ concentration on C:N:P ratio inmarine phytoplankton: a species comparison, Limnol. Oceanogr., 1999, 44, 683-90. https://doi.org/10.4319/lo.1999.44.3.0683
  10. U. Riebesell, U, A. T. Revill, D. G. Holfsworth and J. K. Volkman, The effect of varying $CO_2$ concentration on lipid composition and carbon isotope fractionation in Emiliania huxleyi, Geochim. Cosmochim. Acta, 2000, 64, 4179-92. https://doi.org/10.1016/S0016-7037(00)00474-9
  11. K. A. Hughen, J. T. Overpeck, L. C. Peterson and S. Trumbore, Rapid climate changes in the tropical Atlantic region during the last deglaciation, Nature, 1996, 380, 51-54. https://doi.org/10.1038/380051a0
  12. D. L. Hartmann DL, J. M. Wallace JM, V. Limpasuvan, V, D. W. J. Thompson and J. R. Holton, Can ozone depletion and global warming interact to produce rapid climate change-, Proc. Natl. Acad. Sci. U. S. A., 2000, 97, 1412-1417. https://doi.org/10.1073/pnas.97.4.1412
  13. W. F. Vincent and S. Roy, Solar ultraviolet-B radiation and aquatic primary production: damage, protection, and recovery, Environ. Rev., 1993, 1, 1-12. https://doi.org/10.1139/a93-001
  14. M. J. Behrenfeld, D. R. S. Lean and H. Lee, Ultraviolet-B radiation effects on inorganic nitrogen uptake by natural assemblages of oceanic plankton, J. Phycol., 1995, 31, 25-36. https://doi.org/10.1111/j.0022-3646.1995.00025.x
  15. D. O. Hessen, E. Van Donk and T. Anderson, Growth responses, P-uptake and loss of flagella in Chlamydomonas reinhardtii exposed to UVB, J. Plankton Res., 1995, 17, 17-27. https://doi.org/10.1093/plankt/17.1.17
  16. D. Karentz, J. E. Cleaver and D. L. Mitchell, Cell survival characteristics and molecular responses of Antarctic phytoplankton to ultraviolet-B radiation, J. Phycol., 1991, 27, 326-341. https://doi.org/10.1111/j.0022-3646.1991.00326.x
  17. W. W. C. Gieskes and A. G. J. Buma, UV damage to plant life in a photobiologically dynamic environment: the case of marine phytoplankton, Plant Ecol., 1997, 128, 17-25. https://doi.org/10.1023/A:1009750621449
  18. A. G. J. Buma, T. van Oijen, W. van de Poll, M. J. W. Veldhuis and W. W. L. Gieskes, The sensitivity of Emiliania huxleyi (Prymnesiophyceae) to ultraviolet-B radiation, J. Phycol., 2000, 36, 296-303.
  19. A. G. J. Buma, E. W. Helbling, M. K. de Boer and V. E. Villafane, Patterns of DNA damage and photoinhibition in temperate South-Atlantic picophytoplankton exposed to solar ultraviolet radiation, J. Photochem. Photobiol., B, 2001, 62, 9-18. https://doi.org/10.1016/S1011-1344(01)00156-7
  20. E. W. Helbling, A. G. J. Buma, M. K. de Boer and V. E. Villafane, In situ impact of solar ultraviolet radiation on photosynthesis and DNA in temperate marine phytoplankton, Mar. Ecol. Prog. Ser., 2001, 211, 43-49.
  21. UV Effects in Aquatic Organisms and Ecosystems, ed. H. Helbling and H. Zagarese, Royal Society of Chemistry, Cambridge 2003.
  22. W. F. Vincent and P. J. Neale, Mechanisms of UV damage to aquatic organisms, in The effects of UV radiation in the marine environment, ed. S. de Mora, S. Demers and M. Vernet, Cambridge University Press, Cambridge, 2000, pp. 149-176.
  23. M. P. Lesser, J. J. Cullen, JJ and P. J. Neale, Carbon uptake in a marine diatom during acute exposure to ultraviolet B radiation: Relative importance of damage and repair, J. Phycol., 1994, 30, 183-192. https://doi.org/10.1111/j.0022-3646.1994.00183.x
  24. P. J. Neale, Spectral weighting functions for quantifying the effects of ultraviolet radiation in marine ecosystems, in Effects of UV Radiation on the Marine Environment, ed. S. J. De Mora, S. Demers and M. Vernet, Cambridge University Press, Cambridge, 2000, pp. 73-100.
  25. P. Heraud, P. J. Beardall and J. Changes, in chlorophyll fluorescence during exposure of Dunaliella tertiolecta to ultraviolet radiation exposure indicate a dynamic interaction between damage and repair processes, Photosynth. Res., 2000, 63, 123-134. https://doi.org/10.1023/A:1006319802047
  26. J. Rozema, L. O. Bjorn, J. F. Bornman, A. Gaberscik, D.-P. Hader, T. Trost, M. Gserm, M. Klish, A. Groniger, R. P. Sinha, M. Lebert, Y. Y. He, R. Buffoni-Hall, N. V. J. de Bakker, J. van de Staaij and B. B. Meijkamp, The role of UVB radiation in aquatic and terrestrial ecosystems-an experimental and functional analysis of the evolution of UV-absorbing compounds, J. Photochem. Photobiol., B, 2002, 66, 2-12. https://doi.org/10.1016/S1011-1344(01)00269-X
  27. W. H. Van de Poll, P. J. Janknegt, M. A. van Leeuwe, R. J. W. Visser and A. G. J. Buma, Excessive irradiance and antioxidant responses of an Antarctic marine diatom exposed to iron limitation and to dynamic irradiance, J. Photochem. Photobiol., B, 2009, 94, 32-37. https://doi.org/10.1016/j.jphotobiol.2008.09.003
  28. J. Beardall, S. Roberts and E. Young, Approaches for determining phytoplankton nutrient limitation, Aquat. Sci., 2001, 63, 44-69. https://doi.org/10.1007/PL00001344
  29. J. Beardall, A. Allen, J. Bragg, Z. V. Finkel, K. J. Flynn, A. Quigg, T. A. V. Rees, A. J. Richardson and J. A. Raven, Allometry and stoichiometry of unicellular, colonial andmulticellular phytoplankton, New Phytol., 2009, 181, 295-309. https://doi.org/10.1111/j.1469-8137.2008.02660.x
  30. F. Garcia-Pichell, A model for internal self-shading in planktonic organisms and its implications for the usefulness of ultraviolet sunscreens, Limnol. Oceanogr., 1994, 39, 1704-1717. https://doi.org/10.4319/lo.1994.39.7.1704
  31. J. A. Raven, Responses of aquatic photosynthetic organisms to increased solar UVB, J. Photochem. Photobiol., B, 1991, 9, 239-244. https://doi.org/10.1016/1011-1344(91)80158-E
  32. R. Sommaruga, Y. Chen and Z. Liu, Multiple strategies of bloomforming Microcystis to minimize damage by solar ultraviolet radiation in surface waters, Microb. Ecol., 2009, 57, 667-674. https://doi.org/10.1007/s00248-008-9425-4
  33. J. A. Raven, Small is beautiful. The picophytoplankton, Funct. Ecol., 1998, 12, 503-513. https://doi.org/10.1046/j.1365-2435.1998.00233.x
  34. L. Bopp, O. Aumont, P. Cadule, S. Alvain and M. Gehlen, Response of diatoms distribution to global warming and potential implications: A global model study, Geophys. Res. Lett., 2005, 32, L19606.
  35. A. Bakun, Global climate change and intensification of coastal ocean upwelling, Science, 1990, 247, 198-201. https://doi.org/10.1126/science.247.4939.198
  36. T. Takahashi, S. C. Sutherland, C. Sweeney, A. Poisson, N. Metzl, B. Tilbrook, N. Bates, R.Wanninkhof, R. A. Feely, C. Sabine, J. Olafsson and Y. C. Nojiri, Global sea-air $CO_2$ flux based on climatological surface ocean $pCO_2$, and seasonal biological and temperature effects, Deep-Sea Res., Part II, 2002, 49, 1601-1622. https://doi.org/10.1016/S0967-0645(02)00003-6
  37. J. B. Reiskind, S. Beer and G. Bowes, Photosynthesis, photorespiration and ecophysiological interactions in marine macroalgae, Aquat. Bot., 1989, 34, 131-152. https://doi.org/10.1016/0304-3770(89)90053-3
  38. R. G. Zepp, D. J. Erickson, III, N. D. Paul and B. Sulzberger, Interactive effects of solar UV radiation and climate change on biogeochemical cycling, Photochem. Photobiol. Sci., 2007, 6, 286-300. https://doi.org/10.1039/b700021a
  39. C. Sobrino, M. L. Ward and P. J. Neale, Acclimation to elevated $CO_2$ and ultraviolet radiation in the diatom Thalassiosira pseudonana: Effects on growth, photosynthesis and spectral sensitivity of photoinhibition, Limnol. Oceanogr., 2008, 53, 494-505. https://doi.org/10.4319/lo.2008.53.2.0494
  40. C. Sobrino, P. J. Neale and L. M. Lubian, Interaction of UV radiation and inorganic carbon supply in the inhibition of photosynthesis: Spectral and temporal responses of two marine picoplankters, Photochem. Photobiol., 2005, 81, 384-393. https://doi.org/10.1562/2004-08-27-RA-295.1
  41. J. Beardall, P. Heraud, S. Roberts, K. Shelly and S. Stojkovic, Effects of UVB radiation on inorganic carbon acquisition by the marine microalga Dunaliella tertiolecta (Chlorophyceae), Phycologia, 2002, 41, 268-272. https://doi.org/10.2216/i0031-8884-41-3-268.1
  42. M. Giordano, J. Beardall and J. A. Raven, $CO_2$ concentrating mechanisms in algae: mechanisms, environmental modulation and evolution, Annu. Rev. Plant Biol., 2005, 56, 99-131. https://doi.org/10.1146/annurev.arplant.56.032604.144052
  43. J. Beardall and M. Giordano, Ecological implications of microalgal and cyanobacterial CCMs and their regulation, Funct. Plant Biol., 2002, 29, 335-347. https://doi.org/10.1071/PP01195
  44. P. D. Tortell, G. H. Rau and F. M. M. Morel, Inorganic carbon acquisition in coastal Pacific phytoplankton communities, Limnol. Oceanogr., 2000, 45, 1485-1500. https://doi.org/10.4319/lo.2000.45.7.1485
  45. P. D. Tortell and F. M. M. Morel, Sources of inorganic carbon for phytoplankton in the eastern Subtropical and Equatorial Pacific Ocean, Limnol. Oceanogr, 2002, 47, 1012-1022. https://doi.org/10.4319/lo.2002.47.4.1012
  46. J. Beardall and J. A. Raven, The potential effects of global climate change on microalgal photosynthesis, growth and ecology, Phycologia, 204, 26-40.
  47. J. A. Raven, Physiology of inorganic C acquisition and implications for resource use efficiency by marine phytoplankton: Relation to increased $CO_2$ and temperature, Plant, Cell Environ., 1991, 14, 779-794. https://doi.org/10.1111/j.1365-3040.1991.tb01442.x
  48. J. E. Kubler, A. M. Johnston and J. A. Raven, The effects of reduced and elevated $CO_2$ and $O_2$ on the seaweed Lomentaria articulata, Plant, Cell Environ., 1999, 22, 1303-1310. https://doi.org/10.1046/j.1365-3040.1999.00492.x
  49. J. M. Mercado, F. J. L. Gordillo, F. L. Figueroa and F. X. Niell, External carbonic anhydrase and affinity for inorganic carbon in intertidal macroalgae, J. Exp. Mar. Biol. Ecol., 1998, 221, 209-220. https://doi.org/10.1016/S0022-0981(97)00127-5
  50. A. Israel and M. Hophy, Growth, photosynthetic properties and RUBISCO activies and amounts of marine macroalgae grown under current and elevated seawater $CO_2$ concentrations, Global Change Biol., 2002, 8, 831-840. https://doi.org/10.1046/j.1365-2486.2002.00518.x
  51. S. Collins, D. Sultemeyer and G. Bell, Changes in C uptake in populations of Chlamydomonas reinhardtii selected at high $CO_2$, Plant, Cell Environ., 2006, 29, 1812-1819. https://doi.org/10.1111/j.1365-3040.2006.01559.x
  52. P. J. Neale, R. F. Davis and J. J. Cullen, Interactive effects of ozone depletion and vertical mixing on photosynthesis of Antarctic phytoplankton, Nature, 1998, 392, 585-589. https://doi.org/10.1038/33374
  53. A. T. Banaszak and P. J. Neale, UV sensitivity of photosynthesis in phytoplankton from an estuarine environment, Limnol. Oceanogr., 2001, 46, 592-600. https://doi.org/10.4319/lo.2001.46.3.0592
  54. P. J. Neale, E. Litchman, C. Sobrino, C. Callieri, G. Morabito, V. Montecino, Y. Huot, P. Bossard, C. Lehmann and D. Steiner, Quantifying the response of phytoplankton photosynthesis to ultraviolet radiation: biological weighting functions versus in situ measurements in two Swiss lakes, Aquat. Sci., 2001, 63, 265-285. https://doi.org/10.1007/PL00001354
  55. K. Gao, Y. Wu, G. Li, H. Wu, V. E. Villafane and E. W. Helbling, Solar UV Radiation Drives $CO_2$ Fixation in Marine Phytoplankton: A Double-Edged Sword, Plant Physiol., 2007, 144, 54-59. https://doi.org/10.1104/pp.107.098491
  56. J. A. Raven, Putting the C in Phycology, Eur. J. Phycol., 1997, 32, 319-333. https://doi.org/10.1080/09670269710001737259
  57. M. R. Badger, T. J. Andrews, S. M. Whitney, M. Ludwig, D. C. Yellowlees, W. Leggat and G. D. Price, The diversity and co-evolution of Rubisco, plastids, pyrenoids and chloroplast-based CCMs in the algae, Can. J. Bot., 1998, 76, 1052-1071.
  58. J. Beardall, A. M. Johnston and J. A. Raven, Environmental regulation of the $CO_2$ concentrating mechanism in cyanobacteria and microalgae, Can. J. Bot., 1998, 76, 1010-1017.
  59. J. Beardall and J. A. Raven, Transport of inorganic carbon and the "$CO_2$ concentrating mechanism" in Chlorella emersonii (Chlorophyceae), J. Phycol., 1981, 17, 134-141. https://doi.org/10.1111/j.1529-8817.1981.tb00832.x
  60. K. Palmqvist, L.-G. Sundblad, G. Wingsle and G. Samuelsson, Acclimation of photosynthetic light reactions during induction of inorganic carbon accumulation in the green alga Chlamydomonas reinhardtii, Plant Physiol., 1990, 94, 357-366. https://doi.org/10.1104/pp.94.1.357
  61. J. H. A. Nugent, S. Purton and M. C. W. Evans, Oxygenic photosynthesis in algae and cyanobacteria: electron transfer in photosystems I and II, Adv. Photosynth. Respir., 2003, 14, 133-156.
  62. Y. Song and B. Qiu, The $CO_2$-concentrating mechanism in the bloomforming cyanobacterium Microcystis aeruginosa (Cyanophyceae) and effects of UVB radiation on its operation, J. Phycol., 2007, 43, 957-964. https://doi.org/10.1111/j.1529-8817.2007.00391.x
  63. H. Wu and K. Gao, Ultraviolet radiation stimulated activity of extracellular carbonic anhydrase in the marine diatom Skeletonema costatum, Funct. Plant Biol., 2009, 36, 137-143. https://doi.org/10.1071/FP08172
  64. C. Sobrino, P. J. Neale, J. D. Phillips-Kress, R. E. Moeller and J. A. Porter, Elevated $CO_2$ increases sensitivity to ultraviolet radiation in lacustrine phytoplankton assemblages, Limnol. Oceanogr., 2009, in press.
  65. P. D. Tortell, G. H. Rau and F. M. M. Morel, Inorganic carbon acquisition in coastal Pacific phytoplankton communities, Limnol. Oceanogr., 2000, 45, 1485-1500. https://doi.org/10.4319/lo.2000.45.7.1485
  66. K. Aizawa and S. Miyachi, Carbonic anhydrase and $CO_2$ concentrating mechanisms in microalgae and cyanobacteria, FEMS Microbiol. Lett., 1986, 39, 215-233. https://doi.org/10.1111/j.1574-6968.1986.tb01860.x
  67. I. Berman-Frank, J. Erez and A. Kaplan, Changes in inorganic carbon uptake during the progression of a dinoflagellate bloom in a lake ecosystem, Can. J. Bot., 1998, 76, 1043-1051.
  68. E. Litchman, P. J. Neale and A. T. Banaszak, Increased sensitivity to ultraviolet radiation in nitrogen-limited dinoflagellates: photoprotection and repair, Limnol. Oceanogr., 2002, 47, 86-94. https://doi.org/10.4319/lo.2002.47.1.0086
  69. M. Surpin, R. M. Larkin and J. Chory, Signal Transduction between the chloroplast and the nucleus, Plant Cell, 2002, 14, 327-338.
  70. D. H. Zou, K. S. Gao and Z. X. Run, Daily, timing of emersion and elevated atmospheric $CO_2$ concentration affect photosynthetic performance of the intertidal macroalga Ulva lactuca (Chorophyta) in sunlight, Bot. Mar., 2007, 50, 275-279.
  71. K. Swanson and C. H. Fox, Altered kelp (Laminariales) phlorotannins and growth under elevated carbon dioxide and ultraviolet-B treatments can influence associated intertidal foodwebs, Global Change Biol., 2007, 13, 1696-1709. https://doi.org/10.1111/j.1365-2486.2007.01384.x
  72. V. E. Villafane, K. Sundback,F. L. Figueroa and E. W. Helbling, Photo-synthesis in the aquatic environment as affected by ultraviolet radiation, in UV effects in aquatic organisms and ecosystems, ed. E. W. Helbling and H. Zagarese, Royal Society of Chemistry, Cambridge, 2003, pp. 357-397.
  73. M. J. Behrenfeld, H. Lee and L. F. Small, Interactions between nutritional status and long-term responses of ultraviolet-B radiation stress in a marine diatom, Mar. Biol., 1994, 118, 523-530. https://doi.org/10.1007/BF00350309
  74. A. Veen, M. Reuvers and P. Roncak, Effects of acute and chronic UVB exposure on a green alga: a continuous culture study using a computer-control dynamic light regime, Plant Ecol., 1997, 128, 29-40. https://doi.org/10.1023/A:1009702705519
  75. K. Shelly, P. Heraud and J. Beardall, Nitrogen limitation in Dunaliella tertiolecta Butcher (Chlorophyceae) leads to increased susceptibility to damage by ultraviolet-B radiation but also increased repair capacity, J. Phycol., 2002, 38, 713-720. https://doi.org/10.1046/j.1529-8817.2002.01147.x
  76. K. Shelly, Interactions between UVB radiation and nutrient-limitation in a marine microalga, PhD thesis, Monash University, 2005.
  77. Y. Zheng and K. Gao, 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, 314-323. https://doi.org/10.1111/j.1529-8817.2009.00654.x
  78. J. E. Tillberg and J. R. Rowley, Physiological and structural effects of phosphorus starvation on the unicellular alga Scenedesmus, Physiol. Plant., 1989, 75, 315-332. https://doi.org/10.1111/j.1399-3054.1989.tb04633.x
  79. G. P. Harris and B. B. Piccinin, Phosphorus limitation and carbon metabolism in a unicellular alga: interaction between growth rate and the measurement of net and gross photosynthesis, J. Phycol., 1983, 19, 185-192. https://doi.org/10.1111/j.0022-3646.1983.00185.x
  80. R. J. Geider, J. La Roche, R. M. Greene and M. Olaizola, Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate or iron starvation, J. Phycol., 1993, 29, 755-766. https://doi.org/10.1111/j.0022-3646.1993.00755.x
  81. J. La Roche, R. J. Geider, L. M. Graziano, H. Murray and K. Lewis, Induction of specific proteins in eukaryotic algae grown under iron-, phosphorus- and nitrogen-deficient conditions, J. Phycol., 1993, 29, 767-777. https://doi.org/10.1111/j.0022-3646.1993.00767.x
  82. M. A. Xenopoulos and P. C. Frost, UV radiation, phosphorus, and their combined effects on the taxonomic composition of phytoplankton in boreal lake, J. Phycol., 2003, 39, 291-302. https://doi.org/10.1046/j.1529-8817.2003.02125.x
  83. M. L. Bothwell, D. Sherbot, A. C. Roberge and R. J. Daley, Influence of natural ultraviolet radiation on lotic periphytic diatom community growth, biomass accrual and species composition: short-term versus long-term effects, J. Phycol., 1993, 29, 24-35. https://doi.org/10.1111/j.1529-8817.1993.tb00276.x
  84. M. L. Bothwell, D. M. J. Sherbot and C. M. Pollock, Ecosystem responses to solar ultraviolet-B radiation: influence to trophic-level interactions, Science, 1994, 265, 97-100. https://doi.org/10.1126/science.265.5168.97
  85. L. Aubriot, D. Conde, S. Bonilla and R. Sommaruga, Phosphate uptake behavior of natural phytoplankton during exposure to solar ultraviolet radiation in a shallow coastal lagoon, Mar. Biol., 2004, 144, 623-631. https://doi.org/10.1007/s00227-003-1229-y
  86. C. D. Allen and R. E. H. Smith, The response of planktonic phosphate uptake and turnover to ultraviolet radiation in Lake Erie, Can. J. Fish. Aquat. Sci., 2002, 59, 778-786. https://doi.org/10.1139/f02-050
  87. K. Garde and K. Gustavson, The impact of UVB radiation on alkaline phosphatase activity in phosphorus-depleted marine ecosystems, J. Exp. Mar. Biol. Ecol., 1999, 238, 93-105. https://doi.org/10.1016/S0022-0981(99)00005-2
  88. M. A. Xenopoulos and D. F. Bird, Effect of acute exposure to hydrogen peroxide on the production of phytoplankton and bacterioplankton in a mesohumic lake, Photochem. Photobiol., 1997, 66, 471-478. https://doi.org/10.1111/j.1751-1097.1997.tb03175.x
  89. R. G. Wetzel, P. G. Hatcher and T. S. Bianchi, Natural photolysis by ultraviolet irradiance of recalcitrant dissolved organic matter to simple substrates for rapid bacterial metabolism, Limnol. Oceanogr., 1995, 40, 1369-1380. https://doi.org/10.4319/lo.1995.40.8.1369
  90. P. Heraud, S. Roberts, K. Shelly and J. Beardall, Interactions between UVB exposure and phosphorus nutrition. II. Effects, on rates of damage and repair, J. Phycol., 2005, 41, 1212-1218. https://doi.org/10.1111/j.1529-8817.2005.00149.x
  91. D. Pryputniewicz, L. Falkowska and D. Burska, Adenosine triphosphate in the marine boundary layer in the southern Baltic Sea., Oceanologia, 2002, 44, 461-473.
  92. S. Stojkovic, Studies on the effect of phosphorus loading of streams on the susceptibility of algal biofilms to UVB radiation, PhD Thesis, Monash University, 2005.
  93. K. Shelly, S. Roberts, P. Heraud and J. Beardall, Interactions between UVB exposure and phosphorus nutrition. I. Effects, on growth, phosphorus uptake, and chlorophyll fluorescence, J. Phycol., 2005, 41, 1204-1211. https://doi.org/10.1111/j.1529-8817.2005.00148.x
  94. M. J. Behrenfeld, A. J. Bale, Z. S. Kolber, J. Aiken and P. G. Falkowski, Confirmation of iron limitation of phytoplankton photosynthesis in the equatorial Pacific Ocean, Nature, 1996, 383, 508-511. https://doi.org/10.1038/383508a0
  95. W. H. van de Poll, M. A. van Leeuwe, J. Roggeveld and A. G. J. Buma, Nutrient limitation and high irradiance reduce PAR and UV-induced viability loss in the Antarctic diatom Chaetoceros brevis, J. Phycol., 2005, 41, 840-850. https://doi.org/10.1111/j.1529-8817.2005.00105.x
  96. R. Sommaruga, J. S. Hofer, L. Alonso-Saez and J. M. Gaso, Differential sunlight sensitivity of picophytoplankton from surface Mediterranean coastal waters, Appl. Environ. Microbiol., 2005, 71, 2154-2157. https://doi.org/10.1128/AEM.71.4.2154-2157.2005

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  1. Effects of ultraviolet radiation on the productivity and composition of freshwater phytoplankton communities vol.8, pp.9, 2009, https://doi.org/10.1039/b902604e
  2. Combined effects of solar UV radiation and CO2-induced seawater acidification on photosynthetic carbon fixation of phytoplankton assemblages in the South China Sea vol.55, pp.32, 2010, https://doi.org/10.1007/s11434-010-4119-y
  3. Effect of UV stress on the fatty acid and lipid class composition in two marine microalgae Pavlova lutheri (Pavlovophyceae) and Odontella aurita (Bacillariophyceae) vol.22, pp.5, 2010, https://doi.org/10.1007/s10811-010-9503-0
  4. Horizontal migration of Acartia pacifica Steuer (copepoda) in response to UV-radiation vol.101, pp.3, 2010, https://doi.org/10.1016/j.jphotobiol.2010.07.008
  5. Grazing Rates of Calanus finmarchicus on Thalassiosira weissflogii Cultured under Different Levels of Ultraviolet Radiation vol.6, pp.10, 2009, https://doi.org/10.1371/journal.pone.0026333
  6. Decreased calcification affects photosynthetic responses of Emiliania huxleyi exposed to UV radiation and elevated temperature vol.8, pp.1, 2011, https://doi.org/10.5194/bgd-8-857-2011
  7. Impact of biodiversity-climate futures on primary production and metabolism in a model benthic estuarine system vol.11, pp.None, 2009, https://doi.org/10.1186/1472-6785-11-7
  8. Effects of solar UV radiation and climate change on biogeochemical cycling: interactions and feedbacks vol.10, pp.2, 2009, https://doi.org/10.1039/c0pp90037k
  9. Photosynthetic responses of Emiliania huxleyi to UV radiation and elevated temperature: roles of calcified coccoliths vol.8, pp.6, 2011, https://doi.org/10.5194/bg-8-1441-2011
  10. Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change vol.109, pp.1, 2009, https://doi.org/10.1007/s11120-011-9632-6
  11. Impacts of solar UV radiation on grazing, lipids oxidation and survival of Acartia pacifica Steuer (Copepod) vol.31, pp.5, 2009, https://doi.org/10.1007/s13131-012-0230-2
  12. Dryland biological soil crust cyanobacteria show unexpected decreases in abundance under long‐term elevated CO2 vol.14, pp.12, 2009, https://doi.org/10.1111/1462-2920.12011
  13. Interactive effects of vertical mixing, nutrients and ultraviolet radiation: in situ photosynthetic responses of phytoplankton from high mountain lakes of Southern Europe vol.9, pp.7, 2009, https://doi.org/10.5194/bgd-9-9791-2012
  14. Combined effects of increased UV-B and temperature on the pigment-determined marine phytoplankton community of the St. Lawrence Estuary vol.445, pp.None, 2009, https://doi.org/10.3354/meps09484
  15. Distribution of Mycosporine-Like Amino Acids Along a Surface Water Meridional Transect of the Atlantic vol.64, pp.2, 2009, https://doi.org/10.1007/s00248-012-0038-6
  16. Ocean acidification mediates photosynthetic response to UV radiation and temperature increase in the diatom Phaeodactylum tricornutum vol.9, pp.10, 2009, https://doi.org/10.5194/bg-9-3931-2012
  17. Responses of marine primary producers to interactions between ocean acidification, solar radiation, and warming vol.470, pp.None, 2009, https://doi.org/10.3354/meps10043
  18. Global change and the future of harmful algal blooms in the ocean vol.470, pp.None, 2009, https://doi.org/10.3354/meps10047
  19. Ocean acidification mediates photosynthetic response to UV radiation and temperature increase in the diatom Phaeodactylum tricornutum vol.9, pp.6, 2012, https://doi.org/10.5194/bgd-9-7197-2012
  20. Combined effects of light and nitrate supplies on the growth, photosynthesis and ultraviolet‐absorbing compounds in marine macroalga Gracilaria lemaneiformis (Rhodophyta), with special reference vol.61, pp.2, 2009, https://doi.org/10.1111/pre.12002
  21. Impacts of nitrogen limitation on the sinking rate of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae) vol.52, pp.3, 2009, https://doi.org/10.2216/12-064.1
  22. Interactive effects of vertical mixing, nutrients and ultraviolet radiation: in situ photosynthetic responses of phytoplankton from high mountain lakes in Southern Europe vol.10, pp.2, 2013, https://doi.org/10.5194/bg-10-1037-2013
  23. Domoic Acid Improves the Competitive Ability of Pseudo-nitzschia delicatissima against the Diatom Skeletonema marinoi vol.11, pp.7, 2009, https://doi.org/10.3390/md11072398
  24. Differential effect of ultraviolet exposure (UVR) in the stress response of the Dinophycea Gymnodinium sp. and the Chlorophyta Dunaliella tertiolecta: mortality versus survival vol.160, pp.10, 2013, https://doi.org/10.1007/s00227-013-2247-z
  25. Productivity of aquatic primary producers under global climate change vol.13, pp.10, 2009, https://doi.org/10.1039/c3pp50418b
  26. Elevated CO2alleviates high PAR and UV stress in the unicellular chlorophyte Dunaliella tertiolecta vol.13, pp.9, 2014, https://doi.org/10.1039/c4pp00044g
  27. Photophysiological responses of marine diatoms to elevated CO2 and decreased pH: a review vol.41, pp.5, 2014, https://doi.org/10.1071/fp13247
  28. Effects of ultraviolet radiation and CO2 increase on winter phytoplankton assemblages in a temperate coastal lagoon vol.36, pp.3, 2009, https://doi.org/10.1093/plankt/fbt135
  29. Contribution of chemical water properties to the differential responses of bacterioneuston and bacterioplankton to ultraviolet-B radiation vol.87, pp.2, 2014, https://doi.org/10.1111/1574-6941.12239
  30. Interactive effects of nutrient supply and other environmental factors on the sensitivity of marine primary producers to ultraviolet radiation: implications for the impacts of global change vol.22, pp.None, 2009, https://doi.org/10.3354/ab00582
  31. Effect of CO2, nutrients and light on coastal plankton. I. Abiotic conditions and biological responses vol.22, pp.None, 2009, https://doi.org/10.3354/ab00587
  32. Effect of CO2, nutrients and light on coastal plankton. IV. Physiological responses vol.22, pp.None, 2009, https://doi.org/10.3354/ab00590
  33. Combined impact of ultraviolet radiation and increased nutrients supply: a test of the potential anthropogenic impacts on the benthic amphipod Amphitoe valida from Patagonian waters (Argentina) vol.2, pp.None, 2009, https://doi.org/10.3389/fenvs.2014.00032
  34. Large centric diatoms allocate more cellular nitrogen to photosynthesis to counter slower RUBISCO turnover rates vol.1, pp.None, 2014, https://doi.org/10.3389/fmars.2014.00068
  35. A red tide alga grown under ocean acidification upregulates its tolerance to lower pH by increasing its photophysiological functions vol.11, pp.17, 2009, https://doi.org/10.5194/bg-11-4829-2014
  36. Nitrate limitation and ocean acidification interact with UV-B to reduce photosynthetic performance in the diatom Phaeodactylum tricornutum vol.11, pp.12, 2009, https://doi.org/10.5194/bgd-11-17675-2014
  37. A red tide alga grown under ocean acidification up-regulates its tolerance to lower pH by increasing its photophysiological functions vol.11, pp.5, 2009, https://doi.org/10.5194/bgd-11-6303-2014
  38. Effects of solar UV radiation on photosynthetic performance of the diatom Skeletonema costatum grown under nitrate limited condition vol.29, pp.1, 2014, https://doi.org/10.4490/algae.2014.29.1.027
  39. Carbon limitation enhances CO2 concentrating mechanism but reduces trichome size in Arthrospira platensis (cyanobacterium) vol.26, pp.3, 2009, https://doi.org/10.1007/s10811-013-0181-6
  40. Faster recovery of a diatom from UV damage under ocean acidification vol.140, pp.None, 2009, https://doi.org/10.1016/j.jphotobiol.2014.08.006
  41. Solar UV Irradiances Modulate Effects of Ocean Acidification on the Coccolithophorid Emiliania huxleyi vol.91, pp.1, 2009, https://doi.org/10.1111/php.12363
  42. Impact of elevated pH on succession in the Arctic spring bloom vol.530, pp.None, 2015, https://doi.org/10.3354/meps11296
  43. Nitrate limitation and ocean acidification interact with UV-B to reduce photosynthetic performance in the diatom Phaeodactylum tricornutum vol.12, pp.8, 2009, https://doi.org/10.5194/bg-12-2383-2015
  44. Ocean acidification modulates expression of genes and physiological performance of a marine diatom vol.12, pp.18, 2015, https://doi.org/10.5194/bgd-12-15809-2015
  45. Alleviation of solar ultraviolet radiation (UVR)-induced photoinhibition in diatom Chaetoceros curvisetus by ocean acidification vol.95, pp.4, 2009, https://doi.org/10.1017/s0025315414001568
  46. Interactive Effects of Temperature and UV Radiation on Photosynthesis of Chlorella Strains from Polar, Temperate and Tropical Environments: Differential Impacts on Damage and Repair vol.10, pp.10, 2015, https://doi.org/10.1371/journal.pone.0139469
  47. Interactive Effect of UVR and Phosphorus on the Coastal Phytoplankton Community of the Western Mediterranean Sea: Unravelling Eco-Physiological Mechanisms vol.10, pp.11, 2009, https://doi.org/10.1371/journal.pone.0142987
  48. Limited phosphorus availability is the Achilles heel of tropical reef corals in a warming ocean vol.6, pp.None, 2016, https://doi.org/10.1038/srep31768
  49. Ocean warming alters photosynthetic responses of diatom Phaeodactylum tricornutum to fluctuating irradiance vol.55, pp.2, 2009, https://doi.org/10.2216/15-64.1
  50. Dependency of UVR-induced photoinhibition on atomic ratio of N to P in the dinoflagellate Karenia mikimotoi vol.164, pp.2, 2009, https://doi.org/10.1007/s00227-016-3065-x
  51. Effects of seawater acidification on the growth rates of the diatom Thalassiosira (Conticribra) weissflogii under different nutrient, light, and UV radiation regimes vol.29, pp.1, 2009, https://doi.org/10.1007/s10811-016-0944-y
  52. Atomic ratio of N to P influences the impact of UV irradiance on photosynthesis and growth in a marine dinoflagellate, Alexandrium tamarense vol.55, pp.3, 2009, https://doi.org/10.1007/s11099-016-0670-3
  53. Photosynthesis and Growth of Temperate and Sub-Tropical Estuarine Phytoplankton in a Scenario of Nutrient Enrichment under Solar Ultraviolet Radiation Exposure vol.40, pp.3, 2017, https://doi.org/10.1007/s12237-016-0176-z
  54. Differential photosynthetic responses of marine planktonic and benthic diatoms to ultraviolet radiation under various temperature regimes vol.14, pp.22, 2017, https://doi.org/10.5194/bg-14-5029-2017
  55. Ocean acidification modulates expression of genes and physiological performance of a marine diatom vol.12, pp.2, 2017, https://doi.org/10.1371/journal.pone.0170970
  56. Different physiological responses of cyanobacteria to ultraviolet‐B radiation under iron‐replete and iron‐deficient conditions: Implications for underestimating the negative effects vol.53, pp.2, 2017, https://doi.org/10.1111/jpy.12517
  57. Transcriptome sequencing of an Antarctic microalga, Chlorella sp. (Trebouxiophyceae, Chlorophyta) subjected to short-term ultraviolet radiation stress vol.30, pp.1, 2018, https://doi.org/10.1007/s10811-017-1124-4
  58. Phytoplankton as Key Mediators of the Biological Carbon Pump: Their Responses to a Changing Climate vol.10, pp.3, 2009, https://doi.org/10.3390/su10030869
  59. RNA-Seq-mediated transcriptomic analysis of heat stress response in a polar Chlorella sp. (Trebouxiophyceae, Chlorophyta) vol.30, pp.6, 2009, https://doi.org/10.1007/s10811-018-1455-9
  60. Effects of light intensity on the photosynthetic responses of Sargassum fusiforme seedlings to future CO2 rising vol.50, pp.1, 2009, https://doi.org/10.1111/are.13873
  61. Effects of elevated CO2 on growth, calcification, and spectral dependence of photoinhibition in the coccolithophore Emiliania huxleyi (Prymnesiophyceae)1 vol.55, pp.4, 2009, https://doi.org/10.1111/jpy.12885
  62. Interactive Effects of Ultraviolet Radiation and Dissolved Organic Carbon on Phytoplankton Growth and Photosynthesis in Sanya Bay, Northern South China Sea vol.54, pp.4, 2009, https://doi.org/10.1007/s12601-019-0033-7
  63. Ocean acidification interacts with variable light to decrease growth but increase particulate organic nitrogen production in a diatom vol.160, pp.None, 2009, https://doi.org/10.1016/j.marenvres.2020.104965
  64. The Aureochrome Photoreceptor PtAUREO1a Is a Highly Effective Blue Light Switch in Diatoms vol.23, pp.11, 2009, https://doi.org/10.1016/j.isci.2020.101730
  65. Multiple interacting environmental drivers reduce the impact of solar UVR on primary productivity in Mediterranean lakes vol.10, pp.1, 2009, https://doi.org/10.1038/s41598-020-76237-5
  66. Interactions Between Ultraviolet B Radiation, Warming, and Changing Nitrogen Source May Reduce the Accumulation of Toxic Pseudo-nitzschia multiseries Biomass in Future Coastal Oceans vol.8, pp.None, 2009, https://doi.org/10.3389/fmars.2021.664302
  67. Introducing climate change into the biochemistry and molecular biology curriculum vol.49, pp.2, 2009, https://doi.org/10.1002/bmb.21422
  68. Nitrogen-limitation exacerbates the impact of ultraviolet radiation on the coccolithophore Gephyrocapsa oceanica vol.226, pp.None, 2009, https://doi.org/10.1016/j.jphotobiol.2021.112368