CO2_CMΨ

The enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) fixes around 1,014 kilograms of carbon dioxide per year. As its name indicates, RuBisCO catalyses two competing reactions: carboxylation and oxygenation. However, the diffusion of carbon dioxide through water is much less efficient than that of oxygen, and most of the oceans’ inorganic carbon occurs in the form of bicarbonate. Aquatic photosynthetic microorganisms fix nearly 50% of the carbon dioxide that enters the Earth’s ecosystems. This feat is tied to biophysical carbon dioxide concentration mechanisms (CCMs), which allow RuBisCO to efficiently carry out the fixation process. Over the course of evolution, these CCMs have arisen independently in green algae, diatoms, and cyanobacteria. While these taxa differ in the specific molecular make-up of their CCMs, the general organisation is the same: supramolecular assemblies and the strategic positioning of RuBisCO, membrane bicarbonate transporters, and carbonic anhydrases. While numerous studies have compared how RuBisCO’s properties differ among taxa, the enzyme’s supramolecular structure within particular organelles has only recently become a topic of research. In the model cyanobacteria Halothiobacillus neapolitanus and Synechococcus elongatus, RuBisCO occurs in α- and β-carboxysomes, respectively; these structures are semicrystalline. In the diatom Phaeodactylum tricornutum, RuBisCO is found in pyrenoids, chloroplast organelles without lipid membranes that are semi-rigid. In the green alga Chlamydomonas reinhardtii, the enzyme occurs in a liquid pyrenoid. These three types of microcompartments have different molecular compositions and, presumably, distinct physicochemical properties (e.g., viscosity). They nonetheless harbour functionally equivalent enzyme assemblages. They contain carbonic anhydrases and RuBisCO activase in addition to RuBisCO. Cyanobacteria, diatoms, and green algae inhabit different parts of the environment.

Thus, to understand the ecological relevance of these highly effective supramolecular structures, it is important to clarify how the taxa’s CCMs convergently evolved. CO2_CMΨ will study the physicochemical properties of these microcompartments at multiple scales and determine their influence on carbon dioxide acquisition and fixation. We will perform molecular-level research in which we reconstruct these structures in vitro to compare their physicochemical properties, paying particular attention to how the metabolites of carbon dioxide fixation diffuse therein. We will also perform cellular-level research in which we will observe how microcompartment biogenesis and dissociation relate to carbon dioxide fixation efficiency in different photosynthetic organisms, which will enable us to compare the latter’s relative reliance on CCMs. CO2_CMΨ is unique in its experimental approach, which will be applied to three species of ecophysiological and biotechnological importance that represent different phylogenetic lineages: the heterocystic cyanobacterium Anabaena PCC 7120, the centric diatom P. tricornutum, and the green alga C. reinhardtii. If we can clarify these underlying molecular mechanisms, we can better harness carbon dioxide fixation by single-celled aquatic organisms and design bioinspired solutions for capturing carbon dioxide.