Award: OCE-1736629

Toxic cyanobacterial harmful algal blooms (CHABs) threaten freshwater systems worldwide, posing dangers including disruption of ecosystems, human illness, beach closures, and unsafe drinking water. This project conducted research to understand interactions between the microorganisms present in CHABs and the chemistry of the lakes they inhabit. In particular, it focused on the sources, fate, and effects of hydrogen peroxide, which may control the toxicity and microbial species present within these blooms. The overall goal of this project was to determine the influence of hydrogen peroxide on cyanobacterial community composition and toxicity. The research was carried out in Lake Erie, a source of drinking water for 11 million people that is threatened by CHABs that are dominated by Microcystis, a globally distributed cyanobacterium that produces the toxin microcystin. Field work was conducted on ~weekly research cruises from June to October in 2018-2022 in collaboration with the Cooperative Institute for Great Lakes Research and the NOAA Great Lakes Environmental Research Laboratory. This produced a valuable dataset on the seasonal and interannual variability of hydrogen peroxide concentrations and microbial community composition and also provided samples for laboratory experiments to quantify the sources, fate, and effects of hydrogen peroxide. Hydrogen peroxide concentrations frequently reached levels that are known to inhibit growth of cyanobacteria and other microorganisms, consistent with the idea that hydrogen peroxide has an important effect on microbial communities. Results from experiments indicate that hydrogen peroxide was produced by both photochemistry (in which sunlight reacts with colored dissolved organic matter) and biological processes (photosynthesis and respiration). Rates of hydrogen peroxide production varied across space (including nearshore to offshore) and time (within and between years). Photochemical production of hydrogen peroxide depended on the composition of colored dissolved organic matter, which varied spatially and temporally. Biological production of hydrogen peroxide was largely dependent on light and small particles and was correlated with bacterial community composition, consistent with an important role of bacterial processing of organic carbon molecules generated during photosynthesis. Bacteria were also responsible for the degradation of hydrogen peroxide through peroxidase and catalase enzymes. Overall, these results show that bacteria exert strong control over hydrogen peroxide concentrations and influence the cyanobacterial community composition in Western Lake Erie. Genomic methods were used to investigate the interactions between Microcystis and bacteria. Microorganisms physically associated with Microcystis were distinct from surrounding bulk water and correlated with sampling time and Microcystis strain, suggesting that environmental conditions or symbiotic interactions strongly influence Microcystis-associated microbial communities. Results also indicated the exchange of metabolites between heterotrophic bacteria and Microcystis. Taken together with evidence that the heterotrophic bacteria degrade hydrogen peroxide, thus protecting Microcystis from oxidative stress, these results suggest a mutualistic symbiotic relationship between Microcystis and these "helper" bacteria. Results were integrated into a model that was used to predict the outcome of current nutrient management practices for Western Lake Erie. The results of this modeling study suggest that the proposed reduction of phosphorus inputs into Western Lake Erie could result in an increase in the concentration of microcystin due to an increase in the availability of nitrogen and light, which produces hydrogen peroxide. Both high nitrogen availability and hydrogen peroxide are thought to stimulate toxin production by favoring toxin-producing strains of Microcystis. However, subsequent lab experiments and genome sequencing also showed that Microcystis strains are highly diverse and that hydrogen peroxide does not always favor toxin-producing strains of Microcystis; more research is needed to understand this complexity and update models accordingly. Results of this project were described in 9 peer-reviewed scientific publications, with at least two more forthcoming, and in numerous oral presentations at scientific conferences and to various stakeholders. These results have improved our understanding of how environmental conditions shape production of toxins from harmful algal blooms that threaten drinking water supplies. Thus, there is a potential impact of this research on the important societal issues of water quality, drinking water security, and harmful algal blooms. Overall, the project trained and provided professional development opportunities for 5 graduate students, 11 undergraduate students, 3 postdocs, and 3 technicians, including training in field and laboratory methods as well as bioinformatics and omics analysis. Research was integrated into undergraduate and graduate coursework at the University of Michigan as well as outreach to increase diversity in the earth sciences by involving women and underrepresented minorities in K-12 as well as college and adult educational settings. Last Modified: 04/30/2023 Submitted by: Gregory J Dick