Efficient modulation of cellular phosphorus components in response to phosphorus deficiency in the dinoflagellate Karenia mikimotoi

With an increasing trend of phosphorus limitation in coastal waters, phytoplankton with advantageous strategies to address phosphorus deficiency might be more competitive in their communities. Combining physiological, transcriptomic, and miRNA analyses, the present study analyzed the molecular responses of different intracellular phosphorus components to phosphorus deficiency in the harmful dinoflagellate Karenia mikimotoi, with a specific focus on membrane phospholipid remodeling. The cellular phosphorus components of phospholipids, polyphosphate (polyP), and RNA and the associated gene expression showed dynamic variations over a prolonged phosphorus-stressed period. Under phosphorus deficiency, K. mikimotoi preferred to preserve polyP and RNA but efficiently replaced phospholipids with glycerol glycolipids and a betaine lipid to maintain active growth. This dynamic phospholipid substitution in K. mikimotoi was a combined result of the cessation of phospholipid biosynthesis and an increase in phospholipid breakdown. The expression of the identified miRNAs involved in ATP metabolism indicated that miRNAs may play an important role in regulating energy metabolism in K. mikimotoi. The present study improved the understanding of the molecular mechanism of intracellular phosphorus metabolism in marine phytoplankton and highlighted the strong capability of dinoflagellates to efficiently modulate intracellular phosphorus resources. IMPORTANCE Dinoflagellates are the most common phytoplankton group and account for more than 75% of harmful algal blooms in coastal waters. In recent decades, dinoflagellates seem to prevail in phosphate-depleted waters. However, the underlying acclimation mechanisms and competitive strategies of dinoflagellates in response to phosphorus deficiency are poorly understood, especially in terms of intracellular phosphorus modulation and recycling. Here, we focused on the response of intracellular phosphorus metabolism to phosphorus deficiency in the model dinoflagellate Karenia mikimotoi. Our work reveals the strong capability of K. mikimotoi to efficiently regulate intracellular phosphorus resources, particularly through membrane phospholipid remodeling and miRNA regulation of energy metabolism. Our research improved the understanding of intracellular phosphorus metabolism in marine phytoplankton and underscored the advantageous strategies of dinoflagellates in the efficient modulation of internal phosphorus resources to maintain active physiological activity and growth under unsuitable phosphorus conditions, which help them outcompete other species in coastal phosphate-depleted environments.