Contrasting photoacclimation costs in ecotypes of the marine eukaryotic picoplankter Ostreococcus

Ostreococcus, the smallest known marine picoeukaryote, includes lowand high-light ecotypes. To determine the basis for niche partitioning between Ostreococcus sp. RCC809, isolated from the bottom of the tropical Atlantic euphotic zone, and the lagoon strain Ostreococcus tauri, we studied their photophysiologies under growth irradiances from 15 mmol photons m22 s21 to 800 mmol photons m22 s21 with a common nutrient replete regime. With increasing growth irradiance, both strains down-regulated cellular chlorophyll a and chlorophyll b (Chl a and Chl b) content, increased xanthophyll de-epoxidation correlated with nonphotochemical excitation quenching, and accumulated lutein. Ribulose-1,5-bisphosphate carboxylase/oxygenase content remained fairly stable. Under low-growth irradiances of 15–80 mmol photons m22 s21, O. sp. RCC809 had equivalent or slightly higher growth rates, lower Chl a, a higher Chl b : Chl a ratio, and a larger photosystem II (PSII) antenna than O. tauri. O. tauri was more phenotypically plastic in response to growth irradiance, with a larger dynamic range in growth rate, Chl a, photosystem cell content, and cellular absorption cross-section of PSII. Estimating the amino acid and nitrogen costs for photoacclimation showed that the deep-sea oceanic O. sp. RCC809 relies largely on lower nitrogen cost changes in PSII antenna size to achieve a limited range of s-type light acclimation. O. sp. RCC809, however, suffers photoinhibition under higher light. This limited capacity for photoacclimation is compatible with the stable low-light and nutrient conditions at the base of the euphotic layer of the tropical Atlantic Ocean. In the more variable, high-nutrient, lagoon environment, O. tauri can afford to use a higher cost n-type acclimation of photosystem contents to exploit a wider range of light. Picophytoplankton (cells ,2 mm in diameter) are important contributors to marine primary productivity, biogeochemical cycling, and the function of marine food webs (Partensky et al. 1999; Worden et al. 2004). The photosynthetic prokaryotes Synechococcus and Prochlorococcus often dominate the picophytoplankton biomass, and have often been used as type organisms to characterize the physiological responses of picophytoplankton to support ecological or biogeochemical models (Gregg et al. 2003; Anderson 2005). Distinct ecotypes of Prochlorococcus have been isolated from different marine ecological niches (Partensky et al. 1999). Surfaceand low-light–adapted Prochlorococcus strains show distinct nutrient uptake capacities (Moore et al. 2002) and photophysiological features (Moore et al. 1995). Specifically, the low-light Prochlorococcus ecotypes possess more genes which encode the Prochlorophyte chlorophyll-binding proteins (Pcb) than surface ecotypes, encoding a much larger photosynthetic antenna, organized in large rings around their reaction centers (Bibby et al. 2003). Although a considerable fraction of marine picophytoplankton is prokaryotic, picoeukaryotic phytoplankton can account for a large fraction of the biomass of the euphotic zone (Worden et al. 2004) and are widely represented in marine waters. The green algal class Prasinophyceae (Chlorophyta) is one of the more abundant marine photosynthetic picoeukaryotic groups (Not et al. 2004; Worden et al. 2004). The Prasinophyceae are a primitive group branching at the base of the extant green lineage and are often minute in cell size and fairly simple in morphology, as exemplified by Ostreococcus tauri, the smallest known photosynthetic eukaryote. O. tauri is 1 Present address: Centro Oceanográfico de Canarias (IEO), Ctra. San Andrés s/n, 38180, Sta. Cruz de Tenerife, Spain. 2 Corresponding author ([email protected]; phone: 506 364 2610; fax: 506 364 2505).