Leaf pH Polarization in the Seagrass Zostera marina Enhances Adaxial Surface CO2 Formation and Photosynthesis-Driven Carbon Fixation.

Seagrass photosynthesis is often considered carbon-limited due to slow diffusion rates across leaf diffusive boundary layers (DBLs) and low CO2 availability in seawater. Yet, seagrasses are important carbon sinks in coastal environments, enabled via CO2 concentrating mechanisms (CCMs), allowing for bicarbonate (HCO3 -) utilization in their photosynthesis. However, the role of DBL acidification in seagrass CCMs is not well described. Here, we used pH-sensitive planar optodes with micro-crystalline diamond powder, pH and O2-sensitive optical sensor nanoparticles, and microsensor measurements to determine the pH, O2, and inorganic carbon dynamics on the adaxial and abaxial domains of seagrass (Zostera marina L.) leaves. We provide first experimental evidence of seagrass leaf pH polarization via relative adaxial surface acidification, leading to enhanced CO2 formation at the leaf surface via increased dehydration of HCO3 - and carbonate equilibrium speciation shifts towards CO2. This enabled enhanced photosynthetic O2 evolution and CO2 flux to the adaxial domain of leaves (i.e., ~2-fold higher CO2 availability and flux as compared with the abaxial surface) under low light conditions and at the onset of photosynthesis during dark/light transitions under saturating light. Such a CCM-like mechanism for improved CO2 formation around seagrass leaves can be vital in dense seagrass meadows with high diel fluctuations in water-column light, pH, and O2 concentrations to sustain adequate carbon assimilation.