Removal of Endocrine Disrupting Chemicals in Wastewater by

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Removal of endocrine disrupting chemicals in wastewater by enzymatic treatment with fungal laccases Dennis Becker, Sara Rodriguez-Mozaz, Sara Insa, Rob Schoevaart, Damia Barcelo, Matthias De Cazes, Marie Pierre Belleville, José Sanchez Marcano, Andrea Misovic, Jörg Oehlmann, and Martin Wagner Org. Process Res. Dev., Just Accepted Manuscript • Publication Date (Web): 27 Mar 2017 Downloaded from http://pubs.acs.org on March 27, 2017

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Organic Process Research & Development

Removal of endocrine disrupting chemicals in wastewater by enzymatic treatment with fungal laccases Dennis Becker*a, Sara Rodriguez-Mozazb, Sara Insab, Rob Schoevaartc, Damià Barcelób, d, Matthias de Cazese, Marie-Pierre Bellevillee, José Sanchez-Marcanoe, Andrea Misovica, Jörg Oehlmanna, Martin Wagnera a

Biological Sciences Division, Aquatic Ecotoxicology, Goethe University Frankfurt, Max-von-

Laue-Str. 13, 60438 Frankfurt, Germany b

Catalan Institute for Water Research (ICRA), ParcCientíficiTecnològic de la Universitat de

Girona, Emili Grahit 101, 17003 Girona, Spain c

Chiralvision BV, J.H. Oortweg 21, 2333CH Leiden, Netherlands

d

Water and Soil Quality Research Group, Institute of Environmental Assessment and Water

Research (IDAEA-CSIC), C/Jordi Girona 18-26, 08911 Barcelona, Spain e

Institut Européen des Membranes , ENSCM, UM2, CNRS - Université de Montpellier , CC 047,

Place Eugène Bataillon, 34095 Montpellier, France

ACS Paragon Plus Environment

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Keywords:

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Bisphenol A, enzyme, degradation, micropollutants, sewage treatment, hormones,

trace pollutants, nonylphenol

Abstract

In this study the enzymatic degradation of hormones and endocrine disrupting compounds was investigated in artificial mixtures and in real wastewater by fungal laccases (Trametes versicolor, Myceliophthora thermophila). Several studies have already reported the successful enzymatic degradation of EDCs. However, with regard to a large scale application, the influence of some factors such as enzyme immobilization and costs are often lacking. Furthermore, the majority of studies investigated the removal of EDCs by chemical analysis only, while our main interest was to use bioassays to study the decrease in the endocrine activity. The removal of estrogenic, androgenic and anti-androgenic activity was assessed by yeast-based reporter gene assays and the degradation of industrial chemicals by an additional chemical analysis. It was demonstrated that the degradation of hormones and EDCs by laccases is feasible even at very low enzyme concentrations (2.8 ABTS U/L). In the artificial mixtures the main removal mechanism was adsorption onto immobilization supports. In binary mixtures, immobilized laccase was best in removing EDCs within the first 6 h of exposure (83% for T. versicolor and 87% for M. thermophila) but in the course of the experiment adsorption superimposed this removal after 24 h (99% after 24 h). A similar pattern was seen in wastewater, but with less carrier material (lower adsorption) and a constant enzyme activity, immobilized laccase showed best removal rates of estrogenic (82% removal after 24 h) and androgenic activity (99% removal after 6 h). With this in mind, this enzymatic technology can be a valuable addition to other treatment technologies.


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1

Introduction

Micropollutants comprise of a plethora of different compounds and are constantly released into the environment at low concentrations. Wastewater treatment plant (WWTP) effluents are point sources of these pollutants because many compounds are not, or insufficiently, degraded1, 2. Depending on the compounds, this contamination can be of concern towards organisms which are exposed to these substances. There was the perception that certain chemicals were able to interfere with the functioning of receptors whose normal role is to mediate the effects of the endogenous steroid hormones3. On the one hand natural hormones are able to bind these receptors; on the other hand there are chemicals that are able to do the same. They can act as hormone agonist or antagonist, some of them at likewise low concentrations (in the ng/L range). These substances are called endocrine disrupting chemicals (EDCs) and are worrisome because they can induce adverse effects in aquatic wildlife and are suspected to impair the reproductive functioning or lead to cancer in humans4. For instance, exposure to estrogen-like EDCs induced feminization of fish in situ in rivers and in a whole lake experiment5-7. As many environmental estrogens are also anti-androgenic8, this feminizing effect can be further amplified9. Moreover, some androgens are able to affect the pheromone-mediated behavior of many fish species10. In addition, complex mixtures of diverse EDCs are present in aquatic ecosystems, aggravating the environmental impact11. Therefore, a removal of these compounds from wastewater effluents is of great importance to prevent them from entering natural waters1. There are several approaches to address this issue. One example is to enhance the removal effectiveness of the conventional activated sludge treatment. Other options implement advanced treatment technologies in addition to the biological wastewater treatment. The quaternary treatment can be based on sorption to activated carbon, advanced oxidation processes (e.g.


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ozonation), electrochemical techniques and irradiation. However, these technologies have several limitations including higher costs12, incomplete decontamination or the formation of toxic byproducts2. Some recent studies investigated another biotechnological option, namely, the enzymatic degradation of micropollutants13-17. One promising group of enzymes for this purpose are laccases, which are mainly produced by wood decaying fungi. Laccases are a class of various extracellular ligninolytic enzymes produced by these fungi to degrade lignin and other polyphenolic compounds in wood18. Additionally, laccases have demonstrated their ability to degrade a broad range of xenobiotics including several phenols, hormones, plasticizers, polycyclic aromatic hydrocarbons and others19. The successful degradation of EDCs has already been demonstrated with whole fungi20 and the pure enzyme or enzyme formulations13, 21, 22. However, with regards to a large scale application in WWTPs, the use of enzymes immobilized on carrier materials is recommended. In the immobilized form, enzymes are more robust and can be retained within the system allowing recovery and multiple reuses23, 24. In addition, the use of lower amounts of enzymes is preferable due to their high costs. Furthermore, the majority of studies have investigated the removal of EDCs by chemical analysis only15, 25, 26, while the main interest of this work was to use bioassays to study the removal of the endocrine activity. A sole or concomitant ecotoxicological evaluation is a fundamental factor in degradation studies, for example, Becker et al.17 detected the generation of toxic by-products alongside the successful removal of antibiotics from wastewater. The aim of this study was to investigate the enzymatic degradation of hormones and EDCs in spiked water samples and in real wastewater by fungal laccases with minimal enzyme usage.


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Commercially available laccases from two different species (Trametes versicolor, Myceliophthora thermophila) were used either in free form or immobilized on carrier materials (polymeric beads and ceramic membranes). The mixtures contained natural and synthetic steroids as well as industrial chemicals. A binary mixture and a more complex mixture containing eight different EDCs were monitored for their degradation during enzymatic treatment. To be more realistic, the influent from a WWTP in Southern Germany, nonspiked and spiked with the EDCs mixture were additionally treated and monitored. The removal of estrogenic, androgenic and anti-androgenic activity was assessed by yeast-based reporter gene assays and degradation of industrial chemicals by an additional chemical analysis.


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Materials and methods

2.1 Chemicals, enzymes and carrier materials Estrone (E1), 17β-estradiol (E2), 17α-ethinyl-estradiol (EE2) and bisphenol A (BPA) were purchased in purities ≥ 98% from Sigma Aldrich (Steinheim, Germany). Nonylphenol (NP, 85% purity) and propylparaben (PrPb, ≥ 99.9%) were supplied by Fluka (Sigma Aldrich, Steinheim, Germany). Benzyl-n-butyl phthalate (BBP, ≥ 98%) was acquired from Alfa Aesar (Karlsruhe, Germany). Estriol (E3, 95%) was purchased from Cayman Chemical Company (Michigan, USA). All CAS numbers are listed in the supporting information in Table S1 and molecular structures are displayed in Table 1. Table 1: Molecular structures of steroid hormones and endocrine disrupting compounds used in this study. Steroid hormones O H3C

1

H

Estrone (E1)

H

H HO

CH3

2

OH

H

17ß-estradiol (E2) H

H

HO

OH H3C OH

3

Estriol (E3)

H H

H

HO


6

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OH

CH

H3C

4

H

17α-ethinyl estradiol (EE2) H

H

HO

Endocrine disrupting compounds

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Bisphenol A (BPA)

CH3 HO

OH CH3

CH3

6

Nonylphenol (NP) HO

O

O

H3C

7

Propylparaben (PrPb) OH

O

8

Benzylbutylphthalate (BBP)

O O

CH3

O

Laccase from T. versicolor (51639, Batch: BCBF7247TV) was a product from Sigma Aldrich. Laccase from M. thermophila (NZ51003, Batch: OMN07013) was supplied by Novozymes, Bagsvaerd, Denmark. Two different carrier materials were used in this study, porous polymeric beads (product: IB-EC1 with polyacrylic, carboxylic ester as functional groups, water content


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65% when fully wetted, surface area 250 m²/g, pore volume 2 mL/g and particle size of 350-700 µm) and ceramic membranes (multi-channel membrane (TiO2, 7-channel), 1 cm external diameter, 0.2 cm hydraulic diameter, 25 cm in length, and 1.4 µm of mean pore size, TAMI Industries). The wastewater was provided by a WWTP in Langenau, southern Germany (16,600 population equivalents), 2.5 million m³/year, with high influent of hospital wastewater. The hospital has 375 beds and approximately 9,000 patients per year. The raw wastewater was additionally filtered through a glass fiber filter (1.5 µm pore size, Ø 90 mm, Whatman). 2.2 Enzyme immobilization and activity An amount of 80 mL laccase from Myceliophthora thermophila (644 ABTS U/g) was diluted with 120 mL phosphate buffer (10 mM, pH 6.5) and mixed with a solution of 1 mL 0.5 M pentaethylenehexamine (Aldrich 292753). 200 g fully wetted IB-EC-1 beads (ChiralVision) were mixed with 1.5 mL glutaraldehyde (50%, Sigma-Aldrich 49629) and subsequently mixed with the enzyme solution. These were incubated overnight at 4°C and then washed 3 times with 200 mL demineralized water. The beads with immobilized enzyme were then dried with a stream of air until the LOD was 78% of BPA, NP and E2 and >98% of E1, usually within a very short time (minute range). Advanced treatment with granulated activated carbon results in removal rates of >43% for E2 and EE2, 65% for E1 as well as BPA and 84% for NP. The highest removals have been reported for membrane bioreactors; in raw wastewater, BPA, E1 and E3 are completely removed. In synthetic wastewater, BPA, E2, EE2 and NP are degraded by more than 90% (all data reviewed by Luo et al.53). Stalter et al.54 showed a removal of estrogenic (77–99%) and anti-androgenic activity (63– 96%) by ozonation and activated carbon. In this study with EDC mixtures in ultrapure water and wastewater, a complete removal of PrPb and NP was observed and an almost complete removal of BPA and BBP after 24 h of treatment with laccases immobilized on polymeric beads. Also the estrogenic and antiandrogenic activities decreased by a great extent. While this removal was the result of adsorption to the carrier material and enzymatic degradation, it can be concluded that the performance of this technology is similar to other advanced treatment technologies. However, it has to be taken into account that batch experiments were carried out at the lab scale, while most of the other technologies are ready for application to the full-scale treatment at WWTPs. Given the early stages of development of the enzymatic treatment technology, this comparison can only be preliminary. The estimation of costs of the enzymatic treatment technology is preliminary and, therefore, varies greatly. Depending on the carrier material and the enzyme, latest estimations predict


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additive costs of around 0.018–0.130 €/m3 55. The estimated costs for ozonation or activated carbon are 0.04–0.2 €/m3 56, 57. Consequently, a future reduction in costs of the carrier materials and enzymes, as well as an improvement of enzyme activity and stability, would render enzymatic wastewater treatment a very promising method complementing existing technologies. Apart from the potential use of laccases in wastewater treatment, the fields of application for laccases in industry and biotechnology are manifold. Their main application fields are in the pulp and paper industry, the textile industry as well as the food industry, but also find usage in nanotechnology, petrochemical industry, cosmetics, medical applications, synthetic chemistry or other bioremediation treatments58-59. In pulp and paper industry laccases are used for a variety of processes, such as bleaching, pulping, delignification etc.; an example of a commercial application is the Lignozym®-process60. In textile industry the use of commercial laccases is increasing as well. Their main application is in denim bleaching and finishing, e. g. DeniLite® from Novozymes, or Zylite® from Zytex58. Because laccases have the potential to degrade diverse chemical structures, it also seems an attractive solution for the removal of dyes and other phenolic compounds from industrial effluents or treating industrial process water58, 59. However, in these applications we face the same obstacles as already mentioned with wastewater treatment. There is a need for cheap and high production of optimized enzymes. 5

Conclusions

An effective removal of the endocrine activity of mixtures of EDCs and in wastewater has been demonstrated by laccases from T. versicolor and M. thermophila. It was established that the degradation of hormones and EDCs by laccases is feasible even at very low enzyme concentrations (2.8 ABTS U/L) as well as the depletion of BPA, BBP, NP and PrPb. The enzyme


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activity and its consequential price is an important factor with regards to the scale up and the implementation of this technology. Immobilized enzymes displayed better removal performance compared to the free enzyme. This was the case for the laccases from T. versicolor as well as for M. thermophila. Besides the good performance of the laccase, adsorption to the polymeric carrier was the main factor for the elimination of pollutants. Supporting Information. Compositions of the binary and complex EDC mixtures with relative equivalent potencies, CAS numbers, and EC50 values; weights of carriers and laccase activities; recovery rates for industrial chemicals, removal of BPA, NP, BBP, PrPb in the EDCs spiked wastewater; concentration-response relationships of individual EDCs in the Yeast Estrogen Screen and concentration-response relationships of binary and complex mixtures; removal of estrogenic activity of the spiked wastewater. Corresponding Author * Corresponding author’s email address: [email protected]. Alternative Address †[email protected] Funding Sources European Union’s Seventh Framework Program Acknowledgements This work has received funding from the European Union’s Seventh Framework Program for research, technological development and demonstration under grant agreement No 282818.


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Figure 1: Removal of estrogenic activity of the binary mixture (A, B) and the complex mixture (C, D) over time by laccase from T. versicolor (A, C) and M. thermophila (B, D). The mixtures were treated with free laccase (free Lac), immobilized laccase on acrylic beads (B+Lac) and ceramic membranes (M+Lac) as well as unloaded beads (B-Lac) and membrane (M-Lac). Figure 1 182x189mm (300 x 300 DPI)



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Figure 2: Removal of anti-androgenic activity of the binary mixture (A, B) and the complex mixture (C, D) over time by laccase from T. versicolor (A, C) and M. thermophila (B, D). The mixtures were treated with free laccase (free Lac), immobilized laccase on acrylic beads (B+Lac) and ceramic membranes (M+Lac) as well as unloaded beads (B-Lac) and membrane (M-Lac). Figure 2 179x184mm (300 x 300 DPI)


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Figure 3: Removal of estrogenic (A, B) and androgenic activity (C, D) of the wastewater over time by laccase from T. versicolor (A, C) and M. thermophila (B, D). The wastewater was treated with free laccase (free Lac), immobilized laccase on acrylic beads (B+Lac) and unloaded beads (B-Lac). 1.2 g of beads in case of T. versicolor and 0.6 g for M. thermophila. Figure 3 180x190mm (300 x 300 DPI)



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Figure 4: Removal of estrogenic (A) and androgenic activity (B) of the wastewater over time from T. versicolor. The wastewater was treated with immobilized laccase on acrylic beads (B+Lac) and unloaded beads (B-Lac). The amount of carrier was 0.3 g in this experiment. Figure 4 79x41mm (300 x 300 DPI)


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For Table of Contents Only 287x128mm (150 x 150 DPI)


Removal of Endocrine Disrupting Chemicals in Wastewater by

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