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Role of protective and repair mechanisms in the inhibition of photosynthesis in marine macroalgae

Abstract

The mechanism of photoinhibition was investigated in three representative macroalgal species growing on the coast of Patagonia: the chlorophyte Ulva rigida C. Agardh, the rhodophyte Porphyra columbina Montagne and the phaeophyte Dictyota dichotoma (Huds.) Lamour. Dark adapted specimens were exposed to 15 min unfiltered solar radiation to induce photoinhibition, and subsequently the recovery of the photosynthetic quantum yield was followed for up to 6 h. Photoinhibition is believed to be due to the damage and proteolysis of the D1 protein in the reaction center of Photosystem II. During recovery this protein is resynthesized. In order to prove this hypothesis, inhibitors of the chloroplast protein synthesis, streptomycin and chloramphenicol were applied. Both retarded the repair process indicating an inhibition of the D1 protein resynthesis during recovery after the damage they experienced during light exposure. Some algal groups use the xanthophyll cycle to ameliorate the inhibition by excessive light. Dithiothreitol, an inhibitor of violaxanthin de-epoxidase, was administered, to impair the xanthophyll cycle. It strongly affected both photoinhibition and recovery even in the red algal species, which do not have the xanthophyll cycle, indicating that this drug has significant side effects and should be used with caution for the study of the involvement of this protective cycle in algae. Pigmentation was followed in the three species using absorption spectroscopy of thallus extracts at 665 nm during continuous exposure to natural solar radiation or radiation deprived of the UV component during two days. The results indicated a pronounced variation in pigmentation over time due to bleaching and resynthesis. Solar radiation was monitored during the experiments in three channels (UV-B, UV-A and PAR) using an ELDONET instrument on site.

References

  1. D.-P. Häder, H. D. Kumar, R. C. Smith and R. C. Worrest, Effects on aquatic ecosystems, J. Photochem. Photobiol. B: Biol., 1998, 46, 53–68.

    Article  Google Scholar 

  2. K. Lüning (Ed.), Seaweeds. Their environment, biogeography and ecophysiology, New York, Wiley, 1990.

    Google Scholar 

  3. D.-P. Häder, M. Lebert and E. W. Helbling, Effects of solar radiation on the Patagonian macroalga Enteromorpha linza (L.) J. Agardh–Chlorophyceae, J. Photochem. Photobiol., B, 2001, 62, 43–54.

    Article  Google Scholar 

  4. D.-P. Häder, M. Lebert and E. W. Helbling, Photosynthetic performance of the chlorophyte Ulva rigida measured in Patagonia on site, Recent Res. Devel. Photochem. Photobiol., 2000, 4, 259–269.

    Google Scholar 

  5. K. Bischof, D. Hanelt, H. Tüg, U. Karsten, P. E. M. Brouwer and C. Wiencke, Acclimation of brown algal photosynthesis to ultraviolet radiation in arctic coastal waters (Spitsbergen, Norway), Polar Biol., 1998, 20, 388–395.

    Article  Google Scholar 

  6. D.-P. Häder, M. Porst and M. Lebert, Photosynthetic performance of the atlantic brown macroalgae, Cystoseira abies-marina, Dictyota dichotoma and Sargassum vulgare, measured in Gran Canaria on site, Environm. Exp. Bot., 2001, 45, 21–32.

    Article  Google Scholar 

  7. J. Barber and B. Andersson, Too much of a good thing: light can be bad for photosynthesis, TIBS, 1992, 17, 61–66.

    CAS  PubMed  Google Scholar 

  8. S. P. Long, S. Humphries and P. G. Falkowski, Photoinhibition of photosynthesis in nature, Ann. Rev. Plant Physiol., 1994, 45, 633–662.

    CAS  Article  Google Scholar 

  9. D.-P. Häder and J. Schäfer, Photosynthetic oxygen production in macroalgae and phytoplankton under solar irradiation, J. Plant Phys., 1994, 144, 293–299.

    Article  Google Scholar 

  10. D.-P. Häder, H. Herrmann, J. Schäfer and R. Santas, Photosynthetic fluorescence induction and oxygen production in two Mediterranean Cladophora species measured on site, Aquatic Bot., 1997, 56, 253–264.

    Article  Google Scholar 

  11. J. A. Segui, V. Maire, I. S. Gabashvili and M. Fragata, Oxygen evolution loss and structural transitions in photosystem II induced by low intensity UV-B radiation of 280 nm wavelength, J. Photochem. Photobiol. B: Biol., 2000, 56, 39–47.

    CAS  Article  Google Scholar 

  12. W. Henley, G. Levavasseur, L. Franklin, S. T. Lindley, J. Ramus and C. B. Osmond, Diurnal responses of photosynthesis and fluorescence in Ulva rotundata acclimated to sun and shade outdoor culture, Mar. Ecol. Progr. Ser., 1991, 75, 19–28.

    Article  Google Scholar 

  13. K. Bischof, D. Hanelt and C. Wiencke, Effects of ultraviolet radiation on photosynthesis and related enzyme reactions of marine macroalgae, Planta, 2000, 211, 555–562.

    CAS  PubMed  Article  Google Scholar 

  14. D.-P. Häder, H. Herrmann and R. Santas, Effects of solar radiation and solar radiation deprived of UV-B and total UV on photosynthetic oxygen production and pulse amplitude modulated fluorescence in the brown alga Padina pavonia, FEMS Microbiol. Ecol., 1996, 19, 53–61.

    Article  Google Scholar 

  15. D.-P. Häder, M. Porst, H. Herrmann, J. Schäfer and R. Santas, Photoinhibition in the Mediterranean green alga Halimeda tuna Ellis et sol measured in situ, Photochem. Photobiol., 1996, 64, 428–434.

    Article  Google Scholar 

  16. D.-P. Häder, M. Porst and R. Santas, Photoinhibition by solar radiation in the Mediterranean alga Peyssonnelia squamata measured on site, Plant Ecol., 1998, 139, 167–175.

    Article  Google Scholar 

  17. A. Flores-Moya, D. Hanelt, F.-L. Figueroa, M. Altamirano, B. Vinegla and S. Salles, Involvement of solar UV-B radiation in recovery of inhibited photosynthesis in the brown alga Dictyota dichotoma (Hudson) Lamouroux, J. Photochem. Photobiol. B: Biol., 1999, 49, 129–135.

    CAS  Article  Google Scholar 

  18. M. J. Dring, A. Wagner and K. Lüning, Contribution of the UV component of natural sunlight to photoinhibition of photosynthesis in six species of subtidal brown and red seaweeds, Plant Cell Environ., 2001, 24, 1153–1164.

    CAS  Article  Google Scholar 

  19. M. Altamirano, A. Flores-Moya, F. Conde and F. L. Figueroa, Growth seasonality, photosynthetic pigments, and carbon and nitrogen content in relation to environmental factors: a field study of Ulva olivascens (Ulvales, Chlorophyta), Phycologia, 2000, 39, 50–58.

    Article  Google Scholar 

  20. F. L. Figueroa, S. Salles, J. Aguilera, C. Jiménez, J. Mercado, B. Viñegla, A. Flores-Moya and M. Altamirano, Effects of solar radiation on photoinhibition and pigmentation in the red alga Porphyra leucosticta, Mar. Ecol. Progr. Ser., 1997, 151, 81–90.

    CAS  Article  Google Scholar 

  21. G. Döhler, Effect of UV radiation on pigments of the Antarctic macroalga Leptosomia simplex L, Photosynthetica, 1998, 35, 473–476.

    Article  Google Scholar 

  22. G. Döhler, Changes in the pattern of pigments and free amino acids of the macroalga Laminaria saccharina (L.) Lamour exposed to UV-A and UV-B after addition of 15N-ammonium, J. Plant Physiol., 1998, 153, 214–219.

    Article  Google Scholar 

  23. G. Döhler, M. Lohmann and E. Hagmeier, Effect of solar radiation on pigments of Fucus and Porphyra under natural conditions at the North Sea, Beitr. Biol. Pflanzen, 1998, 70, 93–100.

    Google Scholar 

  24. J. Aguilera, C. Jimenez, F. L. Figueroa, M. Lebert and D.-P. Häder, Effect of ultraviolet radiation on thallus absorption and photosynthetic pigments in the red alga Porphyra umbilicalis, J. Photochem. Photobiol., B, 1999, 48, 75–82.

    CAS  Article  Google Scholar 

  25. C. W. Grobe and T. M. Murphy, Solar ultraviolet-B radiation effects on growth and pigment composition of the intertidal alga Ulva expansa (Setch.) S. & G. (Chlorophyta), J. Exp. Mar. Biol. Ecol., 1998, 225, 39–51.

    CAS  Article  Google Scholar 

  26. K. Bischof, D. Hanelt and C. Wiencke, UV-radiation can affect depth-zonation of Antarctic macroalgae, Mar. Biol., 1998, 131, 597–605.

    Article  Google Scholar 

  27. D. Hanelt, Capability of dynamic photoinhibition in Arctic macroalgae is related to their depth distribution, Mar. Biol., 1998, 131, 361–369.

    Article  Google Scholar 

  28. W. H. van de Poll, A. Eggert, A. G. J. Buma and A. M. Breeman, Effects of UV-B-induced DNA damage and photoinhibition on growth of temperate marine red macrophytes: habitat-related differences in UV-B tolerance, J. Phycol., 2001, 37, 30–37.

    Article  Google Scholar 

  29. D.-P. Häder, M. Porst and M. Lebert, Photoinhibition in common Atlantic macroalgae measured on site in Gran Canaria, Helgol. Mar. Res., 2001, 55, 67–76.

    Article  Google Scholar 

  30. M. A. Rodrigues, C. P. dos Santos, Y. Yoneshigue-Valentin, D. Strbac and D. O. Hall, Photosynthetic light-response curves and photoinhibition of the deep-water Laminara abyssalis and the intertidal Laminaria digitata (Phaeophyceae), J. Phycol., 2000, 36, 97–106.

    CAS  Article  Google Scholar 

  31. U. Karsten, K. Bischof and C. Wiencke, Photosynthetic performance of Arctic macroalgae after transplantation from deep to shallow waters, Oecologia, 2001, 127, 11–20.

    CAS  PubMed  Article  Google Scholar 

  32. A. Krieger-Liszkay, K. Kienzler and G. N. Johnson, Inhibition of electron transport at the cytochrome b6f complex protects photosystem II from photoinhibition, FEBS Lett., 2000, 486, 191–194.

    CAS  PubMed  Article  Google Scholar 

  33. Y. Hui, W. Jie and R. Carpentier, Degradation of the photosystem I complex during photoinhibition, Photochem. Photobiol., 2000, 72, 508–512.

    CAS  PubMed  Article  Google Scholar 

  34. D. Hanelt, K. Huppertz and W. Nultsch, Daily course of photosynthesis and photoinhibition in marine macroalgae investigated in the laboratory and field, Mar. Ecol. Progr. Ser., 1993, 97, 31–37.

    Article  Google Scholar 

  35. J. Komenda, Role of two forms of the DI protein in the recovery from photoinhibition of photosystem II in the cyanobacterium Synechococcus PCC 7942, Biochem. Biophys. Acta, 2000, 1457, 243–252.

    CAS  PubMed  Google Scholar 

  36. J. E. W. Polle and A. Melis, Recovery of the photosynthetic apparatus from photoinhibition during dark incubation of the green alga Dunaliella salina, Aust J. Plant Physiol., 1999, 26, 679–686.

    CAS  Google Scholar 

  37. A. Telfer, T. C. Oldham, D. Phillips and J. Barber, Singlet oxygen formation detected by near-infrared emission from isolated photosytem II reaction centres: direct correlation between P680 triplet decay and luminescence rise kinetics and its consequences for photoinhibition, J. Photochem. Photobiol. B: Biol., 1999, 48, 89–96.

    CAS  Article  Google Scholar 

  38. J. M. Anderson, W. S. Chow, Y.-I. Park, L. A. Franklin, S. P.-A. Robinson and P. R. van Hasselt, Response of Tradescantia albiflora to growth irradiance: Change versus changeability, Photosynth. Res., 2001, 67, 103–112.

    CAS  PubMed  Article  Google Scholar 

  39. B. Förster, C. B. Osmond and J. E. Boynton, Very high light resistant mutants of Chlamydomonas reinhardtii: Responses of Photosystem II, nonphotochemical quenching and xanthophyll pigments to light and CO2, Photosynth. Res., 2001, 67, 5–15.

    PubMed  Article  Google Scholar 

  40. G. N. Johnson, J. D. Scholes, P. Horton and A. J. Young, Relationships between carotenoid composition and growth habit in British plant species, Plant Cell Environ., 1993, 16, 681–686.

    CAS  Article  Google Scholar 

  41. K. Niyogy, A. R. Grossman and O. Björkman, Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion, The Plant Cell, 1998, 10, 1121–1134.

    Article  Google Scholar 

  42. D.-P. Häder, M. Lebert, G. Colombetti and F. Figueroa, European light dosimeter network (ELDONET): 1998 data, Helgol. Mar. Res., 2001, 55, 35–44.

    Article  Google Scholar 

  43. D.-P. Häder, M. Lebert, R. Marangoni and G. Colombetti, ELDONET–European Light Dosimeter Network hardware and software, J. Photochem. Photobiol. B: Biol., 1999, 52, 51–58.

    Article  Google Scholar 

  44. E. W. Helbling, R. Gonçalves, E. S. Barbieri and V. E. Villafañe, Radiación ultravioleta y ozono en Patagonia central IV, Jornadas Nacionales de Ciencias del Mar, Puerto Madryn, Argentina, 2000.

    Google Scholar 

  45. R. Marangoni, D. Gioffre, G. Colombetti, M. Lebert and D.-P. Häder, ELDONET–European light dosimeter network. Structure and functions of the ELDONET server, J. Photochem. Photobiol. B: Biol., 2000, 58, 178–184.

    CAS  Article  Google Scholar 

  46. C. Neubauer, Multiple effects of dithiothreitol on nonphotochemical fluorescent quenching in intact chloroplast, Plant Physiol., 1993, 103, 575–583.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  47. U. Schreiber, U. Schliwa and W. Bilger, Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer, Photosynth. Res., 1986, 10, 51–62.

    CAS  PubMed  Article  Google Scholar 

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

    Google Scholar 

  49. E. Weis and A. Berry, Quantum efficiency of photosystem II in relation to the energy dependent quenching of chlorophyll fluorescence, Biochim. Biophys. Acta, 1987, 894, 198–208.

    CAS  Article  Google Scholar 

  50. F. L. Figueroa, C. Jimenez, L. M. Lubian, O. Montero, M. Lebert and D.-P. Häder, Effects of high irradiance and temperature on photosynthesis and photoinhibition in Nannochloropsis gaditana Lubian (Eustigmatophyceae), J. Plant Physiol., 1997, 151, 6–15.

    CAS  Article  Google Scholar 

  51. L. Goldstein and M. S. Waterman, Poisson, compound poisson and process approximations for testing statistical significance in sequence comparisons, Bull. Math. Biol., 1992, 54, 785–812.

    CAS  PubMed  Article  Google Scholar 

  52. D.-P. Häder and F. L. Figueroa, Photoecophysiology of marine macroalgae, Photochem. Photobiol., 1997, 66, 1–14.

    Article  Google Scholar 

  53. C. B. Osmund, What is photoinhibition? Some insights from comparisons of shade and sun plants, in: N. R. Baker, J. R. Bowyer, (Eds.), Photoinhibition of Photosynthesis from the Molecular Mechanisms to the Field, BIOS Scientific Publ., Oxford, 1994, pp. 1–24.

    Google Scholar 

  54. C. Critchley and A. W. Russell, Photoinhibition of photosynthesis in vivo: the role of protein turnover in photosystem II, Physiol.Plant., 1994, 92, 188–196.

    CAS  Article  Google Scholar 

  55. L. A. Franklin and R. M. Forster, The changing irradiance environment: consequences for marine macrophyte physiology, productivity and ecology, Eur. J. Phycol., 1997, 32, 207–232.

    Google Scholar 

  56. G. Noctor, D. Rees, A. Young and P. Horton, The relationship between zeaxanthin, energy-dependent quenching of chlorophyll fluorescence, and trans-thylakoid pH gradient in isolated chloroplasts, Biochim. Biophys. Acta, 1991, 1057, 320–330.

    CAS  Article  Google Scholar 

  57. B. Demmig-Adams, W. W. Adams III, V. Ebbert and B. A. Logan, Ecophysiology of the xanthophyll cycle, in: H. A. Frank, A. J. Young, G. Britton, R. J. Cogdell, (Eds.), Advances in Photosynthesis. The Photochemistry of Carotenoids, Kluwer Academic Publishers, Dordrecht, Boston, London, 1999, pp. 245–269.

    Chapter  Google Scholar 

  58. G. Öquist, J. M. Anderson, S. McCaffery and W. S. Chow, Mechanistic differences in photoinhibition of sun and shade plants, Planta, 1992, 188, 422–431.

    PubMed  Article  Google Scholar 

  59. M. Harker, C. Berkaloff, Y. Lemoine, G. Britton, A. J. Young, J.-C. Duval and N.-E. Rmiki, Effects of high light and desiccation on the operation of the xanthophyll cycle in two marine brown algae, Eur. J. Phycol., 1999, 34, 35–42.

    Article  Google Scholar 

  60. S. Uhrmacher, D. Hanelt and W. Nultsch, Zeaxanthin content and the degree of photoinhibition are linearly correlated in the brown alga Dictyota dichotoma, Mar. Biol., 1995, 123, 159–165.

    CAS  Article  Google Scholar 

  61. C. B. Osmond, J. Ramus, G. Levavasseur, L. A. Franklin and W. J. Henley, Fluorescence quenching during photosynthesis and photoinhibition of Ulva rotundata Blid, Planta, 1993, 190, 97–106.

    CAS  Article  Google Scholar 

  62. L. Talarico, Phycobiliproteins and phycobilisomes in red algae: adaptive responses to light, in: F. L. Figueroa, C. Jiménez, J. L. Pérez-Lloréns, (Eds.), Underwater light and algal photobiology, Scientia Marina, Barcelona, Spain, 1996, pp. 205–222.

    Google Scholar 

  63. D.-P. Häder, H. Herrmann, J. Schäfer and R. Santas, Photosynthetic fluorescence induction and oxygen production in corallinacean algae measured on site, Bot. Acta, 1996, 109, 285–291.

    Article  Google Scholar 

  64. K. H. Grumbach, H. K. Lichtenthaler and K. H. Erismann, Incorporation of 14CO2 in photosynthetic pigments of Chlorella pyrenoidosa, Planta, 1978, 140, 37–43.

    CAS  PubMed  Article  Google Scholar 

  65. P. Algarra and P. Niell, Short-term responses pigment response of Corallina elongata Ellis et Soland to light intensity, Aquat. Bot., 1990, 36, 127–138.

    CAS  Article  Google Scholar 

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Häder, DP., Lebert, M., Sinha, R.P. et al. Role of protective and repair mechanisms in the inhibition of photosynthesis in marine macroalgae. Photochem Photobiol Sci 1, 809–814 (2002). https://doi.org/10.1039/b206152j

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