From winter dormancy to spring bloom: Regulatory mechanisms in Microcystis aeruginosa post-overwintering recovery

Cyanobacterial blooms pose a significant environmental threat in freshwater ecosystems. These cyanobacteria exhibit resilience to cold and dark conditions during winter and flourish as temperature rise in warmer seasons. However, there is a limited understanding of the dynamic growth recovery process and regulatory signaling mechanisms in cyanobacteria after overwintering. In this study, we employed Microcystis aeruginosa (M. aeruginosa) as a model to simulate its growth recovery when subjected to increasing temperature after overwintering under low temperature (4 °C) and dark conditions. We investigated changes in cell growth, microcystin levels, and signaling pathways throughout this recovery phase. Our results indicated that compared to the non-overwintering treatment (T1), the overwintered treatment (T2) experienced a 55.6 % decrease in algae density and a significant reduction in microcystin-LR (MC-LR) levels within the 15-20 °C temperature range (p < 0.05). Overwintering suppressed photosynthetic efficiency during the recovery phase of M. aeruginosa, activated the antioxidant system, and impaired cellular ultrastructure, making algal cells more vulnerable to death. At the transcriptional level, overwintering down-regulated pathways such as photosynthesis, ribosome, the Calvin cycle, and oxidative phosphorylation, hindering the growth and metabolic capacity of M. aeruginosa. In conclusion, this study highlights the inhibitory impacts of overwintering on growth and metabolism of cyanobacteria during the recovery process. It provides insights into the mechanistic foundations of seasonal cyanobacterial blooms and the crucial role of signaling regulation in these processes.