Remarkable Metabolic Reconfiguration due to N Deficiency and an Ammonium‐to‐Nitrate Shift in the Free‐Living Effrenium voratum (Symbiodiniaceae)

Abstract

AbstractNitrogen (N) controls the growth of phytoplankton and the phytosymbionts of corals, but little is known about N nutrition in free‐living planktonic species of the Symbiodiniaceae family. Here, with physiological and transcriptomic analyses, we investigated how Effrenium voratum responded to N deficiency or a nitrate (NO3−) to ammonium (NH4+) switch. The results from batch cultures showed that E. voratum grew well on both NH4+ and NO3−, but NH4+ supported higher yield. Furthermore, when provided with both NH4+ and NO3−, E. voratum preferentially utilized NH4+ and consumed it faster than NO3−. Inhibitory effects of NH4+ on cell growth and photochemical efficiency were detected at ≥ 440 μM in a dose‐dependent manner. When NH4+ and NO3− were compared, only 582 genes were differentially expressed; NH4+ promoted expression of genes related to N transport, carbon fixation, chlorophyll synthesis, and cell division. In contrast, N deficiency inhibited cell division, decreased Chl a content, and changed expression of a large number (4,553) of genes involved in a wide range of metabolic processes from N acquisition, carbon fixation, photosynthate translocation, glycolysis, ROS production, to the cell cycle. This study provides baseline information about N nutrition in a free‐living symbiodiniacean dinoflagellate, which will be useful for comparative research with symbiotic counterparts. The findings also underscore the need to consider differences among phytoplankton groups in responding to forms (NH4+ versus NO3−) and availability (N repletion versus deficiency) of N‐nutrient in modeling N effects on phytoplankton dynamics.