The CO₂ concentrating mechanism and photosynthetic carbon assimilation in limiting CO₂: how Chlamydomonas works against the gradient

Abstract

SUMMARYThe CO 2 concentrating mechanism (CCM) represents an effective strategy for carbon acquisition that enables microalgae to survive and proliferate when the CO 2 concentration limits photosynthesis. The CCM improves photosynthetic performance by raising the CO 2 concentration at the site of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), simultaneously enhancing carbon fixation and suppressing photorespiration. Active inorganic carbon (Ci) uptake, Rubisco sequestration and interconversion between different Ci species catalyzed by carbonic anhydrases (CAs) are key components in the CCM, and an array of molecular regulatory elements is present to facilitate the sensing of CO 2 availability, to regulate the expression of the CCM and to coordinate interplay between photosynthetic carbon metabolism and other metabolic processes in response to limiting CO 2 conditions. This review intends to integrate our current understanding of the eukaryotic algal CCM and its interaction with carbon assimilation, based largely on Chlamydomonas as a model, and to illustrate how Chlamydomonas acclimates to limiting CO 2 conditions and how its CCM is regulated.

Chloroplast-mediated regulation of CO 2 -concentrating mechanism by Ca 2+ -binding protein CAS in the green alga Chlamydomonas reinhardtii

“…The eukaryotic CCM has been studied in the model green alga Chlamydomonas reinhardtii (5). CCM1/CIA5 was identified as a zinc-finger-type regulatory factor for the induction of most limiting-CO 2 -induced genes, including HLA3 (high-light activated 3), LCIA (low-CO 2 -inducible gene A), and LCIB (low-CO 2 -inducible gene B) (6)(7)(8)(9).…”

Quantitative analysis of the chemotaxis of a green alga, Chlamydomonas reinhardtii, to bicarbonate using diffusion-based microfluidic device

“…14 Due to the variability of dissolved Ci level and 10 000-fold lower diffusion rate of CO 2 in aquatic conditions compared to atmospheric conditions, most microalgae developed the carbon concentrating mechanism (CCM) for acclimation to CO 2 -limiting conditions with active Ci uptake systems to accumulate an intracellular Ci pool. [13][14][15][16] Under neutral to alkaline pH conditions, HCO 3 À is the predominant form of Ci species in the water. 15 Because HCO 3 À is 1000-fold less permeable to lipid membranes relative to CO 2 , internal Ci is accumulated in the form of HCO 3 À to prevent unintended efflux of Ci with the assistance of various carbonic anhydrases (CA) and HCO 3 À transporters.…”

“…[13][14][15][16] Under neutral to alkaline pH conditions, HCO 3 À is the predominant form of Ci species in the water. 15 Because HCO 3 À is 1000-fold less permeable to lipid membranes relative to CO 2 , internal Ci is accumulated in the form of HCO 3 À to prevent unintended efflux of Ci with the assistance of various carbonic anhydrases (CA) and HCO 3 À transporters. 14,16 Chemotaxis is the directional migration of organisms in response to the gradient of chemical stimuli including nutrient sources 17 and toxic compounds.…”

“…Among them, HCO 3 À is the most abundant inorganic carbon source for the aquatic photosynthesis 15 in moderate conditions of aquatic ecosystem. 15 To adapt CO 2 -limiting environment, the microalgae induce CCM for facilitating HCO 3 À uptake and elevating internal inorganic carbon concentration for better carbon fixation efficiency with CAs and HCO 3 À transporters.…”

“…Among them, HCO 3 À is the most abundant inorganic carbon source for the aquatic photosynthesis 15 in moderate conditions of aquatic ecosystem. 15 To adapt CO 2 -limiting environment, the microalgae induce CCM for facilitating HCO 3 À uptake and elevating internal inorganic carbon concentration for better carbon fixation efficiency with CAs and HCO 3 À transporters. 14,16 Since motile microorganisms are capable of detecting and finding the optimal position for a stable supplement of nutrient sources by means of chemotaxis, 23 we thought that HCO 3 À elicits the chemotaxis of a motile microalga, C. reinhardtii.…”