Physiological optimization underlies growth rate-independent chlorophyll-specific gross and net primary production

Abstract

Characterization of physiological variability in phytoplankton photosynthetic efficiencies is one of the greatest challenges in assessing ocean net primary production (NPP) from remote sensing of surface chlorophyll (Chl). Nutrient limitation strongly influences phytoplankton intracellular pigmentation, but its impact on Chl-specific NPP (NPP(*)) is debated. We monitored six indices of photosynthetic activity in steady-state Dunaliella tertiolecta cultures over a range of nitrate-limited growth rates (μ), including photosynthetic efficiency of PSII (F(v)/F(m)), O(2)-based gross and net production, 20 min and 24 h carbon assimilation, and carbon- and μ-based NPP. Across all growth rates, O(2)-based Chl-specific gross primary production (GPP(*)(O(2))), NPP(*), and F(v)/F(m) were constant. GPP(*)(O(2)) was 3.3 times greater than NPP(*). In stark contrast, Chl-specific short-term C fixation showed clear linear dependence on μ, reflecting differential allocation of photosynthate between short-lived C products and longer-term storage products. Indeed, (14)C incorporation into carbohydrates was five times greater in cells growing at 1.2 day(-1) than 0.12 day(-1). These storage products are catabolized for ATP and reductant generation within the period of a cell cycle. The relationship between Chl-specific gross and net O(2) production, short-term (14)C-uptake, NPP(*), and growth rate reflects cellular-level regulation of fundamental metabolic pathways in response to nutrient limitation. We conclude that growth rate-dependent photosynthate metabolism bridges the gap between gross and net production and resolves a controversial question regarding nutrient limitation effects on primary production measures.