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Review

Potential of Laccase as a Tool for Biodegradation of Wastewater Micropollutants

by 1, 2 and 1,*
1
Department of Biochemistry and Biotechnology, Institute of Biological Sciences, Maria Curie-Skłodowska University, Akademicka 19, 20-033 Lublin, Poland
2
Department of Radiochemistry and Environmental Chemistry, Institute of Chemical Sciences, Maria Curie-Skłodowska University, M. Curie-Sklodowska Square 3, 20-031 Lublin, Poland
*
Author to whom correspondence should be addressed.
Water 2023, 15(21), 3770; https://doi.org/10.3390/w15213770
Submission received: 5 October 2023 / Revised: 23 October 2023 / Accepted: 26 October 2023 / Published: 27 October 2023
(This article belongs to the Section Wastewater Treatment and Reuse)

Abstract

:
In the 21st century, humans are facing a high risk of exposure to emerging pollutants. Water contamination has become a major threat due to its devastating impacts on the entire ecosystem. Relatively great danger for aquatic microorganisms is posed by organic micropollutants, which are a consequence of progressing urbanization and industrialization. This review focuses on laccase of mainly fungal and bacterial origin, which provides an eco-friendly strategy for the transformation of these harmful pollutants to less or non-toxic compounds, as it acts oxidatively on the aromatic ring of a wide range of compounds, releasing water as the only by-product. Laccase alone or with the use of mediators has been used successfully to remove micropollutants from wastewater, including pharmaceuticals and personal care products, biocides, endocrine disrupting agents, steroid hormones, and microplastics. Even though the potential of an LMS (laccase–mediator system) is tremendous, the selection of an appropriate mediator and the persistent monitoring of toxicity after treatment are critical and should be performed routinely. Hence, further research is still needed for the optimization of degradation processes to improve our understanding of the different interactions of laccase with the substrate and to develop sustainable advanced water treatment systems.

Graphical Abstract

1. Chemistry of Water Pollution

Water is a multi-component heterogeneous system containing solutes, colloidal substances, and suspensions. The chemical composition of water is an important element in the assessment of its quality. Its physical and chemical parameters change depending on the geographical location, the season, and the load of pollutants transported to waters. Substances in water can exist in various chemical forms: as hydrated free ions, as complexes and ion pairs, as organic compounds, and others. Forms in which substances occur in water depend on many environmental factors. The most important chemical processes affecting water quality are acid–base reactions, air–water exchange processes, the precipitation and dissolution of substances, complexation reactions, oxidation–reduction reactions, and adsorption–desorption processes. The composition of surface waters is strongly influenced by atmospheric precipitation together with the load of atmospheric pollutants and the processes of matter exchange between water and bottom sediment [1]. Surface water pollution is defined as physicochemical or biological factors that reduce the quality and usability of water. Most often, pollutants get into waters as a result of natural processes stimulated or accelerated by humans. Other sources of water pollution are associated with water and land transportation, the use of pesticides and artificial fertilizers, and municipal and industrial waste. Waters are also polluted as a consequence of eutrophication. The water cycle in nature has been disturbed by human activity, i.e., deforestation, improper and excessive agricultural practices, industrialization, and urbanization [2,3].
In the 21st century, all types of pollutants are an extreme global concern. Water contamination has emerged as a major threat due to its devastating impacts on the entire environment, posing a risk for biodiversity conservation [4]. Research conducted in recent years has confirmed that surface waters around the world are contaminated with chemical substances of different origin. They can be grouped into the following categories: inorganic pollutants, heavy metals, and radioactive and organic pollutants.
Inorganic compounds are nonbiodegradable and persist in water systems for a long time. Inorganic pollutants include alkalis, pigments, fluorides, mineral acids, and cyanides [5,6,7]. These contaminants enter water through the release of untreated wastewater resulting from anthropogenic activities like waste mining, particularly the metallurgical operations, refining, and electronic waste mining [8]. These water contaminants have the potential to seriously harm humans and other organisms, especially at higher doses.
The group of metals regarded as environmental pollutants includes such elements as Pb, Zn, Ni, Cd, Cr, Cu, Fe, Hg, Mn, and Mo. Some of them called microelements, e.g., Cu, Cr, Fe, Mn, and Zn, are an important part of the metabolism of most living organisms. Both their deficiency and excess can cause serious health effects; therefore, their concentration in cells is strictly controlled [9]. There are also such metals as Hg, Cd, and Pb, which are perceived as toxic in nature, and their accumulation is always associated with serious disorders in cell metabolism/physiology [10].
Radioactive contaminants enter water sources during the extraction of radioactive elements, research activities, testing nuclear weapons, and accidents at nuclear power plants, storage facilities, disposal, and the transportation of radioactive materials. By emitting hazardous ionization radiations like alpha, beta, and gamma rays, these events have the potential to modify the entire physicochemical properties of water sources and pose a serious ecological threat to human and aquatic life [11,12].
Water pollution with organic compounds is an incredibly popular subject in research. Figure 1 shows the number of publications on the compounds under discussion that have been listed in the Scopus database (www.scopus.com) over the last ten years. It shows an increasing trend which indicates the significance of water pollution with organic compounds.
The most common anthropogenic pollution of surface waters is of organic origin and includes pesticides, surfactants, petroleum hydrocarbons, phenols, chlorinated biphenyl derivatives, microplastics, pharmaceuticals (diclofenac, naproxen, ibuprofen, estrogens, and antibiotics), pesticides, or drugs (cocaine, amphetamine and its derivatives). These compounds can dissolve in surface waters and accumulate in river sediments [13,14]. Owing to their solubility in liquids, organic contaminants effectively bioaccumulate in the aquatic environment, causing dangerous effects. In addition, they greatly change the biological oxygen demand (BOD) and chemical oxygen demand (COD) of water and ultimately deteriorate the water quality. All these compounds pose a great challenge to environmental protection and ecology, as their presence in surface waters is the result of inefficient wastewater treatment processes. Regular consumption of such water by humans may cause kidney tumors, lymphoma, and leukemia. Polluted water severely affects crop quality and quantity when used in irrigation processes [15].
Relatively great danger for water microorganisms is posed by organic micropollutants, i.e., such anthropogenic compounds as pharmaceuticals (steroid hormones, antibiotics, nonsteroidal anti-inflammatory drugs, and hypocholesterolemic, psychiatric, and cardiovascular drugs), home and personal care products (disinfectants, fragrances, preservatives, insect repellents, UV filters, cosmetics), microplastics, and biocides (pesticides), which are ubiquitous in the environment. Given their persistence and bioaccumulative potential, they were categorized as “emerging environmental contaminants”. Urban areas are among the main sources of these compounds due to their inefficient removal in conventional wastewater treatment plants (WWTPs) [16,17]. Besides their toxicity to aquatic organisms, micropollutants may adversely affect terrestrial wildlife. These compounds are not commonly monitored and measured and can cause acute and chronic toxicity at very low concentrations (ng/dm3 to μg/dm3); therefore, their seemingly insignificant amount is critical to aquatic systems and thus human health [18]. In addition, taking into account the growing demand for these chemicals, their consumption and global market is expected to increase year by year and is projected to have a compound annual growth rate (CAGR) of 2.6–12.8% from 2021 to 2030 (Figure 2). With increasing water scarcity, wastewater should be considered as a new potential resource of drinking water. Therefore, both water and food can contain micropollutant particles. However, wastewater reuse is still limited because little information is available on the influence of untreated substances on the ecosystem and their ecotoxicological effect, and methods for removing micropollutants from wastewater are often ineffective [19].

2. Methods for Removing Organic Pollutants from Wastewater

As wastewaters are often complex mixtures, various approaches to successful removal thereof have been proposed based on available technology. They include techniques that can be grouped into physical (sedimentation, flotation, adsorption, barriers), chemical (precipitation, ion exchange, neutralization, adsorption, disinfection), and biological methods, which rely on the use of whole organisms (bacteria, fungi, nematodes) or enzymes produced by them [21]. It should be underlined that the use of enzymes is advantageous to whole organisms, as they are less sensitive to the presence of toxic compounds [22]. The application of biological methods often means not only removal of hazardous compounds from wastewater but often total decontamination via degradation by microbial metabolism or the catalytic abilities of enzymes in cell-free mixtures. Total decomposition of toxic compounds may be achieved by the application of degradation pathways in organisms or enzymes. The choice of the latter is dictated by the substrate (toxic compound) to be degraded, and it is possible in complex wastewater mixtures to use several enzymes or enzymes with low substrate specificity. Biological transformation is the main removal mechanism for many hydrophilic organic micropollutants during wastewater treatment. Numerous studies have focused on enzymes that are able to degrade/inactivate environmental pollutants, suggesting bioremediation as an environment-friendly and cost-competitive alternative for treatment of waste and effluents [18]. Since the enzymes catalyze various reactions, research should focus on lowering or even eliminating the toxicity of wastewater. The global interest in the application of enzymes in industry is growing every year, and predictions for 2022–2031 show that the 6% CAGR (compound annual growth rate) is projected to reach USD 10.2 billion by 2031. The highest growth rate is observed for biocatalysts in the pharmaceutical and biotechnological segments [20]. Every branch is specific, and therefore, generated wastes require different approaches to removal, including diverse enzymes (Figure 3). Removal of wastes comprising large biomolecules (protein, polysaccharides, lipids) requires the application of enzymes with hydrolytic abilities (proteases, lipases, amylases, or cellulases) [22,23]. Therefore, an approach based on the transformation of these molecules into simple monomers is the best solution and the easiest to achieve. Moreover, the resulting monomers may serve as a source of biogenic compounds for microorganisms. On the other hand, wastes from pharmaceutical, personal care products, or pesticides are often of aromatic origin (paracetamol, triclosan, carbofuran) [24]. The decomposition of these chemical compounds requires the breaking of their aromatic ring or aliphatic chain and changes in their substitutes (oxidation, demethoxylation, dechlorination, etc.). Therefore, extracellular oxidoreductases with diverse catalytic abilities and low co-substrate requirements (i.e., oxygen or hydrogen peroxide) are being searched. Most of the proposed solutions involve the use of tyrosinase, lignin peroxidase, horseradish peroxidase, and versatile peroxidase [25,26,27,28,29]. It should be underlined that, in all the industries mentioned previously, laccase is the only common biocatalyst, likely due to its low substrate specificity and oxidizing effect, as well as the diverse source of this enzyme (i.e., fungi, bacteria) and therefore its properties. Moreover, it seems that laccase is readily used in combination with the other aforementioned oxidoreductases [25,27], thus having potential to degrade a wider range of compounds.

3. Laccase Characteristics as a Waste Removal Enzyme

Laccase (EC 1.10.3.2) seems to be ubiquitous in nature, serving an important protective function in all aerobic living systems due to its abilities to catalyze reactions with numerous organic and inorganic substrates. Discovered in 1883 in the lacquer tree [30], laccase has been comprehensively studied in fungal and bacterial organisms [31,32,33] and recently proved to be an important part of animal physiology [34]. However, considering the progress in the field of heterologous protein expression, other laccases from the plant or animal kingdoms may also be considered as useful enzymological tools [35], especially the recently discovered mammalian laccases [36]. This biotechnological potential is related to, e.g., their kinetic parameters: Km, pH, and temperature optima or range. Laccase’s catalytic cycle begins with the mono-electronic oxidation of four equivalent appropriate reducing substrates to create organic radicals at the expense of molecular oxygen, which is then reduced to two molecules of water. The catalytic machinery of this enzyme is a four-membered copper cluster, which is also the location of oxygen coordination and reduction, as well as water production and release [37]. Laccase substrates comprise various derivatives of benzene, naphthalene, furan, indole, pyridine, fluorene, anthracene, and even inorganic/organic metal compounds [38,39,40,41,42,43,44,45,46,47]. With molecular oxygen as a co-substrate, laccases oxidize a range of the aforementioned aromatics with different possible substitutes: hydroxy-, amino-, methoxy-, halide, amino-, methyl-, phenyl-, and thiol [48,49,50,51,52,53,54]. The enzyme is able to catalyze the oxidation of isomers with various substitutes, for example, benzene with hydroxy- groups in position 1, 2, 4 [55], 1, 3, 5 [56], 1, 2, 3 [57], and 1, 2 [58]. All enzymes used for bioremediation are able to oxidize derivatives of benzene and most of them oxidize naphthalene. However, it seems that only laccase is capable of oxidizing indole or pyridine. Moreover, all peroxidases (MnP—manganese peroxidase, DyP—dye decolorizing peroxidase, LiP—lignin peroxidase) require hydrogen peroxide, whereas only laccase and oxygenase catalyze reactions with oxygen. Most laccases considered as biotechnologically important are of microbiological origin, mainly fungal organisms [59,60]. The pH optimum of laccases ranges from 2 to 10 [61,62], while its activity is in the range from 0.5 to 11.5 pH [63,64,65]. Recently, a thermo- and pH-stable laccase was isolated from the litter-decomposing fungus Gymnopus luxurians [66]. It should be underlined that laccase pH optima depend not only on the source but also on the substrate used. Similarly, heme peroxidases are able to oxidize substrates in a pH range of 1–11 [67], whereas dioxygenases prefer less acidic pH from 5 to 10 [68,69]. Most fungal laccases have temperature optima in the range from 20 to 80 °C [70,71] and bacterial laccases even up to 92 °C [72]. It is very important in waste removal that certain laccases (Pycnoporus sp.) appear to be adapted both to cold (30.2% of initial activity at 0 °C) and hot (half-life at 80 °C up to 2.6 h) conditions [73]. It seems that laccase is active over a slightly wider temperature range than peroxidases or oxygenases. As for all oxidoreductases, the enzyme is sensitive to inhibition of cyanides [74], azides [56,75], and halides [76]. Moreover, laccase activity is inhibited by such chelating agents as EDTA [72], denaturing compounds—SDS [77], or organic solvents—chloroform [78]. However, certain laccases may be resistant to salt inhibition, and their activity may even be enhanced by the presence of sodium chloride [79,80]. Moreover, laccases with alkali-, halide-, or detergent-resistant and metal-tolerant properties have been described [81,82,83]. Similar inhibitors have a negative effect on the activities of peroxidases and oxygenases, but it seems that laccase has been very well studied in this respect. Since the application of enzymes for wastewater removal sometimes requires their action in non-optimal conditions, the abilities of fungal laccases to oxidize substrates in hydrophobic solutions seem interesting. Wu et al. [84] observed a 1.5–4.0-fold enhancement of the activity of fungal laccases pre-incubated in organic solvents (DMSO, DMF, ethanol, methanol). Laccases in the genus Bacillus were proved to be tolerant not only to organic solvents (30% concentration) but also to temperature (up to 80 °C) and salts (1 mol/dm3 NaCl) in the reaction mixture [85,86]. Similarly, plant laccase from Rhus vernicifera was reported to be able to catalyze the oxidation of catechol, catechin, and epicatechin in hexane or toluene [87]. Moreover, numerous studies have proved that laccase, trapped in the aqueous phase, may act in different kinds of emulsions, whereas substrates and products remain mainly in the organic phase [88,89,90]. Moreover, the catalytic abilities of laccase were proved to be expanded by the presence of mediators—low molecular mass chemical compounds able to transfer electrons between the enzyme and the substrate [66,91]. Several works have proved that laccase with a mediator is able to oxidize substrates unavailable to the sole enzyme, such as nonphenolic lignin compounds [92,93,94]. Moreover, laccase immobilized in an LMS (laccase–mediator system) offers a flexible approach and far more ease in operation with all the features of immobilized enzymes [95]. For many years, a bottleneck of the large-scale biotechnological application of laccase was its inefficient production, especially heterologous expression. Currently, the enzyme is commercially available for industrial purposes from a number of sources, especially of Chinese origin (Table 1).

4. Laccase-Assisted Biodegradation of Water Micropollutants

Although there are various biological methods for the treatment of organic micropollutants, the fact that laccase is able to effectively degrade and detoxify a variety of these compounds has gained much interest in the field of environmental biotechnology and bioremediation [96,97,98]. The contaminants investigated to date in the context of their removal by laccase from wastewater include a wide range of pharmaceuticals, steroid hormones, personal care products, pesticides, and industrial chemicals. Laccases without any additional agents have been used successfully to remove pharmaceuticals and personal care products (antibiotics, anti-inflammatory analgesics and anti-depressant compounds, active ingredients of sunscreens), biocides (e.g., atrazine, pentachlorophenol, isoproturon, metolachlor, spinosad, triclosan), endocrine disrupting agents (bisphenol A), steroid hormones, and microplastics [75,99,100,101,102,103,104]. While there are no commercially available laccase-based wastewater treatment preparations, there are studies that clearly demonstrate the effectiveness of laccases in removing micropollutants in real wastewater [105,106]. Furthermore, the crude extract obtained from Trametes pubescens MUT 2400 transformed ketoprofen, bisphenol A, naproxen, and diclofenac and decreased up to 60% of their initial concentration in real conditions of municipal wastewater in Northwest Italy (Turin) [107]. In general, the enzyme-based reactions mainly involve oxidation, hydroxylation, dehydration, production of phenoxyl radicals, and oligomerization (radical–radical coupling) (Figure 4). As suggested, the phenol (-OH) group and the amine (-NH) group are the main oxidation sites for laccase [100,108], which may explain the difficulties in biotransformation of, e.g., carbamazepine with complete removal of bisphenol A and acetaminophen by Bjerkandera adusta laccase [100]. Studies have shown that both bacterial and fungal enzymes can be used effectively. Surprisingly, native and heterologous preparations of fungal origin are still preferable [75,96,109,110,111]. In fact, many of the methods for biodegradation of micropollutants described so far are based on Trametes versicolor laccase and Myceliophthora thermophila laccase expressed in A. oryzae (Table 2). This is likely related not only to the origin of the enzyme itself but primarily also to its properties, as shown for the commercial T. versicolor preparation and Streptomyces cyaneus laccase. The bacterial laccase was active in a smaller pH and temperature range (conditions typical of wastewater treatment plants), was more affected by pH inactivation, and has slower degradation kinetics of diclofenac, bisphenol A, and mefenamic acid than the fungal enzyme [112]. Due to the rather low operational stability of laccases, a large amount of research has been focused on immobilizing these enzymes on solid supports to increase enzyme stability. The advantages of this procedure refer especially to the reusability of laccases (increased storability, thermal, and pH stability) and the improvement of their resistance to the action of inhibitors. A promising example of application in WWTP is the immobilization onto spherical nanoparticles of the laccase of the white-rot fungus Coriolopsis polyzona, which retained its activity over one month in effluent water [113]. While under the harsh conditions of real wastewater, laccase from Phoma sp. UHH 5-1-03, cross-linked to polyvinylidene fluoride membranes, was able to remove pharmaceuticals such as indometacin, mefenamic acid, ketoprofen, acetaminophen, bezafibrate, and naproxen with high efficiency [114]. Although enzyme immobilization is an important issue, it has been the subject of a few papers recently [104,111] and will not be covered in this review.
Since fungal and bacterial laccases show differences in their redox potentials [39], this leads to differences in both their activity and their ability to oxidize contaminants. In fact, because the proton is transferred during the reaction, the redox potentials of several aniline and phenolic compounds are pH dependent and decrease with increasing pH [118]. Although laccase has an advantage over conventional treatment options, it is still a challenge to provide a stable source with a high redox potential. Therefore, research is being conducted on the use of laccase alone and in combination with mediators (LMS) that may improve the oxidation properties of the entire enzyme system, seem to enhance the degradation potential of many micropollutants, and show promising results (Table 2). In most cases, the removal of antibiotics was enabled or enhanced by the addition of mediators [119,120]. The mediating compound facilitated the elimination of the estrogenicity of carbamazepine, enabling the formation of less estrogenic compounds [121]. However, the application of laccase–mediator systems is associated with certain costs, i.e., continuous operation is limited due to the need to constantly add the mediator, which ultimately makes the process cost intensive. Moreover, in some cases, the use of the mediator may increase the toxicity of the final product, as previously shown for 1-hydroxybenzotriazole and syringaldehyde [102,120]. When the syringaldehyde–laccase system was used for the removal of antibiotics, a time-dependent increase in toxicity was reported, although the degradation rate had increased [120]. Therefore, the laccase–mediator treatment can make the process ineffective or even disadvantageous by creating another environmental problem. Additionally, the selection of an appropriate mediator and the persistent monitoring of toxicity after treatment are critical and should be performed routinely. The evaluation of the type and dose of the mediating compounds and their effect on laccase stability and effluent toxicity in the removal of trace organic compounds (oxybenzone, pentachlorophenol, atrazine and naproxen) has been reported recently [122]. However, more research is needed in this regard to search for effective natural mediators that will reduce the financial costs of the bioremediation process and be environmentally friendly. In the biodegradation of antibiotics, an alternative to the use of mediators seems to be the addition of metal ions to laccase preparation. It has recently been suggested that the addition of Ag+ and Mn+2 can increase the activity of laccase and manganese peroxidases and has been demonstrated to enhance the degradation of β-lactam antibiotics, tetracycline, and quinolones, which is a promising approach for the biotransformation of pharmaceuticals in the redox mediator-free system [123]. It seems that another interesting alternative that may overcome these limitations is the laccase engineering approach and improving the catalytic performance of the protein by tailoring the enzymes depending on the type of substrate [111,124].
There is no doubt that micropollutants at sublethal concentrations present in the environment cause a wide range of toxicological effects from cellular to population levels of all fauna and flora. Bearing in mind that ecotoxicity is the primary concern for these compounds due to their extremely high bioaccumulation, the toxicological effect of the reaction mixture should be thoroughly investigated and evaluated using specific and appropriate tests at each level of biological organization to determine the associated pathophysiological risk to people and other organisms [17]. Many different bioassays based on growth inhibition tests have been applied for ecotoxicological assessment of laccase-assisted biotransformation reactions (Table 2). As previously mentioned, some laccase–mediator mixtures may be highly toxic. It has been proposed that radicals generated through the oxidation of mediators can interact with crucial biomolecules and induce toxicity [102,122]. In cooperation with syringaldehyde, laccase effectively removes a wide range of antibiotics, but the enhanced transformation reaction induces unspecific toxicity (two bioassay tests), implying formation of hazardous transformation products or radicals [120]. A similar observation has also been reported by Nguyen et al. [125]. However, in general, a reduction in by-product toxicity is observed (Table 2). Reduced toxicity to Vibrio fischerii after treatment was noted for sulfadimethoxine and sulfamonomethoxine when violuric acid and 4-hydroxybenzyl alcohol were applied as mediators. Furthermore, the growth inhibition of algae used as a viability indicator for carbamazepine toxicity showed that 24 h incubation in a carbamazepine solution caused 95% mortality of Chattonella marina cells, whereas the LMS effluent (with a 50-fold higher initial concentration of carbamazepine) had no effect on viability. Micro-toxicity studies were performed on the effect of untreated and laccase-treated ketoconazole on the growth inhibition in fungal species, such as Candida albicans, Cryptococcus neoformans, and Saccharomyces cerevisiae, and freshwater green algae Pseudokirchneriella subcapitata. They demonstrated that laccase-treated ketoconazole and its isolated metabolites had reduced their toxicity (Table 2). Interestingly, incorporation of two redox mediating compounds (violuric acid and syringaldehyde) separately increased laccase degradation of micropollutants. However, a combination of both exerted a reduced effect on carbamazepine, primidone, and ibuprofen. The addition of a mediator increased the toxicity of the bioreactor media, although the membrane permeate (i.e., final effluent) was non-toxic, indicating an additional benefit of adopting a membrane distillation–enzymatic membrane bioreactor [101].
Free radicals produced by laccase-based enzymatic catalysis are able to generate dimers, trimers, tetramers, and oligomers through covalent bonding. Since the final products of such a reaction are polymeric compounds [126], it should be taken into account that this enzyme may also reduce the bioavailability of toxic organic compounds in the environment. Laccase appears to be highly active for the oxidative polymerization of the phenolic compounds, which as polyphenols had reduced solubility in water and were merely dissolved at pH 10–11 [126]. The polymerization of 17β-estradiol by extracellular T. hirsuta laccase was also important in biological detoxification. The resulting complex polymeric structures were characterized by limited solubilities, which significantly reduces their estrogenic activity and ecotoxicity [127,128]. An increase in hydrophobicity of 17β-estradiol as a result of laccase-mediator self-coupling was also observed in the case of the T. versicolor enzyme [129]. These polymerization products, on the other hand, might be easily removed using physical procedures such as precipitation and filtration [126], which also makes them no longer bioavailable.
Table 2. Laccase-based transformation of selected micropollutant representatives with evaluation of their degradation by-product toxicity.
Table 2. Laccase-based transformation of selected micropollutant representatives with evaluation of their degradation by-product toxicity.
Laccase SourceMicropollutant (Substrate)MediatorTransformation EfficiencyProduct ToxicityReference
T. versicolorcarbamazepineCA, AS, SAover 65% for p-coumaric acid in the membrane hybrid reactor with biocatalytic TiO2reduced (algae Chattonella marina and Microcystis aeruginosa viability test with AlamarBlue)[117]
Pleurotus ostreatustriclosanNAover 89.82%reduced (green algae Chlamydomonas reinhardtii and Scenedesmus obliquus growth inhibition studies)[116]
Aspergillus flavuspolyethylene microplasticsNA3.9% mass lossNR[103]
B. adustaacetaminophen, bisphenol A, carbamazepine, sulfamethoxazoleNA100% for bisphenol A and aminophene; about 20% for sulfamethoxazole and carbamazepineNR[100]
T. versicolormetronidazole, salicylic acid, primidone, amitriptyline, carbamazepine, ketoprofen, naproxen, ibuprofen, gemfibrozil, diclofenac, triclosan, propoxur, fenoprop, clofibric acid, atrazine, ametryn, pentachlorophenol, 4-tert-butylphenol, bisphenol A, 4-tert-octolphenol, estriol, estrone, 17α-ethinylestradiol, 17β-estradiol, 17β-estradiol acetate, enterolactone, formononetin, benzophenone, oxybenzone, octocryleneHBT0–99%slightly decreased for crude laccase; increased for laccase–HBT system (bioluminescence inhibition in Photobacterium leiognathi with ToxScreen3 assay)[102]
Pleurotus dryinuscarbendazim, thiabendazole, pyrimethanil, kresoxim methyl, pyraclostrobin, trifloxystrobin, boscalid, iprodione, fludioxonil, diuron, simazine, monolinuron, atrazine, hexazinone, pendimethalin, metolachlor, imazethapyr, metobromuron, bentazon, aldicarb, carbofuran, acetamiprid, parathion, azinphos-methyl, chlorpyrifos, malathion, coumaphos, chlorfenvinphos, spinosadNAup to 100%NR[99]
T. versicolorsulfomethoxazole, isoproturonABTS, SA, AScomplete transformation of both in presence of ABTS, as well as for sulfomethoxazole in presence of AS or SAreduced (green alga P. subcapitata growth inhibition assay)[119]
T. versicolorketoconazoleHBTup to 100%reduced (P. subcapitata, Candida albicans, Cryptococcus neoformans, and Saccharomyces cerevisiae micro-toxicity study)[130]
T. versicolorcarbamazepineABTSover 94%reduced (estrogenicity tests using yeast estrogen screen (YES) assay)[121]
T. versicolornaproxen, diclofenacNAover 90%reduced for encapsulated enzyme; increased for adsorbed laccase (ecotoxicity test against Artemia salina)[115]
T. versicolortriclosanABTSup to 100%reduced for crude laccase; increased with ABTS (Microtox assay with Photobacterium phosphoreum)[131]
T. hirsuta17β-estradiolNAup to 99.3%NR[129]
P. ostreatusnaproxen, atrazine, oxybenzone, pentachlorophenolHBT, SA, VA, HPI, TEMPO, ABTS, VA, vanilin 15–23% for free laccase, ca. 10–98% for LMSNR[122]
T. versicoloramoxicillin, ampicillin, cloxacillin, oxacillin, penicillin G, V, ciprofloxacin, enrofloxacin, sulfamethoxazole, sulfabenzamide, sulfadiazine, sulfamerazine, sulfamethoxypyridazine, sulfadimethoxine, ofloxacin, sulfamethizole, sulfanitran, sulfapyridine, sulfathiazole, sulfisomidin, sulfisoxazole, fluoroquinolones, danofloxacin, difloxacin, enoxacin, orbifloxacin, marbofloxacin, flumequine, norfloxacin, cinoxacin, nalidixic acid, oxolinic acid, pipemidic acid, tetracycline, chlorotetracycline, doxycycline, oxytetracycline, metronidazole, trimethoprimSA32 antibiotics were degraded by >50% after 24 h with SAincreased (a growth inhibition assay against Bacillus subtilis and
the Microtox assay using Aliivibrio fischerii)
[120]
T. pubescensmunicipal WWTP containing mainly bis(2-ethylhexyl) phthalate, ketoprofen, diethyl phthalateNAover 60%reduced ecotoxicity (tests with Raphidocelis subcapitata and Lepidium sativum); reduced estrogenic activity (MELN assay and in vitro E-screen test)[107]
Cerrena unicoloroxytetracycline, tetracycline, ampicillin, sulfamethoxazole, erythromycin, chloramphenicol, trimethoprimABTS80% for oxytetracycline and tetracyclinereduced (Escherichia coli and Bacillus licheniformis)[132]
Streptomyces ipomeaciprofloxacin, norfloxacinNAup to 90%reduced (P. subcapitata)[133]
M. thermophiladiclofenac, bisphenol ASA>95% for bisphenol A and >80% for diclofenacNR[134]
Notes: NR, not reported; NA, not applicable; CA, p-coumaric acid; SA, syringaldehyde, AS, acetosyringone; VA, violuric acid; HBT, 1-hydroxybenzotriazole; ABTS, 2,2-azinobis(3-ethylbenzthiazoline-6-sulphonic acid); HPI, N-hydroxyphthalimide; TEMPO, 2,2,6,6-tetramethyl-1-piperidinyloxy.

5. Conclusions and Future Perspectives

Micropollutants pose a serious obstacle to water treatment procedures. Although there are various biological methods for the elimination of micropollutants, the fact that laccase is exceptional, as in the presence of molecular oxygen without any additional cofactor, it acts oxidatively on the aromatic ring of a wide range of compounds, releasing water as the only by-product. Laccase-based approaches encounter limitations at an industrial scale due to the costs of production; however, this enzyme seems to be increasingly available on a large scale. The availability of robust laccase with high redox potential and/or an efficient non-toxic laccase–mediator combination is one of the main bottlenecks for its bioremediation applications. Since ecotoxicity is the primary concern associated with micropollutants due to their extremely high bioaccumulation, monitoring the toxicity of reaction by-products should be investigated and evaluated in detail. Hence, more studies are still needed for the optimization of degradation processes in a laboratory scale to improve our understanding of the different interactions of laccase with the substrate. These include the exploration of enzyme-based omics approaches to develop scalable and commercially viable technologies that have no impact on the environment and ensure enzyme stability. It seems that the laccase engineering approach and that tailoring enzymes according to the type of substrate can also overcome the limitations associated with the use of laccase and can improve its catalytic performance and functional expression. This could ultimately lead to the transformation of laccases into modern high value-added biocatalysts and to the development of sustainable advanced water treatment technologies.

Author Contributions

Conceptualization, A.P. and G.J.; writing—original draft preparation, A.P., E.S. and G.J.; writing—review and editing, A.P. and G.J.; visualization, A.P., E.S. and G.J.; supervision, A.P. All authors have read and agreed to the published version of the manuscript.

Funding

This work was financially supported by the research program BS/UMCS.

Data Availability Statement

Data sharing not applicable.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

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Figure 1. Increasing trend in the number of publications for years listed in the Scopus (XI.2022).
Figure 1. Increasing trend in the number of publications for years listed in the Scopus (XI.2022).
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Figure 2. Predicted compound annual growth rate (CAGR) for pharmaceuticals, home and garden pesticides, personal care products, and industrial chemicals for 2021–2030 (prepared by the authors based on [20]).
Figure 2. Predicted compound annual growth rate (CAGR) for pharmaceuticals, home and garden pesticides, personal care products, and industrial chemicals for 2021–2030 (prepared by the authors based on [20]).
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Figure 3. Potential enzymes engaged in biodegradation of pharmaceuticals, pesticides, personal care products, and industrial chemicals from wastewater; LiP, lignin peroxidase; VP, versatile peroxidase; HRP, horseradish peroxidase; CPO, heme-containing chloroperoxidase; OPAA, organophosphorus acid anhydrolase; OPH, organophosphate hydrolase.
Figure 3. Potential enzymes engaged in biodegradation of pharmaceuticals, pesticides, personal care products, and industrial chemicals from wastewater; LiP, lignin peroxidase; VP, versatile peroxidase; HRP, horseradish peroxidase; CPO, heme-containing chloroperoxidase; OPAA, organophosphorus acid anhydrolase; OPH, organophosphate hydrolase.
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Figure 4. Possible biodegradation pathways of common micropollutants: (a) naproxen—(2S)-2-(6-Methoxy-2-naphthyl)propanoic acid; (b) diclofenac—{2-[(2,6-Dichlorophenyl)amino]phenyl}acetic acid; (c) triclosan—5-Chlor-2-(2,4-dichlorphenoxy)phenol; and (d) carbamazepine—5H-Dibenzo[b,f]azepine-5-carboxamide by laccase (prepared by the authors based on [115,116,117]).
Figure 4. Possible biodegradation pathways of common micropollutants: (a) naproxen—(2S)-2-(6-Methoxy-2-naphthyl)propanoic acid; (b) diclofenac—{2-[(2,6-Dichlorophenyl)amino]phenyl}acetic acid; (c) triclosan—5-Chlor-2-(2,4-dichlorphenoxy)phenol; and (d) carbamazepine—5H-Dibenzo[b,f]azepine-5-carboxamide by laccase (prepared by the authors based on [115,116,117]).
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Table 1. Some global producers of laccase for industrial purposes (XII.2022).
Table 1. Some global producers of laccase for industrial purposes (XII.2022).
Manufacturer/SupplierProduct DescriptionCost/Price
Mega Pacific Technology, Inc., Arcadia, CA, USALaccase Q10, purity 100%, for indigo bleaching1–5 USD per 1 kg
Xi’an International Healthcare Factory Co., Ltd., Xi’an, China99% min. laccase15–25 USD per 1 kg
Xi’an Multihealth Biotech Co., Ltd., Xi’an, China98%, food grade40–60 USD per 1 kg
Sunson Industry Group Co., Ltd., Beijing, ChinaPurity 99.9%, for paper chemicals16–22 USD per 1 kg
Sunson Industry Group Co., Ltd., Beijing, ChinaActivity of 10,000 U/g, from Aspergillus oryzae for wastewater, papermaking, textile, juice clarification, baking35–55 USD per 1 kg
Qingdao Cemo Technology Develop Co., Ltd.,
Shandong, China
Purity 99%, Novozyme 809, food additive1–10 USD per 1 kg
Botanical Cube Inc., Xi’an, ChinaMW 119.12, nutrition enhancer21–38 USD per 1 kg
Sinobios (Shanghai) Imp. & Exp. Co., Ltd., Shanghai, ChinaLAC8L, liquid, activity ≥ 5000 U/mL, from white-rot fungi, textile auxiliary agent1–5 USD per 1 kg
Novozymes, Denmark (from Merck, Darmstadt,
Germany)
Novozym® 51003, Activity 1000 LAMU (laccase unit)/g, liquid, from A. oryzae450 EUR per 250 dm3
Hebei Mojin Biotechnology Co., Ltd., Shijiazhuang, ChinaPurity 99%100 USD per 25 kg
Career Henan Chemical Co., Zhengzhou, ChinaPurity 98% (HPLC)1 USD per 1 kg
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Janusz, G.; Skwarek, E.; Pawlik, A. Potential of Laccase as a Tool for Biodegradation of Wastewater Micropollutants. Water 2023, 15, 3770. https://doi.org/10.3390/w15213770

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Janusz G, Skwarek E, Pawlik A. Potential of Laccase as a Tool for Biodegradation of Wastewater Micropollutants. Water. 2023; 15(21):3770. https://doi.org/10.3390/w15213770

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Janusz, Grzegorz, Ewa Skwarek, and Anna Pawlik. 2023. "Potential of Laccase as a Tool for Biodegradation of Wastewater Micropollutants" Water 15, no. 21: 3770. https://doi.org/10.3390/w15213770

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