Mean and fluctuating temperatures drive shifts in Microcystis overwintering strategies

The shift in Microcystis life strategy from benthic to pelagic overwintering under global warming poses escalating risks of winter blooms, yet mechanisms linking this transition to warming remain poorly understood. Here, we experimentally evaluated overwintering and regrowth ability of four Microcystis aeruginosa and four Microcystis wesenbergii strains under constant (8 °C), elevated (12 °C), and fluctuating (8 ± 4 °C) temperatures, combined with varying light intensities. Cell viability, proliferation, and photosynthetic performance were assessed using flow cytometry and chlorophyll fluorescence analysis. Our results revealed that Microcystis survived more effectively under (8 ± 4)°C fluctuating temperature condition compared to the constant 8 °C condition, likely due to a lower mortality rate at the dark 4 °C phase and a rapid growth rates at the light 12 °C phase. Non-toxic M. wesenbergii exhibited superior fitness when overwintering in the water column, dominating cell density by 2.1-fold over M. aeruginosa at 12 °C. In water column, Microcystis acclimated to cold-light stress by reducing photosynthetic efficiency (φ_P0 decreased 50 %) and increasing energy dissipation (DI0/RC increased 4000 %), enabling rapid recovery after overwintering. Crucially, light-temperature synergy drove niche partitioning: M. wesenbergii successfully overwintered and thrived in the illuminated pelagic zone, while M. aeruginosa relied on dark sediments to survive the overwintering period. These findings redefine winter bloom dynamics, emphasizing the need to incorporate temperature fluctuations and species-specific photoadaptation into predictive models for mitigating cyanobacterial hazards in warming climates.