The presence of the toxic cyanobacteria and cyanotoxin, microcystin-LR (MC-LR) and other cyanotoxins, in drinking water sources poses a serious risk to public health. Iron based technologies using magnetic zero-valent iron nanoparticles (nZVI) and ferrate ion (FeVIO42−, Fe(VI)) represent greener approaches to remove cyanobacteria and degrade MC-LR in water. This paper reveals that nanoparticles of zero valent iron (nZVI) can destroy cyanobacteria in the source water and may play a preventive role in terms of the formation of cyanobacterial water blooms by removing nutrients like phosphate. Results on MC-LR showed that Fe(VI) was highly effective in removing MC-LR in water. Products studies on the oxidation of MC-LR by Fe(VI) demonstrated decomposition of the MC-LR structure. Significantly, degradation byproducts of MC-LR did not contain significant biological toxicity. Moreover, Fe(VI) was highly effective for the degradation of MC-LR in lake water samples. Mechanisms of removal and destruction of target contaminants by nZVI and Fe(VI) are discussed.

Cyanobacteria have critical functions in terrestrial and aquatic ecosystems, which include oxygen evolution, fixation of nitrogen and carbon dioxide, and biomass production (Huo et al. 2015). However, cyanobacteria are associated with many serious environmental problems, which have implications for water quality and public health (Adamovsky et al. 2015). Cyanobacteria generate many toxins such as microcystins (MCs), cylindrospermopsin, anatoxins nodularins, and saxitoxins, which can cause a significant health hazard in drinking water (Sharma et al. 2012). Toxic effects include hepatotoxicity, cytotoxicity, neurotoxicity, embryotoxicity, dermatotoxicity or immunotoxicity. Additionally, cyanobacteria commonly produce heptatoxic MCs, which are stable in water. MCs have been found in drinking waterbodies worldwide, causing potential risk to human health (Li et al. 2015). Moreover, MCs can easily accumulate in aquatic biota which has implications for human and environmental health. Among the various MCs, MC-LR is the most common of the microcystins. MC-LR is of great concern in water bodies due to its acute toxicity (LD50 = 50 μg kg−1 in mice) (Sharma et al. 2012). The World Health Organization has established a provisional guideline limit of 1 μg L−1 for MC-LR (Ibelings et al. 2014).

In recent years, several technologies have been sought to remove extracellular cyanobacteria and MC-LR in water (Sharma et al. 2012; Jiang et al. 2014). Treatment may be classified into two categories: physical removal and oxidative transformation. Activated carbon, coagulation–flocculation–sedimentation, and sand and membrane filtration are examples of physical–chemical methods. Applications of physical processes generally need replacement of materials (e.g. activated carbon and membranes) and/or cleaning because of fouling. Oxidation methods include UV-based advanced oxidation technologies, photocatalytic and chemical oxidation (Sharma et al. 2012, 2014). MC-LR is stable under natural sunlight and resistant to degradation by UV radiation (Westrick et al. 2010). Photocatalytic degradation of MC-LR using titanium dioxide (TiO2) is promising (Sharma et al. 2012); however, it requires separation of the catalyst after removal of MC-LR and needs additional energy for the photoactivation of photocatalyst. Chlorine, chlorine dioxide, chloramine, ozone, and permanganate have been applied to remove MC-LR in water (Sharma et al. 2012). The reaction of chlorine with MC-LR resulted in chlorine substitution, which generates potentially toxic chlorinated by-products (Acero et al. 2008; Huang et al. 2008). In addition, the possibility of the reaction between chlorine and bromide ion produces HOBr, which can produce toxic brominated by-products (Heeb et al. 2014). The degradation of MC-LR by chloramine was not significant. Chlorine dioxide is capable of degrading MC-LR, but high doses are required. This limits the practical application due to the generation of chlorite and chlorate as by-products after the use of chlorine dioxide (Kull et al. 2004). Applications of ozone and permanganate in oxidizing MC-LR are promising (Sharma et al. 2012).

This paper deals with zero valent iron nanoparticles (nZVI) and high valent tetraoxy compound of iron (ferrate, FeVIO42−, Fe(VI)) based technologies to treat cyanobacteria and MC-LR in water (Marsalek et al. 2012; Jiang et al. 2014). Both of these technologies are environmentally friendly and can address some of the drawbacks of other treatment methods. The effect of nZVI and Fe(VI) ions in treating cyanobacteria and MC-LR under various environmental conditions are reviewed.

ZVI has received tremendous interest in removing various contaminants (Bae & Hanna 2015). ZVI has a high capability to remove various contaminants from groundwater and wastewater. In the past few years, emphasis has been placed on the nano ZVI nanoparticles (nZVI), which have shown remarkable reduction properties to remediate numerous inorganic and organic contaminants (Crane & Scott 2012; Yan et al. 2013; Jarošová et al. 2015). Small size, large surface area, good transport properties and specific mechanism of reaction with water under anaerobic conditions are key properties for its effectiveness to remove contaminants (Klimkova et al. 2011; Mueller et al. 2012; Raychoudhury & Scheytt 2013; Yan et al. 2013; Filip et al. 2014; Baikousi et al. 2015; Jarošová et al. 2015; Soukupova et al. 2015). In recent years, developing composite materials containing nZVI has been emphasized to enhance removing contaminants due to the combination of reduction/sorption or reduction/antimicrobial properties of hybrids (Marková et al. 2013; Petala et al. 2013; Baikousi et al. 2015). ZVI has also shown inactivation of bacteria like Escherichia coli (Lee et al. 2008). In recent years, the role of nZVI in the destruction of cyanobacterial cells was explored (Marsalek et al. 2012).

Application of nZVI to remove cyanobacteria was carried out using water inoculated with a Microcystis aeruginosa laboratory strain that remained in the colonial form (CCT12/2—8) (Marsalek et al. 2012). The average particle size and surface area of applied nZVI were ∼70 nm and ∼25 m2/g, respectively. Detailed chemical, microscopic, and microbiological analyses were performed (Marsalek et al. 2012). The results on nZVI treatment of cyanobacteria showed multiple modes of action: (i) the removal of bioavailable phosphorus, (ii) the destruction of cyanobacterial cells, and (iii) the immobilization of MCs (Marsalek et al. 2012). Release of cyanobacteria may thus be influenced by nZVI. Significantly, the ecotoxicological study demonstrated that nZVI was a highly selective agent (EC50 = 50 mg/L against cyanobacteria). This level of EC50 was 20–100 times lower than that the EC50 for fish, water plants, algae, and daphnids. Figure 1 shows the deformation of cells caused by the aggregated Fe(OH)3, which was generated as the major product from the nZVI treatment of cyanobacteria (Marsalek et al. 2012). Furthermore Fe(OH)3, a nontoxic product, was capable of promoting flocculation, resulting in gradual settling of the decomposed cyanobacterial biomass (Figure 1).
Figure 1

(a) Scanning electron microscope (SEM) images of cyanobacteria before treatment, (b) unused nZVI particles, (c) highly deformed cells after brief exposure to nZVI, and (d) completely destroyed cells surrounded by ferric oxide aggregates. (Adapted from Marsalek et al. (2012) with the permission of the American Chemical Society.)

Figure 1

(a) Scanning electron microscope (SEM) images of cyanobacteria before treatment, (b) unused nZVI particles, (c) highly deformed cells after brief exposure to nZVI, and (d) completely destroyed cells surrounded by ferric oxide aggregates. (Adapted from Marsalek et al. (2012) with the permission of the American Chemical Society.)

Close modal

Fe(VI) ion in the aquatic environment has strong oxidation capability (Sharma 2002). For example, the redox potential of Fe(VI) in aqueous solution is the highest among other conventional disinfectant and oxidants used in water and wastewater treatment (Jiang & Lloyd 2002). Numerous examples have displayed simultaneously disinfection, oxidation, and coagulation properties of Fe(VI) (Eng et al. 2006; Sharma 2007a; Filip et al. 2011; Jiang 2015; Prucek et al. 2015; Sharma et al. 2016). In a single Fe(VI) dose treatment, inactivation of microorganisms, oxidative transformation of inorganic and organic contaminants, and toxins, as well as removal of toxic metals and phosphate can be achieved (Sharma 2010; Jiang 2014, 2015; Yates et al. 2014; Sharma et al. 2015). Fe(VI) as a disinfectant can inactivate a wide range of microorganisms (Sharma 2007b; Jiang 2014). The kinetics of the reactions with various pollutants with a variety of molecular and structural configurations (e.g. sulfide, bisulfite, iodide, cyanides, ammonia, selenium, arsenic, azide, thiols, amines, amino acids) showed the feasibility of their removal by Fe(VI) (Lee et al. 2009, 2014; Lee & von Gunten 2010; Sharma 2011, 2013; Zimmermann et al. 2012). The ferric oxide, generated from Fe(VI), acts as an efficient coagulant to remove humic acids, radionuclides, metals, arsenic and non-metals (Horst et al. 2013; Prucek et al. 2013, 2015). Fe(VI) as a pre-oxidant is able to decrease the concentration of disinfection byproducts, formed during chlorination of water (Gan et al. 2015; Yang et al. 2015). Recently, research in our laboratories has focused on the role of Fe(VI) in removing and oxidatively transforming toxins such as MC-LR. Below is the summary of results observed in studying the kinetics and oxidized products (OPs) and their toxicity in the oxidation of MC-LR by Fe(VI) (Jiang et al. 2014).

Kinetics

The oxidation of the MC-LR by Fe(VI) followed a second-order kinetics (-d[Fe(VI)]/dt = kapp[Fe(VI)][MC-LR]). The values of kapp showed a pH dependence with values ranged from 1.3 ± 0.1 × 102 mol−1 Ls−1 at pH 7.5 to 8.1 ± 0.08 mol−1 Ls−1 at pH 10.0. This indicates a rapid degradation of MC-LR (Jiang et al. 2014). The comparison of the rate constants for the oxidation of MC-LR with different oxidants at neutral pH is presented in Table 1 (Kull et al. 2004; Acero et al. 2005; Onstad et al. 2007; Rodríguez et al. 2007). Ozone showed the highest value of kapp (Table 1). The efficient attack on the double bond of MC-LR by ozone may be responsible for orders of magnitude faster reactivity in comparison with other oxidants. The increasing order of the reactivity with MC-LR may be presented as chlorine dioxide < chlorine < Fe(VI) < Mn(VII) < O3 (Table 1). The half-life (t1/2) for oxidizing MC-LR by O3 is less than a second whereas Fe(VI), Mn(VII), and chlorine oxidize MC-LR in seconds. Ozone, chlorine, Mn(VII), and Fe(VI) are thus suitable oxidants to eliminate MC-LR in water treatment.

Table 1

Second-order rate constants and half-lives for oxidation of MC-LR by different oxidants at 22–25 °C

  k,kapp M−1s−1t1/2
OxidantSpeciesM−1s−1pH 7.0
Ferrate(VI)a HFeO4 (3.9 ± 0.2) × 102 2.5 × 102 155 s 
(pK3 = 7.23)f FeO42− 8.0 ± 2.0   
Permanganateb MnO4 3.6 × 102 3.6 × 102 107 s 
Chlorinec HOCl 1.2 × 102 7.2 × 101 504 s 
(pKa = 7.54)g OCl 6.8   
Chlorine dioxided ClO2 1.0 1.0 13.1 h 
Ozonee O3 4.1 × 105 4.1 × 105 0.08 s 
  k,kapp M−1s−1t1/2
OxidantSpeciesM−1s−1pH 7.0
Ferrate(VI)a HFeO4 (3.9 ± 0.2) × 102 2.5 × 102 155 s 
(pK3 = 7.23)f FeO42− 8.0 ± 2.0   
Permanganateb MnO4 3.6 × 102 3.6 × 102 107 s 
Chlorinec HOCl 1.2 × 102 7.2 × 101 504 s 
(pKa = 7.54)g OCl 6.8   
Chlorine dioxided ClO2 1.0 1.0 13.1 h 
Ozonee O3 4.1 × 105 4.1 × 105 0.08 s 

aThis study and half-life at dose [Fe] = 1 mg L−1 or [FeO42−] = 2.2 mg L−1.

bFrom Rodríguez et al. (2007) and half-life at dose [Mn] = 1 mg L−1 or [MnO4] = 2.2 mg L−1.

cValues at pH 7.2 taken from Acero et al. (2005) and half-life at [HOCl] = 1 mg L−1.

dFrom Kull et al. (2004) and half-life at [ClO2] = 1 mg L−1.

eFrom Onstad et al. (2007) and half-life at [O3] = 1.0 mg L−1.

fAt 25 °C.

gAt 25 °C from Carrell Morris (1966).

OPs

Analysis of OPs of degradation of MC-LR was carried out by high resolution liquid chromatography–mass spectrometry/mass spectrometry technique (Jiang et al. 2014). The proposed structures for the OPs were based on the molecular formula and are summarized in Table 2. Basically, four primary reactions occurred from the attacks of Fe(VI) on the aromatic ring, diene, enone, and amide functionalities of MC-LR by Fe(VI) (Figure 2). In hydroxylation of the aromatic ring, mono, di and trihydroxylation of the aromatic ring were obtained with corresponding m/z = 1011.5510, 1027.5459, and 1043.5408 (Table 2). Monohydroxylation involved the loss of a hydrogen atom to yield a highly stabilized aromatic product (M + 16). Further hydroxylation thus formed di- and tri- hydroxylation products. Hydroxylation of the carbon–carbon double bond in the MHDA moiety also occurred, which resulted in the formation of an enol functional group through the elimination of an H atom. Tautomerization of the enol group gave a chiral center at the alpha position. A pair of diastereotopic isomers consistent with m/z 1011.5510 (M + 16) were thus obtained (Table 2). Fe(VI) also oxidized the diene group of the Adda moiety of MC-LR via dihydroxylation to yield products with M + 34 (Table 2). This corresponded to addition of two HO groups without loss of H atoms. Hydroxylation yielded 1,2-, 3,4-, and 1,4-diol products (Table 2). Significantly, the products seen from the attack on diene moiety were also reported in oxidation performed by photocatalytic and electrochemical process (Antoniou et al. 2008; Zhang et al. 2013; Zong et al. 2013; Liao et al. 2014). The cleavage of peptide bonds in MC-LR by Fe(VI) was also seen, which caused the hydrolysis of amide bonds of D-glu-MDHA and the l-Arg-Methyl d-Asp of the MC-LR by Fe(VI) (Jiang et al. 2014). This step of the attack of Fe(VI) on the peptide bond was similar to the transformation of -NH = C- amino acid functionality by Fe(V) (Bielski et al. 1994; Rush & Bielski 1995).
Table 2

OPs observed during hydroxylation of moieties of MC-LR by Fe(VI)

MoietyOPs
Benzene ring  
MDHA  
Diene  
MoietyOPs
Benzene ring  
MDHA  
Diene  
Figure 2

Fe(VI) attacks on different moieties of MC-LR. (Adapted from Jiang et al. (2014) with the permission of the American Chemical Society.)

Figure 2

Fe(VI) attacks on different moieties of MC-LR. (Adapted from Jiang et al. (2014) with the permission of the American Chemical Society.)

Close modal

Removal and biological toxicity assessment tests

Removal of MC-LR by Fe(VI) was confirmed by conducting tests in water and lake water samples (Brno, Czech Republic) (Jiang et al. 2014). The lake water had total organic carbon of 7.9 mg L−1. In performing tests, the water samples were spiked with MC-LR (25.0 μg L−1) and an addition of FeO42− into the samples was 5.0 mg L−1. The removal of MC-LR in deionized water was almost complete over the entire pH range of 6.0–8.0 at 20 °C (Figure 3). At pH 7.0 and 8.0, the removal percentages were >99.0% (or <1 μg L−1), while a slight decrease at pH 6.0 (96.2%) was noticed. As shown in Figure 3, an Fe(VI) dose of 5.0 mg L−1 as FeO42− could remove ∼ 75% in lake water at pH 7.0. This indicates that the other components present in the lake water (e.g. dissolved organic matter) may also be reacting with Fe(VI) (Horst et al. 2013). Fe(VI) dose >5.0 mg L−1 would be required to completely remove MC-LR in the lake water (Jiang et al. 2014).
Figure 3

Removal of MC-LR in deionized water and lake water by Fe(VI) ([MC-LR] = 25.0 μg L−1, [FeO42−] = 5.0 mg L−1, and temperature 20 °C). (Adapted from Jiang et al. (2014) with the permission of the American Chemical Society.)

Figure 3

Removal of MC-LR in deionized water and lake water by Fe(VI) ([MC-LR] = 25.0 μg L−1, [FeO42−] = 5.0 mg L−1, and temperature 20 °C). (Adapted from Jiang et al. (2014) with the permission of the American Chemical Society.)

Close modal

The MC-LR is an inhibitor of protein phosphatase (PP1 and PP2A) enzymes, therefore, the PP1 inhibition was utilized to evaluate the biological activity of the Fe(VI) treated solutions (Jiang et al. 2014). When MC-LR was totally removed by Fe(VI) ion, the biological activity of OP was almost completely eliminated. This demonstrated that the OPs of MC-LR were not biologically toxic (Jiang et al. 2014).

The removal of MC-LR by photocatalytic oxidation system was also sought (Yuan et al. 2006; Sharma et al. 2010). Figure 4 shows the results in the TiO2-UV-MC-LR, Fe(III)-TiO2-UV-MC-LR, and Fe(VI)-TiO2-UV-MC-LR systems. Both Fe(III) and Fe(VI) ions in the system enhanced the photocatalytic oxidation of MC-LR (Figure 4). The effectiveness of Fe(VI) ion was more than that of Fe(III) ion. Significantly, complete removal of MC-LR was achieved by Fe(VI) in 30 min (Figure 4). Formation of highly reactive intermediate Fe(V) species and also increasing amount of holes (i.e. oxidant) in iron species containing TiO2 photocatalytical systems may have resulted in enhanced removal of MC-LR (Sharma et al. 2010).
Figure 4

The photocatalytic degradation of MCLR. Conditions: [ferrate(VI)] = 0.08 mmol L−1 and Fe(III) = 0.36 mmol L−1. (Adapted from Sharma et al. (2010) with the permission of Springer Inc.)

Figure 4

The photocatalytic degradation of MCLR. Conditions: [ferrate(VI)] = 0.08 mmol L−1 and Fe(III) = 0.36 mmol L−1. (Adapted from Sharma et al. (2010) with the permission of Springer Inc.)

Close modal
  • Both nZVI and Fe(VI) showed their potential as sustainable green materials to remove cyanobacteria and cyanotoxins in water.

  • nZVI was highly effective in destroying cyanobacteria via multiple modes of action.

  • The products of MC-LR oxidation by Fe(VI) were observed from the hydroxylation of benzene ring, diene, enone, and peptide bond of MC-LR, which did not have any significant toxicity.

  • Fe(VI) could degrade MC-LR in water and lake water samples on a time scale of seconds.

  • Magnetic separation of generated iron oxides from nZVI and Fe(VI) treatment can be achieved using a cost effective low-gradient magnetic field.

The authors acknowledge the support of the United States National Science Foundation (CBET-1439314, 1236209, and 1235803) for this research. V. K. Sharma, R. Zboril, and B. Marsalek also acknowledge the support of the Operational Program Research and Development for Innovations–European Regional Development Fund (CZ.1.05/2.1.00/03.0058) and of the Technological Agency of the Czech Republic–the project Environmental Friendly Nanotechnologies and Biotechnologies in Water and Soil Treatment (TE01020218).

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