Integrated multi-omics Mechanism of Optimal Temperatures for Microcystis aeruginosa

Abstract

BackgroundCyanobacterial blooms pose a global environmental challenge, with Lake Taihu being one of the most severely affected regions. Microcystis aeruginosa is the dominant cyanobacterial species responsible for these blooms in Lake Taihu. Temperature is considered a key environmental driver influencing the formation of M. aeruginosa blooms; however, the molecular mechanisms underlying its temperature adaptation remain unclear. Previous studies have suggested that medium- and long-chain fatty acids (MLCFAs) play a crucial role in maintaining membrane stability and regulating energy metabolism, potentially contributing to temperature adaptation. To systematically investigate the adaptive mechanisms of M. aeruginosa under different temperature conditions, this study employed multi-omics approaches to integrate various biological data and elucidate regulatory processes at different levels. Methods In this study, we first measured the growth rates of M. aeruginosa at different temperatures and analyzed the composition of fatty acids under each condition. Pearson correlation analysis was performed to examine the relationship between growth rate and fatty acid content, and transcriptomic data were used to explore the gene expression patterns associated with fatty acid biosynthesis. Furthermore, weighted gene co-expression network analysis (WGCNA) was applied to identify key gene modules associated with temperature adaptation, followed by Gene Ontology (GO) enrichment analysis using TopGO to infer potential biological functions. Finally, an exogenous fatty acid supplementation experiment was conducted to validate the role of specific fatty acids in promoting M. aeruginosa growth under low-temperature conditions. Results Our results showed that the growth rate of M. aeruginosa began to accelerate at 25°C and reached its peak at 29°C. The composition of MLCFAs varied significantly across different temperatures, and correlation analysis revealed a strong positive relationship between total fatty acid content and growth rate. Further analysis of fatty acid metabolic pathways suggested that temperature changes led to increased fatty acid consumption, affecting their intracellular accumulation. The validation experiment confirmed that the supplementation of C18:3n3(9,12,15), C20:3n6(8,11,14), and C20:3n3(11,14,17) significantly enhanced the growth rate of M. aeruginosa at low temperatures (15°C). Transcriptomic analysis revealed extensive transcriptional reprogramming under different temperature conditions, particularly in pathways related to fatty acid biosynthesis, energy metabolism, and stress responses. WGCNA identified key gene modules strongly associated with fatty acid metabolism, suggesting potential regulatory mechanisms involved in temperature adaptation. Conclusion This study provides novel insights into the molecular basis of M. aeruginosa temperature adaptation by elucidating the interplay between growth, fatty acid metabolism, and gene expression regulation. The findings highlight the critical role of fatty acid metabolism in temperature adaptation and reveal coordinated regulation at the gene-transcript-metabolism level in response to temperature variations. These results contribute to a deeper understanding of cyanobacterial bloom dynamics and offer valuable knowledge for developing strategies to manage M. aeruginosa blooms in eutrophic water bodies.