# Removal of Cyanotoxins–Microcystins from Water by Filtration through Granulated Composites of Bentonite with Micelles of the Cation Octadecyltrimethyl Ammonium (ODTMA)

^{1}

^{2}

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## Abstract

**:**

## 1. Introduction

^{2}[11]. The micelle–clay complex ODTMA–bentonite has an excess of positive charges of half of the cation-exchange capacity (CEC) of the clay mineral. Filtration of toxic cyanobacteria suspension through granulated composites yielded a significant reduction in the number of cyanobacteria cells, or filaments, and their corresponding toxins. Furthermore, the micelle–clay complex ODTMA–bentonite demonstrated a high removal rate of microcystins in batch experiments [6].

## 2. Materials and Methods

^{−2}s

^{−1}, to obtain a cell density of ca 1 × 10

^{7}cells mL

^{−1}with a chlorophyll concentration of ca 1000 μg L

^{−1}. Cultures from different growth phases were used for the extraction of microcystins. In addition, Microcystis colonies were collected from Lake Kinneret (Sea of Galilee, Israel) during a Microcystis bloom event (February–March 2018) [13], using a silk plankton net of 63-µm mesh size, to select predominantly Microcystis colonies. Immediately after transport to the laboratory, samples were first filtered through a 200-μm sieve to remove large particles and then through a 63-μm sieve. The collected samples of Microcystis colonies were maintained in a small volume of BG11 medium at 20 °C and continuous light of 15-μmol photons s

^{−1}m

^{−2}until further processing for the extraction of microcystins.

^{®}GF/F 47-mm diameter membrane filter (www.gelifesciences.com/whatman, accessed on 2 March 2021) to obtain a clear solution enriched with MCs. In cases where high concentrations of soluble MCs were detected, the Microcystis biomass was removed by centrifugation, followed by filtration on Whatman

^{®}GF/F membrane filter.

^{−1}. Prior to each experimental run, tap water was added to the columns at a slow rate in an upward direction in order to eliminate air pockets and channeling. Each experiment was conducted in duplicate. A GAC filtration column (10-cm length, 1.4-cm diameter) was prepared as described above, but the column was filled with 9 g of GAC.

^{3}]-RR, MC-RR, MC-WR, MC [D-Asp

^{3}]-WR, and MC-YR—using authentic standards purchased from Enzo Biochem, Inc. (NY, USA). Other eluted MC congeners could be identified by their typical absorption spectra, but due to the lack of standards, they were annotated as MC-like. Sensitivity and accuracy of this method was determined as proposed by [16]. Alternatively, MC concentrations were determined immunologically, using microcystin ELISA kits (Abraxis, Los Angeles, CA, USA), according to US EPA Official Method 546.

_{0}. The beginning and end parts of the filter are at the coordinates X = 0 and X = L, respectively. We consider a situation where a solution containing several (I = 1, …, m) pollutants (e.g., microcystins) is provided at given concentrations, C

_{0i}, i.e., Ci(X,t) = C

_{0i}for X ≤ 0, where t denotes the time.

_{v}is the flow rate (volume/time) and f is the fraction of pore volume out of the total volume of the filter. R(X,t) denotes the molar concentration of free adsorbing sites, i.e.,

_{0}− ∑ RLi(X,t)

_{i}are the forward rate constants of adsorption (M

^{−1}min

^{−1}) and D

_{i}(min

^{−1}) are the rate constants of dissociation.

_{i}(M

^{−1}) = C

_{i}/D

_{i}. Another parameter is R

_{0}, the molar concentration of adsorption sites for a given amount of complex in the filter.

## 3. Results and Discussion

#### 3.1. Removal of MC-LR from Water

#### 3.2. Co-Removal of MC Congeners Originating from Biological Sources

#### 3.3. Fitting the Filtration Model to Experimental Results and Estimation of Adsorption Capacity

_{0}to be used in the calculations in Figure 5 had to be 0.00015 M

^{−1}rather than the 0.0027 M

^{−1}value used in Figure 4.

_{1}and D

_{1}are inversely proportional to the viscosity of the medium. The values used for C

_{1}and D

_{1}in Figure 4 were 3000 M

^{−1}min

^{−1}and 0.003 min

^{−1}, respectively (Table 2), i.e., 3/8 of the values used in Figure 5, but the value of the affinity constant K= C

_{1}/D

_{1}= 10

^{6}M

^{−1}was the same.

_{0}= 0.005 M, C

_{1}= 8000 M

^{−1}min

^{−1}, and D

_{1}= 0.003 min

^{−1}. In the case of a solution of 62 µg/L, we used the same value of R

_{0}and C

_{1}as for the other cases, but D

_{1}was slightly enlarged to 0.005 min

^{−1}(Table 2 and Figure 6).

#### 3.4. Model Calculations for Filtration of Solutions with Several MCs

_{0}and C

_{i}, D

_{i}(I = 1–3). A simplification was introduced by assuming that MC-LR and MC-YR are similar, thus using R

_{0}= 0.005 M and the same kinetic rate constants as previously determined for MC-LR solutions (Table 2). This reduced the number of parameters to be determined to just two: C

_{RR}and D

_{RR.}The model results are presented in Figure 7 together with the measured results. The value of the forward rate constant C

_{RR}, 350 M

^{−1}min

^{−1}was almost 23-fold smaller than C

_{LR}, and the value of D

_{RR}(0.0075 min

^{−1}) was 1.5-fold larger than that of D

_{LR}. This implies that the affinity constant K

_{RR}= C

_{RR}/D

_{RR}= 4.7 × 10

^{4}M

^{−1}is 34-fold smaller than K

_{LR}= 1.6 × 10

^{6}M

^{−1}. It is of interest to note that the use of Lake Kinneret water gave similar efficiency of MC-LR removal as for cell cultures, indicating that the presence of DOC molecules in the lake water had little effect on the adsorption of the toxins by the filter matrix.

_{RR}and D

_{RR}as for Figure 7 (Table 2). The value of R

_{0}was reduced to 0.002 M, in order to fit the large emerging concentrations of the WR and RR toxins. The values determined were C

_{WR}= 1300 M

^{−1}min

^{−1}and D

_{WR}= 0.0012 min

^{−1}, which amount to K

_{WR}= 1.1 × 10

^{6}M

^{−1}, 1.45-fold smaller than K

_{LR}. However, it should be noted that the value of R

_{0}in the case of LR is 2.5-fold larger than that determined for WR. The results in the four parts of Figure 8 were considered as a combined sample of four competing toxins (2 pairs) for adsorption by the filter sites. The values of the statistical criteria for the fits of the calculated values to the experimental ones were RMSE = 3.6 and R

^{2}= 0.944.

_{RR}than that of K

_{WR}and its corresponding larger rate constant of desorption, which results in a reduction in the adsorbed amounts of RR due to the competition with WR, when the available numbers of unoccupied surface sites of the complex in the filter are reduced. The mechanism is not a direct exchange reaction, but rather a statistical preference of occupying sites of the complex, which become vacant instantaneously due to desorption of RR. This effect was analyzed and shown experimentally for a pair of filtered herbicides [17].

#### 3.5. Simulation and Prediction of Toxin Filtration by the ODTMA–Bentonite Granulated Complex—Summary of Kinetic Parameters

_{0}, the total molar concentrations of adsorbing sites, vary as they depend on the concentration of the complex and the fraction of pore volume in the filter. The relatively small values (less than 1) are mainly due to the size of the toxin molecules (molecular masses around 1000 Da). The large values of the kinetic parameters of forward adsorption, C

_{i}, and the small values of the dissociation, D

_{i}, in the cases of the toxins MC-LR and MC-YR reflect their large affinity of adsorption to the complex in the filter, which is expressed by K = C

_{1}/D

_{1}.

^{6}to 2.7 × 10

^{6}M

^{−1}for the same value of R

_{0}. The variation in K-values corresponds to around 20% in the capacity of filters with this toxin.

#### 3.6. The Capacity of the ODTMA–Bentonite Complex for Filtration of Microcystin Solutions

^{3}/kg). However, the calculations indicate that the concentration of MC-LR in the emerging water after filtration of 30 L is only 0.1 µg/L. Extending the filtration to 110 h, or 33 L, would yield a value of the emerging concentration of the toxin, C = 0.9 µg/L, and the capacity would be 4.7 m

^{3}/kg. For the 62 µg/L solution, the corresponding capacity is 2 m

^{3}/kg. A calculation tested the possibility to extend the capacity of the ODTMA–clay granulated material by using a large-scale filter. A 1-m-long filter operated at a flow velocity of 6 m/h yielded an increase in capacity to 6 m

^{3}/kg for a solution of 5.5 µg/L of toxin. For a solution of 5 µg/L of toxin and a velocity of 1 m/h, the capacity would be 8 m

^{3}/kg. Another aspect is the maximal loading of the toxin by the complex during filtration. For a toxin solution of 62 µg/L, the loading is 120 mg/kg. Calculations on the passage of a 1-mg/L solution of MC-LR indicated that a long filter could adsorb up to 1.5 g MC-LR per kg of complex with emerging concentration below 1 µg/L. The total amount of toxin which can be retained in such a filter irrespective of the emerging toxin concentration can reach 3 g per kg of complex. The maximal adsorbed loadings which satisfy emerging concentrations below 1 µg/L were as follows for several other MC congeners: 0.4 g/kg for MC-WR, and a significantly lower value of 0.012 g/kg for MC-RR.

#### 3.7. Granulated Activated Carbon (GAC) to Complement MC Removal by ODTMA–Bentonite Granulated Complex

## Author Contributions

## Funding

## Institutional Review Board Statement

## Informed Consent Statement

## Data Availability Statement

## Conflicts of Interest

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**Figure 1.**Residual MC-LR in effluents following filtration of toxin solution of (

**A**) 10 μg/L; (

**B**) 100 μg/L and (

**C**) 49 μg/L as a function of the accumulated MC-LR loaded on the column. For A and B, pure MC-LR solutions were used. For C, MC-LR originating from Microcystis aeruginosa strain PCC7806 biomass was used. See the text for more details on the experiments. The column in (

**A**) and (

**C**) contained 9 g of granulated complexes of ODTMA–clay, whereas the column in B contained only 1 g of the granules mixed with washed quartz. The black dots in the graphs represent specific MC concentrations in the loaded solutions. Analytical standard error for MC-LR is less than 5%.

**Figure 2.**Residual MC congeners in effluents of filtration experiments, using extracts from M. aeruginosa C1004 cultures from various growth phases, as a function of the accumulated MCs loaded on the columns of granulated complexes of ODTMA–clay. Results for three runs corresponding to different cultures (Table 1) are presented. The upper panels show data for MC-RR and MC [D-Asp3]-RR and lower panels for MC-WR and MC [D-Asp3]-WR. The black dots in the graphs represent specific MC concentrations in the loaded solutions. Analytical standard error for MCs was less than 5%.

**Figure 3.**Residual MC congeners in effluents following filtration experiments using extracts from Microcystis biomass collected from Lake Kinneret, as a function of the accumulated MCs loaded on the columns of granulated complexes of ODTMA–clay. The black dots in the graphs represent specific MC concentrations in the loaded solutions. Analytical standard error for MCs was less than 5%.

**Figure 4.**Removal of MC-LR from a 10-µg/L solution by filtration through a column filled with a granulated complex of ODTMA–clay at a flow rate of 3.2 mL/min for 38 h. Experimental results are presented along with the results of the simulation model (RMSE = 6.6). The parameters used in the calculations were R

_{0}= 0.0027 M, C

_{1}= 3000 M

^{−1}min

^{−1}, D

_{1}= 0.003 min

^{−1}.

**Figure 5.**Experimental and calculated values of removal efficiency of MC-LR from a 100-µg/L solution filtrated through a column of 30-cm length and 1.6-cm diameter, filled with 1 g of granulated complex of ODTMA–clay mixed with excess sand. A flow rate of 4 mL/min was used. The values of the parameters used in the calculations were R

_{0}= 1.5 × 10

^{−4}M, C

_{1}= 8000 M

^{−1}min

^{−1}, D

_{1}= 0.008 min

^{−1}. The fit gave (RMSE = 1.4).

**Figure 6.**Emerging concentrations (measured and calculated) of MC congeners during filtration of a 62-µg/L MC solution. The measured emerging concentrations include both MC-LR and MC-like congeners. The calculated root mean square deviation (RMSE) for the measured vs. calculated values was 2.4, considering both MC-LR and MC-like measured congeners. The parameters used in the calculations were R

_{0}= 0.005 M, C

_{1}= 8000 M

^{−1}min

^{−1}, and D

_{1}= 0.005 min

^{−1}. Using the value D1 = 0.003 min

^{−1}gives calculated emerging values of 0 at all times. The black dots in the graphs represent MC-LR concentrations in the loaded solution.

**Figure 7.**Emerging concentrations (measured and calculated) of MC-LR, MC-YR, and MC-RR during filtration of an MC solution originating from Microcystis biomass collected from Lake Kinneret. The black dots in the graphs represent specific MC concentrations in the loaded solutions. The calculated root mean square error (RMSE) for the measured vs. calculated values for MC-RR was 1.4. Measured and calculated emerging concentrations for MC-LR and MC-YR were 0. The fit of all calculated to experimental points yielded R

^{2}= 0.98.

**Figure 8.**Emerging concentrations (measured and calculated) of MC-WR, MC [D-Asp3]-WR, MC-RR, and MC [D-Asp3]-RR, during filtration of the MC solution originating from Microcystis culture (Figure 2). The black dots in the graphs represent specific MC concentrations in the loaded solutions. The calculated root mean square error (RMSE) for the measured vs. calculated values for the whole combined dataset was 3.6 and the value of R

^{2}was 0.944.

**Figure 9.**Residual MC congeners in effluents of filtration experiments, using extracts from a culture of M. aeruginosa strain C1004 (mid-exponential phase), as a function of the accumulated MCs loaded on a column of granulated activated carbon (GAC). The left panel shows data for MC-RR and MC [D-Asp3]-RR and the right panel for MC-WR and MC [D-Asp3]-WR. The black dots in the graphs represent specific MC concentrations in the loaded solutions. Analytical standard error for MCs was less than 5%.

**Table 1.**MC sources, types, and concentrations, in extracts originating from Microcystis cultures and Microcystis biomass collected from Lake Kinneret (LK) and used in filtration experiments using beds of granulated complexes of ODTMA–clay. Analytical standard error for MCs was less than 5%.

MC Source | DOC (μg/L) | Total MC (μg/L) | Major MC Congeners (μg/L) | |||||
---|---|---|---|---|---|---|---|---|

MC-LR | MC-YR | MC-RR | MC [D-Asp^{3}]-RR | MC-WR | MC [D-Asp^{3}]-WR | |||

M. aeruginosa C1004—Early exponential phase | 5.8 | 250 | n.f. | n.f. | 37 | 17 | 112 | 84 |

M. aeruginosa C1004—Mid-exponential phase | 8.0 | 242 | n.f. | n.f. | 87 | 35 | 73 | 47 |

M. aeruginosa C1004—Late stationary phase | 38.0 | 1553 | n.f. | n.f | 117 | 204 | 383 | 829 |

LK population | 3.3 | 152 | 83 | 43 | 26 | n.f. | n.f. | n.f. |

M. aeruginosa PCC7806 | 3.3 | 49 | 49 | n.f. | n.f. | n.f. | n.f. | n.f. |

**Table 2.**Kinetic parameters used in simulations and predictions of MC toxin filtration of columns filled with ODTMA– bentonite granulated complex.

MC Type and Conc. (µg/L) | R_{0} (M) | C_{1} (M^{−1} min^{−1}) | D_{1} (min^{−1}) | K (M^{−1}) | Data Presented in |
---|---|---|---|---|---|

MC-LR, 10 | 0.0027 | 3000 | 0.003 | 10^{6} | Figure 1A/Figure 4, B1 |

MC-LR, 100 | 0.00015 | 8000 | 0.008 | 10^{6} | Figure 1B/Figure 5, B1 |

MC-LR, 5.5 | 0.005 | 8000 | 0.003 | 2.7 × 10^{6} | Figure 2/Figure 6, B2 |

MC-LR, 26.7 | 0.005 | 8000 | 0.003 | 2.7 × 10^{6} | Figure 2/Figure 6, B2 |

MC-LR, 62 | 0.005 | 8000 | 0.005/0.003 | 1.6 × 10^{6}/2.7 × 10^{6} | Figure 2/Figure 6, B2 |

MC-LR, 83 MC-YR, 43 MC-RR, 25.9 | 0.005 | 8000 8000 350 | 0.005 0.005 0.0075 | 1.6 × 10^{6}1.6 × 10 ^{6}4.7 × 10 ^{4} | Figure 3/Figure 7 |

MC-WR MC-RR | 0.002 | 1300 350 | 0.0012 0.0075 | 1.1 × 10^{6}4.7 × 10 ^{4} | Figure 8 |

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**MDPI and ACS Style**

Sukenik, A.; Viner-Mozzini, Y.; Mizrahi, D.; Tamam, I.; Benitez, A.R.; Nir, S.
Removal of Cyanotoxins–Microcystins from Water by Filtration through Granulated Composites of Bentonite with Micelles of the Cation Octadecyltrimethyl Ammonium (ODTMA). *Appl. Nano* **2021**, *2*, 67-81.
https://doi.org/10.3390/applnano2010006

**AMA Style**

Sukenik A, Viner-Mozzini Y, Mizrahi D, Tamam I, Benitez AR, Nir S.
Removal of Cyanotoxins–Microcystins from Water by Filtration through Granulated Composites of Bentonite with Micelles of the Cation Octadecyltrimethyl Ammonium (ODTMA). *Applied Nano*. 2021; 2(1):67-81.
https://doi.org/10.3390/applnano2010006

**Chicago/Turabian Style**

Sukenik, Assaf, Yehudit Viner-Mozzini, Daniel Mizrahi, Imri Tamam, Ana R. Benitez, and Shlomo Nir.
2021. "Removal of Cyanotoxins–Microcystins from Water by Filtration through Granulated Composites of Bentonite with Micelles of the Cation Octadecyltrimethyl Ammonium (ODTMA)" *Applied Nano* 2, no. 1: 67-81.
https://doi.org/10.3390/applnano2010006