Iron-Regulated Cyanobacterial Predominance and Siderophore Production in Oligotrophic Freshwater Lakes

The frequency and intensity of cyanobacterial blooms (cyanoblooms) is increasing globally. Contrary to existing phosphorus (P) and nitrogen (N) paradigms describing cyanobloom proliferation in eutrophic (nutrient-rich) freshwater lakes, many of the recent cyanobloom reports pertain to oligotrophic (nutrient-poor) freshwater lakes with no prior history of cyanobloom occurrence. There exists a critical research need to re-visit existing conceptual models, identify regulating factors currently unaccounted for and improve our ability to effectively detect and measure cyanobacterial toxins (cyanotoxins) in lakes. Iron (Fe) is required in nearly all pathways of cyanobacterial macronutrient use, though its direct role in regulating cyanobacterial biomass is not well understood. The hypotheses tested were: (1) cyanobacteria will predominate in lakes when concentrations of bioavailable Fe are low; and (2) cyanobacteria overcome this Fe limitation using the siderophore-based Fe acquisition strategy to scavenge Fe providing a competitive advantage over other phytoplankton. It was also hypothesized that (3) the rainbow trout gill cell-W1 cytotoxicity assay (RCA) will be effective in assessing the cytotoxicity of natural lake water samples. Among 25 oligotrophic lakes studied in the Algoma Highlands of central Ontario Canada, the proportion of cyanobacteria was highest at low Fe availability (\u3c 1.0 × 10-19 mol L-1). Within this range of low Fe, hydroxamate siderophore concentration was positively correlated to cyanobacterial density (r2 = 0.77, p \u3c 0.001). Dissolved organic matter (DOM) had an overriding control on the relationship between siderophore concentration and cyanobacterial density, with densities highest where DOM concentrations were low (\u3c 5 mg L-1) and with a degree of humification (HIX) \u3c 5. These findings suggest labile DOM may be a source of Fe and/or siderophores, but refractory DOM may be a sink. The RCA successfully provided a measure of lake water toxicity that could not be reproduced using isolated cyanotoxin standards in the laboratory. These findings provide support for the critical role of Fe in regulating cyanobacterial biomass in lakes and represent the first record of siderophores in lakes in the Algoma Highlands of central Ontario. The RCA is sensitive to cyanotoxins in lakes and may be an important part of routine water quality biomonitoring programs