Acclimation to elevated carbon dioxide and ultraviolet radiation in the diatom Thalassiosira pseudonana: Effects on growth, photosynthesis, and spectral sensitivity of photoinhibition

We studied the effects of elevated CO2 concentrations (0.03% vs. 0.1%) on light absorption, membrane permeability, growth, and carbon fixation under photosynthetically active radiation (PAR) and ultraviolet radiation (UVR) exposures in the diatom Thalassiosira pseudonana. Susceptibility of photosynthesis to UVR was estimated using biological weighting functions (BWFs) for the inhibition of photosynthesis and a model that predicts primary productivity under PAR and UVR exposures. Elevated CO2 concentrations reduced chlorophyll content and increased chlorophyll specific cross section, carbon fixation per chlorophyll, and growth rates. In addition, cells acclimated to high CO2 were more sensitive to photoinhibitory UVR than those under atmospheric levels. Sensitivity to UVR was also related to the growth light regime; despite the fact that no UVR effects were observed on growth, light absorption, or carbon fixation, cells pre-exposed to UVR showed reduced photoinhibition compared to those grown under PAR for both normal and elevated CO2 cultures. Thus, acclimation to UVR partially counteracted the increased susceptibility observed under elevated CO2 conditions. Anthropogenic activities that influence the global environment are mainly those that affect the atmosphere, resulting in, for example, increased exposures to ultraviolet radiation (UVR; 280–400 nm) and higher CO2 levels. The effects of these changes are propagated to aquatic systems through the surface layer (Sabine et al. 2004), where most of the biological processes that sustain life and biogeochemical processes take place. Phytoplankton play a key role in determining the effects of environmental change on the surface layer since they are responsible for dissolved inorganic carbon (DIC) sequestration through photosynthetic processes. CO2 used for photosynthesis can diffuse through the cell membrane of most phytoplankton species, while both CO2 and HCO 3 can be incorporated through adenosine triphosphate (ATP)-dependent mechanisms called CO2 concentrating mechanisms (CCMs) (reviewed by Raven 1997). It is expected that long-term elevation of CO2 would downregulate the activity of CCMs, increasing the energy available for other cellular processes and resulting in increased carbon fixation and growth rates (Raven 1991). However, the effect of elevated CO2 on growth and photosynthesis differs among studies, and more work is still needed to understand phytoplankton response to a rise in CO2 concentrations (Riebesell et al. 1993; Hein and Sand-Jensen 1997; Tortell et al. 2000). A proper evaluation of future CO2 concentrations depends not only on estimates of the carbon emitted from anthropogenic activities and stored in the atmosphere, but also on our knowledge of the physical and biological processes affecting ocean–atmosphere feedback. Recent results have suggested that variation among experiments can be related to both interspecific differences in the mechanisms responsible for carbon incorporation as well as the dependence of biological DIC uptake on other factors, such as nutrients and light availability (Leonardos and Geider 2005). Exposure to UVR is one of the environmental factors that can modify atmospheric CO2 sequestration by phytoplankton. Short wavelengths of solar radiation below 400 nm have enough energy to break molecular bonds and damage phytoplankton cells (reviewed in Vincent and Neale 2000). UVR can also indirectly affect several targets in the cells through oxidative stress. Among these cellular targets, cell membranes can be damaged by UVR through lipid peroxidation, cell wall degradation, or protein channel inhibition (Murphy 1983; Sobrino et al. 2004). Membrane damage might also increase permeability, facilitating CO2 diffusion, but it is unlikely that any benefit from an increase in passive CO2 flux could counteract the UVR damage in cells with compromised membranes. Excessive UVR damage of the membrane can also depress the nitrate and phosphorus uptake mechanisms (Hessen et al. 1995; Sobrino et al. 2004). The specific effect of UV exposure on CCMs is unknown, but effects could be caused by nonspecific damage to deoxyribonucleic acid (DNA), gene transcription machinery, or direct damage to membraneprotein complexes. In fact, a study analyzing the photoinhibitory effect of UVR on inorganic carbon acquisition by Dunaliella tertiolecta showed that carbon incorporation did not change after short-term exposures to UVB (280– 320 nm) in this species (Beardall et al. 2002). As an overall effect of UVR damage on phytoplankton, it has been reported that exposure to UVR decreases primary productivity and biomass in many regions of 1 Present address: Universidade de Vigo, 36310 Vigo, Pontevedra, Spain.