C3 and C4 pathways of photosynthetic carbon assimilation in marine diatoms are under genetic, not environmental, control

Marine diatoms are responsible for up to 20% of global CO2 fixation. Their photosynthetic efficiency is enhanced by concentrating CO2 around Rubisco, diminishing photorespiration, but the mechanism is yet to be resolved. Diatoms have been regarded as C-3 photosynthesizers, but recent metabolic labeling and genome sequencing data suggest that they perform C-4 photosynthesis. We studied the pathways of photosynthetic carbon assimilation in two diatoms by short-term metabolic C-14 labeling. In Thalassiosira weissflogii, both C3 (glycerate-P and triose-P) and C4 (mainly malate) compounds were major initial (2 -5 s) products, whereas Thalassiosira pseudonana produced mainly C3 and C6 (hexose-P) compounds. The data provide evidence of C-3-C-4 intermediate photosynthesis in T. weissflogii, but exclusively C-3 photosynthesis in T. pseudonana. The labeling patterns were the same for cells grown at near-ambient (380 mu L L-1) and low (100 mu L L-1) CO2 concentrations. The lack of environmental modulation of carbon assimilatory pathways was supported in T. pseudonana by measurements of gene transcript and protein abundances of C-4-metabolic enzymes (phosphoenolpyruvate carboxylase and phosphoenolpyruvate carboxykinase) and Rubisco. This study suggests that the photosynthetic pathways of diatoms are diverse, and may involve combined CO2-concentrating mechanisms. Furthermore, it emphasizes the requirement for metabolic and functional genetic and enzymic analyses before accepting the presence of C-4-metabolic enzymes as evidence for C-4 photosynthesis.