Differential Single-Cell Organic Nitrogen and Carbon Uptake Drives Niche Partitioning of Marine Synechococcus and mixotrophic life strategy

Marine Synechococcus is among the most abundant and productive cyanobacteria in the ocean. While known to be capable of mixotrophy, the quantitative contribution of organic nutrients to metabolism of different ecotypes remains poorly constrained, limiting our understanding of their role in marine carbon and nitrogen cycles. Here, we conducted a high-resolution comparison of organic nitrogen (urea, leucine) and carbon (glucose) utilization in oligotrophic and eutrophic Synechococcus ecotypes by combining NanoSIMS-based single-cell uptake measurements from field and laboratory incubations with genomics analysis. Our findings revealed clearly different mixotrophic strategy in different ecotypes. Oligotrophic Synechococcus strains preferred organic nitrogen, particularly urea, deriving ~18% of their nitrogen demand from these sources. This physiological trait is supported by genotypic evidence of enhanced urea transport, including upregulation of high-affinity urea transporter DUR3 in both our oligotrophic study sites and other low-nitrogen regions. In contrast, eutrophic ecotypes preferentially utilized glucose, although its contribution remained only 1-2%. Overall, our findings reveal clear ecotype-specific niche partitioning driven by differential organic nitrogen and carbon preference, providing critical insights into the distinct roles of Synechococcus in marine biogeochemical cycles and improving predictions of primary production in the global ocean.