Factors affecting the growth and toxin content of key cyanobacteria species in a changing world.

Abstract

Cyanobacteria are ubiquitous in marine, freshwater and terrestrial ecosystems. In freshwaters, under certain conditions cyanobacteria can form super abundant blooms. Many cyanobacteria taxa produce secondary metabolites, amongst these are many potent toxins (cyanotoxins), which can present substantial risks to human, animal and environmental health. Where risk mitigation strategies are implemented, they are usually based on cyanobacteria cell counts. However, not all cyanobacteria taxa produce toxins, and the drivers for cyanotoxin production and their eco- physiological role remain unknown. Thus, risk management strategies may over or under estimate risks. A predicted increase in the incidence of toxin producing cyanobacterial blooms has been proposed, linked to climate change driven water temperature increases and eutrophication. Consequently, better understanding of factors modulating cyanobacterial toxicity would assist in more proactive and effective water management. In the first part of this study the effects of biotic and abiotic factors on the growth and toxicity a recently isolated strain of Microcystis sp. (CCAP1450/17) and M. aeruginosa reference strain (PCC7806) were examined. Strains responded similarly under controlled laboratory batch culture systems. Highest cell densities and growth rates were observed at medium light intensity (36 μmol of photons m-2 s-1) compared to high (117 μmol of photons m-2 s-1) and low (15 μmol of photons m-2 s-1) light intensities. Nitrogen was an obligate requirement for microcystin production, but phosphorous was not, indicating that nitrogen eutrophication conditions (caused by agricultural run- off etc) would increase the risk of toxic blooms. Toxin (microcystin) concentrations were positively correlated with cell density, but microcystin synthesis was independent of growth rates under nitrogen replete conditions. Furthermore, smaller cells contained higher levels of toxins. Cellular microcystin content was significantly higher at 20°C compared to 25 & 30°C questioning the paradigm that increased water temperatures (caused by climate change) will favour toxic bloom formation. Although the role of microcystin is not clear, these data indicated that under nitrogen abundant conditions microcystins may perform an eco-physiological function, which is reduced under nitrogen deprivation and/or when cells are rapidly dividing. In the second part of the study time series monitoring of cyanobacteria taxa, toxin concentrations and a range of environmental parameters was undertaken in two connected freshwater reservoirs over a twelve-month period. Cyanobacterial cell counts exceeding UK threshold levels of >20,000 cells mL-1 were recorded on four occasions. Toxins were detected in both reservoirs, concentrations were significantly higher in lake 2 (not stocked with fish) and did not correspond with highest levels of Microcystis cells, indicating that cyanobacterial species other than Microcystis were producing microcystins. Microcystin levels did not exceed the WHO medium health threshold of 20 µg L-1 although low threshold values (1.0 µg L-1) were detected in 16% of samples. Monitoring data indicated complex bottom-up and top-down control mechanisms in the moderation of cyanobacterial taxa abundance and population structure, the latter potentially mediated by the presence of omnivorous fishes. Application of basic general linear modelling to the dataset indicated that approximately 60-65% of the variability could be explained by combined independent abiotic and biotic variables indicating the future applicability of this approach. These results confirmed complex interactions between biotic and abiotic factors in both laboratory and field conditions but were broadly suggestive of additive effects with respect to microcystin production. Although the functional role of microcystins remains unclear it was considered possible that microcystins perform an eco-physiological function, perhaps conferring an advantage over non-toxic strains under nitrogen rich conditions. In environmental monitoring multiple species of cyanobacterial were implicated in toxin production, but cell numbers alone were not directly proportional to toxin levels supporting the proposition that management strategies based on cell counting alone may not be indicative of risk. Trophic relationships that influence cyanobacterial population dynamics and toxin production require further study to generate data to inform predictive models, but this series of studies suggested several avenues for further study which will provide water quality managers with improved tools to enable efficient, active management of water bodies.