Beyond Microcystins: Uncovering the Drivers and Dangers of Co-Occurring Cyanobacteria and Cyanopeptides in Eutrophic Great Lakes Basins
Year: 2025
Type: dissertation
Abstract: Toxic cyanobacterial harmful algal blooms (cyanoHABs) are proliferating in freshwater ecosystems due to excess nutrient inputs, causing eutrophication and threatening human, wildlife, and ecosystem health. These blooms are dominated by cyanobacteria with diverse repertoires of biosynthetic gene clusters (BGCs) that encode for the synthesis of secondary metabolites, bioactive compounds that confer functional advantages beyond growth or reproduction such as defense or competition. Among these are cyanopeptides, a broad class of peptidic metabolites with diverse bioactivities, including disruption of enzymatic and cellular functions. Microcystins, a hepatotoxic subset of cyanopeptides, are classified as cyanotoxins due to their potent toxicity to humans and wildlife. While monitoring often focuses on cyanotoxins, other cyanopeptides, such as anabaenopeptins, may also contribute to bloom toxicity. The cosmopolitan bloom-forming genera Microcystis and Dolichospermum frequently co-occur in freshwater bodies and dominate different bloom phases, each encoding numerous BGCs for both known and uncharacterized metabolites. Intraspecific variability in secondary metabolite production shapes bloom toxicity and drives ecological interactions across trophic levels during cyanoHABs. However, the temporal dynamics, environmental drivers, and health risks of individual and co-occurring cyanopeptides beyond microcystins remain poorly defined. Emerging evidence suggests these compounds may act synergistically, amplifying their toxic effects towards humans, wildlife, and aquatic organisms. To address these gaps, this thesis integrates multi-omics (metagenomics and metabolomics) and toxicological approaches to investigate the dynamics, drivers, and understudied risks of natural cyanoHAB communities and their bioactive metabolites from two geographically distant but similarly eutrophic Great Lakes basins, western Lake Erie (WLE) (USA) and the Winam Gulf of Lake Victoria (Kenya). Chapter 2 investigated the temporal patterns of Microcystis and Dolichospermum dominance, BGC abundance, and cyanopeptide production in WLE. Lower temperatures and nitrogen availability were most closely associated with late season Dolichospermum dominance. Beyond taxonomic shifts, co-varying modules of BGCs and their associated cyanopeptides exhibited distinct temporal patterns, revealing biosynthetic successions across the bloom season that extended beyond microcystins. The cyanopeptide phases were linked to changes in the environment, including eDNA detection of grazers, dissolved organic matter composition, and nitrogen availability, suggesting both top-down and bottom-up controls on cyanoHAB ecology and toxicity. Chapter 3 characterized the cyanobacterial community and its BGC repertoire in the Winam Gulf of Lake Victoria using metagenomic sequencing. Extensive spatial variation in cyanobacterial composition was observed, with Dolichospermum as the dominant genus during most large bloom events, while Microcystis dominated non-visible blooms in turbid regions at the time of sampling. Microcystin production was attributed specifically to Microcystis, resolving a long-standing ambiguity in the region. Additionally, over 300 novel cyanobacterial BGCs with unknown products were identified, revealing a vast and previously unexplored chemical landscape. Chapter 4 evaluated the toxicological effects of two commonly co-occurring cyanopeptide classes, anabaenopeptins and microcystins, on human lung, kidney, and liver cell lines. Varying synergistic interactions between the cyanopeptides were observed across all three cell lines, highlighting the importance of investigating mechanisms of toxicity for co-occurring metabolites. Toxicity assays using Microcystis culture extracts demonstrated that microcystin and anabaenopeptin concentrations alone poorly explained the variation in cytotoxicity across cell lines. This suggests that additional compounds or interactive effects between metabolites may play a more substantial role in overall toxicity. Overall, these findings underscore the need to expand research, monitoring, and management efforts beyond microcystins to better capture the complexity of cyanoHAB toxicity and its risks to public and ecological health.
DOI: 10.7302/28111
Author: Hart, Lauren
Language: English
Subfield: Environmental Chemistry
Field: Environmental Science
Domain: Physical Sciences
Open Access status: green
OpenAlex ID: W7124754945
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