Changes in inorganic carbon uptake during the progression of a dinoflagellate bloom in a lake ecosystem

Abstract

The physiological, biochemical, and genetic aspects of inorganic (Ci) carbon uptake in aquatic plants and algae have been studied extensively. Yet, to date, few studies examined these questions on dominant phytoplankton populations in their natural environment. Lake Kinneret, Israel, provides a good example of a system in which changes in CO2availability play a vital role in the ecophysiology of inorganic carbon uptake and in the population dynamics during the annual bloom of the dinoflagellate Peridinium gatunense Nygaard. In this study we investigated whether the availability of CO2(aq)limited growth rates and primary productivity of in situ populations of P. gatunense and focused on the role of adaptive mechanisms for Ciuptake. At the onset of the bloom, when epilimnetic pH was low ( = 8) and Ciconcentrations were high ( = 2.5 mM), carbonic anhydrase activity and cellular affinity to CO2(aq)were comparatively low. At this time photosynthetic rates, quantum yields, and in situ growth rates were high. As P. gatunense biomass increased, inorganic carbon decreased by 40%, while CO2(aq)concentrations declined 50-fold to values less than 2 µM. The algae adapted by acquiring a CO2-concentrating mechanism indicated by (i) intracellular Ci-concentrations higher by a factor of 5-70 relative to the ambient Ci; (ii) levels of carbonic anhydrase activity higher by 5- to 50-fold than those at the beginning of the bloom; and (iii) enhanced affinity for Ciand CO2(aq)3- and 40-fold higher, respectively, than affinities at the start of the bloom. These mechanistic changes in carbon uptake were reflected in declining photosynthetic rates and quantum yields as well as in the carbon isotopic composition with lower fractionation (13C enrichment) of the algae as the bloom progressed. Finally, despite induction of adaptive uptake mechanisms to low CO2availability; scarcity of other nutrients combined with low CO2concentrations, increased temperatures, and increased turbulence cause a decline in in situ growth rates and the collapse of the dinoflagellate biomass.Key words: dinoflagellates, inorganic carbon uptake, CCM, carbonic anhydrase, Peridinium gatunense.