Solar UV Radiation Drives CO 2 Fixation in Marine Phytoplankton: A Double-Edged Sword

Abstract

Photosynthesis by phytoplankton cells in aquatic environmentscontributes to more than 40% of the globalprimary production (Behrenfeld et al., 2006). Withinthe euphotic zone (down to 1% of surface photosyntheticallyactive radiation [PAR]), cells are exposed notonly to PAR (400–700 nm) but also to UV radiation(UVR; 280–400 nm) that can penetrate to considerabledepths (Hargreaves, 2003). In contrast to PAR, which isenergizing to photosynthesis, UVR is usually regardedas a stressor (Ha¨der, 2003) and suggested to affect CO2-concentrating mechanisms in phytoplankton (Beardallet al., 2002). Solar UVR is known to reduce photosyntheticrates (Steemann Nielsen, 1964; Helbling et al.,2003), and damage cellular components such as D1proteins (Sass et al., 1997) and DNA molecules (Bumaet al., 2003). It can also decrease the growth (Villafan˜ eet al., 2003) and alter the rate of nutrient uptake(Fauchot et al., 2000) and the fatty acid composition(Goes et al., 1994) of phytoplankton. Recently, it hasbeen found that natural levels of UVR can alter themorphology of the cyanobacterium Arthrospira (Spirulina)platensis (Wu et al., 2005b).On the other hand, positive effects of UVR, especiallyof UV-A (315–400 nm), have also been reported.UV-A enhances carbon fixation of phytoplankton underreduced (Nilawati et al., 1997; Barbieri et al., 2002)or fast-fluctuating (Helbling et al., 2003) solar irradianceand allows photorepair of UV-B-induced DNAdamage (Buma et al., 2003). Furthermore, the presenceof UV-A resulted in higher biomass production of A.platensis as compared to that under PAR alone (Wuet al., 2005a). Energy of UVR absorbed by the diatomPseudo-nitzschia multiseries was found to cause fluorescence(Orellana et al., 2004). In addition, fluorescentpigments in corals and their algal symbiont are knownto absorb UVR and play positive roles for the symbioticphotosynthesis and photoprotection (Schlichter et al.,1986; Salih et al., 2000). However, despite the positiveeffects that solar UVR may have on aquatic photosyntheticorganisms, there is no direct evidence to whatextent and howUVR per se is utilized by phytoplankton.In addition, estimations of aquatic biological productionhave been carried out in incubations consideringonly PAR (i.e. using UV-opaque vials made of glass orpolycarbonate; Donk et al., 2001) without UVR beingconsidered (Hein and Sand-Jensen, 1997; Schippersand Lu¨ rling, 2004). Here, we have found that UVR canact as an additional source of energy for photosynthesisin tropical marine phytoplankton, though it occasionallycauses photoinhibition at high PAR levels. WhileUVR is usually thought of as damaging, our resultsindicate that UVR can enhance primary production ofphytoplankton. Therefore, oceanic carbon fixation estimatesmay be underestimated by a large percentageif UVR is not taken into account.