Photosynthesis and photoprotection in symbiotic corals

Abstract

In zooxanthellate corals, excess excitation energy can be dissipated as heat (nonphotochemical quenching), thereby providing protection against oxidative damage by supraoptimal light in shallow reefs. To identify and quantify the photoprotective mechanisms, we studied the diel variability of chlorophyll fluorescence yields and photosynthetic parameters in situ in corals, using moored and SCUBA-based fast-repetition-rate fluorometers. The results reveal that nonphotochemical quenching is triggered prior to saturation of photosynthetic electron transport by downregulation of the reaction centers of Photosystem II (PSII). This process dissipates up to 80% of the excitation energy. On a sunny day in shallow waters, the daily integrated flux of photons absorbed, and subsequently dissipated as heat, is ϳ4 times that used for photosynthesis. Fluorescence quenching is further accompanied by a slight reduction in the functional absorption cross section for PSII that results from thermal dissipation of excitation energy in the light-harvesting antennae. These two processes are highly dynamic and adjust to irradiance changes on timescales consistent with the passage of clouds across the sky. Under supraoptimal irradiance, however, up to 30% of PSII reaction centers become photoinhibited, and these are repaired only after several hours of low irradiance. In shallow corals, between 10% and 20% of the reactions centers are chronically photoinhibited and appear to remain permanently nonfunctional throughout the year. Our results establish, for the first time, the suite of biophysical mechanisms that optimize photosynthesis while simultaneously providing photoprotection in symbiotic corals in situ.In zooxanthellate corals, light is essential for growth of the organisms, yet the light environment of the algal symbionts is dictated primarily by where the animal host lives (Falkowski et al. 1990). Although there is considerable genetic variability within the algal symbionts (Rowan 1998), clonal cultures of the symbiotic dinoflagellates are not readily distinguishable on the basis of their photosynthetic attributes (Chang et al. 1983;Iglesias-Prieto and Trench 1994; Kinzie and Falkowski unpubl. data). Thus, to first order, photosynthetic performance does not appear to be a critical determinant of phenotypic selection. Since the irradiance regimes experienced by zooxanthellate associations are 1 Corresponding author (falko@imcs.rutgers.edu). AcknowledgmentsThis research was supported by the Office of Naval Research as part of CoBOP (Coastal Benthic Optical Properties) under grants 97PR00617-00, N0001496F0013, and N000149910004. We thank Zvy Dubinsky, Charlie Mazel, and Uwe Kils for suggestions on instrument design; Eli Perel, Schwalb Norbert, Kevin Wyman, Steve Boose, Denis Klimov, Val Myrnyi, and Peter Nawrot for technical assistance; Judith Grassle, Oscar Schofield, Richard Geider, and two anonymous reviewers for comments on the manuscript; Emmeline Romana for clerical help; and the staff of Caribbean Marine Research Cent...

The physiological response of reef corals to diel fluctuations in seawater temperature

“…Decreases in F V /F M can signal chronic photoinhibition (damage to the photosynthetic apparatus), or reversible photoinhibition (Gorbunov et al, 2001). Fluorescence measurements were taken on the final night of treatments, using a Diving-PAM (Walz, GmbH, Effeltrich, Germany), after 2.5 h of darkness (~21:00 h).…”

Photosynthetic electron turnover in the tropical and subtropical Atlantic Ocean

“…Instead, we used an approach for calculating electron transport rates ETR that is independent of the need for sample blanks. Our approach is based on that of Gorbunov et al (2001) and uses only two parameters easily obtained from FRR fluorometry in situ under actinic light, the PSII effective absorption cross section, s PSII 0 (Å 2 quanta À1 ), and PSII trapping efficiency of excitons (F q 0 /F v 0 , dimensionless), in addition to the PPFD,…”

“…Electron turnover rates (ETRs, linear e À turnover per unit biomass per unit time) of microalgae can be determined using chlorophyll a fluorescence induction techniques (Gorbunov et al, 2001;Kromkamp and Forster, 2003;Suggett et al, 2003). One such induction technique, Fast Repetition Rate (FRR) fluorescence (Kolber et al, 1998), has become widely used by oceanographers as it avoids the need to incubate discrete water samples and is highly sensitive.…”

Evaluation of biophysical and optical determinations of light absorption by photosystem II in phytoplankton

“…A loss of reaction center functionality may also increase σ PSII (Falkowski and Kolber 1995) in proportion to the fraction of reaction centers lost and the probability of excitation transfer among the remaining functional reaction centers. This may occur, for example, under conditions of nutrient limitation (Greene et al 1994;Berges et al 1996) and photoinhibition (Vasiliev et al 1994;Babin et al 1996;Gorbunov et al 2001). As a result, σ PSII may vary in situ by a factor of about 1.5 to 3 across a range of temporal and spatial scales (Greene et al 1994;Vasiliev et al 1994;Behrenfeld et al 1996;Behrenfeld and Kolber 1999;Gorbunov et al 2001).…”

“…This may occur, for example, under conditions of nutrient limitation (Greene et al 1994;Berges et al 1996) and photoinhibition (Vasiliev et al 1994;Babin et al 1996;Gorbunov et al 2001). As a result, σ PSII may vary in situ by a factor of about 1.5 to 3 across a range of temporal and spatial scales (Greene et al 1994;Vasiliev et al 1994;Behrenfeld et al 1996;Behrenfeld and Kolber 1999;Gorbunov et al 2001). However, few measurements of σ PSII have been obtained from individual taxa under controlled conditions (Dubinsky et al 1986;Berges et al 1996;Koblízek et al 2001;Raateoja and Seppälä 2001), and it is not known to what extent σ PSII is determined by physiological or taxonomic shifts within and across phytoplankton communities.…”