Biophysical carbon concentrating mechanisms in land plants: insights from reaction-diffusion modeling

Carbon Concentrating Mechanisms (CCMs) have evolved numerous times in photosynthetic organisms. They elevate the concentration of CO2 around the carbon-fixing enzyme rubisco, thereby increasing CO2 assimilatory flux and reducing photorespiration. Biophysical CCMs, like the pyrenoid-based CCM of Chlamydomonas reinhardtii or carboxysome systems of cyanobacteria, are common in aquatic photosynthetic microbes, but in land plants appear only among the hornworts. To predict the likely efficiency of biophysical CCMs in C3 plants, we used spatially resolved reaction-diffusion models to predict rubisco saturation and light use efficiency. We find that the energy efficiency of adding individual CCM components to a C3 land plant is highly dependent on the permeability of lipid membranes to CO2, with values in the range reported in the literature that are higher than used in previous modeling studies resulting in low light use efficiency. Adding a complete pyrenoid-based CCM into the leaf cells of a C3 land plant is predicted to boost net CO2 fixation, but at higher energetic costs than those incurred by photorespiratory losses without a CCM. Two notable exceptions are when substomatal CO2 levels are as low as those found in land plants that already employ biochemical CCMs and when gas exchange is limited such as with hornworts, making the use of a biophysical CCM necessary to achieve net positive CO2 fixation under atmospheric CO2 levels. This provides an explanation for the uniqueness of hornworts CCM among land plants and evolution of pyrenoids multiple times.