Are Nutrients the Key Driver in Prompting Dominance of Toxic Cyanobacterial Blooms in a Sub-Tropical Reservoir?

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Burford, Michele

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Shaw, Glen

Bunn, Stuart

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2010
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Toxic cyanobacteria cause major problems, both for drinking and recreation, within water systems and bulk water storages, worldwide. Many investigations have been conducted to determine how, and why, they proliferate as well as why, and when, they produce toxins. A common assumption is that cyanobacteria grow in response to an increase in water column nutrient availability, but this is an oversimplification. In a sub-tropical reservoir (L. Samsonvale, South East Queensland, Australia), the toxic cyanobacterium Cylindrospermopsis raciborskii has been dominating the phytoplankton community in the summer months for many years. The reason for this is unknown. Lake Samsonvale typically has relatively low phosphorus (P) concentrations, relatively high nitrogen (N) concentrations and C. raciborskii can grow without significant nutrient inputs from the catchment or point sources. The relatively high N concentrations in L. Samsonvale mean that it is unlikely to be a key nutrient in promoting dominance of C. raciborskii. The low phosphorus (in particular the phosphate) concentrations on the other hand may suggest a reason for C. raciborskii dominance in L. Samsonvale. Studies of a non-toxic strain of C. raciborskii originally isolated from the northern hemisphere found that a rapid phosphate uptake rate and high phosphorus storage capacity was contributing to its dominance in a phosphate-limited reservoir (Istvánovics et al. 2000). The aim of this thesis was to characterise the relationship between phosphorus and C. raciborskii in L. Samsonvale. To achieve this, three levels of investigation were used: 1. Physiological studies at the species level; 2. Manipulative experiments at the phytoplankton community level; 3. Characterisation of C. raciborskii ecology at the whole of system level. The relationship between C. raciborskii and phosphorus was studied using a multilevel approach. Knowledge gained from this allowed detailed investigation of iii the relationship between the dominance of this species within the phytoplankton community of L. Samsonvale. Using continuous culture experiments, the phosphate uptake and storage capacity of two toxic Australian strains of C. raciborskii was determined. One of these strains was isolated from the reservoir of interest, L. Samsonvale. P dependent growth rate and toxin production were also quantified. Both strains of C. raciborskii had a high maximum phosphate uptake rate (450 – 600 μmol P mg C-1 d-1) with a relative low half saturation constant (0.64 μmol P L-1). This study suggests that C. raciborskii is capable of taking full advantage of any available phosphate that may be introduced (such as run off) or regenerated within the phytoplankton/bacterial community. The P dependent growth rates were similar for both strains of C. raciborskii with a maximum growth rate at the lowest concentration of P tested (0.03 μmol P L-1). Growth rates were lower overall than in other strains of C. raciborskii. When C. raciborskii cells were starved of P, they produced much more toxin than when they were grown in a nutrient sufficient environment. This indicates that toxin production may be related to a stress response. Some phytoplankton have been shown to produce alkaline phosphatase. This enzyme cleaves phosphate from organically bound forms, targeting esters, which can be taken up and used by the cell. Since C. raciborskii appears to proliferate in phosphate limited systems, its potential to secrete this enzyme, and whether it was capable of growth with an organically bound source of phosphate, were investigated. Alkaline phosphatase activity was detected and C. raciborskii was found to be capable of multiplying in a culture media containing only an organic form of P (glucose-6- phosphate, G-6-P). However, the maximum growth rate was lower (~0.13 d-1) when cells were grown in G-6-P compared to phosphate (~0.22 d-1) The ability of C. raciborskii to use: 1. Organic P; 2. Rapidly utilise phosphate; and 3. Grow at a maximum rate at relatively low phosphate concentrations, are likely to make C. raciborskii a dominant competitor in phosphate-limited systems. iv To determine whether C. raciborskii has a competitive advantage over other phytoplankton in the P-limited system of L. Samsonvale, in situ dialysis tube bioassays were used to test the phytoplankton response to nutrient addition. The dialysis tube bioassay is a novel approach aiming to minimise the confounding problem of artificial nutrient limitation associated with traditional closed bottle bioassays. Samples of the phytoplankton population were subjected to nutrient additions at four different times over a summer period, to test whether a change in phytoplankton species composition (with particular reference to C. raciborskii) could be seen after four days. In phytoplankton communities where the proportion of C. raciborskii was equal to, or above, 50% (biovolume), a statistically significant increase in C. raciborskii dominance occurred when phosphate was added as a daily spike at either of two concentrations (0.32 and 16 μM P). However, C. raciborskii dominance decreased when phosphate was constantly added in very high concentrations or when N and P are added together. From the bioassay experiments it can be inferred that C. raciborskii has a competitive advantage in L. Samsonvale due to its ability to rapidly take up phosphate. But, when the phosphate concentration is constantly high (>6.4 μmol P L-1), C. raciborskii loses this competitive advantage. Analysis of historical data has shown that there is no correlation between periodic nutrient inputs (e.g. rainfall) and an increase in C. raciborskii dominance. The mechanisms by which C. raciborskii is accessing phosphate within L. Samsonvale were therefore examined. One theory about how C. raciborskii is accessing phosphate in L. Samsonvale is that it comes from nutrient injections in the bottom waters caused by mixing the reservoir using artificial destratification. The concentration of dissolved organic phosphorus (DOP) may also provide C. raciborskii with available phosphate. To assess these two hypotheses, the nutrient concentration and phytoplankton cell concentrations throughout the water column were measured, both before and after artificial destratification. The DOP fraction was measured over a summer. Phosphate remained v below detection limits throughout the study, therefore the role of the destratifier in injecting phosphate into the water column was difficult to determine. A difference in phytoplankton distribution was noted with C. raciborskii being found at higher concentrations lower in the water column post destratification. In contrast, the other toxic species of cyanobacteria Microcystis aeruginosa present in substantial cell concentrations significantly decreased in cell concentrations after the destratifier was turned on. DOP was found to be a significant fraction (total mean 32%) of the total P in the water column of L. Samsonvale and may therefore provide an important source of P for C. raciborskii under low phosphate conditions. This study has shown C. raciborskii has adapted to the low concentrations of P in L. Samsonvale to gain a competitive advantage. Reservoir management, particularly in relation to nutrient loads, should take this into account, as efforts to reduce P loads may not lead to a decrease in C. raciborskii cell number or phytoplankton dominance.

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Thesis (PhD Doctorate)

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Doctor of Philosophy (PhD)

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Griffith School of Environment

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Toxic cyanobacteria

Lake Samsonvale reservoir

Water quality Queensland

C. raciborskii

Phosphorus

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