White Rot Fungi for Biodegradation of Dyes: Potential for Industrial Uses - A Review

Abstract

White rot fungi produce oxidative and reductive enzymes, which are very important to the ecology of tropical forests and act on the degradation of all types of ligninolytic and cellulosic wastes. Laccases, lignin peroxidases (LiPs), and manganese peroxidases (MnPs) enzymes exhibit significant ability to biodegrade a wide variety of environmental pollutants. The synthetic dyes from the textile industry are organic compounds classified by chromophore groups. The occurrence of dyes in the effluents carries on ecotoxicological hazards and the potential of bioaccumulation, eventually affecting flora and fauna. Previous reports emphasize the classification, impact, and consequences to the health and environment caused by textile dyes, bioremediation processes, enzymes, and immobilization techniques utilized to increase degradation efficiency. In this review, the enzymatic mechanisms of biodegradation, decolorization, and adsorption, the proposed biodegradation pathway from various classes of textile dyes, and structural determination of metabolites using mass spectrometric are described, together with the treatment of dye effluents from white rot fungi species. The approach to applying this biotechnology is discussed, and there are indications that it is a promising alternative for treating effluent-containing dyes.

Keywords:
biorremediation; textile effluent; dyes metabolites; Trametes ; ligninolytic enzymes

1. Introduction

Dyes are widely used in different sectors, such as pharmaceutical, cosmetics, pulp, and textile industries.¹ The textile industry stands out because it releases thousands of tons into the water each year,² accounting for 54% of dye waste that ends up in the environment.³ In this way, dyes reach water resources, which has several consequences for the flora, fauna, and humans.⁴ Indeed, dye ingestion can cause several harms to human health, including deoxyribonucleic acid (DNA) damage.⁵

Besides, dyes are toxic, bioaccumulating, and recalcitrant.⁶ Due to their impact on water resources, it is necessary to use techniques to effectively treat effluents from the textile industry before their disposal. Biological methods can be emphasized among the treatment options. Microbial bioremediation employs microorganisms - bacteria, fungi, algae, and archaea-and/or their enzymes to remove pollutants.⁷ These procedures offer numerous advantages, such as being ecologically harmless and affordable, besides the fact that microorganisms can remove dyes efficiently.⁸

Fungi applications are low-cost and promising alternatives since they are organisms that grow quickly and are easy to cultivate.⁹ An advantage over unicellular organisms is the production of extracellular enzymes, which leads to greater contact between enzymes and the environment, thus providing tolerance to high concentrations of toxic substances and compounds.¹⁰ In particular, white rot fungi (WRF) can degrade compounds with complex structures, such as lignin, their main substrate, which is attributed to the production of three types of enzymes, namely: laccase, lignin peroxidase, and manganese peroxidase, while others produce one or two of them.¹¹ These enzymes are strong non-selective and non-specific oxidants, making these fungi capable of removing recalcitrant compounds by specific reactions and having absorption and accumulation mechanisms.¹⁰

Some recent reviews demonstrate the interest of the scientific community in this topic and its relevance to the potential of fungi for this use. Latif et al.¹² reviewed the application of WRF to treat industrial effluents. In that review, effluents containing dyes are only briefly addressed amid discussion about other types of effluents, such as those containing pharmaceuticals, pesticides, heavy metals, and phenolic compounds, without particularly focusing on effluents with dyes. Moreover, other studies restricted their attention to the degradation of azo dyes. Shi et al.¹³ primarily focused on the degradation of azo groups, while fungal degradation was not the main emphasis of their review. Similarly, the reviews by Ajaz et al.¹⁴ and Goud et al.¹⁵ also took a more general approach to biodegradation rather than specifically concentrating on fungal processes. Patel et al.¹⁶ focused on the different microorganisms that can be used for dye bioremediation, although they dedicated only one topic to the application of WRF for dye bioremediation. Finally, the review by Herath et al.¹⁷ specifically addressed the decolorization of textile effluent by applying WRF. The authors discussed in depth the effects of variables that affect the performance of these organisms in the treatment of dyes and addressed the techniques used to apply these fungi in the treatment.

To the best of our knowledge, this is the first review focused on WRF for dye bioremediation with a multidisciplinary approach, addressing several aspects relevant to the most diverse areas of knowledge, such as organic chemistry - described in biodegradation pathways and elucidation of dye degraded metabolites, environmental engineering, and sanitary engineering. This interdisciplinary strategy was implemented in a didactic manner, making it simple for another area specialist to acquire the technical knowledge of each field. This approach is crucial when one anticipates which technology will be used to treat effluents with dyes on a large scale. Therefore, this review addresses an overview of the concern of dyes, the contamination of water resources, and its consequences, proving the need to treat them effectively. It presents the benefits of using white rot fungi and explains its enzyme mechanisms; discusses the use of white rot fungi to decolorize dye effluent and presents the most recent findings from the scientific community; brings proposals for biodegradation mechanisms of dyes and seeks to elucidate the structures of metabolites. Finally, techniques for removing dyes from water are overviewed, ending with hybrid methods - which involve fungi and other technologies - as it may be one of the most promising directions for applying fungi treatment on an industrial scale. Consequently, it is anticipated that this review will inspire more research applying white rot fungi to treat dye effluents, contributing to developing technologies that promote safe water for the environment and humans.

2. Dyes: Types, Effluent Contamination, Environmental and Human Problems

2.1. Classification

Dyes are synthetic or natural substances that absorb light in the visible spectrum, between 400 and 700 nm, and, therefore, reflect or diffuse complementary radiation.¹⁸ This characteristic of dyes is due to conjugated double bonds and their chromophoric groups. The chromophore is the active site where light-absorbing atoms are found, in which heteroatoms such as nitrogen, oxygen, and sulfur are present.¹⁹

In addition to chromophores, dye molecules have groups of atoms known as auxochromes,²⁰ which allow the dye to be attached to the substrate and modify the color intensity. Some examples of these groups are amines, hydroxy groups, and sulfonates.²¹ Dyes adhere to the surface through solution formation, covalent bonds, adsorption, mechanical retention, or complexation with salts and/or metals.²²

Dyes can be classified as natural and synthetic. Natural dyes are derived from materials that have been used by human civilization since ancient times. They are extracted from animals, insects, plants, or minerals,²³ with organic and inorganic components containing chromophores.²⁴ Besides classifying dyes according to their origin, natural dyes can be further classified according to their chemical structure as indigoids (blue, represented by indigo extracted from mollusks), pyridines (yellow, berberine is an example), carotenoids (extracted from plants, such as carrots, are applied in the food industry), quinonoids (color varies from yellow to red, extracted from flowering plants), flavonoids (the performance of these dyes is improved with the use of mordants, and colors vary between yellow, blue, red, and orange), dihydropyran (dye can be extracted from Brazilwood, and mordants also improve the affinity), betalains (used in the food and pharmaceutical industry), and tannins (dyes are extracted from various parts of plants, the application is also improved with the use of mordants). ²⁵

Humanity relied on natural dyes for centuries until the development of the first synthetic dyes in the 19^th century. However, the use of natural dyes has significantly decreased with the rise of synthetic alternatives.²⁶ These synthetic dyes have become essential in meeting the growing demands of industry, particularly in the textile sector.²⁶ Today, they are widely utilized due to their advantages, such as ease of application and the ability to consistently produce a wide range of shades, including vibrant ones.²⁷

Natural dyes are becoming increasingly attractive as awareness of environmental issues grows. These dyes are generally non-toxic, non-allergenic, biodegradable, and derived from renewable resources.²⁸ However, despite efforts to improve techniques for obtaining and using natural pigments, there are still many challenges for large scale application, such as the difficulty in standardizing natural dyes. Factors like climate, soil conditions, and cultivation techniques can all influence the final dye quality.²⁹ An emerging alternative to overcome these limitations is the production of natural pigments through microbial fermentation, which offers a more controlled and scalable approach.¹⁷ However, due to these challenges, it is likely that the industry will continue to rely on synthetic dyes in the coming years.

Since Henry Perkin patented the first synthetic dye in 1854, the production of synthetic dyes has intensified to the extent that there are reports of more than 100.000 synthetic dyes.²¹ They derive mostly from petrochemical compounds. The dye structure is very important for its degradability or removal.³⁰ In this sense, Table 1 shows the classification of dyes concerning the chromophore group present in their structure. Other heterocyclic rings and functional groups also give rise to examples of chromophores used by dye class names (Figure 1).

Table 1
Chromophore, name and applications of various types of dyes

Dye chemical class	Chromophore	Dye name	Application	Reference
Azo		Azorubine Tartrazine Methyl Yellow	dyeing clothing, paper, food, cosmetics, and other materials	20,31-33
Nitro compounds		Acid Orange 3 Disperse Yellow 9 Disperse Yellow 42	hair coloring products dyeing of textiles	20,34
Nitrous compounds		Naphthol Green B	biological assays	35
Anthraquinones		Vat Yellow 28 Reactive Blue 4 Remazol Brilliant Blue R	textile industry	36,37
Triphenylmethanes		Malachite green	textile, pharmaceutical, paper, leather, cosmetics, and food industries	38
Xanthenes		Rhodamine B, Fluorescein	optical materials and medical diagnostic research	20,39
Phthaleins		Phenolphthalein o-cresolphthalein	pH indicators	20,40
Acridines		Acridine Orange	cell staining, biological assays, medicinal applications, and biosensitive photovoltaic material	41
Oxazines		Brilliant Cresyl Blue Nile Blue O	redox indicators used widely as a photosensitizer	20,42,43
Cyanines		Pinacyanol kryptocyanine	photographic industry, acid-base indicators and pharmaceutical industry	20,44
Quinione-imines		Phenol Blue	redox indicators solvent polarity indicator	20,45
Triarylmethanes		Basic Blue 26 Basic Green 1	textile dyes for silk, wool and cotton, colorants in foods, drugs, and cosmetics industry	20,46
Diarylmethanes		Auramine O	dyeing leather, jute, cotton, and paper	20,47
Indigoids		Indigo Blue Indigo Carmine	the main representative is indigo blue, used to color jeans in the textile industry	48
Phthalocyanines		Copper phthalocyanine	printing inks, paints, coatings, plastics, and textiles	49
Thiazines		Methylene blue	pigmentation, pharmaceuticals, and staining for microscopy	50

Figure 1
Other types of chromophores used by dye classes names.

Table 2 shows another common categorization of dyes according to their application method. A connection between the diverse categorization approaches can be observed. Direct dyes, for instance, comprise dyes containing the chromophores phthalocyanine, oxazine, and azo, among others. Dispersive dyes mostly involve dyes with azo chromophore and are generally recalcitrant compounds due to non-biodegradability. Among the vat dyes, the chromophores groups anthraquinone and indigo are commonly found. Basic dyes involve dyes with chromophores xanthenes, acridine, and triarylmethane.²⁰Table 3 shows structures of example dyes mentioned in Table 2.

Table 2
Dye classification according to application method

Class	Description	Chemical dye class	Solubility	Dye	Reference
Acid	acid dyes consist of molecules with one or more groups that confer an acidic nature (such as COOH) they are applied in acidic pH	azo, anthraquinone, nitro and triphenylmethane	acidic aqueous medium	Acid Blue 7	20,30,51
Direct	direct dyes have an affinity for fiber and are taken up directly and easily; they bind to fibers via adsorption	azo, stibene, oxazine and phthalocyanine	water-soluble	Direct Red 28	20,30
Disperse	disperse dyes are commonly applied from fine aqueous suspensions and color fiber via H-bond and van der Waals force	azo, anthraquinone, and nitro	water-insoluble	Disperse Violet 26	20,30,52
Reactive	reactive dyes can form a covalent bond with the amine or sulfhydryl groups of textile fiber proteins	Azo and anthraquinone	water-soluble	Reactive Red 239	20,53,54
Vat	Vat dyes are solubilized in alkali, so carbonyl groups are changed to C=OH groups and then to soluble sodium derivatives; the parent structure is recovered after dyeing, and the dye molecule links with fiber through H-bonds and van der Waals forces	anthraquinone and indigoids	soluble in hot water	Vat Green 1	20,53
Sulfur	sulfur dyes do not have well‑defined chemical structures, which are specified with the raw material and manufacturing process; after synthesis, the excess sulfur is separated from the dye	chromophores are based on thiazole, thiazone, thianthrenes and phenothiazonethioanthrone structures	water-insoluble	Sulfur Black	20,53
Cationic (basic)	cationic dyes consist of organic bases that have free or substituted amino groups (such as -NH2); their molecules release colored cations in an aqueous solution	azo, diphenylmethane, triarylmethane, xanthene, acridine, and oxazine	soluble in alcohol and methylated spirit but not easily soluble in water	Basic Yellow 2	53
Mordant	mordants are metal salts with an affinity for fiber and dye; if a dye has less or no affinity for fiber, a mordant improves the affinity and makes a dye‑mordant-fiber complex	Azo and triarylmethane		Mordant Black 17	20,53,55
Azoic	azoic dyes are developed in situ cellulosic through a chemical reaction between a diazotized base and naphthol	Azo	water-insoluble	Disperse Yellow 3	20,53

Table 3
Chemical structures of some classes of dyes

Acid Blue 7		20,30,51
Direct Red 28		20,30
Disperse Violet 26		20,30
Reactive Red 239		20,53
Vat Green 1		20,53
Sulfur Black		20,53
Basic Yellow 2		53
Mordant Black 17		20,53
Disperse Yellow 3		20,53

2.2. Contamination of water resources, environmental and human problems

In the textile industry, water is applied in several steps since it acts as a solvent for chemical products and is used for washing. In fact, water is used in stages including dyeing, washing, printing, and finishing.⁵⁶ According to Kant,⁵⁷ a medium-sized textile industry consumes around 1.6 million liters per day to produce 8000 kg of fabric, which results in the discharge of millions of gallons of effluent. Therefore, one of the main routes of contamination of water resources by dyes occurs mainly through industrial effluent disposal without adequate treatment. ⁵⁸

Effluent from the textile industry generally has color, high temperature and pH, elevated concentrations of biochemical oxygen demand (BOD), chemical oxygen demand (COD), and total suspended solids, besides high concentrations of sulfur, naphthol, nitrates, heavy metals, acetic acid, and surfactants. These characteristics may difficult the treatment of these effluents and inadequate disposal may happen.⁵⁷ Consequently, dye effluents can seriously harm the ecosystem, impacting flora and fauna, including humans. Eluding the extent of dye contamination, they have already been found in samples of surface water, drinking water, sediments, soil, fish, and various crops, such as rice, soybeans, potatoes, and watermelon from places where the soil was contaminated with dyes.⁴

Some immediate effects of improperly disposing of dye-containing effluents are decreased dissolved oxygen content, less photosynthetic activity since it impedes sunlight to penetrate the water column, and aesthetic damage. Other indirect consequences include the death of aquatic plants and animals and eutrophication.⁵⁹ Furthermore, dyes can be toxic, recalcitrant, and bioaccumulate in the food chain, which can cause harmful effects on organisms.⁶Figure 2 shows the consequences of the inappropriate disposal of effluents containing dyes, such as the difficulty of sunlight penetrating water, in addition to possible routes of human contamination by dyes. These molecules can reach humans through the direct ingestion of contaminated water and indirectly, such as through contaminated food due to the use of water-containing dyes in irrigation or as a result of bioaccumulation in the food chain. These contamination routes deserve great attention since ingesting or inhaling dyes can harm several organs and systems, such as the skin, liver, kidney, nervous, and reproductive systems.⁶⁰

Figure 2
Possible route for the contamination of water supplies, vegetation, animals and humans by dyes.

Mpountoukas et al.⁶¹ studied the effects of dyes used in foods, namely amaranth, erythrosine, and tartrazine (Figure 3). The authors observed the potentially toxic effects of these dyes on human lymphocytes and highlighted the evidence that these dyes are directly bound to DNA. Chequer et al.⁵ studied the effects of erythrosine and xanthene dyes, concluding that it could cause damage to the DNA structure despite its industrial use (such as in pharmaceuticals and food industries) being permitted.

Figure 3
Chemical structures of the dyes, amaranth, erythrosine and tartrazine.

Due to the severe implications of dye pollution in water resources and the inherent stability of many dye molecules, the need for effective dye removal methods from textile effluents is urgent. In this context, WRF stand out as a promising solution. The genus Trametes, in particular, is frequently cited in studies on dye biodegradation due to its high efficiency and versatility.⁶² This potential of WRF in dye removal will be further explored in the following sections.

3. White Rot Fungi and Their Enzymes

Using fungi to biodegrade dyes offers a sustainable and effective approach to treating textile effluents. These microorganisms not only adsorb the dyes into the microbial biomass but also perform direct biodegradation, altering the original structure of the dye and often completely decomposing it.⁶³ Besides biodegradation, the process of adsorption, (where molecules are retained on the surface of a material) is crucial in the initial removal of dyes. The combination of adsorption and biodegradation provides a comprehensive and effective dual approach to effluent cleaning.

Fungi produce a variety of extracellular enzymes known for their non-specificity and non-selectivity. These enzymes are capable of degrading a wide range of xenobiotics and complex dyes, such as lignin and azo dyes, anthraquinone, and triphenylmethane.⁶⁴ Furthermore, these enzymes can biodegrade the molecular structure of synthetic dyes into less toxic products that are more easily assimilated by the environment.⁶⁵

In addition to their effectiveness in degrading dyes, these filamentous fungi are widely distributed in different natural environments.⁶⁶ The mycelium of these fungi is often used as a biosorbent, which plays a crucial role in the bioadsorption of dyes.⁶⁷ The mycelium consists of a network of fine filaments called hyphae, which provides an excellent specific surface area, allowing efficient adsorption of dyes present in textile effluents, significantly contributing to the removal of dyes from water.⁶⁷

White rot fungi belong mainly to the phylum Basidiomycota and include a variety of genera.⁶⁸ Among the most notable are Pleurotus, known for its ability to decompose a wide range of substrates; Phanerochaete, widely studied for its ligninolytic abilities; and Lentinus, commonly used in biotechnological applications.⁶⁸ The genus Trametes stands out within the order Polyporales, the genus Trametes is frequently cited in studies on the biodegradation of dyes due to its high efficiency and versatility.⁶²

The efficiency of these fungi in degrading dyes is dependent on several critical elements that affect their development, synthesis of enzymes, and decolorization efficiency. These factors - further discussed in this paper - include the nutritional composition of the cultivation matrix, agitation intensity during the process, incubation time, pH of the environment, cultivation temperature, available carbon sources, and oxygen availability. Furthermore, the expression of ligninolytic enzyme genes is regulated by oxygen availability, resulting in greater production of these enzymes.⁶⁹ It occurs because oxygen promotes the formation of reactive oxygen species (ROS), essential for the oxidation and breakdown of dye molecules.

Fungal metabolism is more efficient with oxygen, providing energy for enzyme synthesis and other processes.⁷⁰ Therefore, oxidation reactions are more efficient in aerobic environments, where enzymes maintain their catalytic activity for longer.⁶⁹,⁷¹

The effective bleaching ability, of WRF is paving the way for more sustainable and environmentally friendly methods in the textile industry. By exploring the potential of these fungi, researchers have advanced the development of technologies that aim to reduce pollution associated with textile waste. This not only promotes more sustainable practices in the sector, but also underscores the significant role of white rot fungi in addressing environmental concerns.⁷²

Synthetic dyes may be biodegraded by microorganisms in particular conditions by employing biosynthesized enzymes to break down lignin, which is the primary substrate.⁷³ This bioremediation mechanism, driven by the action of several enzymes that fragment the dyes into different by-products, is fundamental to the decolorization process. The remarkable effectiveness of this mechanism is attributed to the ability of white rot fungi to produce specialized ligninolytic enzymes capable of catalyzing the mineralization of dyes.¹⁷

Therefore, the ligninolytic enzymes of the WRF can degrade both lignin and a wide variety of textile dyes, such as azo, anthraquinone, and triphenylmethane.⁷⁴ White rot fungi are notable for producing all three major lignin-modifying enzymes - laccase, lignin peroxidase (LiP), and manganese peroxidase (MnP) - although some species may produce only one or two of these enzymes.¹⁷ The specific contribution of each enzyme to dye decolorization may vary between different fungal species. These enzymes not only enable fungi to break down lignin - a highly complex and recalcitrant polymer - but also make them proficient in degrading persistent and xenobiotic compounds, including textile dyes. This versatility makes white rot fungi stand out as promising candidates for dye biodegradation.⁷³

3.1. Manganese peroxidase

Ligninolytic enzymes, especially manganese (MnP)-dependent peroxidases, play crucial roles in lignin degradation, acting as oxidases and peroxidases (Figure 4). These enzymes utilize a heme prosthetic group and require hydrogen peroxide to oxidize Mn²⁺ to Mn³⁺ complexed with organic acids cleave lignin.⁶⁸,⁷⁵

Figure 4
Manganese peroxidase catalytic cycle (adapted from Chang et al.⁷⁸).

The catalytic cycle of MnP begins with hydrogen peroxide binding to the enzyme in ferric form, forming an iron-peroxide complex. Mn²⁺ reduces this complex to form Mn³⁺, stabilized by organic acids such as oxalate and malonate, which act as redox mediators attacking organic molecules in a non-specific way.⁷⁶ In addition to lignin, MnP also oxidizes phenolic and non-phenolic compounds, which apply to the degradation of hydrocarbons, synthetic dyes, and chlorinated pollutants.⁷⁷

MnP can be inactivated by high concentrations of H₂O₂, forming a catalytically inactive state. However, in addition to Mn²⁺, some MnPs can oxidize phenolic and non-phenolic aromatic compounds, acting as hybrids of MnP and LiP.⁷⁶ Mn³⁺ chelates with carboxylic acids oxidize phenolic and amino-aromatic compounds, forming radicals that react with dioxygen, resulting in other radicals essential for the degradation of recalcitrant compounds.⁷⁶

3.2. Lignin peroxidase

One of the main enzymes involved in modifying lignin is LiP. It has a heme group as an essential component. These enzymes can directly oxidize lignin, justifying their role as effective ligninases.¹⁷ The ligninolytic enzyme system has been extensively studied by producing model organisms such as Phanerochaete chrysosporium, a known source of LiP, used in biopulping and paper bleaching processes through a series of reaction steps.⁶⁴

LiP is capable of breaking C-C and C-O bonds and also polymerizes phenols. In the LiP catalytic cycle, iron in the ferric form (Fe³⁺) is oxidized to (Fe⁴⁺) by hydrogen peroxide (Figure 5), forming compound I, which oxidizes lignin and related compounds.⁷⁹ The transfer of an electron forms compound II, which returns to its native form in the presence of a reducing agent, although excess hydrogen peroxide can inactivate it. Veratryl alcohol, a fungal metabolite, acts as a reducer for LiP, protecting it from inactivation by preventing excessive oxidation and facilitating its return to its native form.⁷⁹

Figure 5
Lignin peroxidase catalytic cycle (adapted from Ahsan et al.⁸⁰).

3.3. Laccase

Laccase enzymes are monomeric copper-containing extracellular proteins. They are named blue multicopper oxidases and play a crucial role in various industrial processes, including delignification, bleaching of textile dyes, bioremediation, and production of chemical compounds.⁷⁰ They can catalyze the reduction of up to four oxygen electrons while oxidizing organic substrates. The structure includes two to four copper atoms per molecule, and these enzymes are glycoproteins containing carbohydrates such as hexosamine, glucose, and mannose. They can be found inside cells, in the extracellular environment, or associated with the cell wall.⁷⁰ The glycosylation of laccases, ranging from 10 to 44%, is crucial for their stability against the action of proteases. Copper ions are distributed in three types of sites: T1, T2, and T3 (Figure 6). T1 copper, responsible for the blue color of the protein, captures electrons from phenolic substrates, which are then transferred through the His-Cys-His tripeptide to the T2 and T3 sites. These sites form a trinuclear cluster facilitating oxygen reduction to water, completing the enzyme catalytic cycle.¹⁷ Among the white rot fungi, Trametes species are recognized for their laccase biosynthesis.

Figure 6
Catalysis by laccase (adapted from Shanmugapriya et al.).⁸¹

4. White Rot Fungi Applied to Dye Descolo-ri-zation and Adsorption by Ultraviolet-Visible (UV-VIS) Analysis

The effluent from the textile industry has a low rate of natural degradation, which can cause problems both to local ecosystems and to human health since it has high toxicity and can be potentially carcinogenic. Thus, many techniques have already been addressed in the literature (Figure 7), but the white rot fungi offer advantages, such as high efficiency and low cost, promoting the breaking of chemical bonds of synthetic dyes, and allowing a greater neutralization of pollutants. Thus, its application and the obstacles to the consolidation of this technology will be discussed in this sub-section.

Figure 7
Publications on the application of white rot fungus in the treatment of dyes.

A search on Web of Science, Scopus, and ScienceDirect was carried out to quantify the number of publications regarding the application of white rot fungus in the treatment of the dye industry. The search keywords were “White Rot Fungi” AND “treatment” AND “dyes” and the results revealed a total of 2.570 articles that reported in the title, keywords, and abstract of the articles the use of the white rot fungi in decolorization of dyes (Figure 7).

Considering that the number of publications is quite vast and has increased significantly in recent years, it is difficult to analyze each technical and scientific article contributions accurately. Therefore, we considered the most recent articles when analyzing this topic whenever possible since the focus was to present the main factors and operational parameters that affect the decolorization of the white rot fungi, as shown in Figure 8.

Figure 8
Factors and operational parameters affecting white rot fungi.

Analyses of the results in Table 4 showed that the decolorization achieved levels between 41 and 98% regardless of the dye concentration. It demonstrates that the white rot fungus can effectively remediate wastewater from the textile sector. Despite this efficiency, inhibition processes can affect the ideal operational conditions of cultivation and growth medium for the reproduction of the white rot fungi, focusing on the Trametes genus.

Table 4
Dye decolorization using white rot fungi

Dye / effluent matrix	Microorganism / fungal strain	Culture conditions and operational aspects	Decolorization, time, temperature, pH and enzyme	Reference
Reactive Black 5 / real	Trametes versicolor	concentration: 150 mg L-1; volume: 1 L; test duration: 150 h	98%, 144 h (pH 5); MnP and laccase activity and versatile peroxidases (VeP)	82
Orange G / synthetic	Trametes polyzona	concentration: 50 mg L-1; temperature: 30 °C; stirring speed: 160 rpm; pH: 4	50%, 24 h; MnP activity	83
Black 10B / synthetic	Trametes polyzona	concentration: 50 mg L-1; temperature: 30 °C; stirring speed: 160 rpm; pH: 4	80%, 24 h; MnP activity	83
Methyl Green and Reactive Violet 5 / synthetics	Ganoderma lucidum	concentration: 100 mg L-1; temperature: 30 °C; stirring speed: 180 rpm; pH: 5	86.79%, 24 h	84
Reactive Orange 16 (RO-16) / synthetic	Phanerochaete velutina	concentration: 100 mg L-1; volume: 250 mL; temperature: 28 °C; pH: 4.5	50%, 13-15 days	85
Acid Yellow 17 / synthetic	Pleurotus eryngii	concentration: 1 mg L-1; volume: 250 mL; temperature: 28 °C; stirring speed: 150 rpm; test duration: 7 days	90%, 8 h	86
Malachite Green / synthetic	Ganoderma sp.	concentration: 50 mg L-1; volume: 500 mL; temperature: 28 °C; stirring speed: 130 rpm	96%, 7 days; MnP activity	87
Direct Blue 1	Perenniporia subtephropora	concentration: 50 mg L-1; volume: 250 mL; temperature: 20-40 °C; pH 3-9	99%, 12 h, pH 6.68 and temperature 26.49 ºC	88
Remazol Brilliant Blue R (RBBR) / synthetic	Trametes hirsuta	concentration: 28 mg L-1; temperature: 25 °C; stirring speed: 70 rpm; pH: 4.5	97%, 24 h; MnP activity	89
Blue B / synthetic	Trametes versicolor	concentration: 100, 200, 300, 400, and 500 mg L-1; volume: 250 mL; temperature: 28 °C; stirring speed: 160 rpm; test duration: 7 days	85.6%, 48 h MnP activity	90
Green Tosca / real	Trametes hirsuta	concentration: 20 mg L-1; volume: 250 mL; temperature: 27 °C; test duration: 7 days	95%, 144 h; MnP activity	91
Congo Red / synthetic	Trametes flavida	concentration: 100 mg L-1; volume: 500 mL; temperature: 28 °C; stirring speed: 400 rpm; test duration: 10 days	99.48%, 16 h	92
Congo Red / Synthetic	Trametes flavida	concentration: 100 -1500 mg L-1; volume: 500 mL; temperature: 28 °C; stirring speed: 100 rpm; test duration: 8 days	87.28%, 24 h; and 100%, 5 days	92
Remazol Brilliant Blue R (RBBR) / synthetic	Trametes hirsuta	concentration: 300, 500, and 1000 mg L-1; volume: 500 mL; temperature: 28 °C; stirring speed: 120 rpm; test duration: 4 days; glucose: 100 g L-1	86%, 48 h	93
AR dye / real	Trametes pocas	dye concentration: 200 mg L-1; volume: 20 L; temperature: 28°C; pH: 7	90%, 4 days	94
Direct Red 5B	Ganoderma lucidum	dye concentration: 25 mg L-1; volume: 250 mL; stirring speed: 100 rpm; test duration 7 days; temperature: 28 °C	95.16%, 48 h	95
Textile effluent / real	Trametes hirsuta	dye concentration: 50 mg L-1; volume: 250 mL; temperature: 28 °C; stirring speed: 150 rpm; test duration: 5 days; pH: 5	84.57%, 48 h (pH 4)	96
Remazol Brilliant Blue / synthetic	Trametes pubescens	dye concentration: 25 mg L-1; volume: 250 mL; temperature: 25 °C; pH: 3-5	42-95%	97
Indigo Carmine / synthetic	Trametes villosa	dye concentration: 50 mg L-1; volume: 250 mL; temperature: 28 °C; stirring speed: 150 rpm; test duration: 7 days; time: 120 h	81.40%	98
Anthraquinone dyes / synthetic	Trametes gibbosa	dye concentration: 50 mg L-1; volume: 250 mL; temperature: 25 °C; pH :4.5	70%, 14 h	99
Blue Acid 277 / synthetic	Trametes villosa	dye concentration: 10 mg L-1; volume: 250 mL; stirring speed: 180 rpm; test duration: 7 days; temperature: 25 °C; pH: 3, 4, 5, 6, and 7	99%, in 5 cycles (pH 3)	100
Remazol Brilliant Blue R (RBBR) / synthetic	Phanerochaete velutina	dye concentration: 100 mg L-1; volume: 250 mL; temperature: 28 °C; pH: 4.5	80%, 14 days	101
Reactive Blue / synthetic	Trametes hirsuta	dye concentration: 100 mg L-1; volume: 250 mL; temperature: 28 °C; stirring speed: 100 rpm; pH: 4.5	91%, 24 h	102
Reactive Blue 19 / real	Trametes versicolor	dye concentration: 50 mg L-1; volume: 500 mL; temperature: 28 °C; time: 30 days	90%, 5 days / pH 5.3-5.5	103
Reactive Blue 268 - azo dye / synthetic	Trametes versicolor	dye concentration: 100 mg L-1; volume: 250 mL; temperature: 28 °C; stirring speed: 150 rpm; test duration: 7 days	94.4%, 48 h	104
Acid Red 114 / real	Trametes versicolor	dye concentration: 200 mg L-1; volume: 250 mL; temperature: 28 °C; stirring speed: 150 rpm; test duration: 9 days	86.5%, 6 days	105
Textile wastewater / real	Trametes trogii	dye concentration: 100 mg L-1; volume: 250 mL; temperature: 25 °C	65%, 4 days	106

4.1. Effect of dye concentration

In high concentrations, dyes can be toxic to white rot fungi; moreover, the active center of the enzymes is blocked by the dye molecules.¹⁷ Dye concentrations reported in studies ranged from 1 to 1.500 mg L^-1, with color removals greater than 80% achieved even under the highest concentration conditions.⁹²,⁹³ The degradation of pollutants in textile effluent is significantly influenced by enzymatic activity and the initial dye concentration.

Zhang et al.⁹⁰ assessed the effects of dye concentration in their research. The white rot fungi from the species T. versicolor were applied to remove Blue B a type of heterocyclic dye at different concentrations of 100, 200, 300, 400, and 500 mg L^-1. The authors reported that the decolorization efficiency decreased with increasing concentration. For example, at 100 mg L^-1 of dye, removal was 85.6%; however, at 500 mg L^-1 of dye, decolorization dropped to 52.6%.

In contrast, Mahdy et al.⁹³ evaluated the effect of remazol brilliant blue R (RBBR) anthraquinone dye (Figure 9) anthraquinone dye concentration on white rot fungus of the genus T. hirsuta. The results revealed that regardless of the dye concentration, which was 300, 500, and 1000 mg L^-1, the decolorization was above 80% after 12 h. This result was attributed to the adsorption of the dye in the lignocellulosic immobilizing materials and in the mycelial biomass of the fungus, promoting greater removal of the dye.

Figure 9
Chemical structure of the dye Remazol Brilliant Blue R (RBBR).

Regarding the effect of the dye concentration on the effluent discoloration, it was found through Figure 10a that the lowest removal efficiency was obtained at the concentration of 100 mg L^-1 with 50% discoloration. In this sense, the highest removal reported in the literature was 100% with a concentration of 10 mg L^-1. This result is explained by the inhibition of the growth process of the white rot fungus due to the toxicity of the effluent, which limits the interaction of laccases with the dye.

Figure 10
(a) Effect of dye concentration on discoloration. (b) Effect of pH on dye discoloration. (c) Effect of temperature on dye discoloration.⁸²-¹⁰⁶

The majority of the studies in Table 4 employed synthetic wastewater, which could not accurately reflect the unpredictability of the actual effluent from the dye industry. This is an essential factor to consider. Besides the dye concentration and its features, the physico-chemical characteristics of the effluent can affect the decolorization by the white rot fungus. Therefore, the effect of dye concentration should be better investigated in future research.

4.2. The effect of pH

An important operational parameter is pH, as it influences the dye binding sites to the surface of the fungal biomass and the dye chemistry. For a better understanding of the pH effect, Figure 10b illustrates the relationship between pH and the discoloration of dyes in the textile industry in studies reported in the literature. The highest removal efficiencies were above 90% in pH range less than 4.12, while pH above 4.5 obtained efficiency of 50%. This shows that the effect of acidic pH has greater efficiency in the degradation of dyes.

Thampraphaphon et al.⁹⁶ and Rainert et al.¹⁰³ reported that the growth of the white rot fungi of the genera T. versicolor and T. hirsuta obtained the best results at pH 3 to 5 due to the best dye biosorption, which involves physico-chemical interactions, such as adsorption, deposition, and ion exchange between the effluent and the fungal mass. It explains why many researchers have conducted experiments on this pH range (Table 4).⁸³-⁸⁵,⁸⁹,⁹⁶,⁹⁷,¹⁰¹,¹⁰²

However, in the study by Modkovski et al.,¹⁰⁰ it was determined that the pH of 7 inhibited the dye acid blue 277 (Figure 11) from biodegrading when the fungus T. villosa was utilized. Sen et al.⁶⁹ reported that in neutral or alkaline pH conditions, dye degradation is affected by the high concentration of protons, which alters the transport of dye molecules that cross the fungal cell wall, limiting the decolorization of the dye by fungus. Therefore, fungal biomass has a net positive charge at lower pH values.

Figure 11
Chemical structures of the dye Acid Blue 277.

The positive effect on the level of laccase activities was shown by maintaining the pH of the acidic medium at 4.5 after cultivating the Trametes fungus, allowing stability of the enzymes in the supernatant, improving metabolism, growth, and dye degradation activity.¹⁰⁶ Therefore, as textile effluent presents variations in pH between 5.2 and 12.2,⁴⁸ this may be an important variable for future studies since maintaining an acidic pH can be a limitation for implementing the technology on a full scale when it comes to developing countries due to chemical products costs.

4.3. The effect of temperature

Temperature is another important variable in the enzymatic degradation of dyes in the textile industry. The ideal growth temperature for most fungi is around 25 35 °C.¹⁷ Considering that tropical countries naturally present this temperature range, there is a great advantage to applying fungal bio-reactors for decolorizing effluents from the textile industry.

The white rot fungi have ligninolytic enzyme activity leading to decolorization in the temperature range of 25 to 37 °C.⁶⁹ The temperature plays a crucial role in the growth and enzyme production of the fungal culture, affecting the percentage of dye decolorization.

The effect of temperature on the degradation of the different types of dyes was also illustrated, as can be seen in Figure 10c. In this sense, the temperature of 35 °C promoted 100% removal of the dye discoloration, since the growth of the white rot fungus is favored. On the other hand, the temperature of 25 °C promoted 85% of effluent removal from the textile industry due to the lower enzymatic growth of the fungus.

Kalpana et al.¹⁰⁷ investigated the biodegradation and decolorization of dye by T. hirsuta under different temperatures: 20, 25, 30, and 35 °C. The results revealed that the worst performance in decolorization was in the temperature of 20 °C, with 35% removal of the Levafix Blue dye, while the best result was at the temperature of 30 °C, with 100% removal of the dye.

On the other hand, Antošová et al.¹⁰⁶ examined how temperature affected the growth of the Trametes trogii. The initial temperature was 30 °C, and after 15 days, the temperature was adjusted to 20 °C. The assays showed that the growth of the fungus decreased, but the laccase activity of the culture increased, which would not significantly affect reactor performance. The effect of temperature on dye decolorization increases with temperature because the solubility of enzymes increases at high temperatures, thus providing greater enzymatic activity of the fungus in the dye.

The temperature of textile industry effluent varies from 22 to 50 °C.¹⁰⁸ Thus, this variable has an important effect on the application of white rot fungus, as the high temperature of the effluent can cause a thermal shock in the reactor and probably cause thermal denaturation and failure of enzymatic activity, which would affect its performance.⁶⁹

4.4. The effect of the carbon and nitrogen source and the presence of some metals

The effect of the carbon source is an aspect that also affects the decolorization of the dye. Although glucose is the most commonly used source, other sources like starch, maltose, fructose, and sucrose are frequently utilized in research.⁶⁹ Different carbon sources were tested to identify interferences in the decolorization rate of the Cibracon Brilliant Red 3B-A (Figure 12), using fungi of the genus Daldinia concentrica and Xylaria polymorpha.¹⁰⁹ The results revealed that glucose had a degradation efficiency of 97%, while fructose, maltose, lactose, and sucrose had respective removal percentages of 66, 56, 52, and 44%.

Figure 12
Chemical structures of the dye Cibracon Brilliant Red 3B-A.

The amount of nitrogen can cause inhibitory effects on the production of enzymes, consequently affecting the decolorization. Levin et al.¹¹⁰ found that the ideal production of enzymes for T. trogii and T. villosa was achieved using glutamic acid as a nitrogen source, being able to degrade 94% of Indigo Carmine in approximately 30 min. Bankole et al.¹⁰⁹ observed that ammonium nitrate promoted an 88% removal of Cibracon Brilliant Red 3B-A in 48 h.

Merino-Restrepo et al.¹¹¹ reported the effect of the carbon-nitrogen (C:N) ratio on the biodegradation of synthetics dyes Brilliant Blue FCF and Allura Red AC. The results showed that the decolorization of the dyes presented different C:N ratios for the production of ligninolytic enzymes in the three different species studied. The decolorization of the studied genera was influenced by the ideal C:N condition of 20:1, which was 81.41% for T. versicolor, 75.73% for Irpex lacteus, and 62.74% for the species of Bjerkandera adusta.

Trace metals may have a toxic effect on the growth of white rot fungi.¹¹² Despite this, Zafiu et al.¹⁰¹ observed that the presence of Ni and Co metals had no negative impact on the decolorization of Reactive Orange 16, as the removal percentage stayed at 80% utilizing the species Phanerochaete. velutina after 14 days. Trametes pubescence was reported by Enayatizamir et al.¹¹³ to be 99% capable of removing Pb and 8.6% capable of removing Ni at 1000 mg L^-1 concentrations. Nevertheless, after 21 days, laccase activity decreased, which can impact on the decolorization of the wastewater from the textile industry.

5. Biodegradation and Metabolites of Dyes

Biodegradation is the biochemically catalyzed transformation of a substance into one or more metabolites of lower molecular weight. The mineralization is a complete biodegradation process, where the total breakdown of organic molecules into water, carbon dioxide, and/or any other inorganic. Biotransformation is the conversion of an organic compound into an altered molecular structure, inducing the loss of some characteristic properties of the substance, which may alter its toxicity.¹⁰

On the basis of fungal species and environmental conditions, organic substances often undergo progressive biodegradation, which is not caused by the actions of lone specific microorganisms. The substances produced by human activity, like textile industry dye, undergo biotransformation in natural conditions.¹¹⁴ The microorganisms use different metabolic routes and enzyme systems by biotransformation of dyes. Phase I of metabolism generally involves the reactions of OH, NH₂, COOH, and SH and oxidation - for instance, hydroxylation, dehalquilation, delamination, reduction, and hydrolysis. Phase II of metabolism is conjugation with polar molecules for high water solubility. The active enzyme classes in this phase are glutathione S-transferases, UDP-glucuronosyltransferases, sulfotransferases, and N-acetyltransferases.¹¹⁵

The studies about biodegradation usually focus on resistant and xenobiotic dye classes. They are synthesized with ring systems that have groups like azo, nitro, or halogens replaced for them, and they are designed to last under extremely harsh conditions. Some reviews¹⁰,¹³-¹⁷,¹¹⁶-¹¹⁹ explain the characteristics of the enzymatic cleavage of dyes using different biological agents. Most mechanistic studies on textile dyes have focused on azo dyes.¹¹⁷ Besides this group of dyes, the following researches detail the biodegradation pathways and intermediates of triphenylmethane, anthraquinone, indigoid, and phthalocyanine. This paper provides specific information on the capacity of the degrading process of white rot fungi. It has been noted that the majority of research on the biodegradation of textile dyes by fungus focuses on the utilization of wood-rot fungi, which yield enzymes that degraded lignin, such as laccase, manganese peroxidase, and lignin peroxidase, among others;¹²⁰ thus, researchers using ligninolytic fungi have been extensively explored for degrading and decolorizing contaminants. The biodegradation mechanisms proposed below occurred mediated by purified oxidative enzymes and/or white rot fungi. The knowledge provided about the metabolic processes for each type of dye is derived from research investigations.

(i) Azo dye: dyes with variable amounts (from one to many) of -N=N- bonds with aromatic rings. The main mechanism of anaerobic biodegradation of azo dyes by bacteria is reductive cleavage of the azo bonds by azoreductase involving transference of four electrons.¹⁴ Under an anaerobic condition, the reductive decolorization of azo dye occurs mainly in the metabolism of bacteria. In addition, the aromatic amines produced are hazardous and potentially carcinogenic,¹⁴ topics that are outside of the scope of this review.

It has been reported that laccase isolated from fungal Pyricularia oryzae (Ascomycota) oxidizes phenolic azo dyes to produce benzoquinone (MB) and 4-sulfophenylhydroperoxide (SPH). The 2-methyland 2-methoxy-substituted dyes were oxidized to SPH and either 2-methylor 2-methoxy-benzoquinone.¹²¹ Initial oxidative activation of the dyes to a cation radical that can be attacked by water or hydrogen peroxide molecules nucleophilically. Moreover, the azo group cleavage is divided into both symmetric and asymmetric mechanisms (Figure 13).

Figure 13
Proposed biodegradation for peroxidase asymmetric and symmetric sulfonated azo group cleavage, MB: benzoquinone and SPH: 4-sulfophenylhydroperoxide (adapted from Singh et al.,¹¹⁷ Khan et al.¹¹⁸ and Chivukula and Renganathan.¹²⁰

Adnan et al.¹²¹ analyzed the biodegradation metabolites of Reactive Black 5 (RB5) by T. gibbosa. The oxidation of the azo bond formed hydroxyl compounds: 4-sulfooxyethylsulfonyl-1-phenol and 8-amino-naphthalene-1,2-diol (Figure 14). The authors described that laccase was most likely the mediator of this reaction because it is biosynthesized during the first development of fungal. Hydroxylated products have already been described as leading to azo dye biodegradation by the enzyme peroxidase of P. chrysosporium (Figure 13).¹²² The similar metabolites 8-amino-naphthalene-1,2-diol and 4-sulfooxyethylsulfonyl-1-phenol of azo dyes degradation were described by Kalnake et al.¹²³ by mixed white rot fungal cultures, P. chrysosporium and T. versicolor (Figure 14).

Figure 14
Suggested biodegradation pathway of Reactive Black 5 by T. gibbosa¹²¹ and by mixed white rot fungal cultures P. chrysosporium and T. versicolor.¹²³

The biodegradation mechanisms of disperse orange 3 by P. ostreatus suggested asymmetric and symmetric azo group cleavage. The oxidative route was evidenced by 4-nitroaniline, 4-nitrobenzene, 4-nitrophenol, and 4-nitroanisole metabolites. This biodegradation was attributed to the enzymes laccase and lignin peroxidase (Figure 15).¹²⁴ Orange dye was biodegraded by new isolates of white rot fungus and was identified as p-N,N’-dimethylamine phenyldiazine, and p-hydroxybenzene sulfonic acid metabolites (Figure 15).¹²⁵

Figure 15
Proposed biodegradation of azo dyes Disperse Orange 3¹²⁴ and Methyl Orange by new isolates of white rot fungus.¹²⁵

(ii) Triphenylmethane dye: Yang et al.¹²⁶ described the metabolites of Malachite Green dye using crude MnP obtained from I. lacteus F17. This white rot fungal inhabits mainly angiosperm branches and trunks. After 60 min of utilizing the pure MnP enzyme, the biodegradation proposed was N-demethylation followed by oxidative cleavage or directly to the oxidation process (Figure 16).

Figure 16
Biodegradation mechanism of triphenylmethane dyes: Malachite Green by manganese peroxidase¹²⁶ Crystal Violet by P. ostreatus¹²⁷ and Methyl Green by laccase.¹²⁸

In a solid-state medium of rice straw, Yan et al.¹²⁷ reported biodegradation routes and Crystal Violet intermediates by laccase from the white rot fungus P. ostreatus, with a primary reliance on low molecular mass fraction (LMMF). Similar metabolites from N-demethylation followed by oxidative cleavage were shown using LMMF in this biodegradation study (Figure 16).

Casas et al.¹²⁸ showed decoloration and metabolites of biodegradation of triphenylmethane dyes using T. versicolor and commercial laccase. The metabolite p-N,N,N-(dimethyl, ethyl)aminobenzoic acid was detected in the enzymatic biodegradation of methyl green dye (Figure 16). In addition, the degradation products from the Dye Brilliant Green 1 were benzoic acid and diethylamine, which were observed together with the dye. Laccase oxidized the methyl carbon of the dye structure, giving rise to stable products in line with the p-substituted phenyl part.¹²⁸

(iii) Anthraquinone dye: Zhang et al.⁹⁹ described that the white rot fungus T. gibbosa can degrade Alizarin Anthraquinone Red dye in a wastewater matrix. Some metabolites obtained were phthalic acid, 1,1-diphenylethylene, 9,10-dihydroanthracene, and 1,2-naphthalene dicarboxylic acid (Figure 17). The glutathione metabolic route was screened, and binding glutathione S-transferase (GST) activity and glutathione (GSH) content suggested that the glutathione metabolic pathway is involved in the degradation of alizarin. A transcriptome study also revealed that oxidoreductases (MnP and laccase) are essential enzymes for alizarin degradation.⁹⁹

Figure 17
Proposed biodegradation of Alizarin dye by T. gibbosa.⁹⁹

The biotransformation of acid blue 62, an anthraquinone dye, by Pycnoporus sanguineus was compared to white rot fungi strains: Coriolopsis polyzon, Perenniporia ochroleuca, Perenniporia tephropora, P. sanguineus, and T. versicolor, which obtained similar results. It is interesting to note that the original acid blue 62 dye formed dimers and oligomers. In addition, seven metabolites were commonly found with all strains.¹²⁹ Some biodegraded compounds are described in Figure 18.

Figure 18
Proposed biodegradation of Acid Blue by P. sanguineus.¹²⁹

(iv) Indigo dye: new white rot fungal WRF-1 showed the capacity to secrete laccase and promoted the decolorization of synthetic dyes in the economical medium consisting of groundnut shells and dry cyanobacterial biomass. The dye Indigo Carmine degraded to isatin sulfonic acid and 4-amino-3-methylbenzenesulphonic acid (Figure 19). The authors suggested the potential applications of laccase enzyme to decolorizing and detoxifying effluent.¹²⁵

Figure 19
Proposed biodegradation of Indigoid Carmine dye by white rot fungal WRF-1.¹²⁵

(v) Phthalocyanine dye: Conneely et al.¹³⁰ related metabolites of phthalocyanine dye by white rot fungi P. chrysosporium (Figure 20). The proposed dye decolorization and biodegradation mechanism was by ligninolytic extracellular enzymes (laccase and MnP).

Figure 20
Proposed biodegradation pathway for copper phthalocyanine dyes by P. chrysosporium.¹³⁰

5.1. Structure elucidation of dye metabolites: mass spectrometry (MS)

Gas chromatography-mass spectrometry (GC-MS) and liquid chromatography-mass spectrometry (LC-MS) can be used to identify structures of products of biodegradation and also information about the stepwise mechanism of biodegradation. Nuclear magnetic resonance (NMR) spectroscopy is used to determine the molecular structure and physical properties of substances, although most studies utilize MS in biodegradation analyses. The dye is usually extracted from the medium with an organic solvent suitable for its polarity and then analyzed by MS. Polar samples can be derivatized and analyzed by GC-MS and by LC-MS.¹²¹

MS techniques have found several applications in chemistry and biotechnology analyses. However, many dye molecules cannot be ionized by electron ionization (EI) technique, because in EI, the compounds are first volatilized and then ionized, reducing this method to thermally stable compounds with low molecular weight. EI is used as a detector of GC-MS analyses, and the derivatization method can be applied to the dye samples before the analysis.¹²¹ Electrospray ionization and matrix-assisted laser desorption/ionization have been successfully used as a powerful tool for determining the molecular mass and structural information of dye samples. Tandem (MS/MS) techniques have contributed immensely to studies of organic compounds. Ion abundance is plotted against mass/charge ratio (m/z) in mass spectrometry, which provides the origin of mass spectrum, shown as Daltons (Da) per unit charge.¹³¹

The prevalent mass spectrometry methods for analyzing dyes and their metabolites are electrospray (ESI) and matrix-assisted laser desorption/ionization (MALDI). Dye structure elucidation has been the subject of more recent investigations using ESI-MS,¹³²-¹³⁵ primarily due to the simplicity with which may be coupled with high-performance separation methods like high performance liquid chromatography (HPLC). ESI converts the analyte in the gas phase without breaking covalent bonds and yields molecular weight (MW) data. A molecular ion is formed by adding or removing one or several electrons from the sample molecule. The most abundant MS signals were attributed to the ion of the molecular species originating from the molecule by the abstraction of a proton [M - H]^-, or by interaction with a proton or a cation to form a protonated molecule [M + H]⁺ or a cationized molecule [M + Cat]⁺. These ions allow the molecular weight to be deduced. In addition, an adduct ion can be formed by directly combining two separate molecular entities, usually an ion and a neutral molecule. Its MW alone cannot ascertain the structure of an unknown analyte. Therefore, it is necessary to deliberately fragment the gaseous analyte to elucidate its structure. It is possible to ascertain the accurate chemical structure of the unknown analyte sample by examining the fragmentation response (product ion spectra.). The MS/MS spectra allow the identification of structures of the examined compounds on the basis of neutral losses. A cascade of fragmentations of these ions and their product ions allows the production of a mass spectrum.¹³¹

Due to the diversity in the molecular structure and different chemical and physical properties of the distinct classes of dyes, there is no mass fragmentation pattern. The classes of azo and triphenylmethane dyes are most frequently cited by studies concerning biodegradation by white rot fungi.¹³³-¹³⁶ Understanding the correlation between fragmentation behavior and the existence of distinct functional groups and structural characteristics in dye molecules is crucial for interpreting MS/MS spectra of unidentified substances. The functional groups are sulfate, sulfonic, carboxylic, and nitro, among others, and they are present in numerous types of dyes. Dyes most commonly studied are organized according to the different classes and similarities of functional groups, explaining how much they affect the degree of fragmentation.

(i) Azo dye: for anionic azo dyes, including sulfonated dyes, the negative-ion mode of ESI is utilized since the sequence of deprotonated molecules makes it simple to determine the molecular weights and number of acid groups. Correlations between certain functional groups and fragmentation patterns are made possible by thoroughly understanding fragmentation pathways. The negative-ion ESI mass spectrum of dye Reactive Black 5 was used as an example of fragmentation.¹³³ Fuh and Chia¹³⁴ related to the gas-phase fragmentation ion in ESI-MS [M - 2Na + H]^- of Ponceau 3R (di)sulfonated dye. Therefore, the suggestion of the fragmentation mechanism proposed here used this concept of protonation in a fragment ion in negative mode (Figures 21-22). In some cases, acid group deprotonation occurs with hydrogen migration to obtain the more stable ion. Besides the deprotonated monoisotopic, ∆m/z 1/2 for doubly charged ions [M - 2H]^2- were discussed for different azo dyes, for example, Reactive Blue 225 azo sulfonated dye (exact mass: 859.9662), exhibiting [M - H]^- (m/z 858.9587), doubly charged ion, [M - 2H]^2- (428.9758) and triply charged ion [M - 3H]^3- (285.6481).¹³⁷,¹³⁸ Sulfonated dyes can produce molecular ions with distinct charges by adducts with sodium ions or through the subsequent loss of protons. The mass spectrum of disulfonated azo dye Egacid Red 6B detected the ions: [M - H]^- (m/z = 521), [M -2H + Na]^- (m/z = 543) and [M - 2H]^2- (m/z = 260).¹³⁹

Figure 21
Fragmentation proposal for selected functional groups in Mordant Black 15 (a) nitro and (b) sulfonic acid (adapted from reference 133).

Figure 22
Fragmentation proposal for selected functional groups in Mordant Black 15 (a) nitro and (b) sulfonic acid, based on data from Holčapek et al.¹³³

In addition to ESI spectra data, dye Disperse Orange 3 was monitored in P. ostreatus culture by GC-MS analysis to study biodegradation products. The results allowed the identification of 4-nitroaniline, nitrobenzene, 4-nitrophenol, and 4-nitroanisole. These biodegradation metabolites were identified by comparing retention time and fragmentation patterns with known reference compounds, as well as with mass spectra in the NIST spectral library.¹²⁴

(ii) Triphenylmethane dye: laccase of white rot fungus Cerrena sp. was responsible for the biodegradation of Malachite Green (MG) triphenylmethane dye. The LC-MS spectra identified seven intermediates of laccase-catalyzed MG biotransformation. Other metabolites were observed, such as tetradesmethyl MG (m/z 273.14), (methyl aminophenyl)-phenylmethanone (m/z 212.11), and (amino phenyl)-phenyl methanone (m/z 198.09).¹²⁶

6. Overview of Overall Techniques for Treating Water Containing Dyes and Treatment of Industrial Dye Effluents

Due to the complexity of the characteristics of textile effluents and the consequences of their disposal without adequate treatment in the environment, a treatment that effectively removes these contaminants must be applied. Figure 23 provides a summary and some examples of treatment methods that can be applied to remove and/or degrade dyes in industrial effluents.

Figure 23
Types of treatment methods for removing dye from effluent.

6.1. Chemical and physical methods

Coagulation/flocculation are among the most applied techniques in several countries because they are low-cost methods. The treatment consists of adding a coagulant, which stabilizes the charges of the colloidal particles, and a flocculant, which aggregates the stabilized particles. Thus, sedimentation occurs more quickly. However, the technique generates a significant amount of sludge, and the dye removal efficiency is variable, with efficiencies ranging from 58 to 100% removal being reported.⁵⁹ Another aspect to consider is that the characteristics of the effluent to be treated, such as the type of dye to be removed, affect the success of the technique.

The advanced oxidative processes (AOP) are chemical processes that also must be mentioned. These processes have been thoroughly researched for degrading dyes and have been shown to be effective techniques. This type of method involves the degradation of contaminants by very reactive oxidizing species.³⁰ Despite promising results being presented, advanced oxidative processes involve techniques that use chemicals, and it is necessary to be aware of the formation of intermediate compounds that can be toxic.

For example, Luna et al.¹⁴⁰ used photo-Fenton to degrade five dyes. They discovered that although the procedure successfully eliminated color when Vat Green 3 and Reactive Black 5 were degraded, more hazardous byproducts were created than the original molecules. It emphasizes how important it is to do toxicity evaluations when assessing dye removal techniques that modify the chemical structure of the dyes, particularly in situations when total mineralization might not be possible.

It is important to highlight that applying physical processes by itself does not cause the dye to degrade; rather, phase transfer or concentration in a smaller volume. Among physical processes, membrane separation is an alternative attracting increasing attention since membranes, such as nanofiltration membranes, can remove > 90% of dyes.⁶ Membrane separation is a robust process, producing a high-quality permeate with greater independence from the composition of the matrix being treated. In this way, even studies on the treatment of textile industry effluent by applying membranes conducted on a full scale experiment have been successful.¹⁴¹ Furthermore, membrane technologies are becoming increasingly competitive with conventional technologies. However, treating the concentrate stream and managing fouling, which seriously impacts system performance, is still necessary.

Adsorption is a physical approach that may also be used to remove dyes. Recent studies¹,¹⁴² have focused on the development of new adsorbent materials for the removal of dyes, including the development of bio-adsorbents, which are based on low-cost and environmentally-friendly materials, such as banana peel-based adsorbents, which had efficiencies up to 84% in removing dye from effluent.² However, many factors affect the performance of adsorbents, among which the pH of the medium, the dye concentration of the medium, temperature, and adsorbent dosage can be emphasized.¹⁴³ Furthermore, the presence of other pollutants, which is typical in real effluents, can reduce the performance of the adsorbent, as observed by Rasilingwani et al.,¹ who reported dye removal efficiency by adsorption greater than 99% when in aqueous solution, which was reduced to 80% when the matrix was real effluent.

6.2. Biological methods

Biological processes are considered more environmentally friendly, relatively low-cost, and capable of promoting the mineralization of dyes and generating less sludge when compared to other methods. These characteristics often mean that they become alternatives that are more appropriate to the realities of underdeveloped or developing countries.¹⁴⁴ Biological techniques involve the adsorption, absorption, and/or biodegradation of dyes.⁷³ The application of enzymes is a biological technique that involves biocatalysts with specificity and selectivity to the substrate. Ihsanullah et al.¹⁴⁵ highlight studies that found dye removals between 58 and 98% when applying enzymes. However, enzymes are subject to denaturation, and isolating specific enzymes is more expensive than using microorganisms.

Bioremediation using algae has also been studied due to the great availability of organisms and the efficiency of dye removal. Ihsanullah et al.¹⁴⁵ reported studies with dye removal by algae varying between 53.2 and 98%. Algae have functional groups in their cell walls, such as amine, carboxyl, and hydroxy groups, which enable the removal of dyes.¹⁴⁴ Despite the development of algae-based techniques for dye removal,⁸ they still have many limitations that need to be better investigated.¹⁴⁴

A biological method that still has few studies for dye degradation is phytoremediation, which involves the removal of dyes through adsorption, accumulation, and degradation by plant enzymes. Using plants for the bioremediation of dyes can also be an environmentally friendly and economical alternative. The technique has already shown promise for the remediation of heavy metals and has the potential for treating dye effluents. Furthermore, phytoremediation using ornamental plants is attractive due to the aesthetic factor of the treatment system. However, some disadvantages are that most plants are seasonal, it is a slower process compared to physical and chemical methods, most studies were carried out on a laboratory scale associated with other techniques, and more studies are needed to evaluate a large-scale application. Another factor to be evaluated is the destination of the plants after phytoremediation. Their use as an input for biofuel production may be an alternative that deserves further studies.¹⁴⁶

Bacteria are the organisms most used for the degradation of dyes, and several studies have already explored the techniques applying bacteria in its most diverse conditions, such as different pH, salinity, temperature, nutrient sources, and presence or absence of oxygen.¹⁴⁷ They have also been evaluated in operations in consortia or isolated cultures, with consortia performing better.¹⁴⁸ In fact, bacteria are versatile organisms and can adapt to the application conditions to treat real dye effluents.¹⁴⁷ Pinheiro et al.¹⁴⁷ compiled studies that evaluated the degradation of dyes with bacteria with reported maximum efficiencies ranging between 79.8 and 100%.

Fungi have not yet been studied as much as bacteria, but they can also be applied to the treatment of effluents containing dyes, with one of their advantages being the possibility of accelerating their metabolism to achieve optimal conditions. Intracellular and extracellular enzymes such as laccase and lignin peroxidase can increase metabolic activity, promoting greater efficiency for dye degradation.¹⁴⁹ Among these organisms, white rot fungi are highlighted as a potential alternative for removing recalcitrant pollutants, such as dyes.¹⁵⁰ It is discussed throughout the other sections of this review.

6.3. Hybrid treatments applying fungi

Given the complexity of real effluents containing dyes, the necessity of applying more than one treatment method has become apparent. In this context, hybrid processes have emerged as promising alternatives.²⁰ Combining two or more techniques can effectively overcome the individual disadvantages of each method. In this light, hybrid systems involving fungi present a promising future for potential application in industry, surpassing the capabilities of the biological technique alone. Therefore, the potential of hybrid systems involving the application of fungi will be the focus of this topic.

To date, only a few studies have evaluated the combination of treatment with fungi and AOPs. For example, Vanhulle et al.¹²⁹ evaluated the performance of pretreatment with ozonation before applying the white rot fungus P. sanguineus in treating a real effluent. The industrial effluent was mainly composed of acid, direct, and reactive dyes with anthraquinone and azo structures. In terms of color removal, it was observed that ozonation and fungi applied alone achieved an efficiency of 30 and 75%, respectively, while the hybrid process promoted a color removal of 90%. Despite attaining excellent color reductions, the authors brought attention to a crucial point: the real effluent may prevent the fungus from growing, which would lengthen the time needed to treat the effluent.

Regarding hybrid approaches, including AOPs, Kiran et al.¹⁵¹ evaluated the removal of Reactive Blue 222 by Photo-Fenton followed by biological treatment using the white rot fungi P. ostreatus and P. chrysosporium. The AOP had 90% efficiency in color removal in 50 min of reaction, and after biological treatment, removal increased to more than 95%. In isolation, the biological treatment showed a color removal efficiency of over 75% after 48 h. The authors remarked that the hybrid treatment is advantageous, as the biological treatment can promote the biodegradation of byproducts (not reported by the authors) originated due to the AOP. Thus, there is a more economically advantageous route: while AOP degrades the dye more quickly, biological treatment, more economically attractive, can be applied to continue the degradation of byproducts, which would be much more expensive if carried out entirely with Photo-Fenton.

In addition to advanced oxidative processes, membrane bioreactors with fungi (FMBR) have also been investigated, and this treatment route has already been evaluated by a more noteworthy number of studies (Table 5). FMBR is a treatment technique that combines biological degradation and adsorption with membrane separation, generating high-quality permeates and allowing microorganisms to degrade the pollutants in the reaction medium,¹⁵² which is diagrammed in Figure 24. Table 5 shows the high removals of parameters related to the presence of dyes using this treatment route.

Table 5
Membrane bioreactors with fungi (FMBR) and their efficiency for dye removal

Fungi	Membrane	Treatment route	Dye matrix	Parameters related to dyes	Reference
Phanerochaete chrysosporium	photocatalytic membrane (catalyst: ZnO)	fungal membrane bioreactor followed by the photocatalytic membrane reactor	solution of Acid Red 88 (AR88) and Reactive Red 180 (RR180) 100 mg L-1 each	COD: 96-98% Color: > 99.9%	9
Trametes versicolor KCTC 16781	reverse osmosis (RO) and nanofiltration (NF)	FMBR with NF membrane and FMBR with RO membrane	solution of Reactive Blue 19 (2027 mg L-1), Reactive Blue 49 (2000 mg L-1), and Reactive Black 5 (2003 mg L-1)	FMBR with NF decolorization: 76.2‑98.8% TOC: 35.6-45.4% MBR with RO decolorization: 76.9-100.0% TOC: 94.8-99.2%	11
Coriolus versicolor, NBRC 9791 and NBRC 30388	microfiltration	submerged FMBR	100 mg L-1 solution of Poly R-478 and Poly S-119	TOC: >95% Color: 98%	153
Coriolus versicolor	microfiltration	submerged FMBR	100 mg L-1 solution of Poly S119	97% TOC and 99% color removal	154
Coriolus versicolor	microfiltration	submerged FMBR	synthetic wastewater with 100 mg L-1 of Acid Orange II	dye removal: 93%	155
Coriolus versicolour	microfiltration	FMBR with suspended (pellet) and attached growth	synthetic wastewater with 100 mg L-1 of Acid Orange 7	decoloration: > 95%	152
Coriolus versicolour	microfiltration	submerged FMBR and powdered activated carbon (PAC)	synthetic wastewater with Poly S119 and Acid Orange II	TOC removal: > 99%	156
Coriolus versicolor	microfiltration membrane coated with granular activated carbon	FMBR with granular activated carbon layers on the membrane module	synthetic wastewater with Acid Orange II (33-100 mg L-1)	TOC removal > 90% color removal 85-100%	157

Figure 24
Diagram of the operation of a membrane bioreactor with fungi.

Most researchers that assessed the FMBR technique evaluated C. versicolor in a membrane bioreactor (MBR) that operated with a microfiltration membrane in a submerged module (Table 5). In this system, it was evaluated the removal of different dyes (poly S-119 and Acid Orange 7, Figure 25) in different concentrations. The overall removal was greater than 90%.¹⁵²-¹⁵⁷ Some authors have studied the combination of FMBR with other treatment techniques, such as the use of activated carbon,¹⁵⁶,¹⁵⁷ and photocatalytic membranes,⁹ aiming to overcome limitations found in FMBR performance, such as the formation of fouling.

Figure 25
Chemical structures of the dyes, poly S-119 and Acid Orange 7.

Hybrid processes with different principles may be a promising alternative for dye removal. Considering the advantages of biological treatment with fungi, the application of membranes, and photocatalysis, Deveci et al.⁹ evaluated the integration of an FMBR and a bioreactor with photocatalytic membranes. Biodegradation provided COD and color removal of 80-86% and 78-89%. After membrane filtration in FMBR, these parameters increased to 85-94% and 86-92%. After the photocatalytic membrane reactor, COD removal was 96-98%, and color removal was 99.9%. In this way, the authors confirmed the improvement in performance by exploring techniques with different principles, in this case, biological, physical, and chemical.

Furthermore, the need to be attentive to the byproducts originating from the degradation of dye molecules may be a strong reason enough to choose a hybrid process. T. versicolor performed the best out of all the fungal strains that researchers had previously evaluated in the research by Kim et al.¹¹ Reactive blue 19, Reactive Blue 49, and anthraquinone dyes were among the dyes used in solutions that showed > 99% efficiency in decolorization after 8 h, indicating that the performance of the microorganisms was dependent on the chemical structure of the dye. However, the solution with reactive black 5 (Figure 14), which has an azo chromophore, was 95% discolored in the first 8 h, and it took 40 h to reach 99%. Despite color removal, TOC removal by microorganisms varied between 0.4 and 9%. Therefore, the association of the biological technique with reverse osmosis membrane technology improved the performance of the treatment, enabling high TOC removals - also retaining the products of biological degradation of the dyes - and promoting the recycling of fungi in the process.

7. Conclusion

Dyes are used extensively; however, dye industry effluent that is not properly treated is hazardous to the environment and human health. In this context, using white rot fungi for dye decoloration emerges as an efficient and promising remediation technique. In addition, the fungal mycelia can absorb the dye and aid in decontamination. Ensuring an in-depth analysis of the effectiveness of the technique requires the expertise of professionals, such as organic chemistry, to describe the biodegradation pathway and elucidation of dye metabolites and biologist and biochemistry research for enzymatic production. Environmental and sanitary engineering is also essential to investigate operational aspects of the application of white rot fungi, aiming at the treatment of real effluents, to analyze and optimize the aspects that can enable future applications on full-scale.

Significant progress has been achieved in recent years in research on biotechnology, together with physical and chemical methods used for dye decoloration and determination of biodegradation metabolites. These results and the enzymatic mechanisms responsible for biodegradation complete the research cycle in this field.

Aiming to remove various classes of dyes more effectively and affordably, new and comprehensive biological, physical, and chemical techniques-such as membrane bioreactors and hybrid treatment techniques-are now being developed and enhanced. Even if there are still considerable obstacles to overcome, the bioremediation of contaminants like dyes using white rot fungi seems to be a promising alternative for ensuring water security.

Acknowledgments

The authors thank Dr Admir Créso Targino (UTFPR) for his invaluable assistance with the English revision. The authors are grateful for scholarship provided by the Coordination of Superior Level Staff Improvement (CAPES) and financial support provided by the Diretoria de Pesquisa e Pós-Graduação (PROPPG - UTFPR - Dr J.F.S. Daniel) of Federal Technological University of Paraná, Brazil.

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Edited by

• Editor handled this article:
  Paulo Cezar Vieira

Publication Dates

• Publication in this collection
  24 Feb 2025
• Date of issue
  2025

History

• Received
  19 Sept 2024
• Published
  07 Feb 2025