Microcystins are critical for the toxic Microcystis to survive long-term nitrogen starvation

Abstract

Toxic cyanobacterial blooms have expanded and intensified on a global scale, but the physiological role of microcystins during bloom development is not fully resolved. Here, we show that microcystin production can increase the survival and resuscitation rate of Microcystis after long-term nitrogen starvation. Our results showed that microcystin production could enable toxic Microcystis to accumulate more carbon reserves under nitrogen limitation, which is critical to support the survival of cells under stressful conditions. Further analysis showed that genes involved in microcystin synthesis were significantly upregulated at the initial phase of recovery, which could help toxic Microcystis to strengthen glycogen catabolism and fuel recovery. The close genetic traits between Microcystis strains suggest the strategies observed here might be highly conserved. Our findings imply how toxic Microcystis establish a competitive advantage over non-toxic species and provide new insight into the seasonal dynamic of the Microcystis population in natural environment. IMPORTANCEMicrocystins are the most abundant cyanotoxins released during harmful algal blooms. While the factors controlling microcystin production have been widely studied, the function of these toxic secondary metabolites under changing environments remains poorly understood. Here we proved that microcystins are critical to toxic Microcystis to maintaining carbon metabolism under long-term nitrogen starvation and subsequent recovery. Compared to the non-toxic strains, microcystin-producing Microcystis exhibit a higher viability and resuscitation rate after prolonged nitrogen starvation, which is consistent with the dominance of these species at the early stage of cyanobacterial blooms. Our findings shed light on the genetic traits that drive population succession during bloom development, which is important for the modeling and prediction of harmful cyanobacterial blooms.