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Laccase grafted membranes for advanced water filtration systems: a

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Critical Reviews in Biotechnology

ISSN: 0738-8551 (Print) 1549-7801 (Online) Journal homepage: http://www.tandfonline.com/loi/ibty20

Laccase grafted membranes for advanced water filtration systems: a green approach to water purification technology Jagdeep Singh, Vicky Saharan, Sanjay Kumar, Pooja Gulati & Rajeev Kumar Kapoor To cite this article: Jagdeep Singh, Vicky Saharan, Sanjay Kumar, Pooja Gulati & Rajeev Kumar Kapoor (2017): Laccase grafted membranes for advanced water filtration systems: a green approach to water purification technology, Critical Reviews in Biotechnology, DOI: 10.1080/07388551.2017.1417234 To link to this article: https://doi.org/10.1080/07388551.2017.1417234

Published online: 27 Dec 2017.

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Date: 28 December 2017, At: 07:38

CRITICAL REVIEWS IN BIOTECHNOLOGY, 2017 https://doi.org/10.1080/07388551.2017.1417234

REVIEW ARTICLE

Laccase grafted membranes for advanced water filtration systems: a green approach to water purification technology Jagdeep Singh, Vicky Saharan, Sanjay Kumar, Pooja Gulati and Rajeev Kumar Kapoor

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Enzyme Biotechnology and Waste-water Treatment Laboratory, Department of Microbiology, Maharshi Dayanand University, Rohtak, Haryana, India

ABSTRACT

ARTICLE HISTORY

Purpose: Conventional wastewater treatment technologies are not good enough to completely remove all endocrine disrupting compounds (EDCs) from the water. Membrane separation systems have emerged as an attractive alternative to conventional clarification processes for waste and drinking water. Coupling of a membrane separation process with an enzymatic reaction has opened up new avenues to further enhance the quality of water. This review article deliberates the feasibility of implementing enzymatic membrane reactors has been deliberated. Materials and methods: A comprehensive study of conventional water treatment technologies was carried out and their shortcomings were pointed out. Research findings from the leading groups working on enzyme grafted membrane based water purification were summarized. This review also comprehends the patent documents pertinent to the technology of enzyme grafted membranes for water purification. Results: Immobilization of an enzyme on a membrane improves the performance of membrane filtration, and processes for the treatment of polluted water. Research has started exploring the potential for laccase enzymes because it can catalyze the oxidation of a wide range of substrates, structurally comparable to EDCs, by a radical-catalyzed reaction mechanism, with corresponding reduction of oxygen to water in an electron transfer process. Further, in the presence of certain mediators, the substrate range of laccases can be further enhanced to non-aromatic substrates. Conclusions: Removal of EDCs by laccase cross-linked enzyme aggregates in fixed-bed reactors or fluidized-bed reactors and laccase immobilized ultrafiltration (LIUF) membranes are proving their worth in water purification technology. The major operational issues with the use of LIUF membranes are enzyme instability in real wastewater and membrane fouling. In view of the above-stated characteristics, laccases are considered as the most promising enzyme for a greener and less expensive water purification technology.

Received 10 February 2017 Revised 29 November 2017 Accepted 2 December 2017

Introduction Conventional wastewater treatment processes essentially comprising primary (e.g. precipitation, and coagulation/flocculation), secondary (e.g. activated sludge, disinfection), and occasional tertiary treatment processes (e.g. activated carbon adsorption, ozonation, stripping etc.) are able to degrade low levels of several complex polluting compounds including endocrine disruptor chemicals (EDCs), pharmaceuticals and personal care products. It is now understood that such treatment technologies cannot completely remove these compounds from water. Therefore, degradation of polluting compounds in wastewater is a major challenge as they are quite resistant to generally used water treatment and refinement techniques. Over a thousand cancercausing EDCs like triclosan, bisphenol A, perchlorate, phthalate, alkyl phenol polyethoxylates etc. have been CONTACT Rajeev Kumar Kapoor [email protected] Dayanand University, Rohtak, Haryana 124001, India ß 2017 Informa UK Limited, trading as Taylor & Francis Group

KEYWORDS

Enzymatic membrane reactor; laccase; membrane; endocrine disruptor chemicals; wastewater treatment

found in a wide range of daily life products and ultimately these harmful chemicals reach water bodies directly or indirectly [1,2]. EDCs disturb the human body's signaling processes either by mimicking or interfering with the function of our own body hormones or by exaggerating or restraining signaling pathways, particularly those carried out by participating hormones. These disrupted endocrine signals can have a major impact on our body systems. Endocrine disrupting chemicals have been reported to cause many critical health problems including hormonal diseases, neurological defects, thyroid dis-functioning, breast cancer, reproductive system failure, disturbed sexual behavior, heart diseases, delayed puberty, and prostate inflammation in animals [3–6] (Table 1). The World Health Organization and other concerned authorities throughout the world are alarmed over the Enzyme Biotechnology Laboratory, Department of Microbiology, Maharshi

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Table 1. Source and effect of different EDCs on human health. EDCs

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Bisphenol-A

Sources

Effect on humans

Dioxin

All plastic containing bags, food cans, plastic bottles, ATM slips, shopping bills/slips, water pipes, polycarbonate tableware, most of food containers, water storage bottles, and baby milking bottles. Meat, fish, milk, eggs, and butter

Atrazine

Corn crops, drinking water

Phthalate

Plastics, drinking water bottles, pesticides, ventilator tubes, blood collecting bags, and infusion tubing, nutrition feeding bags

Triclosan

Toothpaste, drinking water, face wash, detergent, soap, antibacterial floor cleaners, shampoos and conditioners, shaving gel, deodorants, and antiperspirants

Perfluorooctanoic acid

Carpet-care liquids, treated apparel, treated textiles, treated non-woven medical use apparel, industrial flooring wax and removers, tiles, stone, food wrapping papers, dental floss, many cookware Spray to kill crop pests

Organophosphates pesticides Glycol ethers

Cosmetics, paints, house cleaning products, brake fluid, and oils

Formaldehyde

Woodstoves, Incinerators, refineries, forest fires, and fumes, hair smoothing spa, hair straightening products, skin cleaning agents, glues Milk, drinking water, fertilizers

Perchlorate

Neurological dysfunction, thyroid dysfunction, breast cancer, reproductive failure, and disturbed sexual behavior, heart disease Diabetes, heart problems, reduced fertility, reduced sperm activity and low counts, interfered embryo development and miscarriage, many types of cancers. Breast cancer belated puberty and prostate inflammation in animals, prostate tumors Hormone misbalancing, lower sperm count and reduced mobility, defects in the male reproductive system by birth, diabetes, obesity and thyroid irregularities, uneasy lactation, irregular ovulatory cycles, undescended testicles in men, birth defect in babies, and low numbers of sperm, and testicular tumors and cancers Breast and liver cancer, the risk of food allergy, imbalance hormones, i.e. male testosterone and female estrogen, and may also influence the thyroid systems, which regulate our body, weight, growth, and metabolism. Alteration of thyroid hormone levels. blood serum levels decreased semen quality

Male infertility, bad impact on brain, development in kids, and thyroid dysfunction Causes problems to painters, blood abnormalities, and lowers sperm counts, reduced fertility, unborn child Sinonasal and nasopharyngeal cancer, Skin redness or irritation. Negatively effects body growth and brain development in infants and young children

References [3,5–8]

[5,6]

[1,6] [3,5,6]

[5,7,9]

[3,5–7]

[5,6] [6,7] [6,7] [7,10–12]

problem of water pollution by EDCs; as a result, these authorities are now more sensitive to enforce new water protection acts and commissions [7,13,14]. The failure of the classical water treatment technologies to eliminate EDCs and other polluting compounds has encouraged scientific communities to find means for their effective bio-depletion through advanced membrane technologies. This review article has been compiled with the following objectives: (1) to provide an overview of membrane bioreactor technology for removal of EDCs from polluted water, (2) recent advancements and greener approaches for large and domestic level water filtration systems, and (3) potential of laccase grafted membrane bioreactors for pollutant removal.

under primary, secondary, and occasional tertiary treatment processes. Primary treatment involves the use of coagulants such as alum, ferric chloride, and a polymeric coagulant to remove suspended solids, colloids, and some dissolved organics, which do not settle spontaneously. In secondary treatment, dissolved organics are removed aerobically by a consortium of microorganisms in a sludge or in suspension. This process is known as an activated sludge process (ASP). It is followed by disinfection using chlorination. Nowadays, tertiary treatment processes such as activated carbon adsorption, ozonation, stripping, and filtration are adopted for the final treatment of effluent to remove trace concentrations of the organics [15].

Conventional water treatment technologies

Shortcomings of conventional water treatment technologies

Conventional wastewater treatment technologies were designed to remove most of the suspended solids, dissolved organics, and nutrients from the wastewater. These technologies involve the treatment of wastewater

Not all EDCs are removed following conventional water treatment technologies. While analyzing water samples for 113 synthetic chemical compounds at different

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CRITICAL REVIEWS IN BIOTECHNOLOGY

stages of conventional water treatment, Stackelberg et al. detected 21 compounds in one or more samples of finished water and between 3 to 13 of these compounds per sample [16,17]. This indicates the inefficiency of the conventional water treatment technologies in effectively removing organic synthetic chemicals from finished water. The process of coagulation–flocculation used by primary clarifiers is not very effective for most of the EDCs studied. The percentage removal of various EDCs varied between 15 and 75%, using alum and iron salts, and excess lime/soda ash softening [18]. The incomplete removal of these contaminants is because of their different chemical properties which have a profound impact on its sorption behavior. These properties include: water solubility, polar/ionic character, octanol/ water partition coefficient (log Kow), and acid/base chemistry [19]. The hydrophobicity of the compounds or the log Kow value was found to be a major factor in determining the removal efficiency with coagulation– flocculation. The highest removal (20–50%) was observed for the compounds with log Kow  4 [20,21]. Compounds with high sorption properties can be significantly removed during coagulation–flocculation with efficiencies around 70%. Compounds with lower Kd (equilibrium dissociation constant) values, such as diazepam, carbamazepine, ibuprofen, and naproxen, were removed up to only 25% [16,22]. In addition to the above, the principal disadvantages that might disqualify a wholly physicochemical process for wastewater treatment are the problems associated with the highly putrescible sludge produced, and the recurrent cost of chemicals for its operations [9]. Secondary clarification uses the ASP, whose removal efficiencies of contaminants depends on a number of factors and any deviations from the optimum parameter value causes loss of efficiency. These parameters include: (a) physicochemical characteristics of the pollutants biodegradation abilities are influenced by the chemical structure of the micropollutant for, e.g. recalcitrance increase with an increase in chain length, chain branching, chlorination, bonds and substituting groups, and number of benzene rings [10,16,23,24]; (b) the nature of the microbial community – the inability of human metabolic pathways to completely metabolize and improper disposal of recalcitrant compounds result in increased concentration of pharmaceuticals and personal care products (PPCPs). This elicits a negative effect on biological treatment processes which includes increased production of extracellular polymeric substances, altered community behavior, and fouling. Another reason for the failure of ASP is the resistance of compounds like carbamazepine, diclofenac, triclosan,

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4-octylphenol to biodegradation at low concentrations. Therefore, it becomes difficult to have appropriate operating conditions to remove all the contaminants; (c) operational factors which include temperature, the hydraulic retention time (HRT), and the sludge retention time (SRT) [16,25–27]. Conventional ASPs are unable to retain high biomass concentrations and long SRTs leading to poor biodegradation efficiency of contaminants. Further, some compounds are removed with low sludge age (2–5 days), others are hardly degradable even with sludge age greater than 20 days [12]. A large amount of energy (especially during aeration) is required by ASP. ASP is followed by disinfection with chlorine. Although chlorination is very effective in disinfection, it causes oxidation of organic matter. According to the Environmental Protection Agency (EPA), trihalomethanes (THM) are formed when naturally occurring organic and inorganic materials in the water react with the disinfectants, chlorine, and chloramines. One example of a THM is chloroform, which is a known carcinogen. It is toxic when consumed, such as when drinking unfiltered chlorinated water. Chlorination is ineffective on Helminths as they are transmitted by eggs, and are therefore resistant to chlorine disinfection. Sometimes, tertiary treatment is given for further decontamination. UV radiation works by inflicting photochemical damage on pathogens but UV radiation is an expensive process [28]. Another process for clarification involves the use of activated charcoal. The major shortcoming of this process is that not all organic contaminants are adsorbed by activated carbon at the same rate. Adsorption or percentage removal of a contaminant on an activated surface is dependent on log Kow. Another parameter which can negatively affect adsorption is adsorption of natural organic matter (NOM) and dissolved solids due to which there is a competition with the specific compounds for adsorption sites. This will result in a decreased removal percentage [16,29–31]. Few water treatment plants apply stripping of the wastewater which allows only partial removal of micro-pollutants. Since only volatile organic compounds (VOC’s) can be removed from wastewaters, removal of the contaminants by stripping is negligible compared to other processes because most of emerging compounds are characterized by low volatility [32]. Ozonation leads to removal of more than 90% of the compounds by partial or complete oxidation [33] but is costly and little information is available to confirm the eco-toxicity of the products formed. Therefore, before starting an application using ozone, the fate and effect of oxidation products needs to be extensively investigated [34].

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Enzymes in water treatment It is now well-established that enzyme treatments are more eco-friendly and energy efficient compared to chemical treatments [35,36]. Enzymes suitable for wastewater treatment include: oxidoreductases (polyphenol oxidases, peroxidases, and laccases), hydrolases (proteases, cellulases, esterases, and lipases), and lyases. Oxidoreductases are an important class of enzymes for detoxification of textile industry effluents [37,38] and wastewaters containing EDCs, while hydrolases have the potential to treat only the biological wastes that can more effectively be removed by microorganisms in sludge or wastewater [39,40]. Oxidoreductases, peroxidases, and laccases are capable of targeting a wide range of pollutant substrates. Laccases have also been reported to detoxify phenolics by their oxidation [41,42]. The main source of these extracellular enzymes is ligninolytic fungi [43]. The use of a single enzyme or an association of related enzymes can permit the inactivation of complex molecules, antibiotics, and other EDCs in wastewater effluents, thus eliminating such compounds from the water and environment [41,44–46]. There are sufficient reports to prove the potential of peroxidases in eliminating EDCs, such as phthalate, bis-Phenol-A, triclosan, diclofenac, and tetracyclines [23,47–52]. A study on tetracycline degradation reported 70% to 99% degradation during 4-h enzyme treatment [53,54]. However, there are certain limitations with peroxidases: (a) they are substrate specific, (b) there are a limited number of substrates where they catalyze the degradation reaction, e.g. carbamazepine [55], (c) they require the presence H2O2 as a co-factor to initiate the degradation reactions.

Potential of laccases in water treatment In sharp contrast to peroxidases, laccase, and other oxidoreductases catalyze the oxidation of a wide range of EDCs simply using the dissolved oxygen as the electron acceptor [56–58]. Investigations have proven beyond doubt the successful use of laccase-mediated treatments for the removal of persistent complex pollutants [59–62]. Laccases are being used for the detoxification of wastewater from paper and pulp product industries [63] and for nearly complete degradation of man-made

or synthetic chemicals. Removal of estrogens (natural or synthetic) from water can be achieved within 1 h of laccase treatment [64–66]. Some recent reports show that doxycycline, chlortetracycline, oxytetracycline, and tetracycline antibiotics have been degraded by laccase treatment [53,54,58]. The effectiveness of enzyme towards the elimination of reluctant anti-inflammatory drugs also depends on the type of targeted substrate and the origin of the enzyme. Margot et al. [67] showed that 95% of mefenamic acid and 25% of diclofenac could be degraded by laccase isolated from Trametes versicolor within 20 h of a reaction. Whereas, Lloret et al. [66] reported that commercial laccase extracted from Myceliophthora thermophila was effective against two anti-inflammatory pharmaceuticals drugs (diclofenac and naproxen) and estrogen hormones (estrone, 17bestradiol, and 17a-ethinylestradiol). With the help of mediators, laccase eliminates the estrogens after 15 min of treatment, diclofenac required 1 h of incubation time whereas naproxen required 8 h to achieve nearly 60% elimination. Although both peroxidases and laccases can successfully degrade EDCs from water, laccases are more promising as they have a wide range of substrate specificity and do not require H2O2. Further, by adding a redox mediator in the reaction medium the activity of laccases enzyme can be enhanced towards complex non-phenolic pharmaceutical compounds [54,58,68–71]. These mediators can react with laccase to generate very reactive intermediates, which will deplete the targeted pollutant substrates and then again become regenerated for a new degradation reaction cycle (Figure 1). Some of the well-known laccase mediators which increase the degradation potential and substrate range of laccase are: syringaldehyde, 2,20 -azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) (ABTS), acetosyringone, violuric acid, and vanillin [68,74–76]. Use of laccase along with its redox mediators also increase the depletion rate of EDCs, such as: bisphenol A, phthalates, tetracyclines [58,62,77–79], sulphonamides [68], triclosan, and estrogen hormones [54,66,74,80]. However, the addition of these mediators to the reaction mixture adds to the process costs. Therefore, large-scale treatment by the addition of mediators is not an economically feasible alternative for continuous wastewater treatment. Moreover, the addition of a few of these mediators can

Figure 1. Laccase with a redox mediator in a degradative cycle [72,73].

CRITICAL REVIEWS IN BIOTECHNOLOGY

be toxic, and later pose difficulty for removing them from the reaction mixture.

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Membrane bioreactors (MBR) for water treatment Currently, MBR technology is the most promising alternative available for the purification of waste and drinking water [81–83]. The basic principle is that the membrane establishes a physical barricade, which permits the passage of particles with a certain shape, size, and other specific parameters. Therefore, this barricade is capable of eliminating the dissolved solids, microorganisms, and other contaminating particles. A large advantage to these membranes is that they can be installed in an automated single modular compact arrangement for large-scale wastewater management [10]. The MBR system provides a cost-effective technology because it is automated, does not need significant operator attention and its installation does not require large land area and construction. Progression in MBR technology also offers high removal of impurities and more productivity with less energy consumption. At present, there are four types of membrane filtration processes: microfiltration (MF), ultrafiltration (UF), nanofiltration (NF), and reverse osmosis (RO) which are most commonly used for separation of liquid–solids and even liquid from liquids. These membranes can be configured in a hollow fiber, spiral, and tubular form (Table 2) into an MBR. Depending upon the nature of polluting compounds any of these or a combination of these processes can be used [87]. To a large extent, removal of EDCs by NF and UF membranes is dependent on hydrophobic adsorption and size exclusion. UF membranes typically block EDC on the basis of hydrophobic adsorption whereas, NF blocks many EDC due to both hydrophobic adsorption and size exclusion [88]. Compounds having low logKow values due to: aliphatic/aromatic nitrogen, carbonyl, phosphate, amine, or hydroxyl functional groups are poorly retained. UF could retain 0 to