From seawater to pyrenoid – The molecular architecture of the diatom CO2-concentrating mechanism

Abstract

Diatoms are the most successful group of algae and their photosynthesis accounts for up to 20% of annual global CO2 fixation. A key factor to their ecological success is the operation of an efficient biophysical CO2-concentrating mechanism (CCM) that enriches CO2 for fixation by ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) in a specialized microcompartment called the pyrenoid. The diatom CCM is comprised of the following components, functional modules, and processes: 1) acquisition of external dissolved inorganic carbon (DIC); 2) translocation of internal DIC to the chloroplast stroma; 3) the concentration of DIC and its controlled release as CO2 for fixation by Rubisco in the pyrenoid; and 4) minimization of CO2 leakage from the pyrenoid to prevent futile cycling. To achieve efficient CO2 fixation, diatoms evolved a unique molecular architecture that utilizes different intracellular compartmentalization strategies of DIC – such as HCO3− transporters/channels and carbonic anhydrases – to deliver high concentrations of CO2 to densely-packaged Rubisco surrounded by a protein shell. This architecture simultaneously orchestrates the DIC mobilization, CO2-evolution, and the prevention of CO2 leakage from the diatom chloroplast. In this review, we focus on recent progress in understanding the molecular details of the diatom CCM to provide an updated model.