Photoacclimation modulates excessive photosynthetically active and ultraviolet radiation effects in a temperate and an Antarctic marine diatom

The influence of photoacclimation on the effects of excessive photosynthetically active (PAR; 400–700 nm) and ultraviolet (UVR; 280–400 nm) radiation was assessed for the marine diatoms Thalassiosira weissflogii (Grunow) Fryxell and Hasle and Thalassiosira antarctica (Comber). Low and high PAR acclimated cultures were subjected to simulated surface irradiance (SSI) that mimicked irradiance around noon, including UVR. PSII efficiency, xanthophyll conversion, superoxide dismutase (SOD) activity, carbohydrate buildup, and lipid peroxidation were investigated after 30 min SSI and during 120 min recovery in low irradiance. Furthermore, viability loss was measured during 4 h SSI. Prior to SSI, the diadino-diatoxanthin pool was increased in high irradiance acclimated cells, compared with cells grown under low irradiance. Thirty-minutes SSI caused a pronounced decline in PSII efficiency. This coincided with de-epoxidation of diadinoxanthin in high irradiance acclimated cells, which was completely reversed during recovery in low irradiance. De-epoxidation was lower for low irradiance acclimated cells, whereas PSII efficiency and carbohydrate buildup were lower during the recovery phase. Furthermore, clear UVR effects on PSII efficiency were observed in low irradiance but not in high irradiance acclimated cells. Although 30 min SSI did not increase cellular SOD activity and lipid peroxidation, prolonged (4 h) SSI caused viability loss in low irradiance acclimated cells, which was enhanced by UVR. Therefore, PAR and UVR-induced PSII inactivation and viability loss were reduced by high irradiance–mediated changes in light harvesting and the xanthophyll pigments. In addition to photoacclimation-modulated differences, minor sensitivity differences were found between species. Season, diurnal cycle, weather, and optical properties of particles, detritus, and sediment shape the incident irradiance experienced by phytoplankton (Kirk 1994). Furthermore, deep vertical mixing of the water column imposes strong irradiance oscillations (Denman and Gargett 1983; Neale et al. 2003). This reduces the daily irradiance dose, although phytoplankton occasionally experience periods of excessive irradiance when residing near the surface. These continuous alterations between low and excessive irradiance require regulation and acclimation of light harvesting, photosynthesis, and photoprotection. In response to irradiance limitation, algae maximize light harvesting and photosynthetic efficiency, whereas Calvin cycle activity increases at the expense of light harvesting pigments during saturating irradiance (Falkowski and LaRoche 1991). However, rapid irradiance fluctuations impose challenges to the photoregulation and photoacclimation processes because transition from low to excessive irradiance can overreduce photosynthetic electron transport and initiate formation of reactive oxygen species (ROS). ROS are potentially harmful for all biomolecules and can initiate chain reactions that destroy membranes (Hideg and Vass 1996). Yet initial ROS effects are primarily observed in the chloroplasts causing the inactivation of PSII reaction centers. Protection against excessive irradiance involves down regulation of PSII efficiency to regulate excitation energy for photosynthesis. Short-term adjustment of light harvesting is achieved by thermal dissipation of excessive energy due to de-epoxidation of xanthophylls. The xanthophyll cycle of algae comprises enzymatic conversion of carotenoids such as violaxanthin to antheraxanthin and zeaxanthin in green algae, and diadinoxanthin to diatoxanthin in diatoms (Demming-Adams 1990; Olaizola et al. 1994; Moisan et al. 1998). It is generally accepted that deepoxidation and epoxidation of xanthophylls is controlled by the pH of the lumen (Lavaud et al. 2002). Furthermore, photo-induced PSII damage can be compensated by increased turnover of the D1 reaction center binding protein (Kim et al. 1993). In addition, ROS accumulation can be prevented by antioxidants such as superoxide dismutase (SOD), ascorbate peroxidase, and glutathione metabolism in the chloroplasts (Miyake and Asada 2003). Overall, sensitivity to excessive irradiance is strongly influenced by photoacclimation and nutrient availability because these conditions influence cellular pigment composition and protein turnover rates (Geider et al. 1993; Shelly et al. 2003; van de Poll et al. 2005). Interspecific differences in photoacclimation potential have been reported between a diatom and a green flagellate (Van Leeuwe et al. 2005). Also, differences in PSI and cytochrome b6 f content between the marine diatoms Thalassiosia weissflogii and Thalassiosia oceanea were suggested to initiate changes in sensitivity to fluctuating irradiance (Strzepec and Harrison 2004). Current knowledge on the interactive effects between ultraviolet radiation (UVR) and excessive photosynthetically active radiation (PAR) is still scattered. In addition to excessive PAR (400–700 nm), UVBR (280–315 nm) and UVAR (315–400 nm) cause PSII inactivation that can reduce carbon accumulation under field and laboratory 1 Corresponding author ([email protected]). Acknowledgments We thank the editor and reviewers for their comments. Limnol. Oceanogr., 51(3), 2006, 1239–1248 E 2006, by the American Society of Limnology and Oceanography, Inc.