Transcriptome profiling reveals versatile dissolved organic nitrogen utilization, mixotrophy, and N conservation in the dinoflagellate Prorocentrum shikokuense under N deficiency

Abstract

Harmful algal blooms formed by certain dinoflagellate species often occur when environmental nitrogen nutrients (N) are limited. However, the molecular mechanism by which dinoflagellates adapt to low N environments is poorly understood. In this study, we characterized the transcriptomic responses of Prorocentrum shikokuense to N deficiency, along with its physiological impact. Under N deficiency, P. shikokuense cultures exhibited growth inhibition, a reduction in cell size, and decreases in cellular chlorophyll a and nitrogen contents but an increase in carbon content. Accordingly, gene expression profiles indicated that carbon fixation and catabolism and fatty acid metabolism were enhanced. Transporter genes of nitrate/nitrite, ammonium, urea, and amino acids were significantly upregulated, indicating that P. shikokuense cells invest to enhance the uptake of available dissolved N. Notably, upregulated genes included those involved in endocytosis and phagosomes, evidence that P. shikokuense is a mixotrophic organism that activates phagotrophy to overcome N deficiency. Additionally, vacuolar amino acid transporters, the urea cycle, and urea hydrolysis genes were upregulated, indicating N recycling within the cells under N deficiency. Our study indicates that P. shikokuense copes with N deficiency by economizing nitrogen use and adopting multiple strategies to maximize N acquisition and reuse while maintaining carbon fixation. The remarkable low N adaptability may confer competitive advantages to P. shikokuense for forming harmful blooms in DIN-limited environments.

Keywords: Dinoflagellate; Harmful algal bloom; Mixotrophic; Nitrogen stress; Phagotrophy.