Natural Microcystis populations reveal the presence and abundance of truncated mcy operons and microcystins: a continuing source of research for water quality research

CyanoHABs are often dominated by Microcystis aeruginosa, which produce microcystins, a class of hepatotoxins that have been studied since the 1950s and have been responsible for drinking water crises in recent years. Microcystin toxicity is influenced by distinct structural elements across related molecules encoded by variant mcy operons. Currently over 270 structural variants have been identified through mass spectroscopy. Here, we present findings of a novel, truncated mcy operon that is at times the most abundant genotype across multiple years of sampling in Microcystis populations of Lake Erie. The partial operon contains truncated mcyA, complete mcyB-C, and is missing mcyD-J genes. Metatranscriptomic analysis revealed that this truncated operon is also transcriptionally active. Furthermore, it was predicted to synthesize tetrapeptide molecules. A compound with the same mass as the predicted tetrapeptide was detected in cyanoHAB samples from western Lake Erie. Current methods fail to detect this molecule or genes responsible for its biosynthesis. The persistence and dominance of this mcy genotype in Lake Erie, which has been intensively studied for decades, suggests that such novel genotypes and compounds may be common in natural populations and highlights the utility of shotgun metagenomics to detect novel and potentially toxic compounds produced by cyanobacteria.