THE DUAL ROLE OF THEMICROCYSTIS AERUGINOSAMICROBIOME ON CYANOTOXIN PRODUCTION: COMPETITION FOR AND REMINERALIZATION OF ORGANIC NITROGEN

Abstract

AbstractNutrient-induced blooms of the globally abundant freshwater toxic cyanobacteriumMicrocystisare the cause of worldwide public and ecosystem health concerns. The response ofMicrocystisgrowth and toxin production to new and recycled nitrogen (N) inputs, and the impact of heterotrophic bacteria in theMicrocystisphycosphere on these processes are not well understood. Here, using microbiome transplant experiments, cyanotoxin analysis, and stable isotope tracing to measure N incorporation and exchange at single cell resolution, we monitored the growth, cyanotoxin production, and microbiome community structure of severalMicrocystisstrains grown on amino acids and proteins as the sole N source. We demonstrate that 1) organic N availability shapes the microbiome community structure in theMicrocystisphycosphere; 2) external organic N input leads to lower bacterial colonization of the phycosphere; 3) certainMicrocystisstrains can directly uptake amino acids, but with lower rates than heterotrophic bacteria; 4) biomass-specific microcystin production is not impacted by N source (i.e., nitrate, amino acids and protein) but rather by total N availability; and 5) some bacterial communities compete withMicrocystisfor organic N, but others remineralize organic N, in the process producing bio-available N forMicrocystis. We conclude that organic N input can supportMicrocystisblooms and toxin production, andMicrocystis-associated microbial communities play critical roles by influencing cyanobacterial succession through either decreasing (via competition) or increasing (via remineralization) N availability, especially under inorganic N scarcity.