Modulation of photosynthesis and inorganic carbon acquisition in a marine microalga by nitrogen, iron, and light availability

The marine microalga Dunaliella tertiolecta Butcher expresses a high affinity for dissolved inorganic carbon (DIC) through a carbon-concentrating mechanism (CCM), known to be influenced by CO2 availability and instantaneous light supply. However, the regulation by light and nutrient supply during growth is less understood, although N and Fe limitation impose an energy limitation by compromising the photosynthetic apparatus. Dunaliella tertiolecta was grown under steady-state conditions of limited light, N, and Fe availability, and the affinity for DIC was measured under saturating light. High affinity DIC uptake capacity was maintained by D. tertiolecta under all growth-limiting conditions, but was modulated in response to the limiting resource. Affinity of photosynthesis for DIC(k(0.5)) was significantly reduced in cells grown under low light, both in turbidostats and in batch culture (p <= 0.03), although cell-normalized P-max was not significantly affected. In contrast, N and Fe limitation resulted in a significant reduction in cell chlorophyll, P-max, and maximum photosystem II quantum yield (F-v/F-m), but the affinity for DIC was enhanced with increasing N or Fe stress. While the affinity for DIC improved with increasing N stress (k(0.5) < 17.8 mu M at mu = 0.27 d(-1) versus k(0.5) > 26 mu M at mu >= 0.77 d(-1)), light use efficiency (alpha) was impaired under N limitation, suggesting a trade-off between light harvesting capacity and active DIC uptake. Stable C isotope analysis of Fe-limited cells confirmed a lower fractionation by the most Fe-limited cells, consistent with the k(0.5) data and more active DIC acquisition (delta C-13 = -19.56 at mu = 0.27 d(-1) cf. delta C-13 = -26.28 at mu = 0.77 d(-1)). Assessment of affinity for DIC using k(0.5) was supported by the close fit of P versus DIC curves to Michaelis-Menten kinetics; with the high DIC affinity of D. tertiolecta, there was poor resolution in the initial slope of the P versus DIC curve as a parameter of affinity for DIC. Enhanced DIC uptake efficiency under Fe and N limitation may relate to improved resource-use efficiency conferred by CCM activity.