CO, availability, carbonic anhydrase, and the annual dinoflagellate bloom in Lake Kinneret

Changes with time in the concentration of inorganic carbon in Lake Kinneret subsurface water were followed throughout two seasonal dinoflagellate blooms. The response of natural populations of the dominant dinoflagellate, Peridinium gatunense, to these changes was recorded by examining fluctuations over time in the activity of the enzyme carbonic anhydrase (CA) and in photosynthetic parameters. Our results show distinct fluctuations of both external and cytoplasmic CA activity in P. gatunense throughout the annual bloom. Higher levels of activity were triggered by the decline of total dissolved inorganic C below 1.8 mM and more specifically by low concentrations of dissolved CO, (l-10 PM) during the seasonal bloom decline in May-June. Laboratory studies on cultured P. gatunense confirmed our field observations, suggesting that supplemental mechanisms are activated in P. gatunense that enhance inorganic C uptake when CO, is limiting for photosynthesis. Eventually, the cellular adaptations of P. gatunense to the declining CO2 concentrations could not prevent decline of photosynthetic rates contributing to the subsequent decrease in P. gatunense biomass in May-June. In Lake Kinneret, P. gatunense is succeeded by Peridiniupsis spp., the photosynthetic rates and external CA activities of which were much higher under environmental conditions typical of the end of the bloom. In natural aquatic systems, high primary productivity is often accompanied by decreases in the concentrations of dissolved inorganic carbon species (DIC) and, more specifically, in the sharp decline of CO,(aq), the carbon species fixed in photosynthesis (Talling 1985). Cellular adaptations of phytoplankton to low concentrations of dissolved CO, [CO,(aq)] include mechanisms increasing the flux of inI Present address: Dept. Life Sciences, Bar-Ilan University, Ramat Gan, Israel 52900. This work is in partial fulfillment of the requirements for a Ph.D. thesis at Bar-Ilan University. Acknowledgments We thank M. Hatab and V. Hare1 for help in sample collections, U. Pollingher for letting us use unpublished phytoplankton biomass data, personnel from the chemical laboratory of the Mekorot Watershed Research Unit for supplemental mineral and nutrient concentration analyses, W. Eckert and P. Walline for help with the graphics, A. Nishri for help using PHREEQE and in carbonate chemistry calculations, and A. Kaplan for many insightful discussions. We also thank U. Riebesell and an anonymous reviewer whose comments and suggestions helped clarify the manuscript. organic C across the unstirred layers into the cell and its intracellular accumulation via the carbon-concentrating mechanism (CCM) (see Raven and Johnston 199 1; Kaplan et al. 1990). Carbonic anhydrase (CA), a central enzyme in carbon uptake mechanisms, is involved in maintaining close to or higher than equilibrium concentrations of CO,(aq) at the cell surface by dehydration of HC03(Tsuzuki and Miyachi 1989). Additionally, CA is essential to the CCM in increasing the steady state flux of CO,(aq) from inside the plasmalemma to the site of the enzyme responsible for carbon fixation ribulose 1,5-biphosphate carboxylaseioxygenase (rubisco) and in reducing leakage of CO2 from the intracellular pool (Kaplan et al. 1990). CA and its role in DIC uptake have been studied extensively in a variety of aquatic photosynthetic organisms, ranging from prochlorophytes to macroalgae belonging to many taxa (Tsuzuki and Miyachi 1989). Yet amongst the copious literature on CA, little reference is made to in situ activity of the enzyme in natural populations. More-