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Cyanobacterial Toxins: Our Line of Defense

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Dijana Lalić

Submitted: 01 July 2024 Reviewed: 01 July 2024 Published: 02 September 2024

DOI: 10.5772/intechopen.1006142

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Insights Into Algae Fundamentals, Culture Techniques and Biotechn... Edited by Ihana Aguiar Severo

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Insights Into Algae - Fundamentals, Culture Techniques and Biotechnological Uses of Microalgae and Cyanobacteria

Ihana Aguiar Severo, Walter J. Martínez-Burgos and Juan Ordonez

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Abstract

Cyanobacteria (blue-green algae) are a diverse group of photo-autotrophic organisms where their higher dominance, in favorable conditions, represents a significant indicator of water quality. Some of the cyanobacterial genera are toxigenic and can produce toxins—cyanotoxins, which influence animals and humans’ health, and also plants. Commonly known and studded cyanotoxin groups include hepatotoxins (microcystins, nodularins), cytotoxins (cylindrospermopsin), neurotoxins (saxitoxins, anatoxins, BMAA), dermatotoxins (lyngbyatoxin), and irritant toxins (lipopolysaccharide endotoxins). This chapter provides guideline values for the cyanotoxins in drinking water supply and in water for recreational purposes. This chapter focuses on a critical evaluation of the efficacy of water treatment procedures essential for cyanotoxin control. Such knowledge is extremely important in the future expansion of cyanobacterial toxic compounds from aquatic ecosystems, and according to the newest data, from terrestrial environments, especially due to climate change (global warming) and anthropogenic eutrophication. Here are introduced schemes of cyanobacterial ecology and infiltration of cyanotoxins through the biological cycle jeopardizing human health, and tables of the drinking water treatment, along with proposed therapy and limitations, setting the strong foundation for all future research, which are of outstanding scientific importance.

Keywords

  • cyanobacteria
  • cyanotoxins
  • toxicity
  • therapy
  • drinking water
  • cyanotoxins guideline values

1. Introduction

Cyanobacteria, also known as blue-green algae, are among the oldest known organisms on Earth, with fossils dating back over 3.5 billion years. Cyanobacteria are found in a wide range of habitats, including oceans, freshwater lakes, loess and desert crust, and even Antarctic rocks [1]. These groups are credited with producing a significant portion of the Earth’s oxygen through photosynthesis. Some species of cyanobacteria can “fix” atmospheric nitrogen into a form that plants can use, playing a crucial role in the nitrogen cycle. Cyanobacteria contain a variety of secondary metabolites—pigments (phycocyanin, phycoerythrin, and allophycocyanin), that give them their characteristic blue-green color [1]; UV sunscreen pigments (scytonemin and mycosporine-like amino acids) and toxins (cyanotoxins), which enable them to thrive in diverse environments [1, 2]. Normally, algae are barely visible. Under favorable conditions, this can change as they rapidly increase in size to form large areas of greenish, floating scum on the surface water—cyanobacterial blooms. The incidence of cyanobacterial blooms in freshwaters has increased worldwide in the past decade, and they are one of the main problems that endanger the ecological function of water bodies [3] and now have been considered a global environmental public health issue [3, 4, 5]. Most algal blooms are natural and essential components of any water bodies, and most are non-toxic, however, certain cyanobacteria can produce cyanotoxins, cause foul smell (geosmin and methylisoborneol), and unaesthetic challenges to the environment [6]. The most common toxic cyanobacteria in freshwater are Microcystis spp., Planktothrix rubescens, Raphidiopsis raciborskii (formerly Cylindrospermopsis raciborskii), Nostoc spp., Oscillatoria spp., Schizothrix spp., and Synechocystis spp. [7]. During a cyanobacteria bloom, an excess of dead and decaying cyanobacteria can result in hypoxia or anoxia, resulting in fish kills mortality of fauna, and loss of flora [8, 9].

Cyanobacterial favorable conditions are applied to environmental conditions (bright sunlight, high nutrient levels, calm waters (low wind and circulation), limited number of grazers or predators, temperature and pH) and further, trace metals (such as iron, zinc, copper, and magnesium) and environmental pollutants [10]. Temperature higher than 20°C, with nutrients, promotes mineralization leading to explosive growth of cyanobacteria [9, 11], and leads to increased toxin release [12, 13]. pH promotes the proliferation of cyanobacteria, hence the production of cyanotoxins [14, 15]. Increases in nitrate concentration increased MCs production [16], and a deficiency of trace metals in water bodies stimulates the production of intracellular cyanotoxins to acquire or store these metals [17]. On the contrary, in the situation of high levels of trace metal, cyanobacteria produce extracellular toxins to create metal complexes and detoxify the metals [18]. Sources of nutrients can be from fertilizers in the farm during storm runoff [19] and from organisms or particles within the mat [20]. Their occurrence is most common in shallow waters [6].

Climate change has become a global trend, with warming at an unprecedented rate [21] being one of its most prominent manifestations. A global increase of industrialization and urbanization increased nutrient inputs by industrial wastewaters, agricultural runoff (fertilizer), animal waste, the flux of sewage, and detergent usage—eutrophication [3, 22]. The recent trend of climate warming and declining wind speeds has enhanced algal nitrogen and phosphorus utilization efficiency. The precipitation could affect terrestrial discharge, which possibly brings external nitrogen and phosphorus from the watershed into lakes [23, 24]. This can, as a cumulative reaction, enhance expansive cyanobacterial growth [9, 25, 26, 27, 28]. In developing countries and rural areas, surface water bodies are under severe threat due to the uncontrolled disposal of industrial waste and the application of fertilizers on agricultural lands located near water bodies. Combined effects of eutrophication and climate change have increased the occurrence and intensity of cyanobacterial blooms, causing problems in aquatic ecosystems intended for drinking purposes and recreational use [3]. These increases are linked to the deterioration of water quality and increased threats to human sustainable development, social and economic welfare, and, most importantly, health (Figure 1).

Figure 1.

Cyanobacterial blooms in the environment with toxic cyanobacterial species. (A) Microcystis aeruginosa; (B) Aphanizomenon flos-aquae; (C) Oscillatoria sp. (Created by Author using Canva).

So, it can be concluded that the occurrence of cyanobacteria in surface water bodies is usually a function of climate change (elevated warm temperature), soil erosion from agricultural fields, and eutrophication, dominantly caused by human activities. As a result, water resources for drinking and recreation purposes are adversely affected. The increasing trend of cyanobacterial blooms and associated toxin production will likely continue in the upcoming years [29, 30]. Therefore, it is important to introduce regular testing of water bodies for the presence of cyanobacteria and cyanotoxins to protect human health.

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2. Cyanotoxins

2.1 Characteristics

Cyanobacteria are recognized as producers of a diverse range of secondary metabolites, where 50% of them are known to produce extremely toxic cyanotoxins. Cyanotoxins can be produced widely along with cyanobacterial blooms in the world [2]. The most commonly found cyanotoxins in freshwater bodies are microcystin, nodularin, cylindrospermopsin, anatoxin, guanitoxin (formerly known as anatoxin-a(S)), saxitoxin, lyngbyatoxins, and BMAA. There are over 300 different congeners of microcystins identified to date [31], and one of the most investigated and commonly found is microcystin-LR (MC-LR). CYN is the second most frequently reported cyanotoxin due to negative health effects in humans [32]. Cyanotoxins are a very diverse group of chemicals found in water for irrigation, recreation, and, most importantly, in water for drinking supplies. Cyanotoxins can be very potent and their production may threaten the health of humans and animals [2, 22, 33]. Cyanotoxins can be grouped based on their modes of action and target organs into hepatotoxins, neurotoxins, dermatotoxins, and cytotoxins [34], or based on their chemical structures into alkaloids, organophosphorus, cyclic peptides, and lipopolysaccharides compounds [35].

During the occurrence of cyanobacterial blooms, it is necessary to take caution about water-related activity (Figure 2). Some cyanotoxins have toxicities that are comparable to, or in some cases more potent than, cyanide [3]. The presence of high levels of cyanotoxins in recreational and drinking water may cause a wide range of symptoms such as nausea, vomiting, salivation, incontinence, abdominal pain and diarrhea, headache, fever, skin rashes, muscle tremors, paralysis, respiratory failure, and even death in severe cases. These symptoms can occur in a couple of minutes to days after exposure. Also, they can cause damage to kidney and liver tissues [36]. Chronic effects of cyanotoxins cannot be neglected. Cyanobacteria may be present in water bodies over extended periods, which results in continued exposure to subacute concentrations, leading to the possibility of chronic health effects and possible carcinogenic changes [37, 38, 39]. While the severity of the effects can vary depending on the amount of the cyanotoxin, duration, and frequency of exposure, susceptibility to cyanotoxins may also be increased depending on the age and gender of the victims, and also by the presence of comorbidities (e.g. pre-existing liver or gastrointestinal disease) [40]. Children are more susceptible to toxins because of their lower body weight, behavior, and toxic effects on development [41].

Figure 2.

Chemical structure of cyanotoxins. (Dashed area indicates the moiety most responsible for the cyanotoxin toxicity). (A) MC-LR; (B) NOD; (C) CYN; (D) ATX; (E) STX (Created by Author using ChemSketch).

Adda ((2S, 3S, 8S, 9S) 3-amino-9-methoxy-2, 6, 8-trimethyl-10-phenyl-deca-4, 6-dienoic acid), a common bioactive compound derived from MCs congeners and NOD, imparts cytotoxins with toxicity (Figure 2) [42]. The highest concentration of cyanotoxins is usually contained within the cells (intracellular toxins), and a small amount, rarely above a few μg/L, is dissolved in the water (extracellular toxins) [3, 33]. Anatoxin-a and microcystin are mostly found intracellularly during the growth stage of the bloom. However, in cylindrospermopsin, the reported toxin ratio is about 50% intracellular and 50% extracellular. Extracellular toxins are more difficult to remove than intracellular toxins during drinking water purification, as they can absorb clays and organic material in the water column. The concentration of cyanotoxins significantly increases as a defense mechanism in stressful conditions (lack of nutrients/light) [43], also the death of cyanobacterial cells, at the end of their lifecycle or through measures taken during the control blooms, results in higher concentrations of extracellular toxin. The toxins in the cyanobacterial cells are still active for 21 days after the cell decays [44]. And most importantly, some cyanobacterial species show neurotoxic, hepatotoxic, and cytotoxic action despite not producing any known cyanotoxins [45, 46, 47]. These findings suggest the presence of potentially unknown or uncharacterized toxins, highlighting the necessity to explore and characterize potential new cyanobacterial toxins.

2.2 Exposure routes

Exposure to cyanotoxins can occur through a few main routes, which will be discussed roughly. Ingestion of contaminated water is one of the main routes of exposure and may occur through drinking water containing toxins or eating contaminated fish, shellfish, and bivalves. Irrigation of crops and plants with water contaminated with cyanotoxins is another way of possible intoxication. Bioaccumulation of cyanotoxins, and afterward, their bioavailability in the food chain is another prominent way of exposure that should be monitored more frequently (Figure 3). When cyanotoxins are released into the water, they can be ingested by aquatic invertebrates and aquatic vertebrates [48, 49, 50], and they have been found in plants [51], which poses a potential health risk to animals and humans through the food chain [52, 53]. Ingestion of some toxic amount of cyanotoxins may occur by consumption of nutritional supplements that contain blue-green algae as main or additional ingredients. Blue-green algae have a long history as a superfood for health (supports healthy digestion and strengthens the immune system, as a detoxifying agent, excellent fat burner, for radioactive protection), skin’s ultimate superfood (for eternal youth, skin pigmentation, moisturized skin, and improved skin structure), or medicine by humans for centuries [54]. Cyanobacteria are teeming with a high, unexhausted concentration of proteins, vitamins, minerals, carotenoids, and antioxidants which can promote optimal health in humans. In the United States, 38% of adults opted for alternative medicine over conventional drugs among patients with cardiovascular disease [55]. There has been an increasing demand for nutritional supplements for the prevention of COVID (SARS-CO2019). Mostly used are Spirulina, Chlorella, and Aphanizomenon flos-aquae, and some of them contain some groups of cyanotoxins at levels exceeding the tolerable daily intake values [56]. Aph. flos-aquae originated from the Upper Klamath Lake, Oregon, contaminated with high levels of MCs (up to 60 times higher than safety standards set by Oregon state) [57]. ATX-a and its congeners have been reported in different brands containing both Spirulina and Aph. flos-aquae [58, 59], and STX and BMAA in some strains of Aph. flos-aquae that are used for dietary supplements [60, 61, 62]. And more recently, the global war with COVID-19 raises a question—Could cyanobacterial metabolites be an immune booster against the COVID-19 pandemic, cause toxicosis, or even worse, worsen the condition of already developed lung diseases in patients with COVID? Boosting immunity has been a simple way to resist viral infection and limit fatalities [63, 64]. Cyanotoxins in supplements are a serious health risk. Nevertheless, the chemical composition, bioavailability, biological potency, toxicity, and related mechanisms of dietary supplements, respirators, and nasal sprays need to be investigated in detail [65].

Figure 3.

Cyanotoxin incorporation through environment, jeopardizing human health and environment (Created by Author using Canva).

Another prominent route of exposure to cyanotoxin is direct contact with the skin, through recreational activities, or beauty products based on cyanobacteria. During recreational activities on or near water bodies contaminated with cyanotoxins, a possible route of exposure is inhalation of aerosolized toxins. In recent years, an increased number of investigations have been recorded regarding the impact of aerosolized toxins [66, 67, 68, 69, 70]. In a conducted study [66], cyanobacteria were found at high frequencies in the upper respiratory tract (92.20%) and central airway (79.31%) with no relation to the specific time of year. The increasing spread of cyanobacterial blooms due to climate change and eutrophication worldwide may lead to an increase in aerosolized toxins and negative health effects. The growing populations and tourism near water bodies will further raise the number of people at risk. A population could be at risk for acute and chronic exposures as aerosolized cyanotoxins have been detected a few dozen kilometers away from the source [68]. The levels of aerosolized MCs fluctuated even when the concentrations in the water remained relatively stable. This highlights the significance of meteorological conditions (such as wind speed and direction) and aerosol generation mechanisms (such as wave breaking, spillway, and aeration systems) when assessing the risk of inhaling MCs and their potential impact on human health [70]. The potential chronic effects of cyanotoxins, particularly on vulnerable populations (with earlier noticed liver, gastrointestinal, or lung disease), require attention due to limited available data in this area. Understanding chronic, low-dose exposure to cyanotoxins is needed so that appropriate preventative, diagnostic, and therapeutic strategies can be created [40]. Widespread exposure to cyanobacterial toxins during bloom events in 2018 was evidenced by the presence of MCs in the nasal passages of 95% of the individuals previously studied in South Florida [71].

There are also documented cases of toxicosis by the intravenous route, through dialysis [72] where water sources from the clinique contained MCs and CYN.

2.3 Stability

Cyanotoxins are water-soluble and most of them are very stable in natural conditions due to their unreachable core structure. The cyanotoxins such as microcystin-LR (MC-LR) and STXs are persistent in the aquatic system and thus can directly enter the drinking water treatment. In addition, the half-life of MC-LR is around 90 days, and similarly, the half-life of STXs is approximately 9–28 days, which signifies their stability in natural water resources [73, 74]. MCs are extremely stable in water and only slowly decompose in acidic (pH < 1) and alkaline (pH > 9) conditions, exposed to high temperature (40°C), or by boiling [75], chemical, or biological degradation [76, 77, 78, 79]. However, in most cases, bacteria able to degrade them are not present in the water, and therefore, toxins persist for months/years [78]. Their stability is provided by the cyclic structure and presence of novel amino acids. The cyclic structure of nodularins enables high chemical stability, which provides them resistance to boiling, chemical hydrolysis, and oxidation [80, 81]. Data show that nodularins degraded in negligible amounts while contained within living organisms [76, 77]. Cylindrospermopsin is stable at extreme temperatures, light, and pH, but is almost fully degraded when exposed to sunlight for 3 days [43]. ATX-a is unstable under natural conditions being partially or totally degraded and converted to non-toxic products (dihydroanatoxin-a and epoxyanatoxin-a) [82, 83, 84]. Anatoxin-a(S) is more soluble in water, which increases the rate of biodegradability compared to anatoxin-a. ATX-a(S) is unstable and inactivated at high temperatures (>40°C) or alkaline conditions [85]. Saxitoxins are water-soluble and stable toxins with persistence for more than 90 days in freshwater ecosystems [86]. In most cases, these compounds are progressively degraded into more toxic variants and in such conditions, may potentially increase toxicity. These facts, in combination with their high stability, represent a great problem for water treatment facilities and the implementation of an appropriate drinking water treatment.

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3. Guideline values for cyanotoxins

As previously mentioned, cyanotoxin contamination of water bodies used for drinking or recreational purposes has become common. Reports of cyanotoxins poisoning incidents increase worldwide [2, 14], hence becoming health hazards globally [87]. The lack of official guidelines for cyanotoxin levels in drinking water has a great influence on risks to humans who use surface water which may be unsafe.

The risk of being exposed to toxic cyanobacteria and their toxins is high and will gradually be higher considering climate change and industrialization. Even with that emerging concern, a plan for the prevention of cyanobacterial blooming and regulations are still limited, even absent, in several countries. There are many different approaches dealing with the appearance of cyanobacterial blooms and cyanotoxins in freshwaters and drinking water reservoirs [36]. A number of countries (Canada, Brazil, New Zealand, and Australia) have developed regulations or guidelines for cyanotoxins and cyanobacteria in drinking water, and in some cases, in water used for recreational activity and agriculture (Table 1). In Kenya, there is a scarcity of information on cyanotoxins levels in domestic water sources, in Europe and the USA, and in several Latin American countries, there are no guidelines for any cyanotoxins in domestic water [88]. Despite the fact that there is no official federal legislation for cyanobacterial toxins in water with drinking purposes, Serbia has been working for almost 15 years on the analysis of the state of health and making precautionary measures, with special emphasis on the organization of the system for adequate information and health care [89]. Moreover, neighboring countries are affected by the same problem [34]. Argentina, Brazil, and Uruguay have conducted comprehensive studies to evaluate the distribution of cyanobacterial blooms [90, 91], on the contrary for Peru, Chile, Colombia, and Venezuela, the information is limited to specific water bodies [92, 93].

Due to a lack of toxicity data for other toxins, in the reference [94], a provisional guideline for MC-LR has been set (1.0 μg/L for drinking water), hence cyanotoxins are not federally regulated contaminants. As a result, public drinking water providers are not required to routinely monitor drinking water for cyanotoxins. Setting up guideline values for cyanotoxins in drinking and recreational water and also in dietary supplements and cosmetics products is extremely crucial, so with that aim, Table 1 presents legislation from different countries.

Guideline valuesReferenceGuideline valuesReference
Drinking waterRecreational waters
MC0.1 μg/LEurope[34, 94, 95, 96, 97, 98, 99, 100, 101, 102]Relatively low risk**2–4.0 μg/L MCs20.000 cells/ml[94]
1.0 μg/LBrazil (Regulatory Level); New Zealand; WHO*Moderate significant risk***>20.0 μg/L MCs100.000 cells/ml
1.3 μg/LAustralia (Lifetime exposure); CanadaSituation of high risk****>100.0 μg/L MCsAppearance of visible aggregates
10.0 μg/LAustralia (Brief period)[97, 102]
NOD1.0 μg/LNew Zealand[95, 100, 103]ND
STX0.1 μg/LEurope[96, 97, 98, 101, 102, 103]ND
3.0 μg/LBrazil (suggested); Australia (suggested); New Zealand
ATX-a0.1 μg/LEurope[96, 97, 100, 101, 102, 104, 105, 106]ND
1.0 μg/LAccording to Fawell
1.3 μg/LAustralia
1.5 μg/LCanada
3.0 μg/LAustralia (suggested)
6.0 μg/LNew Zealand
ATX-a(S)1.0 μg/LNew Zealand[100, 107]ND
HATX-a2.0 μg/LNew Zealand[100, 103]ND
CYN0.1 μg/LEurope[96, 98, 101, 103]ND
1.0 μg/LNew Zealand
1.0-15 μg/LAustralia
15.0 μg/LBrazil (suggested)
Dietary supplements
1 ppm microcystins (ODA)[94]
Tolerable daily intake
0.04 μg/kg/day[94]

Table 1.

Guideline values for cyanotoxins.

Brazil [98], China, Czech Republic, Finland, France [99], Japan, Italy, Denmark, Germany, Great Britain, Greece, Korea, New Zealand [101], Norway, Oregon (USA) [108], Poland, South Africa, Spain, USA [109].


Czech Republic, France, Italy, Hungary, Turkey.


Canada, Cuba, Czech Republic, France, Italy, Hungary, Turkey.


France, Italy, Turkey.


A provisional guideline value of l μg/L MC-LR in drinking water for human lifetime exposure and 12 μg/L for short-term exposure, respectively, was recommended by the World Health Organization (WHO) and value for CYN for human lifetime exposure is 0.7 μg/L [36]. Most of legislation are based on the WHO provisional value for drinking water, while others formulated their values, based upon local requirements (e.g. Czech Republic, France, Singapore, Uruguay, South Africa, Australia, Canada, New Zealand, South Korea, and Brazil) [35, 100]. Most countries define cyanotoxin concentration limits in drinking water but not in water used for recreational activities. The guideline value for the maximal acceptable concentration of MC-LR in drinking water was used also for human health risk assessment of microcystins resulting from recreational exposure, consumption of contaminated food, or food supplements [94, 110]. Brazil was the first country to enforce a specific, most comprehensive federal legislation for the control of cyanobacteria and their toxins in water used for drinking supply and recreational activities [100, 111, 112], which includes mandatory standard values for MCs, STXs, and CYN [113]. Concerning cyanotoxins, several countries have implemented monitoring programs based on cyanobacterial biomass for recreational water (cell numbers, chlorophyll-a concentration, and often cyanotoxin concentration) [94].

Due to the lack of relevant guideline values for other types of toxins, they might exhibit greater health risks to humans. Also, there might be a high level of unregulated cyanotoxin congeners, thereby posing unknown health risks. The definition of guideline values for all types of cyanotoxins is needed as the current regulations are insufficient, especially in developing countries and rural areas. Despite the risks associated with cyanotoxins, current regulations for dietary supplements are insufficient to safeguard consumers. These guidelines should determine the values of cyanotoxins in accordance with patients with chronic illnesses and kids. Kids are more susceptible than school-age children through adults considering they consume more water relative to their body weight [14].

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4. Drinking water supply: occurrence of cyanobacteria and water treatment for cyanotoxin removal

4.1 Cyanobacteria and cyanotoxins in drinking water supply

Based on previous literature data, it is clear that almost every part of the world has or will encounter problems with toxic cyanobacteria in its drinking water system. The occurrence of toxic cyanobacterial blooms is increasing in frequency and distribution [2], and so does the chance of losing access to safe drinking water. Of all the routes of cyanotoxin exposure to humans, drinking water is the main source. Despite having a sufficient quantity of water, availability may be limited if the quality does not meet the requirements for its intended use. The increased occurrence of toxic cyanobacteria and cyanotoxins is increasingly being viewed as a contaminant of emerging concern and is considered a major health risk related to surface waters worldwide, which further increases the cost of water resources. This problem was cumulated in Lake Vrutci (Užice, Serbia), where the presence of cyanobacteria Planktothrix rubescens was documented, with the presence of MC-LR in the fish tissue, lake, and the tap water, as well as other types of MCs detected [114]. During this period, 70,000 people living in Užice were left without healthy drinking water. Because of contaminated water with the bloom of Microcystis sp. in Toledo, Ohio, a public advisory shutdown the water supply for 3 days which impacted over 400,000 people [115]. In 2013, in finished drinking water of Carroll Township, Ohio was detected at 1.4 mg/L and 3.6 mg/L of MCs equivalents, and water has been out of use for the 2200 population. Another well-known drinking water crisis has affected municipalities on the shores of Lake Taihu (China), Lake Erie (Ohio, USA) [6], and in July 2018, Greenfield, Iowa; in 2007, residents from Changchun and two million people from Wuxi (Jiangsu Province) went without drinking water due to a cyanobacterial bloom occurrence. The current circumstances compel millions of people to purchase bottled drinking water. Continuous exposure to cyanotoxins in drinking water may reach a lethal dose within the human lifespan, leading to death, in some cases, or in negligible levels, can cause carcinogenicity [114, 116]. Safe drinking water remains a challenge worldwide in many rural communities [36], which causes 1.2 million deaths per year [117, 118].

Mass occurrences of toxic cyanobacteria and their toxins in reservoirs represent a great challenge for the production of safe drinking water through the application of adequate water treatment techniques.

4.2 Water treatment for cyanotoxin removal from drinking water supply

Drinking water sources pose a great challenge for drinking water facilities. Fresh cyanobacterial blooms often smell like fresh-cut grass, while older blooms can stink like pig pens. Older blooms are more likely to release toxins when dying as their cells break down. Filamentous cyanobacteria cause problems in water treatment systems by clogging in filters for drinking water supply. In that manner, during the water treatment process, cyanobacterial cells, odor, and color need to be reduced and cyanotoxins eliminated. The mass presence of the potentially toxic cyanobacteria represents a real threat to human and animal health, and an important indicator of the rapid water quality deterioration [119], which further poses a serious problem to water treatment facilities because not all water treatment technologies can remove all cyanotoxins below acceptable levels [4]. The health issues caused by cyanotoxins presence have led to efforts by water suppliers to develop effective treatments and management approaches for the production of safe drinking water. To minimize the risk from cyanotoxins in drinking water, a multi-barrier approach is needed; incorporating prevention, source control, adequate treatment, and a monitoring system. Prevention of bloom appearance is a crucial step as a defense mechanism over invasive cyanobacterial blooms in water reservoirs. Bad management of water purification systems can lead to serious problems.

A lot of cases are documented where the treatment process previously used was ineffective against cyanobacterial blooms which caused serious human poisoning likewise 2000 cases of gastroenteritis and diarrhea, including 88 deaths after drinking boiled water from the dam [120]; gastrointestinal illness among 9000 people receiving drinking water from rivers in West Virginia [121]; gastroenteritis with abdominal pain and vomiting affecting 5000–8000 persons where drinking water treatment by precipitation, filtration, and chlorination was not sufficient to remove the toxins in Ohio river [122, 123]; or gastroenteritis with vomiting and headache among 149 persons in Australia, Solomon Dam, where treating bloom with copper sulfate resulted in the liberation of toxins [124]. Serious human poisonings happened in Charleston, West Virginia even precipitation, filtration, and chlorination were applied [125]. Drinking water supply without a proper basic drinking water purification process in Zimbabwe, Africa, caused gastroenteritis, skin rashes, itching, and eye sores in children [126]. Also, there is animal intoxication cases after drinking contaminated water, for example, several hundred livestock died within hours in Australia [127, 128], in South Africa [129], Switzerland [130], Sweden [131], and the USA [132, 133, 134, 135]. When inappropriate treatment was used, cyanobacteria cells were not degraded, stayed intact after water treatment, and caused blooms in the post-treatment drinking water tanks. In reservoir Vrutci, Serbia slow-sand filtration was applied, but was not a sufficient method that led to sickness of people and deaths of animals [114], also people who use water from Malpas Dam, Armidale experienced serious chronic effects like liver damage [136, 137], or in China development of primary liver cancer [138, 139].

Most cyanotoxins are cell-bound and are released when the cells age, die, or are lysed through employed purification systems [140, 141], which present a hazard to animals and humans using the water, especially when used as a potable water source. Not all countries have appropriate means to deal with cyanobacteria problems, as well as sensitive and precise analytical methods for cyanotoxin detection, which are usually expensive and inaccessible. However, over 300 analogs of MCs have been identified, but not all are presently monitored, therefore, any conclusions based only on the presence of MC-LR can be misleading. Chronic exposure to low concentrations of MC increases the risk of developing cancer (e.g. China, Florida, Serbia). This situation can be linked to the country where the populations receive drinking water from surface accumulations that are frequently blooming [142]. The unequal geographical distribution of liver cancer in Serbia was visible and outbreaks can be correlated with drinking water supplies, where districts with a higher risk of developing primary liver cancer are using reservoirs that are continuously blooming, and low-risk regions have purification systems of drinking water [142].

Different techniques have to be included in order to reduce cyanobacterial growth and cyanotoxins [3]. Effective removal of cyanobacterial toxins depends on the type and concentrations of chemicals used in the water treatment processes, also physical parameters of water (e.g. pH and the contact time), as well as concentrations and types of cyanotoxins entering the treatment and also varies among cyanobacterial species (Table 2). For example, chloramine is the least effective oxidant for inactivating Microcystis aeruginosa, Oscillatoria sp., and Lyngbya sp. [143], and coagulation/flocculation/sedimentation completely removes cells of, for example, Aphanizomenon flos-aquae, Merismopedia sp., Phormidium corium, while M. aeruginosa and Gloeocapsa sp. were intact [144]. MCs have been reported in final drinking water in many countries including Argentina, Australia, Bangladesh, Canada, Czech Republic, China, Finland, France, Germany, Latvia, Poland, Thailand, Turkey, Serbia, Spain, Switzerland, and the USA [121, 122]. A survey of 45 drinking water supplies in Canada and the United States detected MC in 80% of the raw and treated water observed, but only 4% of the samples exceeded the WHO drinking water guideline [145].

Treatment techniqueExpected removalAdditional comments
IntracellularExtracellular
Auxiliary process
Pre-ozonationAuxiliary process—Auxiliary process for enhancing coagulation, however this process can lead to toxin release.
Pre-chlorinationPre-chlorinationAuxiliary process—Useful to assist coagulation of cells, with subsequent treatment steps which will remove dissolved toxins. Depends on the type of chlorine.
Free chlorine—> 100%Effective on degradation of microcystin, cylindrospermopsin, and saxitoxin, but not for anatoxin-a.
Chloramine—NegligibleIneffective.
Chlorine dioxide—NegligibleIneffective (with doses used in drinking water treatment).
Conventional water treatment
CoagulationCoagulation> 90%< 10%This treatment may cause lysis of cyanobacterial cells. NOM decrease removal efficiencies.
Ferrate oxidation-coagulation—> 93%This process has advantage over using chlorine, ozone or peroxide for oxidation.
FiltrationSlow sand filtration<86%Probably significantVery useful if combinated with other water treatments.
Rapid filtration>60%<10%This method causes lysis of cyanobacterial cells. Usually employed after coagulation to remove the particles.
Membrane processes>96%UncertainEffective in the removal of whole cells. Depends on pore size of RO and NF membranes, and water quality, dissolved MCs have been removed. This treatment causes cells lysis.
AbsorptionPACNegligible>85%Effective in toxin removal but with very high doses of PAC. Generally effective for removal of MC, ATX-a and CYN. DOC will reduce capacity. It has to change frequently which significantly increased treatment costs.
GAC>60%>95%DOC competition and presence of NOM decreases toxin adsorption process. GAC filters with proper replacement can be used as an auxiliary barrier for MC, but less effective for ATX-a and CYN.
Biological GACExcellent>90%Better effectiveness in toxin removal than GAC.
OzonationPotassium permanganate—95%Advantages: low cost, ease of handling, effectiveness over a wide pH range;
Disadvantages: long contact time, gives water pink color, toxic, cause skin irritation, fatal if swallowed.
Ozonation—>98%It is best to use oxidation to degrade dissolved cyanotoxins after the removal of algal cells by a coagulation and filtration. The initial cost of ozonation equipment is high, ozone is highly corrosive and toxic, and requires higher level of maintenance and operator skill; leads to cell lysis.
Hydrogen peroxide—UncertainNot effective on its own.
Advanced oxidation technologies (AOTs)
AOTsUV radiation/AOTs—NegligibleEffective in removing of MC-LR, ATX-a, and CYN, but only at impractically high doses. Because of the high doses required, low to medium pressure lamp, UV treatment is not recommended as a viable treatment barrier for cyanotoxins. Leads to lysis of the cell wall.
Titanium dioxide/AOTs—100%One of the most promising AOTs, inexpensive and photocatalytic active catalyst under UV and visible light; without utilizing or producing hazardous compounds. This treatment resulted in complete degradation of the cyanotoxin under UV light.
Fenton and Photo-Fenton processes—60–100%Fenton process depends on the pH, concentration of H2O2 and Fenton reagent. The highest degradation efficiency was achieved when UV radiation was involved, during the Photo-Fenton process.
Sonolysis—Reduction of algae cellsBest if applied with AOTs. Significantly enhance reduction of algae cells, without lysis of cells. Application of ultrasonic irradiation requires frequencies that lead to extreme conditions. Without chemical addition.
Biodegradation—100%Sphingomonas sp., Paucibacter toxinivorans gen. Nov. Sp. nov, Burkholderia, Arthrobacter sp., Brevibacterium sp., Rhodococcus sp., and Methylobacillus sp. are capable to degrading some types of cyanotoxins. Better in conjunction with UV/H2O2, ozone, PAC, or GAC. Advantages: reliable, cost-effective, which does not involve any use of harmful chemicals; disadvantages: long reaction time of hours to days.

Table 2.

Effectiveness of water treatment on removal of cyanotoxins.

Abbreviations: AOTs-advanced oxidation technologies; ATX-anatoxins; ATX-a(S)-antoxin-a (S); CYN-cylindrospermopsin; DOC-dissolved organic carbon; GAC-granular activated carbon; MC-microcystins; NF-nanofiltrattion; NOD-nodularin; NOM-natural organic matter; PAC-powdered activated carbon; RO-reverse osmosis; STX-saxitoxins.

From all the statements from Table 2, it could be concluded that no single treatment method can remove all contaminants from water, thus more efficient and cost-effective technology needs to be developed. Water treatment can be highly effective in removing cyanobacterial cells and toxins (especially MCs) with the appropriate combination of treatments. Some most common treatments of water contaminated with cyanobacterial blooms use pre-oxidants (such as ozone, chlorine, chlorine dioxide, chloramine, potassium permanganate, ferrate, and copper sulfate) which while killing cells will result in the release of cyanotoxins [146], so demand subsequent step to remove dissolved extracellular toxins (Table 2). Further processes involve conventional water treatment-coagulation, flocculation, and absorption (sedimentation). Coagulation provides high removal rates of intracellular toxins (> 90%), and somewhat less important of extracellular toxins (< 10%), but this process may cause lysis of cyanobacterial cells. Coagulation supplemented with ferrate (ferrate oxidation-coagulation) has an advantage over using chlorine, ozone, or peroxide for oxidation, with expected removal rates of less than 93% for extracellular toxins, and negligible for intracellular toxins. Filtration is very useful if combined with other water treatments, and usually is employed after coagulation to remove the particles. Slow sand filtration provides the removal of intracellular toxins over 86%, and rapid filtration less than 60%. Membrane filtration processes are effective in the removal of whole cells, depending on the pore size of RO and NF membranes, and water quality. However, filtration causes cell lysis and promotes the increase of dissolved cyanotoxins [4, 146]. The removal efficiency of cyanobacterial cells with conventional water processes is species-specific [144], however, the established opinion is that these treatments were insufficient for the complete removal of cyanobacterial cells, especially of toxins [144, 147]. Given the lack of cyanotoxin removal using coagulation and filtration, a possible way to eliminate cyanotoxins below the WHO guidelines value is the application of these treatments combined with the addition of PAC/GAC. PAC is effective for the removal of MC, ATX-a, and CYN, and GAC for MC, but less effective for ATX-a and CYN [4]. Absorption has excellent removal of extracellular toxins, with PAC less than 85%, and GAC 95%. The choice of a form of activated carbon (PAC or GAC) is typically a function of operating conditions. When using GAC, the formation of biofilms (biological GAC) can occur which has been shown to give higher cyanotoxin removal [148]. A further step for improvement of the water purification system is ozonation, which degrades dissolved cyanotoxins after the removal of algal cells by coagulation, filtration, and sedimentation. Usage of ozonation achieves removal of extracellular toxins higher than 98%. However, the equipment required for ozonization is demanding, keeping in mind that ozone is highly corrosive and toxic, and requires a higher level of maintenance and operator skill; also leads to cell lysis. The application of hydrogen peroxide has shown uncertain toxin removal. Potassium permanganate accomplishes the removal of extracellular toxins up to 95%, and as an advantage, it is inexpensive, easy to handle, and effective over a wide pH range. However, this treatment is toxic and can cause skin irritation, and it can be fatal if swallowed. Advanced oxidation processes (AOTs) involve the use of UV, UV/H2O2, ultrasound, and ozone. The most recent study [149] showed that the removal rate of M. aeruginosa increased with the extension of time and the removal effect of static ultrasound was better than with dynamic ultrasound. However, the release of toxins was less in dynamic ultrasound radiation. UV radiation/AOTs is effective in removing MC-LR, ATX-a, and CYN, but only at impractically high doses, therefore is not recommended as a step in treatments for cyanotoxins. Titanium dioxide/AOTs is one of the most promising AOTs (expected removal: intracellular toxins negligible, extracellular 100%), inexpensive, and photocatalytic active catalyst under UV and visible light, without utilizing or producing hazardous compounds. This treatment completes degraded cyanotoxins under UV light. The Fenton process (for intracellular toxins - ineffective, for extracellular - 60–100% effectiveness) depends on the pH, concentration of H2O2, and Fenton reagent. The highest degradation efficiency was achieved when UV radiation was involved, during the Photo-Fenton process. Sonolysis is best if applied with AOTs, significantly enhances the reduction of algae cells without lysis of cells. The application of ultrasonic irradiation requires frequencies that lead to extreme conditions. Biodegradation is being explored as a treatment for the efficient removal of cyanotoxins from drinking water, with the expected removal of extracellular toxins of 100%. Sphingomonas sp. [150, 151], Paucibacter toxinivorans gen. Nov. Sp. nov, Burkholderia, Arthrobacter sp., Brevibacterium sp., Rhodococcus sp., and Methylobacillus sp. [152, 153] are capable of degrading some types of cyanotoxins. Biological degradation is better in conjunction with UV/H2O2, ozone, PAC, or GAC. This treatment is reliable, cost-effective, does not involve the use of harmful chemicals, and has a long reaction time of hours to days. Advanced oxidation processes show promising results for the destruction of intact cyanobacterial cells and cyanotoxins in drinking water.

MCs, ATX-a, CYN, and some STXs are adsorbed from the solution by both granular activated carbon and, less efficiently, by powdered activated carbon. Adequate contact time and pH are needed to achieve optimal removal of cyanotoxins. Therefore, the practice of prechlorination or pre-ozonation is not recommended without a subsequent step to remove dissolved cyanobacterial toxins. So, Figure 4 provides our model for a sufficient purification system of water contaminated with cyanobacteria.

Figure 4.

Water treatments specific to certain cyanotoxins. Abbreviations: AOTs-advanced oxidation technologies; ATX-anatoxins; ATX-a(S)-antoxin-a (S); CYN-cylindrospermopsin; GAC-granular activated carbon; MC-microcystins; NOD-nodularin; PAC-powdered activated carbon; STX-saxitoxins.

The problem regarding cyanobacteria and their toxins in water bodies is an urgent matter and should be changed in the near future. The monitoring of water supply systems for cyanobacteria and cyanotoxins, especially reservoirs for drinking purposes, is not yet common practice in most of the countries in the world. Therefore, various techniques and methods in water treatment procedures must be employed as necessary measures for the preservation of the local environment, and water quality. Furthermore, financial support plays an important obstacle, when it comes to cyanotoxin monitoring and treatment measurements implementation. All points which are given in previous paragraphs point out the harmfulness of cyanobacteria and their toxins and implicate the necessity of introduction of legislation concerning the determination and monitoring of these toxins. To avoid risks to human health, an appropriate drinking water treatment is necessary for cyanotoxin elimination from water, which poses a great problem, as some treatment leads to cell lysis and the release of cyanotoxins, which are mostly water-soluble. Table 2 (supplemented with Figure 4) addresses the methods available for its removal and also the difficulties faced in each process. Treatments that have been proven to reduce cyanotoxins below toxic levels include activated carbon, slow sand filtration, conventional filtration, membrane filtration, advanced UV, and ozone [4]. Assessment of water treatment procedures has shown that most methods would result in a reduction of cyanobacterial toxins concentrations below the WHO guideline value of 1 μg/L drinking water [108]. It is important to emphasize that most of the water treatments are developed for successful MC-LR elimination, as it is the most common toxin found in aquatic environments. However, these treatments do not guarantee the successful elimination of other known MC equivalents (>300) and other groups of cyanotoxins that can occur. Therefore, the development of various robust, accurate, and affordable techniques and methods in water treatment procedures must be employed as necessary measures for the preservation of the local environment and water quality. Although satellite remote sensing technology cannot detect cyanotoxins [154], they can be used for detecting and quantifying cyanobacterial bloom abundance [155]. This method can help prioritize locations with greater exposure to blooms and is used to assist in prioritizing management actions for water with drinking and recreational purposes and may provide an indicator for human and ecological health protection (hypoxic events, phytoplankton composition, light availability) [156, 157, 158]. A few recent studies have shown that the detection and quantification of cyanotoxins (MCs) in water can be achieved with passive samplers, which can be used effectively at low levels (of μg/L and ng/L) of toxins [159, 160, 161, 162]. The study [161] monitored MC levels in different stages of water treatment, and also at different depths of the lake. Nowadays, there are different commercially available passive samplers, like polar organic compound integrative sampler (POCIS), Chemcatcher (passive water quality sampler for micropollutants), or SPATT devices (specialized for cyanotoxins).

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5. Proposed therapy for cyanobacterial blooms intoxications

Toxicoses caused by cyanotoxins are a serious condition that requires immediate medical attention to prevent fatality. Based on available literature, diagnostic tests for cyanotoxins are currently not available for clinical use. The fact that robust, inexpensive, and widely accessible assays are not available to facilitate rapid diagnosis and therapy of cyanobacterial intoxication represents a crucial problem in the modern health system. As previously mentioned, the significant number of poisoning cases caused by cyanotoxins, and the potential for future increases in such cases, underscores the urgent need to develop effective therapies. These therapies should eventually be incorporated into standard treatment practices. The detection of cyanotoxins in blood, respiratory mucosa, and urine samples to diagnose acute or chronic intoxication is difficult and requires sophisticated, expansive analysis techniques. Some specialized laboratories can perform tests (electrolytes and liver enzymes; renal function tests, serum glucose, and urine tests; chest radiographs) to identify intoxications caused by the presence of cyanobacteria/cyanotoxins.

It is important to find simple and quick methods to address this issue. As the occurrence of toxic cyanobacterial blooms and human exposures become more common, the recently developed method [163] using Immunocapture-Protein Phosphatase Inhibition Assay may be used as a simple and robust assay to detect cyanotoxins (MCs) in human plasma. Unlike previous methods that engage in acute exposure to MCs [164, 165, 166, 167], this method was developed for the detection of low-level MC exposures (through inhalation) [163]. Studies performed earlier have detected MCs in urine samples (mouse and human), plasma (mouse), and serum samples (mouse and human) [164, 165, 166, 167]. Previously, quantification of MC and NOD concentration was measured in human urine by Immunocapture-Protein Phosphatase Inhibition assay [165]; MCs by a simple colorimetric method [167], or in urine, plasma, and serum through development and applications of solid-phase extraction and liquid chromatography-mass spectrometry methods [166]. The presence of specific antibodies in serum could be used as exposure biomarkers to complement epidemiological studies and medical diagnosis of cyanotoxin intoxications.

There are no antidotes for cyanotoxins [168]. Decontamination, administration of cholestyramine, and symptomatic therapy in combination with supportive care consisting of fluids, mucosal protectants, vitamins, antibiotics, and nutritional supplements may be considered as one of the strategies in cases of toxicities with cyanobacteria [169]. Respiratory support may provide sufficient time for detoxication followed by recovery of respiratory control [168]. Therefore, a crucial step in future studies is introducing adequate therapy in case of cyanotoxin poisonings for treating both animal and human cases.

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6. Limitations

There are some limitations that will be a problem in future research regarding cyanotoxins in water bodies for drinking and recreational use. The primary limitation is that the number of cases analyzed in the literature is limited to available reports, databases, and literature published so far. The data are unavailable or limited in many countries (e.g. Argentina, Chile, Paraguay, Colombia) [170, 171]. Also, the number of scientists and interest in the field of health and environment are scarce in rural regions and developing countries [2]. Research on cyanotoxins and cyanobacteria, as well as the number of reported cases, varies among the countries, where financial support plays an important role. Also, insufficient medical and veterinary training and knowledge of the public community are recognized in developing countries and rural regions. There was a correlation between the level of education and the number of reported symptoms, with higher education levels associated with fewer reported symptoms [69]. Moreover, there is no routine monitoring of cyanotoxins in freshwater bodies. Laws and regulations in different countries mostly do not oblige monitoring of cyanotoxins, therefore, the actual number of cases is most likely higher than reported.

According to the latest data, there are over 300 different MC variants [31], and drinking water treatments and toxicity tests are usually tested only for MC-LR. Standards for cyanotoxins detection are very expensive, and unreachable; also there is demand for (expensive) equipment and highly educated technicians. So main question is: What about other groups of cyanotoxins? For some groups of cyanotoxins, there are no standards. They are all present in the water but unmonitored and pass by, undercovered. And just like that, silently, they change the environment and cause health issues. More recently published information of toxic effects caused by cyanobacterial species that cannot produce cyanotoxins increases the importance of preventing the appearance of cyanobacteria, and furthermore of their safe removal from water bodies intended for drinking and recreational purposes.

Thorough, detailed overcoming of limitations is the key to combating powerful cyanobacteria.

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7. Conclusion

Available, bacteriologically safe drinking water is essential. The government aims to tackle the issue of water scarcity, particularly in rural areas, where residents are impoverished and unable to access clean, safe drinking water. An appropriate drinking water treatment is necessary to eliminate cyanobacteria and their toxins from the water. A combination of different, advanced treatments for cyanotoxin removal should be performed. However, their elimination from the drinking water supply is challenging. Different types of cyanotoxins, even metabolites from non-toxin-producing species, have different characteristics, stability, and structure. Depending on the source organisms, they can be distributed at different depths through water samples. Therefore, the most important thing in the fight against cyanobacteria is the spread of knowledge, the prevention of their appearance and spread, and appropriate behavior when they appear on the water surface.

Sharing knowledge about the environmental conditions that encourage bloom formation and their toxins is crucial for managing the risks associated with cyanobacterial toxin issues. The medical employees and also residents have to be capable of recognizing the occurrence of cyanobacterial blooms and how to behave accordingly. The deepest research is necessary to identify populations with underlying comorbidities that may increase susceptibility to cyanotoxin exposure and to develop an adequate therapy for treating animal and human cases caused by cyanotoxin intoxication. A crucial step in the improvement of the cyanotoxin control system is the setting guideline values for all cyanotoxins, which also includes monitoring their fate in aquatic food chains, during food processing, and routine control of food supplements and healthy food.

A future study should focus on determining potentially harmful cyanobacterial compounds, and all types of cyanotoxins in water reservoirs, and expand studies related to cyanotoxins in countries in development. A diagnostic test that does not require a standard for detection is necessary to identify toxicoses. The data gathered indicates the need for future research to focus on developing reliable and precise, yet affordable and widely accessible, analytical techniques for detecting cyanotoxins, available to wealthier and developing countries, and also to rural aeries. The incorporation of new methodologies, likewise passive samplers, satellite-based remote sensing tools, or in vivo pigment fluorescence, could provide consistent, low-cost data for the development of large geographical monitoring programs and should be considered for analysis carefully in future studies.

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Acknowledgments

This work was supported by the Ministry of Science, Technological Development and Innovation of the Republic of Serbia (Grants No. 451-03-66/2024-03/200125 & 451-03-65/2024-03/200125).

I would like to express my deepest appreciation to my dear colleague Dr. Gorenka Bojadžija Savić for helpful contributions, constructive advice, and insightful suggestions.

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Conflict of interest

The author declares no conflict of interest.

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Abbreviations

AOTs

advanced oxidation technologies

ATX-a

anatoxin-a

ATX-a(S)

anatoxin-a(S)

BMAA

β-N-methylamino-L-alanine

CYN

cylindrospermopsin

GAC

granular activated carbon

LPS

lipopolysaccharides

MC

microcystin

MC-LR

microcystin-LR

NOD

nodularin

NOM

natural organic matter

NSTX

neosaxitoxin

PAC

powdered activated carbon

RO

reverse osmosis

STX

saxitoxin

WHO

World Health Organization

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Submitted: 01 July 2024 Reviewed: 01 July 2024 Published: 02 September 2024

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