Harsh temperature induces Microcystis aeruginosa growth enhancement and water deterioration during vernalization

Cyanobacterial blooms are seasonal phenomena in eutrophic water. Cyanobacteria grow fast in the warm spring/summer while disappearing in cold autumn/winter. The temperature change induces algal vernalization. However, whether vernalization affects cyanobacterial blooms, and the regulatory signaling mechanisms are unclear. This study used Microcystis aeruginosa as the model cyanobacteria, and 4 °C and 10 °C as the low-temperature stimulation to explore the cell growth, metabolites, and signaling pathways in cyanobacteria vernalization. Low temperatures induced M. aeruginosa vernalization; the growth rate and cell density increased by 35±4% and 33±2%. Vernalization influenced peptidoglycan synthesis and cell permeability. Soluble microbial products (SMPs) in water increased by 109±5%, resulting in water deterioration. Polysaccharides were the predominant SMPs during the initial term of vernalization. Tryptophan protein-like & humic acid-like substances became the main increased SMPs in the middle-later period of vernalization. Harsh temperatures triggered quorum sensing and two-component system. Signaling sensing systems upregulated photosynthesis, glycolysis, TCA cycle, oxidative phosphorylation, and DNA replication, enhancing M. aeruginosa growth and metabolism during vernalization. This study verified that low temperature stimulates cyanobacteria growth and metabolism, and vernalization possibly aggravates cyanobacterial blooms and water deterioration. It provides new insights into the mechanism of seasonal cyanobacterial blooms and the pivotal role of signaling regulation.