Rubisco kinetic diversity and effectiveness of CO2-concentrating mechanisms in aquatic photosynthetic organisms.

Aquatic photoautotrophs experience strong physicochemical constraints on inorganic carbon acquisition due to low CO2 and O2 diffusion in water producing a strong reduction in the gas conductance. These limitations have driven the widespread evolution of CO2-concentrating mechanisms (CCMs), which enhance CO2 availability around Rubisco and mitigate its catalytic inefficiencies. A compilation of the Rubisco kinetics and apparent photosynthetic CO2 affinities (1/Km CO2) for a wide range of taxa shows that, despite the structural diversity of CCMs, there is an evolutive convergence among cyanobacteria, diatoms, haptophytes, and some rhodophytes and chlorophytes with similarly high 1/Km CO2, therefore operating almost CO2-saturated photosynthesis under ambient conditions. Notably, none of the compiled species achieves CO2 saturation solely through Rubisco kinetics, underscoring the central role of CCMs in aquatic carbon fixation. CCM effectiveness (the ratio between Rubisco CO2 semi-saturation constant under 21% O2 and apparent photosynthetic semi-saturation constant for CO2, Kcair/Km CO2) varies widely across the compiled species but is consistently higher in organisms possessing Rubisco-containing microcompartments, although pyrenoids are not strictly required for concentrating CO2 around Rubisco above ambient levels. Furthermore, an inverse relationship between Rubisco carboxylation efficiency and 1/Km CO2 supports a divergent CCM-Rubisco coevolutionary trajectory compared with terrestrial plants, likely influenced by intracellular photosynthetic O2 accumulation under submerged conditions. The present review synthesizes current knowledge on CCM diversity and its regulation under future global change scenarios but also reanalyzes CCM effectiveness and its co-evolution with Rubisco kinetic traits across aquatic oxygenic phototrophs, highlighting major knowledge gaps to be filled by future research.