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Vol. 18 No. 2 - April 2012

Cyanobacterial toxins: A Growing Environmental Concern

By: Rakhi Bajpai* & M.R. Suseela

Cyanobacteria are morphologically diverse group of phototrophic prokaryotes. Eutrophication and climatic changes have increased the frequency and intensity of cyanobacterial blooms in freshwater bodies across the globe. Many of the bloom forming cyanobacteria produce toxic substances or cyanobacterial toxins thus posing serious threat to public health. Amongst the different categories of cyanobacterial toxins, microcystins (MCs) are the most prevalent in various freshwater bodies across the globe. Why do some cyanobacteria produce toxins? Whether toxins production confers any ecological advantage to the producer is still an open question, and their natural role remains an enigma. This article focuses on various aspects of cyanobacterial toxins especially the factors affecting cyanotoxin production, environmental fate of the cyanotoxins and their ecological role.

In the last 20 years, excessive pouring of nutrients and climatic changes have resulted in exuberant growth of cyanobacteria (a condition termed as ‘cyanobacteria bloom’) in freshwater bodies across the globe. Such blooms adversely affect the ecosystems and their biota, and are referred as ‘CyanoHABs (Cyanobacterial Harmful Algal Blooms)’. CyanoHABs have far reaching effects on species interactions, microbial population, macrophyte population, aquatic biota, human health, ecosystem integrity as well as on industries and economies. Many of the surface-bloom forming cyanobacteria produce toxins (cyanotoxins) and present a potential risk to public health. In the present scenario, cyanotoxins emerge as a global environmental concern. Climate change has led to the geographical expansion of some toxic cyanobacteria.

Cyanobacterial toxins or Cyanotoxins

Cyanobacteria produce a variety of secondary metabolites, some of which are toxic to invertebrates, mammals and other aquatic organisms. Toxic cyanobacteria are widely distributed, and have been recorded from every continent including Antarctica. Codd (1995) reported that 50-75% of the cyanobacterial blooms are toxic. However, toxicity varies at species and intra-species level, and with environmental conditions. A toxic cyanobacterium may or may not produce toxins. Likewise, it may produce more than one toxic compound. In freshwater habitats, Microcystis is the most common toxic cyanobacterium. Other genera include Anabaena, Oscillatoria, Nostoc, Anabaenopsis, Planktothrix, Aphanizomenon, Cylindrospermopsis, Raphidiopsis, Lyngbya, Nodularia and Phormidium.

Cyanotoxins vary widely in their chemical nature and structure, toxic potency, mode of action and organ affected (de Figueiredo et al., 2004). The most widely used approach to categorise cyanotoxins is based on the tissues affected (Sivonen and Jones, 1999). Accordingly, cyanotoxins are - hepatotoxins (microcystins and nodularins), neurotoxins (anatoxins and saxitoxins) and dermatotoxins (lipopolysacharides). Hepatotoxins and neurotoxins have emerged as a major concern to the water supplying agencies due to high exposure risk and lethality, while lipopolysacharides are produced by majority of cyanobacteria and have little health concern.

In natural freshwater bodies infested with cyanobacteria, microcystins (MCs) are the most prevalent cyanotoxins. One of the best-documented incidences of cyanotoxin related human causalities is from Caruaru (Brazil). In February 1996, 126 patients became seriously ill after dialysis, of which 60 patients died in hospital. Later, it was found that water for dialysis came from a local reservoir infested with heavy cyanobacterial bloom (Jochimsen et al., 1998). Analyses of the reservoir water revealed the presence of microcystins. MCs have been reported in a drinking water supplying reservoir in the Brazilian-Amazonia region (Vieira et al., 2005). Nodularin has limited presence in cyanobacteria contaminated freshwaters.

In general, neurotoxins are less frequent in freshwaters; hence offer lesser exposure risk to that of MCs. Neurotoxins such as anatoxin-a, -a(s) and saxitoxins are alkaloids highly toxic to nerves. Anatoxin binds to the nicotinic receptor and acts as a postsynaptic depolarizing neuromuscular blocking agent. Acute exposure of anatoxin causes death within minutes to a few hours depending on the species and the amount of toxin ingested. Edwards et al. (1992) reported that dog poisonings in Scotland were due to the consumption of Oscillatoria containing anatoxin-a. Saxitoxin is a tricyclic alkaloid; it blocks neuronal transmission by binding to Na+ channels in nerve cells. Resultantly, sodium gradient is stopped leading to muscle paralysis and death. Additional concern regarding the importance of cyanotoxins is reflected by their inclusion in the US Environmental Protection Agency (USEPA) drinking water contaminant list and in major reviews along with chemical warfare agents (Richardson and Ternes, 2005).

Environmental factors affecting cyanotoxins production

Light and temperature are the two important factors influencing cyanotoxins production in cyanobacteria. It was reported that under red and green light toxin production as well as toxicity (toxin to protein ratio) of the cyanobacteria increases compared to that of white light. Toxicity of the bloom also increases when light intensity decreases below 40 µE m-2s-1 (Utkilen and Gjølme, 1992). Optimum temperature for cyanotoxins production is 20-25°C (Watanabe and Oishi, 1985). Utkilen and Gjølme (1995) studied the effect of iron on toxin production by Microcystis aeruginosa. Jiang et al. (2008) used statistical approach to study the effect of different environmental factors (light intensity, temperature and iron, etc.) on the growth and MCs production by Microcystsis aeruginosa. The intracellular MC content is related to N: P ratio of the medium. Level of cyanotoxins (extracellular) in a water body shows seasonal fluctuation depending upon the physico-chemical factors of water bodies and cyanobacterial species dominating at particular time. Kurmayer (2011) studied the effect of physiological factors on the production of the toxic heptapeptide MC from Nostoc sp. strain 152 and found that MC content per cell showed a maximum under P-PO4-reduced and irradiance-reduced conditions. Both intra- and extracellular MC concentrations were negatively related to P-PO4 and irradiance. Joung et al. (2011) measured the dynamics of toxic and non-toxic cyanobacterium Microcystis in correlation with environmental factors using molecular techniques.

Environmental fate of cyanotoxins

Cyanotoxins are either membrane-bound or occur free within the cells. They are released passively in the medium with the aging and death of cyanobacterial population. During early growth phase, cyanotoxins remain inside the cells and released in the environment at late-log growth phase or after cell lyses. Active release of toxins may also occur from young growing cells. Watanabe and Oishi (1983) investigated the toxicity of a cultured strain of M. aeruginosa during different growth phases (lag, exponential and stationary phases). They found maximal toxicity during late exponential or at stationary growth phase. Release (concentration) of cyanotoxins in the medium also increases with various water treatment practices.

In natural ecosystems, released cyanotoxins undergo photo- and bacterial degradation. In addition, a significant fraction of released cyanotoxin becomes unavailable (for exposure) due to adsorption over the soil surfaces depending upon environmental factors, soil property and total organic content of the soil (Edwards et al., 2008). Degradation is generally preceded by a lag period of about 9 to 10 days. MC-LR is stable in waters with high pH and temperatures, but readily biodegraded in ambient waters with a half-life of about one week (Codd and Bell, 1996).

Ecological role of cyanotoxins

Though substantial progress has been made on the toxicity of cyanotoxins, a little is known about the benefit it provides to the producing organisms. Most of the organisms used in toxicity tests (invertebrates and mammals) are neither natural enemies nor consumers of cyanobacteria. Ecological and physiological role of cyanotoxins remain an enigma. In natural ecosystems, MCs are supposed to be involved in metal ion chelation (Humble et al., 1997), intraspecific signaling (Dittmann et al., 2001), and protection against predators such as zooplankton (Rohrlack et al., 2001) and in allelopathic interactions against competitive photoautotrophic organisms (Pflugmacher, 2002). Allelopathy refers to an inhibitory or stimulatory effect of plants and microorganisms on other plant species or microorganisms through the release of organic compounds. Such interactions occur in all aquatic habitats including phytoplankton communities. Phytoplankton allelopathy alters succession and the pattern of species dominance (Prince et al., 2008). However, information related to allelopathic role of cyanotoxins on associated bacteria (phycospheric biota) and other algae are meagre.

Cyanotoxins have adverse effect on other aquatic biota. Use of cyanobacteria infested waters for irrigation is perceived as a threat to the yield and quality of crop products (Bibo et al., 2008). Symptoms of MCs toxicity may result directly due to toxic fraction and indirectly involving oxidative damage induced by the toxin. Järvenpää et al. (2007) found that exposure of MCs to broccoli (Brassica oleracea–Greenia Hg) seedlings had mild (<10%) growth inhibitory effect, while mustard (Sinapis alba) seedlings remained unaffected. MCs exposure inhibits superoxide dismutase and peroxidase activities in rape (Brassica napus L.) and rice (Oryza sativa L.) seedlings resulting in oxidative damage to the plants (Chen et al., 2004). A substantial proportion of MCs present in the irrigation water is retained by the plants, and accumulates differentially in various parts, maximal in root tissues (Järvenpää et al., 2007).

Growth inhibitory effect of MCs has also been reported in Phaseolus vulgaris L. and Solanum tuberosum L. (McElhiney et al., 2001), Lepidium sativum L. (Gehringer et al., 2003), Brassica napus L. and Oryza sativa L. (Chen et al., 2004), Brassica oleracea var. italica and Sinapis alba (Järvenpäa et al., 2007), Spinacia oleracea (Plugmacher et al., 2007), Pisum sativum, Lens esculenta, Zea mays and Triticum durum (Saqrane et al., 2008). Uptake and translocation of cyanotoxins into edible plant parts could expose consumers to medically relevant toxic concentrations. Bioaccumulation of cyanotoxins in food chain and their effect on human health is an important issue.

The Microcystins (MCs)

MCs are cyclic heptapeptides consisting of five common amino acids and two variable L-amino acids. Based on single letter code classification of amino acids, variables of MC have been given different names depending upon the amino acids present at 2 and 4 positions (variable positions) of the structure. For example, MC-LR (the most common cyanotoxin found in water supplies around the world) contains amino acids Leucine (L) and Arginine (R) at the position 2 and 4, respectively. The unusual aromatic amino acid Adda, a common constituent of all MCs is solely responsible for the toxicity of MCs. It is a common constituent of all MCs. More than 80 congeners of MC are known, variations in the amino acids at other positions also give rise to various MC variants.

During bloom formation, different variants of MCs may be produced causing repeated but varied poisoning in animals visiting the water bodies. The levels and relative proportions of MC variants are regulated by external growth stimuli. World Health Organization (WHO) has set a threshold limit (1 µg l-1) for MC-LR in drinking waters. The International Agency for Research on Cancer (IARC) has classified MC-LR as a possible human carcinogen (group 2B) (IARC, 2006). Chronic consumption of MCs present in tap waters (at lower doses) could be a substantial risk factor for liver and colorectal cancer (Hernández et al., 2009). MCs inhibit protein phosphatase particularly, type-1 (PP1) and type-2 (PP2A) (members of protein serine/threonine phosphatase family) in liver cells causing rapid reorganization of all three major cytoskeleton components, microfilaments, microtubules and intermediate filaments.

Concluding remarks and future perspectives

Cyanobacterial toxins pose a threat to the water bodies and due to changing climate and increasing environmental pollution they are now considered as serious environmental concern.  To minimize the risks associated with cyanotoxins exposure, there is a need to monitor toxin producing cyanobacterial species, and environmental factors responsible for the production of cyanotoxins. The physical and chemical parameters regulating the toxin production should be identified in order to develop better understanding of the mechanisms controlling toxin production. Understanding the regulatory factors will lead to the development of means to control the harmful cyanobacterial blooms.

*Algology Section, Plant Diversity, Systematics and Herbarium Division, National Botanical Research Institute, Lucknow, India, *E mail: rakhi.bajpayi@gmail.com

This article has been reproduced from the archives of EnviroNews - Newsletter of ISEB India.

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