Bioaccumulation of microcystins in terrestrial food plants and the development of novel sorbents for monitoring microcystins in irrigation water

Abstract

In the past few decades, South Africa's freshwater resources have faced a severe problem of eutrophication and frequent occurrence of cyanobacterial blooms. This is of great concern since some of the cyanobacteria species have the potential to produce cyanotoxins that pose health risks to livestock and humans. Recently, there have been evidence of the toxic effects of microcystins (MCs) and cylindrospermopsin (CYN) on terrestrial plants including plants used for food. Ever since, the use of surface waters contaminated with cyanobacteria and cyanotoxins for agricultural purposes has been receiving growing attention. In hypereutrophic waters, such as commonly found in impoundments around major metros in South Africa, MCs co-exist with other pollutants such as metals and Linear Alkylbenzene Sulfonates (LAS), and these can have synergistic effects on the crops irrigated by such waters and exacerbate the human health risks posed by MCs. The current study investigated the bioaccumulation and effects of MCs on food plants, developed and evaluated the use of crosslinked chitosan (sorbents) passive samplers to monitor the bioavailability of MCs in water intended for irrigation. The findings are presented in six major sections. The first section detailed literature on the impacts of cyanotoxins on food plants with emphasis on the South African context. The reviewed literature demonstrated the potential of exposure of irrigated plants to multiple stressors such as MCs, LAS, metals, endocrine disrupting chemicals (EDCs) and high levels of dissolved salts around South Africa’s urban provinces. The literature also showed that South Africa lacks research on human exposure to cyanotoxins via irrigated crops and regulations to manage emerging pollutants such as MCs in irrigation water. Such lack of data and policies thus prompts an urgent need for local evidence-based research to guide policies and guidelines on cyanotoxins in irrigation water, food plants and, water used for livestock. In the second part of the thesis, the bioaccumulation of MCs in parts of the plants Brassica oleracea (cabbage) and Solanum tuberosum (common potato) was investigated in pot-culture experiments. Water used to irrigate the plants was collected from Roodeplaat Dam and had total MCs ranging from 0.12–2.84 μg L-1. The pH for the water was slightly alkaline (pH 7.29±0.71 to 10.03±0.29) whilst the Electrical Conductivity (EC) ranged from 296.67±13.87 to 878.67±42.44 μS cm-1. The findings showed that the two plants can bioaccumulate MCs to concerning levels when irrigated with water derived from Roodeplaat Dam. MCs accumulation levels in the two tested plants ranged from 0.00142 to 0.136 mg kg-1 DW for individual MC congeners. These findings demonstrated that terrestrial food crops can bioaccumulate MCs to levels that can pose human-health risks. v The third part of the thesis investigated the uptake and accumulation of metals Al, Mn and Sr in distinct parts of the plants Brassica oleracea and Solanum tuberosum in the presence of the anionic surfactant LAS. Pot-culture experiments were conducted to assess the effect of LAS on the accumulation of the three metals by watering the plant with Roodeplaat dam water containing 3.48 mg L-1 of LAS and Mn (0.257mgL-1), Al (0.6mgL-1) and Sr (0.16mgL-1). Findings indicated that the presence of LAS, in the irrigation water, did not enhance the uptake of Sr, Mn and Al by the two plants as demonstrated by the comparable levels of the metals in plants exposed to the metals in presence and absence of LAS. The fourth section investigated the uptake and the accumulation of MCs in distinct parts of the plants B. oleracea and S. tuberosum in the presence of the anionic surfactant LAS. Pot-culture experiments were conducted with the two plant species watered Roodeplaat dam water containing 3.48 mg L-1 of LAS and MCs with mean concentrations of: MC-LR: 10.47±3.879; MC-RR: 6.158± 4.127 and MC-YR: 8.160 ± 2.544 μg L-1. Findings indicated that the presence of LAS in the irrigation water at the levels investigated did not enhance the uptake of MCs by the two plants, even though in some cases the levels of MCs bio-accumulated by the two plants exceeded WHO-recommended tolerable daily intake (TDI). These findings imply that, the tested levels of LAS and MCs did not have any synergic effects on the two plant species. The fifth part of the thesis focused on the synthesis of a composite of glutaraldehyde-crosslinked chitosan and multiwalled carbon nanotubes (ChMWCNT) for application in the Solid Phase Adsorption Toxin Tracking (SPATT) for monitoring MCs in freshwaters. Batch experiments were conducted to evaluate the adsorption efficiency of the composite. The composite was found to be efficient in adsorbing MC-LR showing 97% removal and maximum adsorption capacity of 4.639 μg g-1 under optimized conditions of 5 μg L-1 of MC-LR, adsorbent dose of 0.03g 5 mL-1, and contact time of 30 mins. For desorption, 100% methanol was most effective, with efficiency of 84.71 %. When applied for the adsorption of MCs in raw dam water, the composite was saturated within two days of exposure and effectively adsorbed and desorbed three congeners tested in the order MC-LR>MC-RR>MC-YR. The last part of the thesis evaluated the field applicability of the newly synthesised glutaraldehyde crosslinked chitosan hydrogel (ChGLA) and the composite of glutaraldehyde-crosslinked chitosan and multiwalled carbon nanotubes (ChMWCNT) in a SPATT bag format and compare them to the commonly used DIAION HP20 resin. The constructed SPATT samplers were deployed in canals and farm dams around Roodeplaat and Hartbeespoort Dam sites. The findings elucidated a good vi correlation between the MCs detected by the two newly synthesized sorbents (ChGLA and ChMWCNT) and grab samples. The detected total MCs for the ChGLA samplers were: 0.003 and 1.742 (μg g-1) and for the ChMWCNT samplers 0.006 and 3.300 (μg g-1) (lowest and highest respectively). In conclusion, the two plants were found to accumulate MCs to levels that can pose human-health risks when water derived from the Roodeplaat Dam was used for irrigation. The effects of other pollutants such LAS found in hypereutrophic water bodies on the uptake and accumulation of MCs in food plants was for the first times tested on terrestrial food plants. The findings showed that the presence of LAS had no impact on the uptake of MCs and heavy metals such as Al, Mn and Sr. For the first time, chitosan-based sorbents were synthesized and applied in SPATT for MCs. The use of the chitosan sorbents demonstrated a lot of promise for the monitoring of MCs in water and can possibly be used as an early warning sign for the presence of MCs in irrigation water derived from eutrophicated impoundments in South Africa.