Abstract
In the last few decades, there has been a growing interest in the occurrence of cyanotoxins and their potential toxicity in the aquatic environment. However, the used of dried toxic cyanobacteria cells as fertilizer or the used of surface water contaminated with cyanotoxins for agricultural crops irrigation can be source of soil contamination. In addition, surface waters presenting dense toxic blooms of cyanobacteria and used for agricultural practices are not controlled and are often used without prior treatment. Once in soil, cyanotoxins may be transported again to water bodies by leaching, runoff and drainage processes or can be accumulated in soils and, therefore, may cause contamination of vegetation by absorption from soils or by surface pollution of plants. In addition to possible effects on human health, elevated levels of cyanotoxins in soils can negatively affect plant vigour, animal health, microbial processes and overall soil health. Consequently, the focus of this chapter of soil contamination is cyanotoxins as contaminants of emerging concern in the soil, identifying sources of contamination, determining their fate and effects in the soil, and understanding their bioaccumulation in agricultural plants used for feed and food and consequences on animal and human health.
Keywords
- cyanotoxins
- microcystins
- soil
- fate
- phytotoxicity
- plant
- bioaccumulation
1. Introduction
The occurrence of toxic cyanobacterial blooms has become increasingly frequent throughout freshwater bodies in the world. To date, factors identified as contributing towards their global expansion included increased nutrient inputs, transport of cells or cysts via anthropogenic activities and/or migratory birds, increased aquaculture production and/or overfishing, altering food webs and permitting harmful species to dominate algal communities [1, 2]. It has also been shown that an increase in surface water temperatures and CO2 concentrations due to changing global climate could play a role in the proliferation of cyanobacterial blooms [3–6] and may also affect the strain composition within a cyanobacterial community and consequently change the concentration of cyanotoxins, such as microcystins [7, 8]. The problems associated with cyanobacterial blooms in fresh waters are diverse, from the environment asphyxiation due to excessive consumption of oxygen to purely aesthetic problems in recreational areas when the blooms are a colourful and often smelly scum on the surface of the water [9]. To these problems possibly affecting the economic development of specific areas, productions of cyanotoxins as secondary metabolites can represent a human and animal health threat [10]. Humans can be indeed exposed to cyanotoxins through both direct routes, including contamination of drinking and recreational waters, and indirect routes, including food supplements made from cyanobacteria or through consumption of contaminated food after toxin accumulation in fish, shellfish and other aquatic organisms, as well as in vegetables after using contaminated water for irrigation [11]. In the case of use of surface waters contaminated by cyanotoxins for the supply of drinking water, the potential health risks are managed at the level of the treatment station. In general, a strengthening of clusters of treatment and a complete operation and correct of this station would avoid any risk of contamination of the drinking water [12–20]. By contrast, the raw water used in irrigation often comes from a natural water body or an artificial pond for agricultural purposes and is not subject to any control or supervision. Consequently, the presence of cyanotoxins in irrigation water may cause toxic effects in the biological activity of the soil and in edible plants presenting therefore, a threat to animals and humans health (Figure 1). In fact, many studies have shown that the presence of microcystins in the irrigation water can have a considerable impact on the germination, growth and development of cultivated plants (reviewed in Ref. [10]). However, the fate of these toxins in the soil and their effects on the microfauna (protozoa, nematodes) and the microflora (bacteria, fungi and algae) of cultivated soils are scarce. This chapter aims to provide a current description of knowledge of cyanotoxins present in the irrigation water and their effects on soil and consequences on animals and public health.
2. Cyanotoxins and their producers
Some cyanobacteria species belong essentially to the genera
3. Sources and occurrence of cyanotoxins in the soil
The main source of contamination of soils by cyanotoxins is by using cyanotoxin-contamined water for agricultural purposes. Among the cyanobacterial toxins, microcystins are the most widespread group with microcystin-LR (MC-LR) the more toxic and the main congener detected in freshwaters [10]. Recently, concerns are also focused in the increasing occurrence of the cytotoxic cylindrospermopsin in temperate areas [52]. However, cyanobacterial neurotoxins are less reported in the literature and studies regarding their effects on organisms of soils and plants are relatively scarce. The concentrations of microcystins in the surface water are generally comprised between 1 and 100 µg L−1 [10] and the use of this microcystin-contaminated water for agricultural purposes has already been reported in several countries such as Morocco [53], Finland [54], Spain [55], New Zealand [56], Algeria [57], Australia [58], Tunisia [59], Turkey [60], Saudi Arabia [61], India [62], China [63] and Guatemala [64]. In addition to the contamination of soils by dissolved cyanotoxins and with the strong occurrence of cyanobacterial blooms worldwide, a strong quantity of cyanobacterial biomass (from thousand to million tons) is removed from water and discharged directly into croplands and forest land without another treatment [65]. This alternative represents a possible source of soil pollution with cyanotoxins. Another source of soil contamination by cyanotoxins consists of direct application of cyanobacterial biomass as an organic fertilizer as in China [66, 67]. In fact, since 1970s, the cyanobacteria were known for their interest in rice culture, as a biofertilizer. In wetland rice and wheat crops, free living cyanobacteria allowed nitrogen fixation to supplement soil nitrogen [68–70]. Cyanobacterial and rhizobacterial associations are used with the objective to increase soil fertility and crop yields, but the cyanobacteria and their secondary metabolites represent also interesting properties and can be involved as natural biocide or bio-control agents (see review in Ref. [71]). In a recent study Han et al. [72], they related the use of algae waste as an organic fertilizer after composting. This process can allow the degradation of 90–95% of the total microcystins containing in cyanobacteria between 1 and 35 days [73, 74]. The microbial degradation of cyanotoxins, during composting, may be due to the diversity of microorganisms present, the conditions of composting and the type of cyanotoxins present in the bloom, as observed for microcystins by Dawson [75] and Kormas and Lymperopoulou [76]. In addition, several studies reported that the presence of cyanotoxins in
4. Fate and transport of cyanotoxins in agricultural systems
4.1. Persistence in the soil and adsorption in particles
The most abundant cyanotoxins, microcystins, have a cyclic structure that provides a high chemical stability in the environment. Once these toxins are present in the soil, they can be removed according to various processes such as photochemical degradation by UV and biodegradation by some bacteria species [10, 80–84]. The photochemical degradation of microcystins can last from 2 to 6 weeks [85, 86] in freshwater. But in the soil, this process was not studied, however as observed in water it depends on the adsorption on soil particles that is more important than in water. In fact, numerous studies on sediments and soil particles showed that the adsorption induced a diminution of photochemical degradation of microcystins [83]. The time of total degradation of MC-RR in cropland should be about 6 days according Bibo et al. [87], whereas Chen et al. [67] founded a relatively long time of microcystins persistence with a half-life ranging between 6 and 18 days. Another study, where the scums of
4.2. Transport and uptake into biota and infiltration in groundwater
As described above regarding the microcystins adsorption in cropland soils, it is suggested that the adsorption of these toxins is generally low, which can therefore potentially result in their higher bioavailability for plants and the groundwater contamination due to infiltration into the soil. Consequently, Eynard et al. [96] suggested that the soil was unable to protect groundwater contamination by microcystins. Chen et al. [67] reported that microcystins can migrate from the surface to deeper layers of the soil following precipitation, leading to possible groundwater contamination. In a recent study, Corbel et al. [93] showed that when the radiolabeled 14C-MC-LR was introduced in a column of silty-sand agricultural soil, it underwent a weak microbial mineralization under aerobic conditions and therefore the large amounts of the toxin remained in soil aqueous extracts. In addition, the authors reported that the lixiviation of this toxin by CaCl2 was even stronger than soil application was recent. These results were confirmed by other environmental measures, where microcystins were found in groundwater [61, 65]. For example, Chen et al. [65] found a concentration of 2.5 µg L−1 in lixiviate water that was higher than the WHO recommendation in drinking water (1 µg L−1). The risk associated with the underground stock in water is the long-time persistence of toxins, in result of low microbial degrading activity. In fact, Holst et al. [97] did not detect any degradation of microcystins in groundwater maintained under oxic and anoxic conditions after a 100-day period. The toxins present in the soil solution are also available for soil organisms’ uptake such as plants. For example, Pflugmacher et al. [98] demonstrated a rapid uptake of 14C-MC-LR by aquatic plant (
5. Impacts of cyanotoxins on soil organisms
5.1. Microorganisms
Secondary, metabolites produced by cyanobacteria seem to have several activities as antiviral, antifungal and antibacterial [71]. In aquatic environments, several studies revealed an inhibition of bacterial growth after 8 days of exposure to cyanobacterial extract containing microcystins or pure microcystin standards [105]. In the same way, Giaramida et al. [106] reported that the exposure to cyanobacterial extract containing microcystins induced changes in structure and physiology of bacterial communities. The measure of arylsulfatase, phosphatase, urease and β-D-glucosidase activities in the soil, after irrigation with cyanobacterial extract of
5.2. Invertebrates
The impact of cyanotoxins on aquatic invertebrates was well documented (for review, see Ref. [114]). However, the effects of these toxins on soil invertebrates are scarce. The effects of microcystins on soil nematods
5.3. Plants
The phytotoxicity of cyanotoxins was observed on aquatic plants but in the last years several studies investigated this field for terrestrial plants. As described in the review of Corbel et al. [10], the phytotoxicity of neurotoxins and cytotoxic alkaloids is less studied in comparison to microcystins. In laboratory conditions, several studies reported that the rate of germination of several plants decreased with an EC50 of 11 mg eq. MC-LR L−1 for
6. Bioaccumulation of cyanotoxins in agricultural plants and consequences on human and animal health
Humans were exposed to cyanobacteria toxins through many routes, including drinking water, recreational contact and health food products made from cyanobacteria, and food chain. While some of these routes are well enough informed the others are them less, notably that corresponding to the consumption of crop plants. Although, no case of poisoning by these products has been reported worldwide, this eventuality must not be ignored. Indeed, a recent epidemiological study showed that the excessive incidence of amyotrophic lateral sclerosis in the population of the islands of Guam in the Pacific was linked to a consumption of the seeds of cycas contaminated by a neurotoxin, β-methylamino-L-alanine (BMAA), produced by a species of cyanobacteria of the genus
Nevertheless, the ability of microcystins and cylindrospermopsin to accumulate in the tissues of different agricultural plants has been reported in the literature, and it was recently reviewed by Corbel et al. [10]. Microcystins have been detected in tissues of terrestrial plants [92, 93, 104, 122, 136, 137], indicating that they can be absorbed and transported in plants although their transport mechanism is unclear yet. However, the ability of absorbing microcystins and their accumulation in different tissues was variable among different plant species and depends on toxins’ concentrations [99, 107, 127]. For example, Järvenpää et al. [138] reported that microcystins were detected on roots (a non-edible plant tissue for human but can be for animal) but not detected in leaves of mustard and broccoli. Furthermore, numerous studies concerning accumulation of cyanotoxins in agronomic plants growing in the soil were reported in radish roots, leaves of arugula and dill [61], in rice grains [65], in leaves of lettuce and cabbage [61, 139], in leaves and stems of water spinach [139] and in fruits and seeds of tomato and pepper [64]. However, a recent study based on the use of 14C-labelled MC-LR showed that tomato fruits did not accumulate the toxin [92].
7. Conclusion and future directions
The occurrence of toxic cyanobacterial blooms, in surface waters that can be used without treatment for irrigation in agricultural purposes, has become increasingly frequent worldwide. With this increased awareness, research has been recently focused towards the fate of cyanotoxins in soils and health risk due to their potential transfer and accumulation in plants. Although there is much basic information on the concentrations of cyanotoxins found in freshwaters, there are very significant gaps in our knowledge of their effects on the biological activity of the soil and their bioaccumulation, and the role of detoxication and covalent binding in the agricultural plants irrigated with cyanotoxin-contaminated water. The great majority of the studies published recently were performed in hydroponic conditions and focused on microcystins (MCs) and specifically on a single MC variant (MC-LR) out of the almost more than 100 variants known and with high no relevant environmental concentrations. To protect consumers from the adverse effects of MCs, the WHO proposed a provisional upper limit in drinking water of 1 μg/L for the most toxic congener MC-LR and a tolerable daily intake (TDI) of 0.04 μg/kg body weight (bw). The available data on the phytotoxicity of microcystins indicate that their concentrations in edible tissues of various agricultural plants can exceed the WHO-TDI guideline. Consequently, more information on this aspect is urgently needed for risk assessment purposes such as
The fate of cyanotoxins in agricultural soils and the biochemical, physiological and ecological processes that control their trophic transfer in different plants remain to be clarified.
Furthermore, even the provisional guidelines that exist for MCs in water are only recommendations, and policy will not only need to clarify acceptable levels but also address to monitor and enforce these guidelines. As such, improvements, validation and standardization of methods for chemical analysis of MCs—towards effective monitoring and enforcement in agriculture food webs—will be crucial.
Acceptable levels for foodborne cyanotoxins are based entirely on data from waterborne toxins and are not likely to be accurate in terms of exposure through agriculture foods; therefore, reliable exposure scenario and more good quality data should be collected before robust conclusions on the health risks.
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