Microcystin production is important for toxic Microcystis to survive long-term nitrogen starvation

Toxic cyanobacterial blooms have expanded and intensified on a global scale. Although microcystins are known as the most abundant cyanotoxins released during cyanobacterial blooms, the physiological role of these toxic secondary metabolites has not been fully resolved. Here, we show that microcystin production is important for toxic Microcystis to maintain carbon metabolism under long-term nitrogen starvation and subsequent recovery. Compared to carbon metabolism in the nonmicrocystin-producing strains, toxic Microcystis could accumulate more carbon reserves under nitrogen limitation, which is important for the survival of cells under stressful conditions. Transcriptomic analysis revealed that the genes involved in microcystin synthesis were significantly up-regulated at the initial recovery phase, indicating their essential role in strengthening glycogen catabolism and fueling recovery. Flow cytometry analysis showed that compared to nontoxic strains, microcystin-producing Microcystis exhibited a higher survival and recovery rate after prolonged nitrogen starvation, which is consistent with the dominance of these species at the early stage of cyanobacterial blooms. The close genetic traits between Microcystis strains suggest that the strategies observed here might be highly conserved. Our results imply that toxic Microcystis establishes a competitive advantage over nontoxic species and provides insights into the seasonal succession of natural Microcystis populations.