Genomic blueprint enables early intervention in cyanobacterial risk management

While existing early-warning systems struggle to achieve cross-species cyanobacterial risk prediction with the required synchronicity and accuracy in aquatic ecosystems, our study pioneers a genome architecture-driven monitoring paradigm through decoding 317 cyanobacterial metagenome-assembled genomes from the world's largest phosphorus-limiting water transfer system, the Middle Route of the South-to-North Water Diversion Canal (MR-SNWDC). We found an evolutionary blueprint where genome minimization (<3 Mbp) confers ecological dominance under phosphorus scarcity. These streamlined genomes showed predominance and remarkable seasonal dynamics and demonstrated metabolic specialization in phosphorus turnover, light harvesting, and carbon fixation compared to larger genomes. Importantly, we identified a 3 Mbp genomic threshold distinguishing low-risk cyanobacterial consortia from their toxin-producing counterparts. This genome-proxy system enables preemptive risk mitigation by predicting toxic transitions through genome size tracking, fundamentally advancing algal management from reactive monitoring to proactive regulation in water transfer networks.