Hydrogen isotope fractionation is controlled by CO₂ in coccolithophore lipids.

ABSTRACT: Hydrogen isotope ratios (δ²H) represent an important natural tracer of metabolic processes, but quantitative models of processes controlling H-fractionation in aquatic photosynthetic organisms are lacking. Here, we elucidate the underlying physiological controls of ²H/¹H fractionation in algal lipids by systematically manipulating temperature, light, and CO₂(aq) in continuous cultures of the haptophyte Gephyrocapsa oceanica. We analyze the hydrogen isotope fractionation in alkenones (α_alkenone), a class of acyl lipids specific to this species and other haptophyte algae. We find a strong decrease in the α_alkenone with increasing CO₂(aq) and confirm α_alkenone correlates with temperature and light. Based on the known biosynthesis pathways, we develop a cellular model of the δ²H of algal acyl lipids to evaluate processes contributing to these controls on fractionation. Simulations show that longer residence times of NADPH in the chloroplast favor a greater exchange of NADPH with ²H-richer intracellular water, increasing α_alkenone. Higher chloroplast CO₂(aq) and temperature shorten NADPH residence time by enhancing the carbon fixation and lipid synthesis rates. The inverse correlation of α_alkenone to CO₂(aq) in our cultures suggests that carbon concentrating mechanisms (CCM) do not achieve a constant saturation of CO₂ at the Rubisco site, but rather that chloroplast CO₂ varies with external CO₂(aq). The pervasive inverse correlation of α_alkenone with CO₂(aq) in the modern and preindustrial ocean also suggests that natural populations may not attain a constant saturation of Rubisco with the CCM. Rather than reconstructing growth water, α_alkenone may be a powerful tool to elucidate the carbon limitation of photosynthesis.

SUBMITTER: Torres-Romero I 

PROVIDER: S-EPMC11214045 | biostudies-literature | 2024 Jun

REPOSITORIES: biostudies-literature