Abstract
The effects of PAR and UV radiation on PS II photochemistry were examined in natural phytoplankton communities from coastal waters off Rhode Island (USA) and the subtropical Pacific. The photochemical energy conversion efficiency, the functional absorption cross section and the kinetics of electron transfer on the acceptor side of PS II were derived from variable fluorescence parameters using both pump and probe and fast repetition rate techniques. In both environments, the natural phytoplankton communities displayed marked decreases in PS II photochemical energy conversion efficiency that were correlated with increased PAR. In the coastal waters, the changes in photochemical energy conversion efficiency were not statistically different for samples treated with supplementary UV-B radiation or screened to exclude ambient UV-B. Moreover, no significant light-dependent changes in the functional absorption cross section of PS II were observed. The rate of electron transfer between QA - and QB was, however, slightly reduced in photodamaged cells, indicative of damage on the acceptor side. In the subtropical Pacific, the decrease in photochemical energy conversion efficiency was significantly greater for samples exposed to natural levels of UV-A and/or UV-B compared with those exposed to PAR alone. The cells displayed large diurnal changes in the functional absorption cross section of PS II, indicative of non-photochemical quenching in the antenna. The changes in the functional absorption cross section were highly correlated with PAR but independent of UV radiation. The time course of changes in photochemical efficiency reveals that the photoinhibited reaction centers rapidly recover (within an hour or two) to their preillumination values. Thus, while we found definitive evidence for photoinhibition of PS II photochemistry in both coastal and open ocean phytoplankton communities, we did not find any effect of UV-B on the former, but a clear effect on the latter. The results of this study indicate that the effects of UV-B radiation on phytoplankton photosynthesis are as dependent on the radiative transfer properties of the water body and the mixing rate, as on the wavelength and energy distribution of the radiation and the absorption cross sections of the biophysical targets.
Similar content being viewed by others
References
Aro E-M, Virgin I and Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113–134
Ben-Amotz A, Shaish A and Avron M (1989) Mode of action of the massively accumulated beta-carotene of Dunaliella bardawil in protecting the alga against damage by excess irradiation. Plant Physiol 91: 1040–1043
Behrenfeld MJ, Hardy J, Gucinski H, Hanneman A, Lee HIIII and Wones A (1993) Effects of ultraviolet-B radiation on primary production along latitudinal transects in the south Pacific Ocean. Mar Environ Res 35: 349–363
Braun J and Tevini M (1993) Regulation of UV-protective pigment synthesis in the epidermal layer of rye seedlings (Secale cereale L. cv. Kustro). Photochem Photobiol 57: 318–323
Caldwell MM, Teramura AH and Tevini M (1989) The changing solar ultraviolet climate and the ecological consequences for higher plants. Trends in Ecology and Evolution 4: 363–367
Crofts AR and Wraight CA (1983) The electrochemical domain of photosynthesis. Biochim Biophys Acta 726: 149–185
Cullen JJ, Neale PJ and Lesser MP (1992) Biological weighting function for the inhibition of phytoplankton photosynthesis by ultraviolet-radiation. Science 258: 646–650
Cullen JJ and Neale PJ (1994) Ultraviolet radiation, ozone depletion, and marine photosynthesis. Photosyn Res 39: 303–320
Demmig-Adams B and AdamsIII WW (1992) Photoprotection and other responses of plants to high light stress. Ann Rev Plant Physiol Plant Mol Biol 43: 599–626
Dunlap WC, Chalker BE and Oliver JK (1986) Bathymetric adaptations of reef-building corals at Davies Reef, Great Barrier Reef, Australia. III. UV-B absorbing compounds. J Exp Mar Biol 104: 239–248
Falkowski PG (1994) The role of phytoplankton photosynthesis in global biogeochemical cycles. Photosyn Res 39: 235–258
Falkowski PG, Wyman K, Ley AC and Mauzerall DC (1986) Relationship of steady-state photosynthesis to fluorescence in eucaryotic algae. Biochim Biophys Acta 849: 183–192
Falkowski PG, Kolber Z and Fujita Y (1988) Effect of redox state on the dymamics of Photosystem II during steady-state photosynthesis in eucaryotic algae. Biochim Biophys Acta 933: 432–443
Falkowski PG, Greene R and Kolber Z (1994a) Light utilization and photoinhibition of photosynthesis in marine phytoplankton. In: Bowyer J and Baker NR (eds) Photoinhibition of Photosynthesis—From Molecular Mechanisms to the Field, pp 409–434. Bios Scientific, London
Falkowski PG, Kolber Z and Mauzerall D (1994b) A comment on the call to throw away your fluorescence induction apparatus. Biophys J 66: 923–925
Fitzwater SE, Knauner GA and Martin JH (1982) Metal contamination and its effect on primary production measurements. Limnol Oceanogr 27: 544–551
Genty B, Harbinson J, Briantais JM and Baker NR (1990) The relationship between non-photochemical quenching of chlorophyll fluorescence and the rate of photosystem-2 photochemistry in leaves. Photosyn Res 25: 249–257
Greenberg BM, Gaba V, Canaani O, Malkin S, Mattoo AK and Edelman M (1989) Separate photosensitizers mediate degradation of the 32 kDa photosystem II reaction center protein in the visible and UV spectral regions. Proc Natl Acad Sci USA 86: 6617–6620
Horton P and Ruban AV (1992) Regulation of photosystem-II. Photosyn Res 34: 375–385
Jerlov NG (1976) Marine Optics. Elsevier, 194 pp
Jones LW and Kok B (1966) Photoinhibition of chloroplast reactions. I. Kinetics and action spectra. Plant Physiol 41: 1037–1043
Kirilovsky D, Cucouet J-M and Etienne AL (1990) Primary events occurring in photoinhibition in Synechocystis 6714 wild-type and an atrizine-resistant mutant. Biochim Biophys Acta 1020: 87–93
Kirk JTO (1994) Light and Photosynthesis in Aquatic Ecosystems. Cambridge University Press, 509 pp
Kolber Z and Falkowski PG (1993) Use of active fluorescence to estimate phytoplankton photosynthesis in situ. Limnol Oceanogr 38: 1646–1665
Kolber Z, Zehr J and Falkowski PG (1988) Effects of growth irradiance and nitrogen limitation on photosynthetic energy conversion in Photosystem II. Plant Physiol 88: 72–79
Krause GH and Weis E (1991) Chlorophyll fluorescence and photosynthesis — the basics. Ann Rev Plant Physiol Plant Mol Biol 42: 313–349
Kyle DJ, Ohad I and Arntzen J (1984) Membrane protein damage and repair: Selective loss of a quinone-protein function in chloroplast membranes. Proc Natl Acad Sci USA 81: 4070–4074
Kyle DJ, Osmond CB and Arntzen CJ (eds) (1987) Photoinhibition. Elsevier, New York, 315 pp
Lambert CE and Oviatt CA (1986) Manual of biological and geochemical techniques in coastal areas. MERL Series Report No. 1, Second Edition, The University of Rhode Island, Kingston, RI
Larkum A and Wood WF (1993) The effect of UV-B radiation on photosynthesis and respiration of phytoplankton, benthic macroalgae and seagrasses. Photosyn Res 36: 17–23
Ley AC and Mauzerall D (1982) Absolute absorption cross sections for photosystem II and the minimum quantum requirement for photosynthesis in Chlorella vulgaris. Biochim Biophys Acta 680: 95–106
Long SP, Humphries S and Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Ann Rev Plant Physiol Plant Mol Biol 45: 633–662
Mauzerall D and Greenbaum NL (1989) The absolute size of a photosynthetic unit. Biochim Biophys Acta 974: 119–140
Middleton EM and Teramura AH (1993) The role of flavonol glycosides and carotenoids in protecting soybean from ultraviolet-B damage. Plant Physiol 103: 741–752
Neale PJ (1987) Algal photoinhibition and photosynthesis in the aquatic environment. In: Kyle DJ, Osmond CB and Arntzen CJ (eds) Photoinhibition, pp 39–65. Elsevier, New York
Ohad I, Koike H, Shochat S and Inoue Y (1988) Changes in the properties of reaction center II during the initial stages of photoinhibition as revealed by thermoluminescence measurements. Biochim Biophys Acta 933: 288–298
Pilson MEQ, Oviatt CA and Nixon SW (1980) Annual nutrient cycles in a marine microcosm. In: Giesy JP (ed) Microcosms in Ecological Research, pp 753–778. DOE Symposium Series, Augusta, GA. Nov. 8–10, 1978, CONF 781101, NTIS
Prasil O, Adir N and Ohad I (1992) Dynamics of photosystem II: mechanism of photoinhibition and recovery processes. In: The Photosystems: Structure, Function and Molecular Biography, Barber J (ed), Vol 11, pp 295–348. Elsevier, Amsterdam
Renger G, Völker M, Eckert HJ, Fromme R, Hohm-Veit S and Gräber P (1989) On the mechanism of Photosystem II deterioration by UV-B irradiation. Photochem Photobiol 49: 97–105
Robinson HH and Crofts AR (1983) Kinetics of the oxidation-reduction reactions of the photosystem II quinone acceptor complex, and the pathway for deactivation. Febs Lett 153: 221–226
Rundel RD (1983) Action spectra and estimation of biologically effective UV radiation. Physiol. Plant 58: 360–366
Ryther JH (1956) Photosynthesis in the ocean as a function of light intensity. Limnol Oceanogr 1: 61–70
Smith RC and Baker KS (1979) Penetration of UV-B and biologically effective dose-rates in natural waters. Photochem Photobiol 29: 311–323
Smith RC, Prezelin BB, Baker KS, Bidigare RR, Boucher NP, Coley T, Karentz D, MacIntyre S, Matlick HA, Menzies D, Ondrusek M, Wan Z and Waters KJ (1992) Ozone depletion: ultraviolet radiation and phytoplankton biology in Antarctic waters. Science 255, 952–957
Strid A, Chow WS and Anderson JM (1990) Effects of supplementary ultraviolet-B radiation on photosynthesis in Pisum sativum. Biochim Biophys Acta 1020: 260–268
Sukenik A, Wyman KD, Bennett J and Falkowski PG (1987) A novel mechanism for regulating the excitation of photosystem II in a green alga. Nature 327: 704–707
Taguchi S (1976) Short-term variability of photosynthesis in natural marine phytoplankton populations. Mar Biol 37: 197–207
Vincent WF, Neale PJ and Richerson PJ (1984) Photoinhibition: Algal responses to bright light during diel stratification and mixing in a tropical alpine lake. J Phycol 20: 201–211
Wilson MI and Greenberg BM (1993) Protection of the DI photosystem-II reaction center protein from degradation in ultraviolet-radiation following adaptation of Brassica napus to growth in ultraviolet-B. Photochem Photobiol 57: 556–563
Author information
Authors and Affiliations
Additional information
The submitted manuscript has been authored under Contract No. DE-AC02-76CH00016 with the U.S. Department of Energy. Accordingly, the U.S. Government retains a nonexclusive, royalty-free license to publish or reproduce the published form of this contribution, or allow others to do so, for U.S. Government purposes.
Rights and permissions
About this article
Cite this article
Vassiliev, I.R., Prasil, O., Wyman, K.D. et al. Inhibition of PS II photochemistry by PAR and UV radiation in natural phytoplankton communities. Photosynth Res 42, 51–64 (1994). https://doi.org/10.1007/BF00019058
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00019058