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Cyanobacterial Blooms and Their Implications in the Changing Environment

Sonal Mishra 1, Neha Kumari 1, Donat-P. Häder 2, Rajeshwar P. Sinha 1,*

  1. Laboratory of photobiology and Molecular Microbiology, Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi-221005, India

  2. Emeritus of Friedrich-Alexander University, Department of Biology, Neue Str. 9, 91096, Möhrendorf, German

Correspondence: Rajeshwar P. Sinha

Academic Editor: Petros Ganatsas

Special Issue: Cyanobacterial Blooms

Received: January 03, 2022 | Accepted: March 09, 2022 | Published: March 16, 2022

Adv Environ Eng Res 2022, Volume 3, Issue 1, doi:10.21926/aeer.2201011

Recommended citation: Mishra S, Kumari N, Häder DP, Sinha RP. Cyanobacterial Blooms and Their Implications in the Changing Environment. Adv Environ Eng Res 2022; 3(1): 011; doi:10.21926/aeer.2201011.

© 2022 by the authors. This is an open access article distributed under the conditions of the Creative Commons by Attribution License, which permits unrestricted use, distribution, and reproduction in any medium or format, provided the original work is correctly cited.

Abstract

Cyanobacteria are the most ancient phytoplankton that first appeared at least 2.5 billion years ago and have a prolonged evolutionary history. They can form impenetrable and toxic blooms in aquatic ecosystems such as freshwater and marine environments. Cyanobacterial blooms produce cyanotoxins that endanger ecosystem functioning and deteriorate water quality used for recreation, drinking, and in fisheries, thus, adversely affecting human health and the economy. Some bloom-producing genera are Aphanizomenon, Planktothrix, Cylindrospermopsis, Nodularia, Trichodesmium, Dolichospermum, and Microcystis. They increase turbidity and suppress submerged aquatic vegetation. Due to the microbial bloom-mediated environmental degradation, oxygen scarcity might occur, inducing hypoxia and anoxia, and resulting in the death of fish and benthic invertebrates. Several cyanotoxins cause many diseases related to digestion, liver, and neurological disorders when ingested by birds and mammals, including humans. Global changes resulting from human impacts like eutrophication, rising CO2 levels, and global warming are major driving forces for the enhancement of cyanobacterial blooms in many aquatic systems worldwide. Various management strategies such as nutrient load reduction, hydrodynamic changes, and chemical and biological controls have been used to reduce bloom occurrence and proliferation of cyanobacteria. In this chapter, we have discussed the approaches regarding the understanding of how global changes affect cyanobacterial blooms and also suggested effective prediction and management strategies.

Keywords

Cyanobacterial blooms; climate change; eutrophication; management strategies

1. Introduction

The occurrence and potency of cyanobacterial blooms and economic losses related to these events have increased in both freshwater and marine ecosystems [1]. Cyanobacterial blooms can severely affect water quality. They enhance turbidity and strangulate submerged aquatic vegetation [2]. Cyanobacterial blooms deplete oxygen, resulting in hypoxia and anoxia, causing the death of fish and benthic invertebrates. They also alter the nutrient biogeochemistry of water bodies and affect the diversity and abundance of other species. Various compounds related to taste and odor are produced by cyanobacteria, which affect the recreational functions of lakes and drinking water reservoirs. A high concentration of cyanotoxins is also produced, which cause diseases related to liver, digestive, and neurological disorders when consumed by birds and mammals, including humans [3,4].

The factors responsible for the increase in these cyanobacterial blooms include an increase in nutrient inputs, CO2 levels, global warming, the transfer of cells or cysts via human activities, and the enhancement of aquaculture production or overfishing, which can alter food webs and enable the growth of harmful species [1]. Cyanobacterial blooms increase water temperatures by absorbing excessive light using their photoprotective and photosynthetic pigments [5]. The increase in surface water temperatures resulting from changing global climate may promote cyanobacterial blooms [6]. Cyanobacterial blooms are caused by multiple factors [1]. Blooms caused by the enormous growth of certain cyanobacteria, followed by the production of toxic compounds, occur in eutrophic to hypertrophic lakes, ponds, and rivers around the world [7].

Several toxic compounds (cyanotoxins) are produced by cyanobacteria that occur in freshwater and marine ecosystems [7]. These toxic compounds have many harmful effects on aquatic organisms, animals, and humans. The toxicity of different cyanotoxins depends on cyanobacterial growth and the extent of their toxin production [3,7]. Different abiotic factors, including light intensity, temperature, pH, and nutrients, determine the growth of different cyanobacteria and their ability to produce toxins [7,8,9]. Cyanotoxins play an important role in chemical defense, providing survival advantages to the cyanobacteria over other microbes or deterring predators. Cyanotoxins may also participate in chemical signaling.

Cyanotoxins pose risks to human and animal health. Depending on the concentration in the aquatic environment, they can cause severe poisoning, produce chronic diseases such as cancer, and even cause death. There are many groups of cyanobacterial neurotoxins, classified according to their structure, including alkaloids (anatoxin-a, homoanatoxin-a, and saxitoxins), non-proteinogenic amino acids, e.g., BMAA and the phosphate ester, and anatoxin-a(s). Cyanotoxin hepatotoxicity causes inhibition of serine/threonine protein phosphatases and affects the regulation of cellular protein hyperphosphorylation [10]. Neurotoxicity results in neuromuscular blockade [11], anti-acetylcholinesterase activity, anti-phosphatase activity, postsynaptic cholinergic agonist activity, and also affects protein kinase C activators.

2. Cyanotoxins

Bloom-forming cyanobacteria produce different secondary metabolites, and most of them are toxic to plants, lower animals, and humans at naturally occurring concentrations [4]. Some bloom-forming cyanobacteria such as Microcystis aeruginosa, Merismopedia sp., Anabaenopsis sp., Anabaena sp., and Oscillatoria sp. from different water reservoirs in Varanasi, India are shown in Figure 1 [12,13]. Cyanobacterial blooms contain both toxic and non-toxic strains. Therefore, the toxin content and the toxin composition of cyanobacterial blooms depend on the composition of the strain [14]. Cyanobacterial blooms degrade water quality, deteriorate ecosystem stability, and adversely affect human health by producing cyanotoxins in potable, fishable, and recreational water sources. The concentration and types of toxins are highly dependent on the interactions between environmental factors (e.g., light, temperature, pH, nutrient and CO2 availability etc.) which can promote the expression of toxin genes and toxigenic genotypes [15,16]. Cyanobacteria, and the toxins released by them, disturb the zooplankton (cladocerans and rotifers) population structure, which can alter ecological processes [17]. Due to cyanobacterial blooms, Daphnia populations may decrease when other food sources are depleted. Different species of Daphnia, such as D. pulicaria and D. pulex, can grow in the presence of some toxic cells [18], which affects the dynamics of the zooplankton population. Cyanobacterial toxins can be classified based on their chemical structures, such as cyclic peptides (microcystin and nodularin), alkaloids (anatoxin-a, anatoxin-a(s), saxitoxin, cylindrospermopsin, aplysiatoxins, lyngbyatoxin-a), and lipopolysaccharides (Table 1). Most cyanotoxins are neurotoxins or hepatotoxins [19].

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Figure 1 Bloom-forming cyanobacteria from different reservoirs in Varanasi, India. (A) Microcystis aeruginosa, (B) Merismopedia sp., (C) Anabaenopsis sp., (D) Anabaena sp., and (E) Oscillatoria sp. [12,13].

Table 1 The toxins produced by cyanobacteria and some dinoflagellates and their mechanism of action.

2.1 Neurotoxins

Neurotoxins are organic molecules that affect the nervous system of vertebrates and invertebrates. Neurotoxins usually have acute effects on vertebrates, with rapid paralysis of the peripheral skeletal and respiratory muscles. Other symptoms include loss of coordination, twitching, irregular gill movement, tremors, altered swimming, and convulsions before death due to respiratory arrest [7,11].

2.1.1 Anatoxins

Anatoxin-a (Figure 2a) is an alkaloid cyanotoxin that is neurotoxic to mammals and birds [3]. It is produced by Aphanizomenon spp. (Dolichospermum spp.), Anabaena, Phormidium, and Oscillatoria [36]. They inhibit transmissions at the neuromuscular junction by mimicking the neurotransmitter acetylcholine (blocks post-synaptic depolarization). They are chemically unstable and degrade in water by photolysis. Therefore, they accumulate to a lesser extent in the tissues of aquatic organisms [11]. Anatoxin-a(s) (Figure 2b) is an N-hydroxyguanidine methyl phosphate ester and is the only known natural organophosphate. It blocks acetylcholinesterase and has been isolated from Anabaena flos-aquae in North America, Anabaena lemmermannii in Denmark, and Anabaena crassa in South America [37]. It is a strong presynaptic and postsynaptic depolarizing agent competing with acetylcholine for nicotinic receptors in the central nervous system (CNS) [38].

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Figure 2 The chemical structures of (a) Anatoxin-a and (b) Anatoxin-a(s).

2.1.2 Saxitoxins

Saxitoxins are heterocyclic guanidines produced by freshwater cyanobacteria and are species-specific. Some examples of saxitoxin-producing cyanobacteria (Figure 3) include Geitlerinema amphibium, Lyngbya wollei, Cylindrospermopsis raciborskii, Phormidium uncinatum, Geitlerinema lemmermannii, and Cylindrospermum stagnale [39,40]. The production and distribution of saxitoxins in Anabaena and Cylindrospermopsis is associated with environmental stress, especially ionic stress, including those related to pH and Na+ concentration. When the concentration of Na+ increases in the medium, the concentration of saxitoxins decreases in Anabaena circinalis and increases in C. raciborskii, but the ratio of the intracellular and extracellular content remains similar [41]. Anabaena circinalis can reduce the production of saxitoxins when the pH increases up to 9. The complete sequence of the saxitoxin produced by C. raciborskii T3 strain encodes 26 genes (sxtA-sxtZ) [42].

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Figure 3 The chemical structure of Saxitoxin.

2.1.3 β-N-Methylamino-L-Alanine (BMAA)

BMAA is a non-protein amino acid with a molecular weight of 118 Da (Figure 4). It can be produced by all known groups of cyanobacterial blooms and also by diatoms and dinoflagellates [43]. BMAA exists freely in the environment and tissues but is mostly associated with proteins and can bioaccumulate and biomagnify along the food chain. It is found in Cycas seeds and produced by Nostoc blooms that have a symbiotic association with the cycad roots (in the Western Pacific) and is transported to the plant [44].

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Figure 4 The chemical structure of β-N-methylamino-l-alanine.

2.2 Hepatotoxins

Hepatotoxins are produced by many cyanobacterial species and cause the death of fish, birds, wild animals, livestock, and humans around the world [45]. Eukaryotic protein phosphatase type 1 and type 2A are altered by the cyclic heptapeptides or microcystins that cause excessive phosphorylation of cytoskeletal elements resulting in liver failure. They bind to the anion transport system in the hepatocyte cell membranes. [7,11].

2.2.1 Microcystins

Microcystins (Figure 5) are cyclic heptapeptides with many amino acids and can inhibit protein phosphatases [10]. Microcystins are the largest group of cyanotoxins, with more than 70 structural variants [46]. Microcystin is the only cyanotoxin for which the biosynthetic pathway and the gene cluster have been identified [47]. Their concentrations differ between cyanobacterial blooms and also within a single bloom. Intracellular microcystin content can differ from 10 to 420 femtogram/cell (fg/cell) in Planktothrix rubescens and from 100 to 4,000 fg/cell in Microcystis aeruginosa [14,48]. The symptoms of fish poisoning include flared gills because of difficulty in breathing and weakness or the inability to swim. Channel catfish, Ictalurus punctatus, can be affected by  ̴50 to 75 ng microcystin/L [49]. Affected fish may die within 24 h of exposure. Microcystins are produced by Microcystis, Planktothrix, Oscillatoria, Dolichospermum [50], and Merismopedia sp. (based on their 2-D sheet morphology) [51]. Dolichospermum flos-aquaee and Dolichospermum lemmermanni are found in lakes of Norway, Finland, Canada, and also the Baltic Sea [52,53,54]. A high concentration of microcystins (103 mg/L) caused the death of zebras, blue wildebeest, and rhinos in South Africa [55].

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Figure 5 The chemical structure of microcystin.

2.2.2 Nodularins (NOD)

Nodularins are cyclic pentapeptides (Figure 6) structurally similar to microcystins. Nodularins are produced by Merismopedia minutissima (based on their 2-D sheet morphology) [51] and Nodularia spumigena found in brackish water [56]. Nodularia does not form dense colonies and blooms during late summer under nitrogen-deficient conditions. Low or sufficient concentrations of N/P and high temperatures favor their growth [57]. Toxic strains of Nodularia are found in Australia, New Zealand, Nevada, and the Baltic Sea [4]. The highest concentrations of NOD have been reported in organisms from the Baltic Sea, for example, 2.5 µg/g in mussels and 0.91 µg/g DW in fish muscle. Nodularins are produced nonribosomally by multienzyme complexes encoded by the ndaS gene cluster [58] in Nodularia spumigena NSOR10.

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Figure 6 The chemical structure of nodularin.

2.2.3 Cylindrospermopsin (CYN)

Cylindrospermopsin (Figure 7) is a guanidine alkaloid synthesized by Cylindrospermopsis raciborskii and several other cyanobacteria. It affects several organs and tissues, inhibiting protein synthesis in plants and animals [20]. Cylindrospermopsis raciborskii is a harmful species that caused a waterborne, hepatitis-like illness in humans from Palm Island, Australia, in 1979 [59]. Cylindrospermopsin is also produced by Anabaena lapponica, Aphanizomenon (Chrisosporum) ovalisporum [60], Raphidiopsis curvata [29], and Aphanizomenon flos-aquae [61]. It shows hepatotoxic, nephrotoxic, and cytotoxic effects and acts as a carcinogen. It inhibits glutathione, cytochrome P450, and protein synthesis [62] (Figure 8). The highest concentration of cylindrospermopsin (173 µg/L) was found in an arid lake in Saudi Arabia [63]. Photodegradation occurs in the natural environment and depends on the water depth. Aeromonas sp. can remove cylindrospermopsin and the efficiency of removal depends on the pH and temperature [64]. Generally, cylindrospermopsin is present in small amounts in drinking water, but it was found in tap water samples (0.69 - 2.2 µg/L) from the Kinmen Island [65]. Cylindrospermopsin is hydrophilic, and its intestinal absorption and uptake into hepatocytes may be mediated by an active transport system such as the bile acid transport system, e.g., cholate and taurocholate.

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Figure 7 The chemical structure of Cylindrospermopsin.

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Figure 8 The pathways illustrate the mechanism of action of cylindrospermopsin (modified from [66]).

2.3 Dermatotoxin

2.3.1 Lipopolysaccharides (LPS)

Lipopolysaccharides (Figure 9) are present in the outer membrane of Gram-negative bacteria, including cyanobacteria [3,67]. They cause blisters, gastrointestinal disorders, and human skin irritation. Other skin irritants and inflammatory cyanotoxins produced by marine cyanobacteria are jamaicamides, aplysiatoxins, and lyngbyatoxins [7]. Anacystis nidulans, Microcystis, Anabaena, Spirulina, and Oscillatoria, produce LPS toxins [68].

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Figure 9 The chemical structures of (a) lyngbyatoxins and (b) aplysiatoxins.

3. Factors Affecting Cyanobacterial Blooms

3.1 Eutrophication

Nutrient pollution, such as that due to nitrogen (N) and phosphorus (P) (Figure 10), has increased in aquatic ecosystems due to various anthropogenic activities and gained more attention than other environmental drivers. Nutrient loading has increased due to wastewater and runoff from impervious surfaces. Atmospheric pollution has increased due to the increase in the rates of fossil fuel combustion in urbanized areas [69]. Eutrophication is responsible for the excessive growth of cyanobacteria or cyanobacterial blooms. Other harmful algal blooms (HABs) have also increased due to the increase in the human population [1]. When the nutrient content of freshwater bodies increases excessively (predominantly P), the phytoplankton community is dominated by cyanobacteria [70]. Experimental models speculate that in hot environmental conditions and summer, phytoplankton communities are dominated by cyanobacteria for P concentrations of ̴ 100 - 1,000 µg L-1 [71].

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Figure 10 Several factors affect cyanobacterial blooms, such as eutrophication, global warming, and increasing CO2 concentrations. Global warming affects cyanobacterial blooms by increasing temperatures and light intensity. Cyanobacteria have evolved advanced CO2-concentrating mechanisms such as the uptake systems of atmospheric CO2 and bicarbonate ions. Nutrient pollution, such as those associated with nitrogen and phosphorus, has increased in aquatic ecosystems due to urban and agricultural discharges and is responsible for eutrophication which causes cyanobacterial blooms (Illustration by S. Mishra).

The potential of cyanobacteria to uptake organic P with phosphatases and to retain abundant P vary across species. Fifty cyanobacterial strains in about 10 genera show remarkable differences in their ability to uptake P from different organic molecules [72]. Some Rivulariaceae and non-Rivulariaceae were tested to determine the production of nutrient P from most organic molecules. Rivulariaceae such as Calothrix, Dichothrix, and Gloeotrichia yielded a higher level of P than non-Rivulariaceae such as Anabaena, Fischerella, Lyngbya, and Tolypothrix. Among the tested cyanobacterial genera, Gloeotrichia notably expressed high extracellular phosphomonoesterase (PMEase) activity [72]. Similarly, variability in the capacity to store abundant P might exist in cyanobacteria. It could be more beneficial to some taxa relative to others during P deficiency. For example, Anacystis can take up more P than Anabaena, Plectonema, and Synechococcus [73].

Several cyanobacterial genera are responsible for forming blooms, where some species may be controlled by the availability of P and N [70,74]. Cyanobacteria-rich water bodies that play a role in bloom formation are known as cyanobacterial pools. Several studies have investigated cyanobacterial blooms to determine the level of P and N in cyanobacterial pools. Most cyanobacterial pools that consist of soluble N and P are composed of organic compounds [75]. The soluble or dissolved organic N and P are used by several cyanobacteria [74].

Inorganic nutrient pools are insufficient as a source of organic nutrients to account for the long duration of dense cyanobacterial blooms [1]. Researchers must examine the effects of all nutritive species and micronutrients such as Fe to comprehensively understand the factors that influence the density of cyanobacterial blooms. The effect of Fe is also found in diazotrophs as they require high levels of Fe for the enzyme nitrogenase, and thus, many studies have determined the effect of Fe on diazotrophs [76]. The recent development of molecular examinations for cyanobacteria has helped to understand how harmful cyanobacteria respond to various nutrients at the cellular level.

3.2 Global Warming

Global warming affects cyanobacteria in different ways by increasing the temperature and light intensity (Figure 10). Cyanobacteria grow rapidly in warmer water and a brighter environment [77]. Cylindrospermopsis raciborskii can grow profusely in freshwater under different environmental conditions and become toxic by bloom formation [78]. This species grows optimally at 30 °C [78]. Trichodesmium is a nitrogen-fixing marine cyanobacterium adapted to live under conditions of low nutrient, bright light, and clear surface water found in tropical and subtropical oceans [79]. Many cyanobacterial species grow better in warm water. Trichodesmium erythraeum bloomed in the Canary Islands Archipelago in August 2004, the hottest period (27.5 °C) recorded since 1912 [80]. A T. erythraeum bloom had not previously been recorded anywhere along the boundary of the African upwelling zone. This bloom was associated with unusual dust storms and warm weather in the area [80]. Trichodesmium bloom may also favor increased vertical stratification that is enhanced by the warming of sea surface waters. Cyanobacteria are found predominantly in the warmer months in subtropical estuaries (Pensacola Bay, FL) [81].

An increase in the frequency of blooming of a marine benthic Lyngbya sp. was recorded in the nearshore environments in the past decade [82,83]. The active growth of Lyngbya majuscula resulted in bloom formation, which was recorded in Moreton Bay, Australia, for several years. Several environmental parameters were evaluated before and during the bloom to determine the factors responsible for bloom dynamics [84]. The authors were monitoring a pulse of rainfall before the Lyngbya bloom, and periods of the high incident light, water temperatures above 24 °C, and cool weather were associated with the onset of the bloom. The cyanobacterium Phormidium corallyticum shows the highest photosynthetic activity in oxygenic environments at water temperatures of 30 - 37 °C.

Common corals are attacked by the black band disease that is caused by cyanobacteria, of which, Phormidium corallyticum is the prime constituent of the microbial consortium [85]. Many cyanobacterial species influence not only their growth rate but also their toxin production in response to light and temperature [86]. Toxin production in Microcystis aeruginosa increased as a response to irradiation under low-light conditions [87]. The microcystin composition of Planktothrix agardhii shifted with an increase in the amount of a toxic variant associated with high light intensity [88]. However, cyanobacteria did not grow densely under warm experimental conditions [89].

3.3 Increasing CO2 Concentrations

The partial pressure of CO2 in the atmosphere is correlated with the concentration of dissolved CO2 in water. However, cyanobacterial blooms can endure rising CO2 concentrations due to their photosynthetic capacity [90]. Cyanobacteria have evolved advanced CO2-concentrating mechanisms such as uptake systems of CO2 and bicarbonate [91,92]. Eukaryotic phytoplankton (green algae) are superior competitors at high concentrations of dissolved CO2, while prokaryotic phytoplankton (cyanobacteria) are better competitors at low concentrations of dissolved CO2 [93].

Various inorganic carbon uptake systems are regulated in cyanobacteria by many pathways, causing significant differences in CO2 responses across taxa [92,94]. Microcystis strains with high-affinity bicarbonate uptake systems are favored at low concentrations of dissolved CO2, as confirmed by selection experiments and lake examination [92,95]. Additionally, at high concentrations of dissolved CO2, the Microcystis strains, with a higher affinity to uptake bicarbonate than eukaryotic phytoplankton, are favored [96]. This study argues that the genetic diversity and physiological flexibility of cyanobacterial CO2-concentrating mechanisms enable quick acclimatization of bloom-forming cyanobacteria to high CO2 concentrations. Sharp CO2 gradients at the air-water interface increase the flow of CO2 into the surface layer, which can be prevented by surface-dwelling blooms [97]. Laboratory experiments and mathematical models speculate that cyanobacterial blooms are probably accelerated in eutrophic and hypertrophic waters in response to increasing atmospheric CO2 concentrations [90,96].

4. Effects of Cyanotoxins on Humans and Animals

The cytotoxic effects related to cyanotoxin ingestion, dermal contact, or intraperitoneal injection have been reported in several studies [98,99]. Respiratory symptoms are the most common complaints, and specific respiratory reactions associated with cyanobacterial blooms include sore throat, hay fever, and cough [98]. Inflammatory responses may occur in humans after inhaling cyanobacterial compounds in the air [99]. Various types of cyanotoxins and many analogs are produced by cyanobacterial blooms that vary in toxicological potential and other properties. Also, animal and in vitro studies have reported that crude cell extracts are more potent than dose-equivalent quantities of cyanotoxins [100].

4.1 Cylindrospermopsin

Cylindrospermopsin affects the liver and kidneys. Acute hepatic damage is confined to the centrilobular areas causing hepatocyte vacuolization and enhanced pigmentation of the nucleus and the cytoplasm. Renal toxicity is associated with necrosis, and the lumen of proximal tubules widens and changes in the glomerulus. Cytotoxic effects are related to oxidative stress due to an increase in H2O2 in a concentration-dependent manner, a reduction in the activity of SOD and CAT, an increase in glutathione peroxidase and apoptosis, and a decrease in the potential to fight pathogenic microorganisms [101,102]. Human peripheral blood neutrophils react to cylindrospermopsin (0.01 - 1 µg/mL), which reduces the production of reactive oxygen species (ROS) [103]. Apoptosis occurs in the human umbilical vein endothelial cell line (HUVEC) cells, causing morphological changes, including nucleolar segregation with altered nuclei, deterioration of the Golgi apparatus, and increase in granules. In primary rat hepatocytes, cylindrospermopsin induces transcription of the antioxidant response element (ARE)-binding factor, Nrf2. When RBCs (red blood cells) were exposed to cylindrospermopsin for 21 days, they showed abnormal spikes and very high cholesterol levels in the RBC membrane due to the inhibition of plasma lecithin cholesterol acyl transferase [104]. Chromosome alterations were not observed in Chinese hamster ovary (CHO)-K1 cells exposed to CYN with or without metabolic activation [105]. A high cylindrospermopsin concentration resulting from a cyanobacterial bloom caused the death of cattle in north Queensland [106]. CYN may impede the functions of fish phagocytic cells and affect their immunity [107].

4.2 Nodularins

Nodularins inhibit protein phosphatases, mainly PP2A (IC50 = 0.17 nM in the human red blood cell) [108]. NOD induces inflammation, endoplasmic reticulum (ER) stress, and associated unfolded protein response (UPR) in liver cells by acting through tumor necrosis factor α (TNF-α) [109]. NOD impedes nuclear excision repair (NER) by deactivating the excision repair cross complementation group 1-XPF and activating oxidative DNA damage in the human hepatoblastoma cell line HepG2 and the Chinese hamster ovary (CHO) cells [110]. NODs promote tumors, and in the two-stage carcinogenesis model in rats, NOD (25 µg/kg bw i.p.) activates the formation of placental glutathione S-transferase (GST-P) liver foci in initiated animals. NOD alone can cause hepatocyte growth until week 18 and also induce apoptosis and hyperphosphorylation of signaling proteins in cultured rat hepatocytes [111]. In the flatfish, Platichthys flesus, NODs cause oxidative stress resulting in the reduction of GST and CAT activity leading to an increase in the vulnerability of the cells to ROS [112].

4.3 Saxitoxins

Saxitoxins block voltage-gated Na+ neuron channels and arrest the transmission of action potentials resulting in rapid paralysis [113]. They accumulate in shellfish, and the related human illness is known as paralytic shellfish poisoning. Anatoxin-a can affect blood pressure, heart rate, and gas exchange, causing hypoxia, respiratory arrest, and severe acidosis, resulting in the death of the animals [114]. Antillatoxin is a novel ichthyotoxic (LC50 = 0.1 µM) substance isolated from Lyngbya majuscula [115]. Kalkitoxin (Figure 11) is toxic to the goldfish (Carassius auratus) and the brine shrimp (Artemia salina) with an LC50 of 700 and 170 nM, respectively [116].

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Figure 11 The chemical structure of Kalkitoxin.

4.4 Microcystins

Microcystins (MCs) can cause normocytic anemia and severe liver damage; other mammalian tissues are also affected. Additionally, MCs can have tumor-promoting, pulmonary, neurological, and reproductive effects [117]. Serine/threonine type 1 and 2A protein phosphatases (PP1 and PP2A, respectively) are inhibited by microcystin. Microcystin is not mobilized from the lung to the liver and the respiratory tract, indicating that it cannot easily cross the blood-air barrier in the lungs. Cyanobacterial bloom cells may be deposited in the lower respiratory tract [118]. Two types of human bronchial epithelial (HBE) cells express genes encoding organic anion transport proteins that are responsible for the cellular uptake of MC-LR [119]. At necropsy, severe lesions may be observed in liver tissues. MC-LR causes normocyte anemia and bone marrow injury and also affects the immune system of rabbits [120]. They also cause hepatotoxicity and neurotoxicity, kidney impairment, allergies, eye, ear, and skin irritation, and some gastrointestinal disorders such as nausea/vomiting and diarrhea in humans [19]. The large-scale death of lesser flamingos (Phoeniconaias minor Geoffroy) was reported in lake Manyara of Tanzania due to microcystin toxicity [121], where at least 6,000 birds belonging to 47 species, including endangered species such as the marbled teal (Marmaronetta angustirostris) and white-headed duck (Oxyura leucocephala), died due to the toxic effects of MC-LR at the Doñana National Park, Spain [122].

4.5 Lipopolysaccharides

Lipopolysaccharides (LPSs) cause fever in mammals and are involved in septic shock syndrome and liver injury [123]. They can impair the immune system and also affect the detoxification system of various organisms [124]. The function and effect of BMAA on human health are not well-known, but due to neurotoxic properties, it can cause severe neurodegenerative diseases, including amyotrophic lateral sclerosis (ALS). It might be incorporated in proteins, causing protein misfolding and leading to several neurodegenerative diseases [125]. BMAA affects motor neurons via many mechanisms; for example, BMAA can act on glutamate NMDA (N-methyl d-aspartic acid) and AMPA (alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid) receptors or induce oxidative stress and reduce glutathione [30].

5. Effects of Cyanobacterial Blooms on Aquatic Ecosystems

5.1 Effects of Cyanobacterial Blooms on Community Dynamics

Alterations in benthic and planktonic microbial communities are caused by cyanobacterial blooms. The composition of cyanobacterial species changes due to considerable shifts in the cyanosphere community [126]. Significant alterations in the taxonomic composition and gene expression of the cyanosphere community might occur with the different phases of bloom development. Mainly, heterotrophic bacteria related to the biodegradation of complex organic molecules become prominent during the lysis of cyanobacterial blooms [127]. In lake Taihu, microcystin degrading alphaproteobacteria of the family Sphingomonadaceae dominated the cyanosphere during the decomposition of a Microcystis bloom [128].

The temperature of the surface blooms in the Baltic Sea was approx. 1.5 °C above that of the ambient water [129]. The surface temperatures within cyanobacterial blooms in lake Ijsselmeer, Netherlands, were higher than those in the blooms of the surrounding surface waters [130]. Cyanobacteria can increase surface temperatures, which increases their competitive dominance over eukaryotic phytoplankton.

5.2 Other Effects of Cyanobacterial Blooms on the Ecosystem

Cyanobacterial blooms disrupt ecosystems by producing toxins, and several organisms are affected at different trophic levels. Cyanobacterial blooms adversely affect ecosystems by producing large amounts of organic matter, even without producing toxins, following bloom senescence. Huge amounts of decaying biomass are found at the bottom of the water bodies due to bloom die-offs, which cause hypoxic and anoxic conditions. Several benthic dwellers die due to low dissolved oxygen. Hence, the benthic diversity declines, resulting into the loss of primary producers and reduced food web functioning. The effect continues throughout the food web as enough nutrients are not available to the biota at intermediate and upper levels. This results in the loss of biological diversity at all levels, including the reduction in the population size of organisms that serve humans as food sources, food stock, and recreational activities. Habitat loss may also affect ecosystem sustainability leading to the growth of less desirable populations such as toxigenic cyanobacteria due to the absence of competition. Cyanobacterial blooms are generally found in areas with poor water quality and environments impeded by various stressors. The associated effects of the stressors are antagonistic or additive. This causes considerable ecological changes as the ecosystem reaches an ecological threshold beyond which it is unable to revert to its original state [100].

Aquatic organisms may be harmed either through direct ingestion of toxic cyanobacterial cells or through contact with cyanotoxins. Cyanotoxins can affect Daphnia pulicaria, reducing its filtration capacity and survival of offspring [131]. Cyanotoxins also affect algae, diatoms, and plants. Fischerellin, produced by Fischerella muscicola, inhibits the photosynthesis of other cyanobacteria [132]. Microcystin affects neuromuscular communication and, thus, significantly reduces the beat rates of the thoracic legs, mandibles, foregut, and second antennae in Daphnia. It also arrests the peristaltic movements of the midgut. Daphnia specimens that are fed microcystin-producing PCC 7806 wild-type cells suffer lethal poisoning. Consumption of microcystin (10.2 ng and 18.3 ng /mg body weight) caused rapid death of Daphnia galeata [133]. Low doses of microcystin do not affect Daphnia magna but high concentration for a long time inhibits the activity of the enzyme phosphatase [134]. Microcystins inhibit photosynthesis and growth and also cause the cells of Nostoc muscorum and Anabaena to break [135]. Anabaena lemmermannii, Aphanizomenon flos-aquae, and Nodularia spumigena inhibited the growth of the red alga Rhodomonas sp. and the diatom Thalassiosira weissflogii in vitro [136]. Microcystin (1.0 µgL−1) decreased the growth of Ceratophyllum demersum [137]. Microcystin can accumulate in tissues of Lymnaea stagnalis and reduce egg production [138]. Dreissenia polymorpha mussels fed on Microcystis aeruginosa CCAP 1450/10 showed a reduction in food intake, filtration, absorption, and fecal loss, and the net energy balance was impaired [139].

Saxitoxins produced by Aphanizomenon issastchenkoi decreased the somatic growth of Daphnia magna; also, reproduction rates of Daphnia pulex and Moina micrura were reduced by saxitoxins produced by C. raciborskii [140,141]. Cyanobacterial blooms can also harm fish by damaging the gills, digestive tract, and liver, causing death. The intake of microcystin increases after gill damage and leads to liver necrosis. Cyanobacterial blooms cause damage to the liver, heart, kidney, skin, gills, and spleen [34]. The effects of microcystins on various species of fish are summarized in Table 2. Generally, juvenile and sub-adult fish are more sensitive to toxic compounds than their adult counterparts. This may be due to the presence of a thin epithelial layer, relatively large body surface area, and high metabolic rate [142].

Cyanobacterial blooms affect the larval development in the carp Cyprinus carpio. Microcystis sp., Aphanizomenon flos-aquae, and Planktothrix agardhii showed embryotoxic effects such as significant fish mortality, delayed hatching, lower number of hatched embryos, the suppression of embryonic development, problems in filling the air bladder, and significant inhibition of glutathione S-transferase (GST). Survival rates decreased to 40% and 20% when the embryos of Danio rerio were given 50 or 5 µg/L MC-LR and MC-RR, respectively. Anatoxin-a caused fast opercular movement and abnormal swimming in Cyprinus carpio. Exposure to 400 µg/L of anatoxin-a changed the heart rate at several developmental phases of Danio rerio [143]. When Danio rerio embryos were given 500 µg/L saxitoxin, 34% of the embryos showed abnormal development; mainly, abnormalities in the lateral and ventral body curvature, edema, and mortality occurred during larval development after 21 days. Saxitoxins of Cylindrospermosis raciborskii changed the swimming behavior of Danio rerio [144]. Dissolved saxitoxins also reduced the spontaneous swimming behavior and touch response in larval herring (Clupea harengus pallasi) [145].

Table 2 The effects of microcystins in fishes.

6. Management Strategies for Cyanobacterial Blooms

Several management strategies, such as nutrient load reduction, hydrodynamic changes, and chemical and biological control have been developed to stop cyanobacterial blooms.

6.1 Nutrient Load Reduction

Nutrient load reduction can effectively improve water quality. The nutrient load can often be manipulated and, therefore, should be a central part of the strategy to mitigate cyanobacterial blooms. Nutrient load reduction requires national and international efforts in eutrophic, cyano-bloom susceptible lakes, rivers, estuaries, and coastal waters through a broad range of diffuse and point sources. In the 1970s and 1980s, the use of P in detergents was banned, and strict regulations were implemented on the use of N and P fertilizers to reduce nutrient contamination. Despite this step, it can take many years or even decades to successfully reduce external nutrients [150,151] and recycle internal nutrients, especially P, from lake sediments [152]. Additionally, delays in recovery might occur if the initial period of eutrophication has progressed in a lake ecosystem that is more resistant to change and is in a potentially stable state [153].

In many lakes, besides P binding soils, shifting of the lake sediment by sediment capping has been implemented to reduce internal P loading and promote lake recovery [154,155]. Additionally, sediments from shallow waters can be more readily reabsorbed by aerial and benthic organisms. For example, fish can reintroduce nutrients into the water column. Accordingly, these approaches for controlling blooms can be used simultaneously with external nutrient depletion for successful and extensive mitigation of blooms [156].

6.2 Hydrodynamics

To suppress cyanobacterial blooms, the artificial mixing of lakes may be an expensive but efficient process [97]. In this process, the cyanobacterial bloom is prevented by vertical mixing that overtakes the flotation velocity. Thus, the cyanobacteria are replaced by diatoms and green algae [97,157]. Elevated water flow or hydrodynamics can reduce cyanobacterial blooms and provide an effective mitigation strategy for stagnant rivers and reservoirs [158].

6.3 Chemical Control

Although chemical treatment can rapidly eliminate cyanobacterial blooms, it is a short-term solution. The chemically controlled mechanism of cyanobacterial blooms has not been approved because the chemicals persist in the environment. Chemicals such as copper sulfate, diuron, and many other algicides have toxic effects on other aquatic organisms [159]. Moreover, cell lysis and the release of cyanotoxins are also caused by the chemical treatment, which deteriorates water quality. Cyanobacteria are more sensitive to hydrogen peroxide than eukaryotic phytoplankton, and thus, cyanobacterial blooms are effectively eradicated using low concentrations of hydrogen peroxide [160,161]. A major benefit of this method is that the added hydrogen peroxide decays into water and oxygen within a few days and does not leave any chemical traces in the environment [160].

6.4 Biological Control

 

Cyanobacterial blooms can be controlled biologically, but this management strategy is not simple. Cyanobacterial blooms might be regulated effectively by the application of viruses, pathogenic bacteria, and fungi [162]. However, the occurrence of many resistant cyanobacterial strains renders these host-specific microbial antagonists ineffective [161,163]. Viral or fungal contaminations can cause rapid destruction of cyanobacterial biomass but rarely elicit a long-term reduction in cyanobacterial blooms [163,164]. Mollusks, such as the zebra mussel Dreissena polymorpha, filter water abundantly and eliminate phytoplankton and other suspended particles. The effect of Dreissena polymorpha on cyanobacterial blooms is under investigation. Dreissenid mussels from European lakes can significantly reduce cyanobacterial blooms since they filter many species of cyanobacteria, regardless of their toxicity [165].

In the Great Lakes of North America, dreissenid mussels can filter most single cells and small colonies. These lakes favor large and buoyant colonial cyanobacteria [166]. Zebra mussel invasions in the 1980s and 1990s occurred simultaneously with Microcystis blooms in Lake Erie and Lake Huron [167]. The zebra mussels of Europe and North America may vary in their genetic traits, adaptation history, and nutrient status [168]; these differences may have different effects and require further investigation. In many shallow lakes, the entire food web is disrupted by the elimination of planktivorous and benthivorous organisms and the addition of piscivorous fish[7,142,146]. Phytoplankton biomass is under the control of bio-direction. Bio-direction or biocontrol helps in suppressing fish-induced sediment resorption and increases the abundance of large zooplankton. Submerged macrophytes increase water transparency. The accessible nutrients are captured by the submerged macrophytes; thus, suppressing further sediment resorption and making the water clearer. Preliminary results are promising in waters with elevated internal nutrient load and continuous external nutrient inputs [169]. Therefore, this strategy might be worthwhile in the long term, provided the external nutrient load is effectively reduced [169,170].

7. Conclusion

Cyanobacteria can rapidly colonize aquatic ecosystems. The continued eutrophication, global warming, and increasing atmospheric CO2 concentrations are responsible for an increase in the incidence, intensity, and duration of harmful cyanobacterial blooms. Cyanobacterial blooms produce various secondary metabolites, and most of these are cyanotoxins which are harmful to plants, invertebrates, and vertebrates, including humans, at naturally occurring concentrations. These blooms adversely affect potable and irrigation water supplies, other recreational sources, and fisheries [171]. Bloom-forming cyanobacteria and their uncontrolled growth are the cause of many complications and require large-scale efforts to regulate bloom formation. Along with nutrient depletion, authorities tackling cyanobacterial blooms have to consider the physicochemical and hydrological effects of climate change in their management strategies, accounting for regional, climatic, and anthropogenically driven changes. Studies that focus on the effects of cyanobacterial blooms and their toxins on the individual components of ecosystems and their interactions need to be conducted. This could be achieved by performing culture, microcosm, mesocosm, and ecosystem field studies. Removing water from deep within the reservoir could be an effective strategy to minimize the algal concentrations in the water supply during cyanobacterial blooms. Additional observational studies are required to understand the process of excess bloom formation and regulate the species composition and production of cyanotoxins. Suitable management strategies, such as nutrient load reduction, hydrodynamics, biological control, and chemical control strategies, are required for bloom reduction. Some of these strategies were successful in the long term, while others had only short-term effects.

Acknowledgments

Sonal Mishra is thankful to the University Grants Commission (UGC), New Delhi, India, for the financial assistance in the form of a fellowship as a Junior Research Fellow. Neha Kumari is grateful to CSIR, New Delhi, India, for providing financial support in the form of a Senior Research Fellowship.

Author Contributions

S. Mishra and N. Kumari wrote the manuscript. RP Sinha and D-P Häder conceptualized the topic, and edited the manuscript.

Competing Interests

The authors have declared that no competing interests exist.

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