Early Seasonal Increases and Persistence in Relative Abundance of Potentially Toxic Cyanobacteria: Concerning Impacts of Extended Ice-Free Periods in Northern Temperate Lakes

Cyanobacteria threaten public and ecosystem health globally through the production of secondary metabolites including potent toxins, and disruption of water treatment processes. Warmer water temperatures and high nutrient availability are key characteristics associated with the occurrence of cyanobacteria. There is typically concern of cyanobacteria blooms (e.g., visible biomass accumulations) occurring in the summer season of eutrophic systems. However, in this study, the proliferation of cyanobacteria in lakes across all seasons and in absence of visual biomass indicators of bloom condition was observed in three oligotrophic lakes of the Turkey Lakes Watershed (TLW) in Ontario, located within a sugar maple dominated forest on the Canadian Shield. Almost 40 years of ice phenology data showed that rising temperatures have led to significantly longer ice-free periods and aquatic growing seasons in TLW. Warming is especially evident in the autumn, with the onset of ice-on periods commencing significantly later in the year. Cyanobacterial communities in three interconnected temperate, oligotrophic lakes were characterized over an 18-month period from July 2018 to January 2020 (across 10 synoptic sampling events) using amplicon sequencing of the V4 region of the 16S rRNA gene. During the winter, there was low abundance or occasional absence of cyanobacteria; however, a non-photosynthetic basal lineage of cyanobacteria (Melainabacteria) was present during periods of ice cover. Notably, photosynthetic populations reappeared in the water column immediately following the loss of ice-cover--they were especially abundant in lakes with surficial geology and lake morphometry that favor greater availability of fine sediment and associated nutrients. Thus, this collective analysis demonstrates that the convergence of key abiotic and biotic factors--climate forcing of hydrological and biogeochemical processes, and intrinsic landscape features--enable increases in the relative abundance of potentially toxic cyanobacteria within the temperate forest biome of Canada over increasingly longer periods of time.