Phylogenomic insights into toxic bloom formation in the Baltic Sea

The Baltic Sea is a unique and delicate brackish water ecosystem with high primary productivity driven by oceanic biogeochemical cycles of oxygen, iron, silicon, nitrogen and phosphorus. Elevated anthropogenic nutrient loading into the Baltic ecosystem is associated with an increase in the intensity of cyanobacterial blooms. The toxic cyanobacterium Nodularia spumigena forms blooms when phosphate has been depleted from surface waters. Here we analyze the genomes of 53 cyanobacteria isolated from the Baltic Sea for the presence of secondary metabolite biosynthetic pathways as well as metabolic pathways for the acquisition, transport and storage of phosphorous. Bioinformatics analysis and HR-LC-MS analysis demonstrate the production of nodularins, microcystins and cylindrospermopsins in strains of cyanobacteria isolated from planktonic and benthic habitats of the Baltic Sea. Growth experiments demonstrate that a series of phosphonates, phytic acid and phosphite all support the growth of toxic cyanobacteria as the sole source of phosphorous. These results indicate that toxic cyanobacteria can utilize several phosphorus compounds previously unknown to contribute to eutrophication in the Baltic Sea, which may aid in understanding how such organisms dominate phytoplankton blooms under phosphate-limiting conditions and help inform future efforts to mitigate eutrophication.