Linking Cyanobacterial Genomes to Toxin Dynamics Through Genome-Resolved Metagenomics

Global climate change and nutrient pollution from agricultural systems increase cyanobacterial bloom and toxin release events, and will pose a significant concern for public health and safety over the coming decades. Many in situ studies have focused on environmental, chemical, and microbial community changes and their impact on cyanobacterial bloom frequency and toxicity. However, fine-scale genetic differences in the genomes of bloom-forming cyanobacteria may also impact the quantity and types of toxins produced. Metagenomic approaches allow resolution of strain- and nucleotide-level changes within microbial communities and can improve our understanding of the factors that affect cyanobacterial bloom dynamics and toxicity. Here, we conduct a metagenomic analysis of the bloom-forming cyanobacterial genus Microcystis across a 10-month lake time series from the Valle de Bravo Reservoir, to assess how within-genus genotype-level changes are linked to intracellular toxin production and extracellular toxin release, as well as how single nucleotide variation may affect the types of microcystin toxins produced. Our results demonstrate that the abundances of both toxigenic and non-toxigenic Microcystis genotypes are significantly related to microcystin toxin concentrations. In addition to these genome-wide ("strain"-level) associations, specific single nucleotide variants show strong associations with chemical variants of microcystin in the environment. Our work highlights the importance of fine-scale analysis of microbial community composition for understanding cyanobacterial bloom dynamics and toxin production.