Effects of Elevated Overwinter Temperature on the Growth Strategies of Microcystis aeruginosa

ABSTRACT Overwintering is a crucial stage in the seasonal cycle of Microcystis , which is often overlooked as a state of “suspended animation”. With global warming and increasing heatwaves, temperature rise during the overwintering phase causes earlier recruitment or blooms. However, the impact of elevated overwinter temperatures on the growth of toxic Microcystis aeruginosa remains poorly understood. This study aimed to elucidate the physiological, metabolic and molecular mechanisms at different overwintering temperatures (4°C, 6°C, 4°C → 6°C → 8°C, 6°C → 8°C) by cellular growth, photosynthetic effect, metabolic products, enzyme activities and transcriptomic analysis. Elevated overwinter temperatures (4°C → 6°C → 8°C, 6°C → 8°C) significantly promoted the growth of M. aeruginosa . Photosynthetic activity responded rapidly, reaching its peak at the 9°C–16°C temperature range. Elevated overwinter temperatures also enhanced the secretion of microcystins and extracellular polymeric substances. These temperatures favoured the expression of rbcL and mcyB genes associated with photosynthetic and microcystin production, with significant activation of RuBisCO and FBA enzymes during recruitment. Furthermore, transcriptomic analysis revealed 321 genes with significant differential expression under elevated overwinter temperatures, including 156 up‐regulated and 165 down‐regulated genes. The interaction network highlighted proteins with the highest connectivity, comprising ribosomal proteins and RNA polymerase proteins, triggering processes related to oxidative phosphorylation and photosynthesis. This study sheds light on the intricate interplay of temperatures with the physiological and molecular dynamics of M. aeruginosa during overwintering, offering valuable insights into the effects of global warming on algae growth in the future.