Metabolite diversity of Microcystis strains shows tight correspondence to genotype and may contribute to ecotype specificities.

Microcystis is one of the most common bloom-forming cyanobacteria colonizing freshwater ecosystems worldwide. This genus remarkably produces numerous bio-active accessory metabolites, which are believed to be potentially involved in different ecological and/or physiological processes. However, their genuine contribution to the evolutionary success of Microcystis blooms remains undetermined. To better depict the potential relationship between the local genetic diversity of blooming Microcystis populations and their respective associated chemical diversity, we conducted a joint genomic and metabolomic analysis of 65 Microcystis strains collected from various lakes in France and surrounding Western European countries. Interestingly, both core and pan-gene phylogenetic analysis place 57 of these strains in 11 distinct genotypes with at least 2 genomes, being widely distributed along the entire Microcystis phylogeny and presenting specific signatures of accessory metabolite biosynthesis. The direct chemical analysis of metabolite diversity produced by these strains, cultured under laboratory conditions, reveals the production of stable metabolite cocktails, with minimal variations over replication, growth phases and culture conditions. Remarkably, these strains belonging to 11 different genotypes correspond to 13 distinct chemotypes according to an accurate one-chemotype-for-one-genotype rule. Furthermore, these genotypes also appear distinguishable regarding their respective ecotoxicological traits and might be considered as specific toxico-ecotypes. Overall, our investigations reveal that the production of accessory metabolites constitute well conserved chemical traits across the different Microcystis genotypes, suggesting these molecules may be involved in key adaptive and selective processes, that still remain under-explored.