Inorganic carbon uptake in a freshwater diatom, Asterionella formosa (Bacillariophyceae): from ecology to genomics

Inorganic carbon availability can limit primary productivity and control species composition of freshwater phytoplankton. This is despite the presence of CO2-concentrating mechanisms (CCMs) in some species that maximize inorganic carbon uptake. We investigated the effects of inorganic carbon on the seasonal distribution, growth rates and photosynthesis of a freshwater diatom, Asterionella formosa, and the nature of its CCM using genomics. In a productive lake, the frequency of A. formosa declined with CO2 concentration below air-equilibrium. In contrast, CO2 concentrations at 2.5-times air-equilibrium did not increase growth rate, cell C-quota or the ability to remove inorganic carbon. A pH-drift experiment strongly suggested that HCO3− as well as CO2 could be used. Calculations combining hourly inorganic carbon concentrations in a lake with known CO2 and HCO3− uptake kinetics suggested that rates of photosynthesis of A. formosa would be approximately carbon saturated and largely dependent on CO2 uptake when CO2 was at or above air-equilibrium. However, during summer carbon depletion, HCO3− would be the major form of carbon taken up and carbon saturation will fall to around 30%. Genes encoding proteins involved in CCMs were identified in the nuclear genome of A. formosa. We found carbonic anhydrases from subclasses α, β, γ and θ, as well as solute carriers from families 4 and 26 involved in HCO3− transport, but no periplasmic carbonic anhydrase. A model of the components of the CCM and their location in A. formosa showed that they are more similar to Phaeodactylum tricornutum than to Thalassiosira pseudonana, two marine diatoms.