Date of Award

Spring 2021

Project Type

Thesis

Program or Major

Biological Sciences

Degree Name

Master of Science

First Advisor

James F Haney

Second Advisor

Jeffrey Schloss

Third Advisor

Todd Guerdat

Abstract

Cyanobacteria are the oldest known photosynthetic organisms on Earth. They are found in a wide range of habitats worldwide but have recently become an increasing issue in both freshwater and marine systems due to anthropogenic eutrophication and climate change. Cyanobacteria produce an array of toxins harmful to wildlife and humans, some of which have been found to accumulate in plant and animal tissues. Microcystins (MCs) are the most common toxins produced, occurring in 40 – 75% of cyanobacteria blooms worldwide. They are highly stable, water and fat soluble, cyclic heptapeptides that cause acute toxicity in the liver by the inhibition of cellular protein phosphatase 1 and 2a, resulting in the breakdown of hepatic tissues. MCs are also tumor promotors and have been linked with non-alcoholic liver disease with long-term exposure. β-methylamino-L-alanine (BMAA) is a non-protein coding amino acid that acts as a neurotoxin, is produced by all groups of cyanobacteria, and has been linked to neurodegenerative disorders such as Amyotrophic Lateral Sclerosis (ALS), Alzheimer’s, and Parkinson’s diseases. While many studies have reported the accumulation of MCs by various crop plants after exposure to high concentrations of toxin via irrigation water, relatively few studies have investigated such accumulation of BMAA, and none have investigated aerosolized cyanotoxins as a possible route of exposure. In this study, lettuce and radish seedlings were placed in hydroponic systems under small low-tunnels on the shore of Lake Attitash in Amesbury, MA and exposed to low levels of natural, lake-derived cyanotoxins in four treatments via lake water in the hydroponic reservoirs and deposited aerosols emitted from the lake. After three weeks, plant tissues were collected, separated, and analyzed for MCs and BMAA via Enzyme-Linked Immunosorbent Assay (ELISA) analysis. In a second experiment, particulate and dissolved fraction lake aerosols were collected in one open and one sealed/HEPA filtered tunnel using modified Compact-Lake-Aerosol-Monitors (CLAMs) to quantify aerosols emitted from Lake Attitash and to determine if aerosols had penetrated the filtered tunnel treatments. The average concentration of MCs and BMAA in water from Lake Attitash throughout the three-week experiment was 78.9 ng MC L-1 ± 7.06, and 350.0 ng BMAA L-1 ± 75.0. Lettuce plants had overall average dry weight MCs concentrations of 7.16 ± 0.38 ng g-1 in leaves, 5.65 ± 0.21 ng g-1 in stems, and 3.59 ± 0.77 ng g-1 in roots. Overall average MCs concentrations in radish tissues were 10.39 ± 1.20 ng g-1 in leaves, and 3.83 ± 0.23 ng g-1 in roots. BMAA concentrations displayed a similar trend, with dry weight concentrations of 7562.39 ± 1148.31 ng g-1 in lettuce leaves, 4018.54 ± 269.43 ng g-1 in lettuce stems, 551.88 ± 96.39 ng g-1 in lettuce roots, 4710.13 ± 490.27 ng g-1 in radish leaves, and 3223.60 ± 557.46 ng g-1 in radish taproots. This trend of higher toxin concentrations in the upper tissues of the plants is generally the opposite of what has been reported previously in the literature. CLAM samples collected in the early fall of 2017 had average particulate and dissolved MCs aerosol concentrations of 2.60 pg m-3 and 10.16 pg m-3, respectively, for an average total aerosol concentration of 12.76 pg m-3. The total average BMAA aerosol concentration was 1176.91 pg m-3, which was comprised of 630.86 pg m-3 dissolved and 546.05 pg m-3 particulate aerosols. This represents the first report of concurrent BMAA and MCs aerosols from the same water body, and one of the first reports on the concentration of BMAA in lake aerosols. Overall, there were few differences in toxin concentrations in each of the plants between treatments, and those that were present indicated that cyanotoxin aerosols were likely a significant source for accumulation in this system. Lettuce had significantly higher MCs and BMAA concentrations in the tissues exposed to aerosols (leaves and stems) compared to the roots, opposite the trend generally observed in the literature (Two-way ANOVA, n = 36, p < 0.001). In addition, there were no significant differences between the lake water and tap water treatments for lettuce leaf and stem tissues (two-way ANOVA, n = 36, p = 0.068), though lettuce roots from the lake water treatments had a higher average MCs concentration than roots from the tap water treatments (one-way ANOVA, n = 12, p = 0.019). For radishes, the leaves from the open tunnel/tap water treatment had a higher MCs concentration than the other three treatments (two-way ANOVA, n = 12, p = 0.0037), and interestingly, the taproot tissues from the lake water treatments had a lower average MCs concentration than those from the tap water treatments (two-way ANOVA, n = 12, p = 0.036). In conclusion, this study demonstrated that accumulation of lake-derived cyanotoxins by crop plants can occur from lakes with relatively low levels of toxins, and that aerosols, especially the dissolved fraction, are likely playing an important role in the contamination of crops. However, further research on lake-derived cyanotoxin accumulation in crops via exposure to aerosols and irrigation water is needed to evaluate this potential risk for low-level, long term exposure to these toxins.

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