Inorganic carbon acquisition in coastal Pacific phytoplankton communities

Abstract

Despite significant advances in the understanding of carbon acquisition in eukaryotic algae and cyanobacteria, very little information is available on the mechanisms of C uptake in natural phytoplankton communities or the effects of CO2 variations on marine primary productivity. In this article, we present the results of a 3‐yr study of C acquisition in coastal Pacific phytoplankton populations and their responses to experimental CO2 manipulations. Diatom‐dominated phytoplankton assemblages collected without incubation showed photosynthetic characteristics indicative of a carbon concentrating mechanism. Cells possessed a high affinity for external inorganic C (apparent Km ~1 µM CO2) and accumulated internal inorganic C pools that were ~3–5.5‐fold higher than those in the external medium. Evidence of in situ carbonic anhydrase expression was found in some of the phytoplankton populations we examined, and inhibitor experiments showed that this enzyme was essential for C fixation by cells. The presence of carbon concentrating mechanisms enabled the phytoplankton to maintain rapid growth rates over a wide range of CO2 concentrations (3–32 µM). In five of six long‐term (~2–5‐d) CO2 manipulation experiments, no difference in growth rates could be detected across treatments. However, a significant decrease in growth rate (30%) was observed in one experiment at the lowest CO2 level tested (3 mM). Although phytoplankton growth rates were generally unaffected by the CO2 manipulations, significant CO2‐dependent changes occurred in the cellular biochemistry and physiology of two assemblages that were examined. Cells grown at low CO2 showed higher short‐term rates of C uptake (indicative of transport system up‐regulation), as well as enhanced expression of Rubisco and carbonic anhydrase. In one of these two incubation experiments, lower C:N and carbohydrate:protein ratios were observed at low CO2 . Phytoplankton from both incubations showed low C isotope discrimination relative to the 13C/12C of the available CO2. Photosynthetic fractionation factors (ϵp) ranged from ~3.5‰ to 7.5‰ and were independent of both cellular growth rates and aqueous CO2 concentrations. Our data indicate that nutrient‐replete, rapidly growing coastal phytoplankton can use carbon concentrating mechanisms and respond physiologically and biochemically to changing dissolved CO2 concentrations. Future field studies should examine the effects of CO2 on the growth of nutrient‐limited phytoplankton and assess the potential long‐term ecological shifts that may result from CO2 variations.