Biosensing of microcystins in water samples; recent advances

Highlights

• Quality and safety of water has paramount importance for animals and human health.

• Contamination of water with Microcystins causes serious health threatening problems.

• Monitoring water quality is necessary due to the hepatotoxicity potential of MC-LR.

• Sensitive analytical methods are vital for controlling of Microcystins levels.

• Biosensors are emerged as precious and sensitive tools for Microcystins detection.

Abstract

Safety and quality of water are significant matters for agriculture, animals and human health. Microcystins, as secondary metabolite of cyanobacteria (blue–green algae) and cyclic heptapeptide cyanotoxin, are one of the main marine toxins in continental aquatic ecosystems. More than 100 microcystins have been identified, of which MC-LR is the most important type due to its high toxicity and common detection in the environment. Climate change is an impressive factor with effects on cyanobacterial blooms as source of microcystins. The presence of this cyanotoxin in freshwater, drinking water, water reservoir supplies and food (vegetable, fish and shellfish) has created a common phenomenon in eutrophic freshwater ecosystems worldwide. International public health organizations have categorized microcystins as a kind of neurotoxin and carcinogen. There are several conventional methods for detection of microcystins. The limitations of traditional methods have encouraged the development of innovative methods for detection of microcystins. In recent years, the developed sensor techniques, with advantages, such as accuracy, reproducibility, portability and low cost, have attracted considerable attention. This review compares the well-known of biosensor types for detection of microcystins with a summary of their analytical performance.

Introduction

Water is the most important natural resource for living organisms since life is not possible without it (Velichkova et al., 2020). This indicates the necessity for precious monitoring and global management of water resources (Garrote, 2017; Pradinaud et al., 2019). Water contamination and water-borne diseases can lead to the universal scale damage (Pandey et al., 2014). Cyanobacterial harmful algal blooms (Cyano-HABs) are one of the most important origins of water contamination, providing signs like color, odor and production of extremely toxic compounds, which are known as cyanobacterial toxins (cyanotoxins) (Pelaez et al., 2010). The existence of cyanotoxins in drinking water is considered as a hazardous problem for human health, because they can gather in aquatic organisms and then be transferred to human through the food chain (Codd et al., 2017). Cyanotoxins are classified as hepatotoxins, neurotoxins, cytotoxins and dermatotoxins, based on their mode of action (Vankova et al., 2019; Vogiazi et al., 2019). Also, according to their chemical structure, the major types of cyanotoxins are alkaloids, cyclic peptides and lipopolysaccharides (Vankova et al., 2019).

Microcystins (MCs) are the most common cyclic heptapeptide cyanotoxins with high toxicity and broad distribution (Chen et al., 2016b; Humbert, 2009) which is known as serious human and animal health threatening (Codd, 2000). MCs are secondary metabolites of different species of freshwater cyanobacteria (formerly known as blue-green algae) such as Anabaena, Microcystis, Nostoc and Plankothrix (Bartram and Chorus, 1999; Bownik and Skowroński, 2007). This toxin is released in water when cells are lysed under stress or age and may be transferred to sea-foods. Hence, consuming of MCs-contaminated foods and swimming in water contaminated with MCs would cause some health problems like headaches, fever, diarrhea, abdominal pain, nausea and vomiting. MCs are composed of an unusual aromatic amino acid, ADDA (3-amino-9-methoxy-2,6,8-trimethyl-10-phenyldeca-4,6-dienoic acid), and two variable amino acids (Fig. 1A) (Pravda et al., 2002; Van Apeldoorn et al., 2007). The unique structure of MCs causes the great stability at warm and cold water and in different pH. More than 100 different variants of MCs have been identified (Chen et al., 2016b). Microcystin-leucine arginine (microcystin-LR; MC-LR) (Fig. 1B) is the most prevalent and toxic MC in saltwater and freshwater worldwide (Rastogi et al., 2014).

MCs are specific and strong inhibitors of eukaryotic protein serine/threonine phosphatases 2A and 1 (PP2A and PP1), which have key roles in the regulation of apoptosis and organization of cytoskeleton (Chen et al., 2016b). Interaction of MCs with PP2A subunits results in cellular damage mainly through disruption in oxidative phosphorylation system and homeostasis of mitochondrial respiratory chain (Campos and Vasconcelos, 2010; McLellan and Manderville, 2017). There is also considerable evidence for MCs-induced oxidative stress in various organs such as the kidney, liver, intestine, brain and testis (Wang et al., 2010). MC-LR also leads to disturbance of the endoplasmic reticulum and mitochondrial pathways, inducement of apoptosis as well as upregulating proapoptotic genes (Zhou et al., 2015). MCs also demonstrate carcinogenic potential in many organs which is noticeable by upregulation of proto-oncogenes (Vichi et al., 2016). So, the growing concern about MCs in the aquatic ecosystems, especially in drinking water, shows an important aspect to the detection of MCs. Estimating the risk of MCs in water to human populations needs both experimental and epidemiological toxicological research. The maximum acceptable concentration of MC-LR recommended by World Health Organization (WHO) is 1 μg L⁻¹ in drinking water (Pham and Utsumi, 2018).

Over the past few years, several conventional strategies have been employed for the detection of MCs, including high-performance liquid chromatography (HPLC), the enzyme-linked immunosorbent assay (ELISA), thin layer chromatography (TLC), gas chromatography–mass spectrometry (GC-MS), liquid chromatography–mass spectrometry (LC-MS) and nuclear magnetic resonance (NMR). ELISA has been frequently applied for the determination of MCs in water, being it an on-site detection method. GC-MS can detect and quantify MCs based on complex procedures as compared with LC-MS, and thus the accuracy of GC-MS is lower than LC-MS. However, low sensitivity and specificity, being time-consuming, high-cost, requiring experienced operators and the difficulties in sample preparation are the drawbacks of these methods (Table 1). These limitations favor the development of portable, fast and sensitive devices such as biosensors or integrated analysis systems as appropriate alternatives to the classical approaches. Biosensor-based methods provide a great sensitivity and specificity and are fast, low-cost and reproducible with no need, in many cases, to difficult sample preparations as compared to conventional methods (Hassanpour et al., 2018a, 2018b). Hence, the purpose of this review is to give an update of the literature regarding the use of biosensors for the determination of MCs.