Polar Biology

, Volume 28, Issue 8, pp 607–618 | Cite as

Ultraviolet-B effects on photosystem II efficiency of natural phytoplankton communities from Antarctica

  • Josée Nina Bouchard
  • Suzanne RoyEmail author
  • Gustavo Ferreyra
  • Douglas A. Campbell
  • Antonio Curtosi
Original Paper


The impact of UVB on the Antarctic phytoplankton photosystem II repair cycle, involving the rapidly cycled D1 protein, was studied during summer 2002. On sunny and overcast days, phytoplankton (from 1-m depth) were exposed to natural light (+UVB) and Mylar-screened (−UVB) conditions. Half of the samples from each treatment were inoculated with lincomycin, an inhibitor of synthesis of chloroplast-encoded proteins including the D1 protein. Blocking D1 repair caused significant Fv/Fm depressions on sunny days but had not effect on the overcast day. Most of the Fv/Fm depression was caused by PAR and UVA with a non-significant contribution from UVB. In the presence of D1 repair, suppressing UVB had no effect on Fv/Fm when the samples originated from a weakly stratified water column with no defined upper mixed layer (UML) while it alleviated Fv/Fm depression when the phytoplankton samples originated from within an UML deeper than the depth of UVB penetration. These results suggest that UVB had more effect on the D1 repair process than on the damage process itself but that phytoplankton sensitivity to surface UVB exposure was influenced by their previous light history, partly determined by the vertical structure of the water column.


Phytoplankton Lincomycin Phytoplankton Assemblage Stratify Water Column PSII Efficiency 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This research was supported by grants from the InterAmerican Institute (IAI) for Global Change Research and from the Natural Science and Engineering Research Council of Canada (NSERC)—Collaborative Research Opportunities and NSERC Discovery grants to Serge Demers, S.R. and D.C.—and Instituto Antártico Argentino (IAA) grant IAA-38 to G.F. We thank the support of the IAA technical team (Oscar González, Leonardo Cantoni, Alejandro Ulrich, Nestor Villacorta and R. De Ricota), the personnel from the Argentinean Navy for logistic support at Melchior Station, Silvia Rodríguez for phytoplankton enumeration and Agrisera AB ( for providing the Global Antibody used to detect PsbA protein pools. This work is a partial fulfilment of J.N.B.’s PhD thesis at the Université du Québec à Rimouski, Québec, Canada.


  1. Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134Google Scholar
  2. Banaszak AT (2003) Photoprotective physiological and biochemical responses of aquatic organisms. In: Helbling EW, Zagarese H (eds) UV Effects in Aquatic Organisms and Ecosystems. The Royal Society of Chemistry, Cambridge, pp 329–356Google Scholar
  3. Barbieri ES, Villafañe VE, Helbling EW (2002) Experimental assessment of UV effects on temperate marine phytoplankton when exposed to variable radiation regimes. Limnol Oceanogr 47:1648–1655Google Scholar
  4. Bergmann T, Richardson T, Paerl HW, Pinckney JL, Schofield O (2002) Synergy of light and nutrients on the photosynthetic efficiency of phytoplankton populations from the Neuse River Estuary, North Carolina. J Plankton Res 24:923–933Google Scholar
  5. Bouchard JN, Campbell DA, Roy S (2005) Effects of ultraviolet-B radiation on the D1 protein repair cycle of natural phytoplankton communities from three latitudes (Canada, Brazil, Argentina). J Phycol. DOI 10.1111/j-1529–8817.2005.04126.xGoogle Scholar
  6. Bracher AU, Wiencke C (2000) Simulation of the effects of naturally enhanced UV radiation on photosynthesis of Antarctic phytoplankton. Mar Ecol Prog Ser 196:127–141Google Scholar
  7. Büchel C, Wilhelm C (1993) In vivo analysis of slow chlorophyll fluorescence induction kinetics in algae: process, problems and perspectives. Photochem Photobiol 58:137–148Google Scholar
  8. Buma AGJ, Gieskes WWC, Thomsen HA (1992) Abundance of Cryptophyceae and chlorophyll b-containing organisms in the Weddell–Scotia Confluence area in the spring of 1988. Polar Biol 12:43–52Google Scholar
  9. Denman KL, Gargett AE (1983) Time and space scales of vertical mixing and advection of phytoplankton in the upper ocean. Limnol Oceanogr 28:801–815Google Scholar
  10. Figueroa FL, Salles S, Aguilera J, Jimérez C, Mercado J, Viñegla B, Flores-Moya A, Altamirano M (1997) Effects of solar radiation on photoinhibition and pigmentation in the red alga Porphyra leucosticta. Mar Ecol Prog Ser 151:81–90Google Scholar
  11. Franklin LA, Larkum AWD (1997) Multiple strategies for a high light existence in a tropical marine macroalga. Photosynth Res 53:149–159Google Scholar
  12. Garcia-Pichel F (1994) A model for internal self-shading in planktonic organisms and its implications for the usefulness of ultraviolet sunscreens. Limnol Oceanogr 39:1704–1717Google Scholar
  13. Hanelt D (1996) Photoinhibition of photosynthesis in marine macroalgae. Sci Mar 60:243–248Google Scholar
  14. Helbling EW, Villafañe V, Ferrario M, Holm-Hansen O (1992) Impact of natural ultraviolet radiation on rates of photosynthesis and on specific marine phytoplankton species. Mar Ecol Prog Ser 80:89–100Google Scholar
  15. Helbling EW, Villafañe V, Holm-Hansen O (1994) Effects of ultraviolet radiation on Antarctic marine phytoplankton photosynthesis with particular attention to the influence of mixing. In: Weiler CS, Penhale PA (eds) Ultraviolet radiation in Antarctica: measurements and biological effects. American Geophysical Union, pp 207–228Google Scholar
  16. Helbling EW, Chalker BE, Dunlap WC, Holm-Hansen O, Villafañe VE (1996) Photoacclimation of Antarctic marine diatoms to solar ultraviolet radiation. J Exp Mar Biol Ecol 204:85–101Google Scholar
  17. Heraud P, Beardall J (2000) Changes in chlorophyll fluorescence during exposure of Dunaliella tertiolecta to UV radiation indicate a dynamic interaction between damage and repair processes. Photosynth Res 63:123–134Google Scholar
  18. Holm-Hansen O, Mitchell BG, Hewes CD, Karl DM (1989) Phytoplankton blooms in the vicinity of Palmer station, Antarctica. Polar Biol 10:49–57Google Scholar
  19. Holm-Hansen O, Lubin D, Helbling EW (1993) Ultraviolet radiation and its effects on organisms in aquatic environments. In: Young AR, Björn LO, Moan J, Nultsch W (eds) Environmental UV Photobiology. Plenum Press, New York, pp 379–425Google Scholar
  20. Holm-Hansen O, Hewes CD, Villafañe VE, Helbling EW, Silva N, Amos T (1997) Distribution of phytoplankton and nutrients in relation to different water masses in the area around Elephant Island, Antarctica. Polar Biol 18:145–153Google Scholar
  21. Lesser MP, Cullen JJ, Neale PJ (1994) Carbon uptake in a marine diatom during acute exposure to ultraviolet B radiation: relative importance of damage and repair. J Phycol 30:183–192Google Scholar
  22. Lesser MP, Neale PJ, Cullen JJ (1996) Acclimation of Antarctic phytoplankton to ultraviolet radiation: ultraviolet-absorbing compounds and carbon fixation. Mol Mar Biol Biotech 5:314–325Google Scholar
  23. Li X, Qin X, McKay RML (2003) Physiological and biochemical response of freshwater cryptomonads (Cryptophyceae) to Fe deficiency. J Basic Microb 43:121–130Google Scholar
  24. Litchman E, Neale PJ, Banaszak AT (2002) Increased sensitivity to ultraviolet radiation in nitrogen-limited dinoflagellates: photoprotection and repair. Limnol Oceanogr 47:86–94Google Scholar
  25. Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Ann Rev Plant Physiol Plant Mol Biol 45:633–662Google Scholar
  26. MacDonald TM, Dubois L, Smith LC, Campbell DA (2003) Sensitivity of cyanobacterial antenna, reaction centre and CO2 assimilation transcripts and proteins to moderate UVB: light acclimation potentiates resistance to UVB. Photochem Photobiol 77:405–412Google Scholar
  27. Madronich S, McKenzie RL, Björn LO, Caldwell MM (1998) Changes in biologically active ultraviolet radiation reaching the Earth’s surface. J Photochem Photobiol B Biol 46:5–19Google Scholar
  28. Marwood CA, Smith REH, Furgal JA, Charlton MN, Solomon KR, Greenberg B (2000) Photoinhibition of natural phytoplankton assemblages in lake Erie exposed to solar radiation. Can J Fish Aquat Sci 57:371–379Google Scholar
  29. Mattoo AK, Hoffman-Falk H, Marder JB, Edelman M (1984) Regulation of protein metabolism: coupling of photosynthetic electron transport to in vivo degradation of the rapidly metabolized 32-kilodalton protein of chloroplast membranes. Proc Natl Acad Sci USA 81:1380–1384Google Scholar
  30. Mitchell BG, Holm-Hansen O (1991) Observations and modeling of the Antarctic phytoplankton crop in relation to mixing depth. Deep Sea Res 38:981–1007Google Scholar
  31. Moline MA, Claustre H, Frazer TK, Grzymski J, Schofield O, Vernet M (2000) Changes in phytoplankton assemblages along the Antarctic Peninsula and potential implications for the Antarctic food web. In: Davison W, Howard-Williams C, Broady P (eds) Antarctic ecosystems. Models for wider ecological understanding. SCAR VII Proceedings, the Caxton Press, Christchurch, New Zealand, pp 263–271Google Scholar
  32. Neale PJ, Davis RF, Cullen JJ (1998) Interactive effects of ozone depletion and vertical mixing on photosynthesis of Antarctic phytoplankton. Nature 392:585–589Google Scholar
  33. Neale PJ, Helbling EW, Zagarese HE (2003) Modulation of UVR exposure and effects by vertical mixing and advection. In: Helbling EW, Zagarese H (eds) UV effects in aquatic organisms and ecosystems. The Royal Society of Chemistry, Cambridge, pp 107–134Google Scholar
  34. Nishiyama Y, Yamamoto H, Allakhverdiev SI, Inaba M, Yokota A, Murata N (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J 20:5587–5594Google Scholar
  35. Osmond CB (1994) What is photoinhibition? Some insights from comparisons of shade and sun plants. In: Baker NR, Bowyer NR (eds) Photoinhibition of photosynthesis, from the molecular mechanisms to the field. Oxford University Press, Oxford, pp 1–24Google Scholar
  36. Parkhill J-P, Maillet G, Cullen JJ (2001) Fluorescence-based maximal quantum yield for PSII as a diagnostic of nutrient stress. J Phycol 37:517–529Google Scholar
  37. Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, Toronto, pp 173Google Scholar
  38. Prásil O, Adir N, Ohad I (1992) Dynamics of photosystem II: mechanism of photoinhibition and recovery processes. In: Barber J (ed) The photosystems: structure, function and molecular biology. Topics in photosynthesis, Vol. 11, Elsevier, Amsterdam, pp 295–348Google Scholar
  39. Rodríguez J, Varela M, Zapata M (2002a) Phytoplankton assemblages in the Gerlache and Bransfield Straits (Antarctic Peninsula) determined by light microscopy and CHEMTAX analysis of HPLC pigment data. Deep Sea Res II 49:723–747Google Scholar
  40. Rodríguez J, Jiménez-Gómez F, Blanco JM, Figueroa FL (2002b) Physical gradients and spatial variability of the size structure and composition of phytoplankton in the Gerlache Strait (Antarctica). Deep Sea Res II 49:693–706Google Scholar
  41. Roy S (2000) Strategies for the minimisation of the UV-induced damage. In: de Mora SJ, Demers S, Vernet M (eds) The Effects of UV Radiation in the Marine Environment. Cambridge University Press, United Kingdom, pp 177–205Google Scholar
  42. Samuelsson G, Öquist G (1977) A method for studying photosynthetic capacities of unicellular algae based on in vivo chlorophyll fluorescence. Plant Physiol 40:315–319Google Scholar
  43. Sass L, Spetea C, Maté Z, Nagy F, Vass I (1997) Repair of UV-B induced damage of photosystem II via de novo synthesis of D1 and D2 reaction centre subunits in Synechocystis sp. PCC 6803. Photosynth Res 54:55–62Google Scholar
  44. Schloss I, Estrada M (1994) Phytoplankton composition in the Weddell–Scotia Confluence area during austral spring in relation with hydrography. Polar Biol 14:77–90Google Scholar
  45. Smith RC, Prézelin BB, Baker KS, Bidigare RR, Boucher NP, Coley T, Karentz D, McIntyre S, Matlick HA, Menzies D, Ondrusek ME, Wan Z, Waters KJ (1992) Ozone depletion: ultraviolet radiation and phytoplankton biology in Antarctic waters. Science 255:952–959Google Scholar
  46. Stambler N (2003) Primary production, light absorption and quantum yields of phytoplankton from the Bellingshausen and Amundsen Seas (Antarctica). Polar Biol 26:438–451Google Scholar
  47. Strid A, Chow WS, Anderson JM (1990) Effects of supplementary ultraviolet-B radiation on photosynthesis in Pisum sativum. Biochim Biophys Acta 1020:260–268Google Scholar
  48. Throndsen J (1978) Preservation and storage. In: Sournia A (ed) phytoplankton manual. Monographs on oceanographic methodology 6, UNESCO, Paris, France, pp 69–74Google Scholar
  49. Tyystjärvi E, Aro EM (1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proc Natl Acad Sci USA 93:2213–2218Google Scholar
  50. Utermöhl H (1958) Zur Vervollkommung der quantitativen Phytoplankton-Methodik Mitt. Int Ver Theor Angew Limnol 9:1–38Google Scholar
  51. Vassiliev IR, Prasil O, Wyman KD, Kolber Z, Hanson Jr AK, Prentice JE, Falkowski PG (1994) Inhibition of PSII photochemistry by PAR and UV radiation in natural phytoplankton communities. Photosynth Res 42:51–64Google Scholar
  52. Villafañe VE, Helbling EW, Holm-Hansen O, Chalker BE (1995) Acclimatization of Antarctic natural phytoplankton assemblages when exposed to solar ultraviolet radiation. J Plankton Res 17:2295–2306Google Scholar
  53. Villafañe VE, Sundbäck K, Figueroa FL, Helbling EW (2003) Photosynthesis in the aquatic environment as affected by UVR. In: Helbling EW, Zagarese H (eds) UV effects in aquatic organisms and ecosystems. The Royal Society of Chemistry, Cambridge, pp 357–397Google Scholar
  54. Villafañe VE, Barbieri ES, Helbling EW (2004) Annual pattern of ultraviolet radiation effects on temperate marine phytoplankton off Patagonia, Argentina. J Plankton Res 26:167–174Google Scholar
  55. Waldron HN, Attwood CG, Probyn TA, Lucas MI (1995) Nitrogen dynamics in the Bellingshausen sea during the austral spring of 1992. Deep Sea Res 42:1253–1276Google Scholar
  56. Xiong FS, Day TA (2001) Effects of solar ultraviolet-B radiation during springtime ozone depletion on photosynthesis and biomass production of Antarctic vascular plants. Plant Physiol 125:738–751Google Scholar
  57. Yentsch CS, Menzel DW (1963) A method for the determination of chlorophyll and phaeophytin by fluorescence. Deep Sea Res 10:221–231Google Scholar
  58. Zar JH (1984) Biostatistical Analysis, 2nd edn. Prentice Hall, Englewood Cliffs, NJ, pp 718Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Josée Nina Bouchard
    • 1
  • Suzanne Roy
    • 1
    Email author
  • Gustavo Ferreyra
    • 1
    • 3
  • Douglas A. Campbell
    • 2
  • Antonio Curtosi
    • 1
    • 3
  1. 1.Institut des Sciences de la Mer de Rimouski (ISMER)Université du Québec à RimouskiRimouskiCanada
  2. 2.Department of Biology and Coastal Wetlands InstituteMount Allison UniversitySackvilleCanada
  3. 3.Instituto Antártico ArgentinoBuenos AiresArgentina

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