Effects of irradiance and ultraviolet radiation on photoadaptation in the zooxanthellae of Aiptasia pallida: primary production, photoinhibition, and enzymic defenses against oxygen toxicity

Marine Biology - Tập 102 - Trang 243-255 - 1989
M. P. Lesser1, J. M. Shick1
1Department of Zoology and Center for Marine Studies, University of Maine, Orono, USA

Tóm tắt

Cnidarians which contain symbiotic algae are constantly faced with the challenges of a changing photic regime and a hyperoxic environment. Zooxanthellae (Symbiodinium sp.) from the sea anemone Aiptasia pallida (Verrill), collected and cultured at Bermuda Biological Station in 1986, exhibit a suite of compensatory responses to changes in irradiance, ultraviolet radiation (UV), and to the toxicity resulting from their interaction with photosynthetically produced oxygen. Superoxide dismutase (SOD) and catalase inactivate superoxide radicals (O2 -) and hydrogen peroxide (H2O2), which are mediators of oxygen toxicity, show an increase in specific activity with irradiance and in response to UV, both in cultured zooxanthellae (CZ) and freshly isolated zooxanthellae (FIZ) from acclimated anemones. CZ and FIZ exposed to environmentally realistic UV levels show a 30 to 40% increase in SOD activities compared with zooxanthellae exposed to similar irradiances without UV. CZ consistently show higher activities of both SOD and catalase compared to FIZ. Both CZ and FIZ exhibit changes in chlorophyll content and in the relationship between photosynthesis and irradiance which suggest photoadaptive changes in CO2-fixing enzymes, the photosynthetic-electron transport system, or in photosynthetic unit size (PSU). UV has a greater effect on the photosynthetic capacity (P max) of FIZ when compared to CZ acclimated at an equivalent irradiance with or without a UV component. UV also enhances the photoinhibition observed at high irradiance in both CZ and FIZ. Differences in enzyme activity between CZ and FIZ suggest an important role for the host in the protection of zooxanthellae against the direct effects of environmentally realistic UV while the photosynthetic performance of zooxanthellae in situ may not be as well protected.

Tài liệu tham khảo

Ahles, M. D. (1967). Some aspects of the morphology and physiology of Symbiodinium microadriaticum. Ph. D. thesis, Fordham University, New York

Allen, J. F. (1977). Superoxide and photosynthetic reduction of oxygen. In: Michelson, A. M., McCord, J. M., Fridovich, I. (eds.). Superoxide and superoxide dismutases. Academic Press, New York, p. 417–436

Asada, K., Kanematsu, S., Okada, S., Hayakawa, T. (1980). Phylogenetic distribution of three types of superoxide dismutase in organisms and in cell organelles. In: Bannister, J. V., Hill, H. A. O. (eds.). Chemical and biochemical aspects of superoxide and superoxide dismutase. Elsevier, Amsterdam, p. 136–153

Asada, K., Takahashi, M. (1987). Production and scavenging of active oxygen in photosynthesis. In: Kyle, D. J., Osmond, C. B., Arntzen, C. J. (eds.). Photoinhibition. Elsevier, Amsterdam, p. 228–287

Bannister, J. V., Bannister, W. H., Rotilio, G. (1987). Aspects of the structure, function, and applications of superoxide dismutase. In: CRC Critical Reviews in Biochemistry. Boca Raton, FL., Vol. 22, Issue 2, p. 111–180

Beauchamp, C., Fridovich, I. (1971). Superoxide dismutase: improved assays and assay applicable to acrylamide gels. Analyt. Biochem. 44: 276–285

Beers, R. F., Jr., Sizer, I. W. (1952). A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J. biol. Chem. 195: 133–140

Berland, B. R., Maestrini, S. Y. (1969). Study of bacteria associated with marine algae in culture. II. Action of antibiotic substances. Mar. Biol. 3: 334–335

Berner, T., Achituv, Y., Dubinsky, Z., Benayahu, Y. (1987). Pattern of distribution and adaptation to different irradiance levels of zooxanthellae in the soft coral Litophyton arboreum (Octocorallia, Alcyonacea). Symbiosis 3: 23–40

Burns, B. D., Beardall, J. (1987). Utilization of inorganic carbon by marine microalgae. J. exp. mar. Biol. Ecol. 107: 75–86

Calkins, J., Thordardottir, T. (1980). The ecological significance of solar UV radiation on aquatic organisms. Nature, Lond. 283: 563–566

Cavanaugh, G. M. (1975). Formulae and methods VI of the Marine Biological Laboratory Chemical Room, Marine Biological Laboratory, Woods Hole, MA

Chang, S. S., Prézelin, B. B., Trench, R. K. (1983). Mechanisms of photoadaptation in three strains of the symbiotic dinoflagellate Symbiodinium microadriaticum. Mar. Biol. 76: 219–229

Claustre, H., Gostan, J. (1987). Adaptation of biochemical composition and cell size to irradiance in two microalgae: possible ecological implications. Mar. Ecol. Prog. Ser. 40: 167–174

Clayton, R. K. (1977). Light and living matter, Vol. 2. The biological part. Robert E. Krieger Publ. Co., Huntington, New York

Coles, S. L., Jokiel, P. L. (1978). Synergistic effects of temperature, salinity and light on the hermatypic coral Montipora verrucosa. Mar. Biol. 49: 187–195

Cook, C. B. (1983). Metabolic interchange in algae-invertebrate symbiosis. Int. Rev. Cytol. Suppl. 14: 177–209

Crossland, C. J., Barnes, D. J. (1977). Gas exchange studies with the staghorn coral Acropora acuminata and its zooxanthellae. Mar. Biol. 40: 185–194

Davis, B. J. (1964). Disc electrophoresis — II method and application to human serum proteins. Ann. N. Y. Acad. Sci. 121: 404–427

D'Aoust, B. G., White, R., Wells, J. M., Olsen, D. A. (1976). Coralalgal associations: capacity for producing and sustaining elevated oxygen tensions in situ. Undersea Biomed. Res. 3: 35–40

Dunlap, W. C., Chalker, B. E., Oliver, J. K. (1986). Bathymetric adaptations of reef-building corals at Davies Reef, Great Barrier Reef, Australia. III. UV-B absorbing compounds. J. exp. mar. Biol. Ecol. 104: 239–248

Dustan, P. (1982). Depth-dependent photoadaptation by zooxanthellae of the reef coral Montastrea annularis. Mar. Biol. 68: 253–264

Dykens, J. A. (1984). Enzymic defenses against oxygen toxicity in marine cnidarians containing endosymbiotic algae. Mar. Biol. Lett. 5: 291–301

Dykens, J. A., Shick, J. M. (1982). Oxygen production by endosymbiotic algae controls superoxide dismutase activity in their animal host. Nature, Lond. 297: 579–580

Dykens, J. A., Shick, J. M. (1984). Photobiology of the symbiotic sea anemone, Anthopleura elegantissima: defenses against photodynamic effects, and seasonal photoacclimatization. Biol. Bull. mar. biol Lab., Woods Hole 167: 683–697

Elstner, E. F. (1982). Oxygen activation and oxygen toxicity. A. Rev. Pl. Physiol. 33: 73–96

Elstner, E. F., Heupel, A. (1976). Inhibition of nitrite formation from hydroxylammonium-chloride: a simple assay for super-oxide dismutase. Analyt. Biochem. 70: 616–620

Falkowski, P. G., Dubinsky, Z., Santostefano, G. (1985). Light-enhanced dark respiration in phytoplankton. Verh. Internat. Verein. Limnol. 22: 2830–2833

Foote, C. S. (1976). Photosensitized oxidation and singlet oxygen: consequences in biological systems. In: Pryor, W. A. (ed.). Free radicals in biology. Academic Press, New York, Vol. II, p. 85–133

Freeman, B. A., Crapo, J. D. (1982). Biology of disease: free radicals and tissue injury. Lab. Invest. 47: 412–426

Fridovich, I. (1978) The biology of oxygen radicals. Science, N.Y. 201: 875–880

Fridovich, I. (1981). Superoxide radical and superoxide dismutases. In: Schaefer, K. E., Gilbert, D. L. (eds.) Oxygen and living processes. Springer-Verlag, New York, p. 250–272

Fridovich, I. (1986). Biological effects of the superoxide radical. Archs Biochem. Biophys. 247: 1–11

Gallagher, J. C., Alberte, R. S. (1985). Photosynthetic and cellular photoadaptive characteristics of three ecotypes of the marine diatom, Skeletonema costatum (Grev.) Cleve. J. exp. mar. Biol. Ecol. 94: 233–250

Gallagher J. C., Wood, A. M., Alberte, A. M. (1984). Ecotypic differentiation in the marine diatom Skletonema costatum: influence of light intensity on the photosynthetic apparatus. Mar. Biol. 82: 121–134

Glynn, P. W., Peters, E. S., Muscatine, L. (1985). Coral tissue microstructure and necrosis: relation to catastrophic coral mortality in Panamá. Dis. aquat. Organisms 1: 29–37

Goreau, T. F. (1964). Mass expulsion of zooxanthellae from Jamaican reef communities after hurricane Flora. Science, N.Y. 145: 383–386

Groden, D., Beck, E. (1979). H2O2 destruction by ascorbate-dependent systems from chloroplasts. Biochim. Biophys. Acta. 546: 426–435

Guillard, R. R. L. (1973). Division rates. In: Stein, J. R. (ed.). Handbook of phycological methods-culture methods and growth measurements. Cambridge University Press, Boston, p. 290–311

Halldal, P. (1968). Photosynthetic capacities and photosynthetic action spectra of endozoic algae of the massive coral Favia. Biol. Bull. mar. biol. Lab., Woods Hole 134: 411–424

Halliwell, B. (1982). The toxic effects of oxygen on plant tissues. In: L. W. Oberley (ed.). Superoxide dismutase. CRC Press, Boca Raton, Vol. I., p. 89–123

Hill, H. A. O. (1981). Oxygen, oxidases, and the essential trace metals. Phil. Trans. R. Soc. Lond. (Ser B) 194: 119–128

Imlay, J. A., Chin, S. M., Linn, S. (1988). Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science, N.Y. 240: 640–642

Itzhaki, R. F., Gill, D. M., (1964). A micro-biuret method for estimating proteins. Analyt. Biochem. 9: 401–410

Jaap, W. C. (1979). Observations on zooxanthellae expulsion at Middle Sambo Reef, Florida Keys. Bull. mar. Sci. 29: 414–422

Jeffrey, S. W., Humphrey, G. F. (1975). New spectrophotometric equations for determing chlorophylls a, b, c, and c 2 in higher plants, algae and natural phytoplankton. Biochem. Biophys. Pfl. 167: 191–194

Jokiel, P. L. (1980). Solar ultraviolet radiation and coral reef epifauna. Science, N.Y. 207: 1069–1071

Jokiel, P. L., York, R. H. Jr. (1982). Solar ultraviolet photobiology of the reef coral Pocillopora damicornis and symbiotic zooxanthellae. Bull. mar. Sci. 32: 301–315

Jokiel, P. L., York, R. H. Jr. (1984). Importance of ultraviolet radiation in photoinhibition of microalgal growth. Limnol. Oceanogr. 29: 192–199

Krause, G. H., Cornic, G. (1987). CO2 and O2 interactions in photoinhibition. In: Kyle, D. J., Osmond, C. B., Arntzen, C. J. (eds.). Photoinhibition. Elsevier, Amsterdam, p. 169–196

Kyle, D. J. (1987). The biochemical basis for photoinhibition of photosystem II. In: Kyle, D. J., Osmond, C. B., Arntzen, C. J. (eds.). Photoinhibition. Elsevier, Amsterdam, p. 197–226

Kyle, D. J., Ohad, I. (1986). The mechanism of photoinhibition in higher plants and green algae. In: Staehlin, L. A., Arntzen, C. J. (eds.). Encyclopedia of plant physiology, Vol. 19. Photosynthesis III, photosynthetic membranes and light harvesting systems. Springer-Verlag, Berlin, p. 468–475

Lewis, M. R., Smith, J. C. (1983). A small volume, short-incubation-time method for measuring photosynthesis as a function of incident irradiance. Mar. Ecol. Prog. Ser. 13: 99–102

Ludlow, M. M. (1987). Light stress at high temperature. In: Kyle, D. J., Osmond, C. B., Arntzen, C. J. (eds.). Photoinhibition. Elsevier, Amsterdam, p. 89–110

Margulis, L. (1981). Symbiosis in cell evolution. W.H. Freeman and Company, San Francisco

Maske, H. (1984). Daylight ultraviolet radiation and the photoinhibition of phytoplankton carbon uptake. J. Plankton Res. 6: 351–357

McAuley, P. J. (1986). Isolation of viable uncontaminated Chlorella from green hydra. Limnol. Oceanor. 31: 222–224

Muller-Parker, G. (1984). Photosynthesis-irradiance responses and photosynthetic periodicity in the sea anemone Aiptasia pulchella and its zooxanthellae. Mar. Biol. 82: 225–232

Muller-Parker, G. (1987). Seasonal variation in light-shade adaptation of natural populations of the symbiotic sea anemone Aiptasia pulchella (Carlgren, 1943) in Hawaii. J. exp. mar. Biol. Ecol. 112: 165–183

Muscatine, L., McCloskey, L. R., Martin, R. E. (1981). Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol. Oceanogr. 26: 601–611

Nakano, Y., Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Pl. Cell Physiol., Tokyo 22: 867–880

Neale, P. J. (1987). Algal photoinhibition and photosynthesis in the aquatic environment. In: Kyle, D. J., Osmond, C. B., Arntzen, C. J. (eds.). Photoinhibition. Elsevier, Amsterdam, p. 39–65

Ogren, W. L. (1984). Photorespiration: pathways, regulation, and modification. A. Rev. Pl. Physiol. 35: 415–442

Osmond, C. B. (1981). Photorespiration and photoinhibition, some implications for the energetics of photosynthesis. Biochim. Biophys. Acta. 639: 77–98

Oyanagui, Y. (1984). Reevaluation of assay methods and establishment of kit for superoxide dismutase activity. Analyt. Biochem. 142: 290–296

Palincsar, J. S., Jones, W. R., Palincsar, E. E. (1988). Effects of isolation of the endosymbiont Symbiodinium microadriaticum (Dinophyceae) from its host Aioptasia pallida (Anthozoa) on cell wall ultrastructure and mitotic rate. Trans. Am. microsc. Soc. 107: 53–66

Patton, J. S., Burris, J. E. (1983). Lipid droplets, medium of energy exchange in the symbiotic anemone Condylactis gigantea: a model coral polyp. Mar. Biol. 75: 137–149

Platt, T., Gallegos, C. L., Harrison, W. G. (1980). Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J. mar. Res. 38: 687–701

Porter, J. W., Muscatine, L., Dubinsky, Z., Falkowski, P. G. (1984). Primary production and photoadaptation in light- and shadeadapted colonies of the symbiotic coral, Stylophora pistillata. Proc. R. Soc. Lond. (Ser. B) 222: 161–180

Powles, S. B. (1984). Photoinhibition of photosynthesis induced by visible light. A. Rev. Pl. Physiol. 35: 15–44

Prézelin, B. B. (1987). Photosynthetic physiology of dinoflagellates. In: Taylor, F. J. R. (ed.). The biology of dinoflagellates. Blackwell, Oxford, p. 174–223

Ralston, M. L., Jenrich, R. I. (1978). DUD, a derivative-free algorithm for nonlinear least squares. Technometrics 20: 7–14

Renger, G., Voss, M., Gräber, P., Schulze, A. (1986). Effects of UV irradiation on different partial reactions of the primary processes of photosynthesis. In: Worrest, R. C., Caldwell, M. M. (eds.) Stratispheric ozone reduction, solar ultraviolet radiation and plant life. Springer-Verlag, New York, p. 171–184

Richardson, K., Beardall, J., Raven, J. A. (1983). Adaptation of unicellular algae to irradiance: an analysis of strategies. New Phytol. 93: 157–191

Roberts, L. (1987). Coral bleaching threatens Atlantic reefs. Science, N.Y. 238: 1228–1229

SAS Institute (1982). SAS user's guide: statistics SAS Institute Inc., Cary, North Carolina, USA

Schoneberg, D. A., Trench, R. K. (1980). Genetic variation in Symbiodinium microadriaticum (Freudenthal) and specificity in its symbiosis with marine invertebrates. II. Morphological variation in S. microadriaticum. Proc. R. Soc. Lond. (Ser. B) 207: 429–444

Shick, J. M., Dykens, J. A. (1985). Oxygen detoxification in algal-invertebrate symbioses from the Grerat Barrier Reef. Oecologia 66: 33–41

Siebeck, O. (1988). Experimental investigation of UV tolerance in hermatypic corals (Scleractinia). Mar. Ecol. Prog. Ser. 43: 95–103

Sisson, W. B. (1986). Effects of UV-B radiation on photosynthesis. In: Worrest, R. C., Caldwell, M. M. (eds.) Stratispheric ozone reduction, solar ultraviolet radiation and plant life. Springer-Verlag, New York, p. 161–169

Smith, C. S., Baker, K. S. (1979). Penetration of UV-B and biologically effective dose-rates in natural waters. Photochem. Photobiol. 29: 311–323

Sokal, R. R., Rohlf, F. J. (1979). Biometry, 2nd ed. W. H. Freeman and Co., San Francisco

Spinrad, R. W., Yentsch, C. M. (1987). Observations on the intra-and interspecific single cell optical variability of marine phytoplankton. Appl. Optics (Easton, Pa.) 26: 357–362

Steen, R. G. (1986). Evidence for heterotrophy by zooxanthellae in symbiosis with Aiptasia pulchella. Biol. Bull. mar. biol. Lab, Woods Hole. 170: 267–278

Sterrer, W. (ed.) (1986). Marine flora and fauna of Bermuda. Wiley-Interscience, New York

Thinh, L. V., Griffiths, D. J., Winsor, H. (1986). Ultrastructure of Symbiodinium microadriaticum (Dinophyceae) symbiotic with Zoanthus sp. (Zoanthidea). Phycologia 25: 178–184

Trench, R. K. (1979). The cell biology of plant-animal symbiosis. A. Rev. Pl. Physiol. 30: 485–531

Trench, R. K., Blank, R. J. (1987). Symbiodinum microadriaticum Freudenthal, S. Goreauii sp. nov., S. kawagutii sp. nov., S. pilosum sp. nov.: gymnodinioid dinoflagellate symbionts of marine invertebrates. J. Phycol., 23: 469–481

Tytler, E. M., Trench, R. K. (1986). Activities of enzymes in β-carboxylation reactions and of catalase in cell-free preparations from the symbiotic dinoflagellates Symbiodinium spp. from a coral, a clam, a zoanthid and two sea anemones. Proc. R. Soc. Lond. (Ser. B) 228: 483–492

Valenzeno, D. P., Pooler, J. P. (1987). Photodynamic action. BioSci. 37: 270–276

Weis, V. M., Smith, G. J., Muscatine, L. (1989). A “CO2 supply” mechanism in zooxanthellate cnidarians: role of carbonic anhydrase. Mar. Biol. 100: 195–202

Wilkerson, F. P., Kobayashi, D., Muscatine, L. (1988). Mitotic index and size of symbiotic algae in Caribbean reef corals. Coral Reefs 7: 29–36

Wood, W. F. (1987). Effect of solar ultra-violet radiation on the kelp Ecklonia radiata. Mar. Biol. 96: 143–150

Worrest, R. C. (1982). Review of literature concerning the impact of UV-B radiation upon marine organisms In: Calkins, J. (ed.). The role of solar ultraviolet radiation in marine ecosystems. Plenum Press, New York, p. 429–457

Yentsch, C. M., Horan, P. K., Muirhead, K., Dortch, Q., Haugen, E. Legendre, L., Murphy, L. S., Perry, M. J., Phinney, D. A., Pomponi, S. A., Spinrad, R. W., Wood, M., Yentsch, C. S., Zahuranec, B. J. (1983). Flow cytometry and cell sorting: a technique for analysis and sorting of aquatic particles. Limnol. Oceanogr. 28: 1275–1280

Zar, J. H. (1984). Biostatistical analysis. Prentice-Hall, Inc., Englewood Cliffs, N. J.

Zimmerman, R. C., SooHoo, J. B., Kremer, J. N., D'Argenio, D. Z. (1987). Evaluation of variance approximation techniques for non-linear photosynthesis-irradiance models. Mar. Biol. 95: 209–215

Zvalinskii, V. I., Leletkin, V. A., Titlyanov, E. A., Shaposhnikova, M. G. (1980). Photosynthesis and adaptation of corals to irradiance. 2. Oxygen exchange. Photosynthetica (Praha, Czecholslovakia) 14: 422–430

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Marine Biology

Tập 102

243-255

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