Molecular insights into nitrogen constraint for niche partitioning and physiological adaptation of coastal Synechococcus assemblages.

Coastal nitrogen input has substantially increased due to human activity. However, much remains unknown about the nitrogen-driven patterns and the underlying genetic basis of coastal picoplankton. To investigate the response and mechanisms of picoplankton induced by nitrogen variation, we conducted in-situ investigations using high-throughput sequencing in the Bohai Sea and performed laboratory nitrogen simulation experiments accompanied by physiological, genomic, and transcriptomic analyses, with Synechococcus as a representative. The results of in-situ investigation revealed that Synechococcus clades I, III, WPC1, and VI of subcluster 5.1 (S5.1) are prevalent in strait areas characterized by robust water exchange with the North Yellow Sea, while clades II, VIII, and IX of S5.1, as well as subcluster 5.2 (S5.2) and subcluster 5.3 (S5.3) are more abundant in central and bay areas experiencing elevated nitrate and nitrite loads. The laboratory experiments further confirmed that inorganic nitrogen is a crucial determinant of diversity and niche partitioning of Synechococcus lineages. Besides, the raising inorganic nitrogen concentration within the current in-situ range (0.1-10 μmol L) enhances photosynthesis and carbon fixation of Synechococcus, however further escalation of inorganic nitrogen (100 μmol L) may hinder these processes instead. The phenomenon could be associated with the differential expression of genes in metabolic pathways regulating nitrogen metabolism, photosynthetic system II, and photosynthesis-antenna proteins in response to nitrogen concentration and type variation. These findings expand our understanding of the impact of macronutrient variation resulting from human activities on marine picoplankton and biogeochemical cycles.