Genomic Identification and Characterization of Saxitoxin Producing Cyanobacteria in Western Lake Erie Harmful Algal Blooms

Abstract

Saxitoxins (STXs), a group of closely related neurotoxins, are among the most potent natural toxins known. While genes encoding STX biosynthesis have been observed in Lake Erie, the organism(s) responsible for producing STXs in the Laurentian Great Lakes have not been identified. We identified a full suite of STX biosynthesis genes in a Dolichospermum metagenome-assembled genome (MAG). The content of sxt genes suggest that this organism can produce STX, decarbamoyl and deoxy-decarbamoyl saxitoxins, and other congeners. The absence of sxtX indicates this organism is unable to produce neosaxitoxin, a potent congener. However, a distinct, lower abundance sxt operon from an unidentified organism did contain sxtX, indicating neosaxitoxin biosynthesis potential. Metatranscriptomic data confirmed STX biosynthesis gene expression. We also recovered highly similar Dolichospermum MAGs lacking sxt genes, implying gene loss or horizontal gene transfer. sxtA was detected by quantitative polymerase chain reaction during 47 of 76 sampling dates between 2015 and 2019, demonstrating higher sensitivity than metagenomic approaches. sxtA gene abundance was positively correlated with temperature and particulate nitrogen:phosphorus ratio and negatively correlated with ammonium concentration. All Dolichospermum MAGs had genes required for nitrogen fixation. Collectively, this study provides a foundation for understanding potential new threats to Lake Erie water quality.