Cyanobacterial metagenomes reflect the spatiotemporal variations in a coastal brackish lagoon

Abstract Cyanobacteria play vital roles in aquatic ecosystems by driving photosynthesis, nitrogen fixation, carbon sequestration, and forming symbiotic relationships with diverse organisms. However, their proliferation can trigger harmful algal blooms, posing risks to aquatic biodiversity and public health. Despite their ecological significance, the interplay between cyanobacterial genomic traits and ecosystem dynamics remains poorly resolved. Here, we employed culture-independent metagenomic approaches to reconstruct cyanobacterial metagenome-assembled genomes (MAGs) from Chilika Lagoon, India, and investigate their spatiotemporal distribution and functions. Our analysis revealed distinct temporal patterns in cyanobacterial MAG abundance, with salinity emerging as the primary environmental driver of community structure and functional gene composition. Genes associated with biogeochemical cycling and toxin synthesis displayed pronounced seasonal variation, suggesting that functional genomic traits, rather than taxonomic identity govern species selection. Notably, five MAGs harboured the complete phosphate acetyltransferase-acetate kinase (Pta-Ack) pathway, a critical component of the Wood–Ljungdahl pathway, indicating an underappreciated potential for alternative carbon fixation mechanisms alongside the canonical Calvin-Benson-Bassham cycle. Furthermore, genomic variability, rather than phylogenetic relatedness was the dominant factor shaping cyanobacterial dynamics in the lagoon. This study establishes a direct link between physicochemical fluctuations and cyanobacterial functional diversity, offering critical insights into how climate-driven changes in salinity and nutrient regimes may influence aquatic ecosystems. By elucidating the genomic basis of cyanobacterial adaptation, these findings enhance our capacity to predict ecological outcomes of harmful algal blooms and inform strategies to safeguard ecosystem services in vulnerable coastal habitats. Importance This study employs culture-independent metagenomics to reconstruct cyanobacterial metagenome-assembled genomes (MAGs) in Chilika Lagoon, India, unraveling their spatiotemporal distribution and functional traits. Salinity emerged as the primary driver shaping community structure and functional gene composition, with seasonal fluctuations influencing genes tied to biogeochemical cycling (e.g., carbon, nitrogen) and toxin synthesis. Notably, functional genomic traits—rather than taxonomic identity—governed species selection, highlighting adaptive strategies under environmental stress. Intriguingly, five MAGs harbored the complete Pta-Ack pathway, a component of the Wood-Ljungdahl pathway, suggesting cyanobacteria may employ alternative carbon fixation mechanisms alongside the Calvin-Benson-Bassham cycle under fluctuating conditions. These findings link physicochemical variables (e.g., salinity, nutrients) to functional diversity, revealing how genomic adaptations underpin ecological resilience. The study provides critical insights into cyanobacterial responses to environmental change by bridging microbial genomic plasticity with ecosystem-level impacts. This framework aids in predicting bloom dynamics and toxin risks, offering actionable tools to mitigate ecological threats in vulnerable coastal habitats, thereby informing conservation and management strategies amid climate variability.