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Marine Biology

, Volume 158, Issue 5, pp 1029–1041 | Cite as

Heterogeneity in the photoprotective capacity of three Antarctic diatoms during short-term changes in salinity and temperature

  • K. Petrou
  • M. A. Doblin
  • P. J. Ralph
Original Paper

Abstract

The Antarctic marine ecosystem changes seasonally, forming a temporal continuum of specialised niche habitats including open ocean, sea ice and meltwater environments. The ability for phytoplankton to acclimate rapidly to the changed conditions of these environments depends on the species’ physiology and photosynthetic plasticity and may ultimately determine their long-term ecological niche adaptation. This study investigated the photophysiological plasticity and rapid acclimation response of three Antarctic diatoms—Fragilariopsis cylindrus, Pseudo-nitzschia subcurvata and Chaetoceros sp.—to a selected range of temperatures and salinities representative of the sea ice, meltwater and pelagic habitats in the Antarctic. Fragilariopsis cylindrus displayed physiological traits typical of adaptation to the sea ice environment. Equally, this species showed photosynthetic plasticity, acclimating to the range of environmental conditions, explaining the prevalence of this species in all Antarctic habitats. Pseudo-nitzschia subcurvata displayed a preference for the meltwater environment, but unlike F. cylindrus, photoprotective capacity was low and regulated via changes in PSII antenna size. Chaetoceros sp. had high plasticity in non-photochemical quenching, suggesting adaptation to variable light conditions experienced in the wind-mixed pelagic environment. While only capturing short-term responses, this study highlights the diversity in photoprotective capacity that exists amongst three dominant Antarctic diatom species and provides insight into links between ecological niche adaptation and species’ distribution.

Keywords

Cyclic Electron Transport Pelagic Environment Photoprotective Pigment Pelagic Condition Photosynthetic Plasticity 
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.

Notes

Acknowledgments

Thanks to Olivia Sackett for experimental assistance and Marlene Zbinden and Vinod Kumar for HPLC analyses. This work was supported by the Australian Research Council grant (DP0773558) awarded to Peter J Ralph, with additional support provided by Aquatic Processes Group and the Department of Environmental Sciences, University of Technology, Sydney. Katherina Petrou was supported by an Australian Postgraduate Award and Commonwealth Scientific and Industrial Research Organisation (CSIRO) Flagship top-up scholarship.

References

  1. Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci 8:15–19CrossRefGoogle Scholar
  2. Almandoz GO, Ferreyra GA, Schloss IR, Dogliotti AI, Rupolo V, Paparazzo FE, Esteves JL, Ferrario ME (2008) Distribution and ecology of Pseudo-nitzschia species (Bacillariophyceae) in surface waters of the Weddell Sea (Antarctica). Polar Biol 31:429–442CrossRefGoogle Scholar
  3. Antal T, Matorin D, Ilyash L, Volgusheva A, Osipov V, Konyuhov I, Krendeleva T, Rubin A (2009) Probing of photosynthetic reactions in four phytoplanktonic algae with a PEA fluorometer. Photosynth Res 102:67–76CrossRefGoogle Scholar
  4. Arbones B, Figueiras FG, Zapata M (1996) Determination of phytoplankton absorption coefficient in natural seawater samples: evidence of a unique equation to correct the pathlength amplification on glass-fibre filters. Mar Ecol Prog Ser 137:293–304CrossRefGoogle Scholar
  5. Arsalane W, Rousseau B, Duval J-C (1994) Influence of the pool size of the xanthophyll cycle on the effects of light stress in a diatom: competition between photoprotection and photoinhibition. Photochem Photobiol 60:237–243CrossRefGoogle Scholar
  6. Beans C, Hecq JH, Koubbi P, Vallet C, Wright S, Goffart A (2008) A study of the diatom-dominated microplankton summer assemblages in coastal waters from Terre Ade′lie to the Mertz Glacier, East Antarctica (139E–145E). Polar Biol 31:1101–1117CrossRefGoogle Scholar
  7. Demmig-Adams B, Adams WW (1996) Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. Planta 198:460–470CrossRefGoogle Scholar
  8. Dierssen HM, Smith RC, Vernet M (2002) Glacial meltwater dynamics in coastal waters west of the Antarctic peninsula. PNAS 99:1790–1795CrossRefGoogle Scholar
  9. Dimier C, Corato F, Tramontano F, Brunet C (2007) Photoprotection and xanthophyll-cycle activity in three marine diatoms. J Phycol 43:937–947CrossRefGoogle Scholar
  10. Dimier C, Giovanni S, Ferdinando T, Brunet C (2009) Comparative ecophysiology of the xanthophyll cycle in six marine phytoplanktonic species. Protist 160:397–411CrossRefGoogle Scholar
  11. Falkowski PG, La Roche J (1991) Acclimation to spectral irradiance in algae. J Phycol 27:8–14CrossRefGoogle Scholar
  12. Finkel Z, Irwin AJ (2001) Light absorption by phytoplankton and the filter amplification correction: cell size and species effects. J Exp Mar Biol Ecol 259:51–61CrossRefGoogle Scholar
  13. Gleitz M, Thomas DN (1992) Physiological responses of a small Antarctic diatom (Chaetoceros sp.) to simulated environmental constraints associated with sea-ice formation. Mar Ecol Prog Ser 88:271–278CrossRefGoogle Scholar
  14. Guillard RR, Ryther JH (1962) Studies of marine planktonic diatoms I. Cyclotella nana Hudstedt and Detonula confervacea Cleve. Can J Microbiol 8:229–239CrossRefGoogle Scholar
  15. Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophyll a, b, c1, and c2 in higher plants and natural phytoplankton. Biochem Physiol Pfl 165:191–194Google Scholar
  16. Kopczynska EE, Savoye N, Dehairs F, Cardinal D, Elskens M (2007) Spring phytoplankton assemblages in the Southern Ocean between Australia and Antarctica. Polar Biol 31:77–88CrossRefGoogle Scholar
  17. Kropuenske L, Mills M, van Dijken G, Bialey S, Robinson D, Welschmeyer N, Arrigo K (2009) Photophysiology in two major Southern Ocean phytoplankton taxa: photoprotection in Phaeocystis antarctica and Fragilariopsis cylindrus. Limnol Oceanogr 54:1176–1196CrossRefGoogle Scholar
  18. Lavaud J (2007) Fast regulation of photosynthesis in diatoms: mechanisms, evolution and ecophysiology. Func Plant Sci Biotech 1:267–287Google Scholar
  19. Lavaud J, van Gorkom H, Etienne A-L (2002) Photosystem II electron transfer cycle and chlororespiration in planktonic diatoms. Photosynth Res 74:51–59CrossRefGoogle Scholar
  20. Lavaud J, Rousseau B, Etienne A-L (2004) General features of photoprotection by energy dissipation in planktonic diatoms (Bacillariophyceae). J Phycol 40:130–137CrossRefGoogle Scholar
  21. Lavaud J, Strzepek R, Kroth PG (2007) Photoprotection capacity differs among diatoms: possible consequences on the spatial distribution of diatoms related to fluctuations in the underwater light climate. Limnol Oceanogr 52:1188–1194CrossRefGoogle Scholar
  22. Lavergne J, Briantais J-M (1996) Photosystem II heterogeneity. In: Ort DRaY CF (ed) Oxygenic photosynthesis: the light reactions. Kluwer, Dordrecht, pp 265–287Google Scholar
  23. Lazar D (2006) The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Func Plant Biol 33:9–30CrossRefGoogle Scholar
  24. Lazar D, Pospíšil P (1999) Mathematical simulation of chlorophyll a fluorescence rise measured with 3-(3′, 4′-dichlorophenyl)-1, 1-dimethylurea–treated barley leaves at room and high temperatures. Eur Biophys J 28:468–477CrossRefGoogle Scholar
  25. Lizotte MP (2001) The contributions of sea ice algae to Antarctic Marine primary production. Am Zool 41:57–73CrossRefGoogle Scholar
  26. Melis A, Homann PH (1976) Heterogeneity of photochemical centres in system II of chloroplasts. Photochem Photobiol 23:343–350CrossRefGoogle Scholar
  27. Meyer A, Tackx M, Daro N (2000) Xanthophyll cycling in Phaeocystis globosa and Thalassiosira sp.: a possible mechanism for species succession. J Sea Res 43:373–384CrossRefGoogle Scholar
  28. Mock T, Hoch N (2005) Long-term temperature acclimation of photosynthesis in steady-state cultures of the polar diatom Fragilariopsis cylindrus. Photosynth Res 85:307–317CrossRefGoogle Scholar
  29. Murphy LS, Haugen EM (1985) The distribution and abundance of phototrophic ultraplankton in the North Atlantic. Limnol Oceanogr 30:47–58CrossRefGoogle Scholar
  30. Nedbal L, Trtílek M, Kaftan D (1999) Flash fluorescence induction: a novel method to study regulation of Photosystem II. J Photochem Photobiol B Biol 48:154–157CrossRefGoogle Scholar
  31. Palmisano AC, SooHoo JB, Moe RL, Sullivan CW (1987) Sea ice microbial communities. VII. Changes in under-ice spectral irradiance during the development of Antarctic sea ice microalgal communities. Mar Ecol Prog Ser 35:165–173CrossRefGoogle Scholar
  32. Petrou K, Hill R, Doblin MA, McMinn A, Johnson R, Wright SW, Ralph PJ (2011) Photoprotection of sea ice microalgal communities from the East Antarctic pack ice. J Phycol 47, (in press)Google Scholar
  33. Prasil O, Kolber Z, Berry JA, Falkowski PG (1996) Cyclic electron flow around Photosystem II in vivo. Photosynth Res 48:395–410CrossRefGoogle Scholar
  34. Ralph PJ, McMinn A, Ryan K, Ashworth C (2005) Short-term effect of temperature on the photokinetics of microalgae from the surface layers of Antarctic pack ice. J Phycol 41:763–769CrossRefGoogle Scholar
  35. Ralph PJ, Ryan KG, Martin A, Fenton G (2007) Melting out of sea ice causes greater photosynthetic stress in algae than freezing in. J Phycol 43:948–956CrossRefGoogle Scholar
  36. Roberts D, Craven M, Cai M, Allison I, Nash G (2007) Protists in the marine ice of the Amery Ice Shelf, East Antarctica. Polar Biol 30:143–153CrossRefGoogle Scholar
  37. Ruban A, Lavaud J, Rousseau B, Guglielmi G, Horton P, Etienne A-L (2004) The super-excess energy dissipation in diatom algae: comparative analysis with higher plants. Photosynth Res 82:165–175CrossRefGoogle Scholar
  38. Ryan K, Ralph P, McMinn A (2004) Acclimation of Antarctic bottom-ice algal communities to lowered salinities during melting. Polar Biol 27:679–686CrossRefGoogle Scholar
  39. Sarthou G, Timmermans KR, Blain S, Tréguer P (2005) Growth physiology and fate of diatoms in the ocean: a review. J Sea Res 53:25–42CrossRefGoogle Scholar
  40. Schansker G, Toth S, Strasser R (2006) Dark recovery of the Chl a fluorescence transient (OJIP) after light adaptation: the qT-component of non-photochemical quenching is related to an activated photosystem I accepter side. Biochim Biophys Act (BBA) 1757:787–797CrossRefGoogle Scholar
  41. Schreiber U (2004) Pulse-amplitude-modulated (PAM) fluorometry and saturation pulse method. In: Papagiorgiou GG (ed) Advances in photosynthesis and respiration, vol 19. Springer, Dordrecht, pp 279–319Google Scholar
  42. Smetacek V (1999) Diatoms and the ocean carbon cycle. Protist 150:25–32CrossRefGoogle Scholar
  43. Thomas DN, Dieckmann GS (2002) Antarctic sea ice-a habitat for extremophiles. Science 295:641–644CrossRefGoogle Scholar
  44. van Heukelem L, Thomas C (2001) Computer-assisted high-performance liquid chromatography method development with applications to the isolation and analysis of phytoplankton pigments. J Chromatogr A 910:31–49CrossRefGoogle Scholar
  45. van Leeuwe M, van Sikkelerus B, Gieskes WW, Stefels J (2005) Taxon-specific differences in photoacclimation to fluctuating irradiance in an Antarctic diatom and a green flagellate. Mar Ecol Prog Ser 288:9–19CrossRefGoogle Scholar
  46. Wagner H, Jakob T, Wilhelm C (2006) Balancing the energy flow from captured light to biomass under fluctuating light conditions. New Phytol 169:95–108CrossRefGoogle Scholar
  47. Wilhelm C (1990) The biochemistry and physiology of light-harvesting processes in chlorophyll b- and chlorophyll c-containing algae. Plant Physiol Biochem 28:293–306Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Plant Functional Biology and Climate Change Cluster and Department of Environmental SciencesUniversity of TechnologySydneyAustralia

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