Author's personal copy Environmental Sustainability https://doi.org/10.1007/s42398-020-00150-w REVIEW Mycoremediation of synthetic dyes by yeast cells: a sustainable biodegradation approach M. Danouche1,2 · H. EL Arroussi1 · N. El Ghachtouli2 Received: 19 December 2019 / Revised: 25 October 2020 / Accepted: 20 November 2020 © Society for Environmental Sustainability 2021 Abstract Dye effluents released from various industries, notably the textile sector, are hazardous, and can cause significant damage to the environment. Thus, treatment and detoxification of these toxic dyes are of major concern for compliance with environmental legislations. So far, a number of physicochemical dye-removal methods have been proposed. However, despite their effectiveness in dye decolorization, by-products of chemical degradation methods may be more toxic than their parent dye molecules. The cost of these processes is also very high, thereby limiting their large-scale application. The use of yeast cells for the removal of toxic dyes is a comparatively effective, eco-friendly and cost-effective method. In this review, we describe the adverse effects of synthetic dyes on living organisms and enzymatic biodegradation mechanisms involved in mycoremediation processes of synthetic dyes. In addition, the influence of various physico-chemical factors on the decolorization performance of yeast cells, the analytical techniques used to identify the intermediates of dye biodegradation, the assessment of their toxicity and the molecular aspects of their biodegradation are also highlighted. This study may provide a basis for the development of dye bio-removal methods using yeast cells. Graphical abstract Keywords Yeast · Decolorization · Enzymatic biodegradation · By-product identification · Toxicity assessment Introduction * M. Danouche mohammed.danouche@usmba.ac.ma Extended author information available on the last page of the article Since the beginning of the industrial revolution in the nineteenth century, the equation for balanced economic growth while protecting the environment has not yet been resolved. In fact, soil, air, and water pollution are among the main global challenges facing the world today. More critical than 13 Vol.:(0123456789) Author's personal copy Environmental Sustainability ever, there is a growing concern about the impact of water contamination on aquatic life and public health. Compared to other industrial sectors, the textiles industry consumes large quantity of water; it was estimated that about 200–500 L of water is required to produce 1 kg of finished textile products (Waghmode et al. 2012a). Therefore, this sector generates significant volume of wastewater composed of suspended solids, surfactants, heavy metals and several synthetic dyes (Balapure et al. 2015; Chen et al. 2009). The exact amount of dyes released into the environment is uncertain, it has only been estimated that the overall use of dyes in the textile sector is more than 10 000 tons per year, and about 10–15% of this amount is lost as waste during the dyeing process, due to the low chemical affinity of the dyes used on textile fibers (Kunamneni et al. 2008; Saratale et al. 2011). Consequently, the release of such xenobiotics leads to significant pollution, which not only affects the aesthetic quality of water but also leads to serious impacts on exposed organisms including humans (Lellis et al. 2019; Puvaneswari et al. 2006). To cope with this issue, legislations have been enacted worldwide for the management and the treatment of these contaminants prior to their release into the environment. A variety of physicochemical methods have therefore been used, particularly membrane processes, photochemical oxidation, and electrochemical processes (Arslan et al. 2016). Although these methods are effective, they require a large amount of chemicals and energy-intensive facilities, which makes them expensive, thereby limiting their large-scale applications (Barakat 2011; Fu and Wang 2011). The most recommended approach is the use of biological techniques, due to their advantages, including treatment efficiency, appropriate cost, and a minimal ecological impact (Srinivasan and Viraraghavan 2010). The emergence of this promising solution is based on the exploitation of the ecological principles of bacteria, fungi, and microalgae in the treatment of toxic dyes (Chen et al. 2009; Jafari et al. 2014; Miranda et al. 2013). While bioprocesses have several advantages, some drawbacks may also be noted, such as the long time required for the bio-removal of dyes using filamentous fungi or microalgae (Singh and Arora 2011). Moreover, the decolorization of dyes using bacteria requires two phases; the anaerobic reduction of Azo bonds, followed by aerobic mineralization of the resultant aromatic amines (Abiri et al. 2017; Roșu et al. 2019). However, the use of yeast cells overcomes this drawback; they do not only grow rapidly like bacteria, but exhibit great plasticity and ability to adapt to adverse growth conditions like pH fluctuation or temperature changes. Also, yeast does not require special biphase growth conditions like bacteria. In addition, the biodegradation mechanisms of dyes using yeast cells involve different oxidases, that can directly break the azo dyes through non-specific free radical mechanisms, avoiding therefore the production of toxic intermediates like aromatic 13 amines, that are typically produced after the specific cleavage of the azo bond of synthetic dyes by bacteria (Pandey et al. 2007; Dave et al. 2015). Furthermore, yeast have a special flocculating characteristic that allows them to aggregate into multicellular masses (flakes), facilitating, therefore, their recovery after treatment of colored effluents (Soares and Soares 2012). Hence, the use of yeast cells in the bioremoval of synthetic dyes has attracted more interest (Jafari et al. 2014; Sen et al. 2016). Several studies focusing on the decolorization mechanisms of the ascomycete and basidiomycete strains of yeast have demonstrated the involvement of three bioremoval strategies, with active and/or passive metabolism pathways, namely: extracellular biosorption (Dil et al. 2017; Mahmoud 2016), intracellular bioaccumulation (Das et al. 2010; Gönen and Aksu 2009) and/or intra and extracellular biodegradation (Martorell et al. 2018; Tan et al. 2019). The present review focuses on the harmful effects of synthetic dyes on aquatic environments and the state-ofthe-art of the biodegradation mechanisms of synthetic dyes by yeast cells. Sequential summary studies on the biodegradation of synthetic dyes using different yeast species are also discussed. Much emphasis will be projected towards oxidoredactase enzymes involved in the biodegradation of dyes, as well as the influence of operating factors on this bioprocess. Besides, the analytical methods used in the chemical characterization of dye biodegradation by-products and the evaluation of their toxicity will be discussed. Throughout the last section, the molecular aspects of the degradation of dyes by yeast cells will be addressed in order to identify the future scope of this research. Adverse effects of synthetic dyes on aquatic ecosystems Since the dawn of human civilization, colorants have played a crucial role in different aspects of everyday life. Before the end of the nineteenth century, all dyes used were obtained from natural sources, until the first artificial dye was discovered by W.H Perkins (1838–1907) through an accidental production of Mauveine. This successful discovery paved the way for the synthesis of chemical dyes as we know them today. Since then, many chemical compounds have been identified as coloring substances (Rai et al. 2005). Thus, the use of these chemicals has continued to increase, notably in textile and leather industries. In addition to the type of color emitted by these chemicals, other physicochemical requirements have become more stringent in textile sectors including resistance to various environmental conditions, such as persistence of colored fabrics against washing, exposure to light, chemicals and biological attacks (Khan et al. 2013). However, the same requirements that confer higher resistance qualities, Author's personal copy Environmental Sustainability could complicate the dye’s removal from wastewater by traditional methods. Meanwhile, the release of untreated or inadequately treated colored wastewater into aquatic environments can lead to various signs of toxicity to exposed living organisms (Moopantakath and Kumavath 2018). The high concentration of dyes in aquatic ecosystems may prevent the penetration of light into the depths, thus disturbing the photosynthetic activity of autotrophic organisms, and impacting the re-oxygenation potential of the receiving waters (Carmen et al. 2009). Moreover, the toxicity of synthetic dyes may occur in aquatic ecosystems across the food chains. Numerous studies have focused on the adverse effect of dyes on species from various trophic levels, including producer and consumer species (Puvaneswari et al. 2006; Tkaczyk et al. 2020). For instance, the microalgae’s morphological, biochemical, and metabolic properties can be influenced by increasing concentrations of dyes. Gita et al. (2019) reported that a concentrationdependent decrease in the specific growth rate and pigment contents of Chlorella vulgaris was observed after exposure to increasing concentrations of the textile dyes Drimarene Blue, Optilan Yellow and Lanasyn Brown. Similarly, Indigo dye induced a significant growth reduction of Scenedesmus quadricauda, and altered its morphological characteristics (Chia and Musa 2014). Likewise, zooplankton organisms can be directly or indirectly influenced by dyes. Hernández-Zamora et al. (2016) showed that exposure to low concentrations of Congo Red or feeding on microalgae that already accumulated this dye, induced adverse effects on the survival and reproduction of Ceriodaphnia dubia. Additionally, many toxic dyes have shown a direct effect on primary consumers like fish. For instance, Kaur and Kaur (2014) investigated Poikilocytosis occurrence in Labeo rohita fish as an indicator of stress caused by the azo dye Basic Violet-1, with a highly toxic effect (96-h LC50) at 0.45 mg L−1 concentrations. Srivastava et al. (2017) also noted that the exposure of L. rohita to sublethal concentrations of Eriochrome Black T caused considerable histopathological abnormalities and altered antioxidant enzyme activities in the epidermis. Hence, the accumulation of these xenobiotics in aquatic organisms and their transmission to humans through the consumption of sea food from polluted sources may provoke many human health problems (Chung 2016; Mendes et al. 2011). To prevent these environmental issues, it is necessary to introduce standards and framework laws to limit the use of hazardous dyes or to substitute them with new synthetic dyes that can meet industrial requirements, and that can also be easily biodegradable. Therefore, research in synthetic chemistry of dyes must not only compete with the criteria of resistance, but also their fate in nature. On the other hand, it is important to establish promising approaches for the treatment of these pollutants before their release into the environments. Biodegradation of synthetic dyes by yeast Biodegradation is defined as an energy-dependent process, involving the decomposition of organic compounds, into smaller and simpler by-products, through different enzymatic reactions (Kaushik and Malik 2009). When the biodegradation is completed, the bioprocess is called mineralization. This form of treatment produces simpler products, such as H2O, CO2, NH3, CH4, H2S and PO3, which are less harmful. The same process is defined as biotransformation if the organic compounds are not completely mineralized (Martorell et al. 2017a). Many microorganisms belonging to various taxonomic classes (bacteria, fungi, and microalgae) have shown the ability to decompose a broad variety of anthropogenic compounds, including synthetic dyes (Chen et al. 2009; El-Sheekh et al. 2009; Jafari et al. 2014; Miranda et al. 2013). In recent years, mycoremediation or the biotechnological application of fungi has become a model example for bioremoval of pollutants. It has been documented that a diversity of fungal species could be used for removing a variety of toxic dyes, mainly with white-rot fungi like Trametes versicolor and Phanerochaete chrysosporium. Other fungi species such as Rhizopus oryzae and Aspergillus niger, have also been reported (Sen et al. 2016). Regarding the use of yeast in the bioremediation of synthetic dyes, it was first mooted back in 1992, when the yeast strain of Candida curvata was used for the treatment of colored wastewater (Kakuta et al. 1992). Until today, reports on the biodegradation of synthetic dyes using yeast cells are limited compared to other investigations on the biodegradation of dyes using other microorganisms. The most studied yeast strains for the biodegradation of synthetic dyes are Candida sp., Saccharomyces cerevisiae, and Pichia sp. which belong to the Ascomycetes phylum, and only a few reports involve Basidiomycetous yeast strains, such as Trichosporon sp. and Pseudozyma rugulosa (Pajot et al. 2014). Enzymes involved in the biodegradation of dyes by yeast The biodegradation of synthetic dyes using yeast cells is performed with various intra-extracellular oxidase and reductase enzymes (Fig. 1). Oxidases are the most studied enzymes for the biodegradation of dyes by yeast. Moreover, the activity of certain reductases has also been reported in 13 Author's personal copy Environmental Sustainability Fig. 1 Intracellular and extracellular enzymatic biodegradation of synthetic dyes in yeast cells some yeast strains (Table 1). The suggested mechanism for the enzymatic biodegradation of azo dyes is shown in Fig. 2. Oxidases are a class of enzymes that use O2 as an electron acceptor to catalyze oxidation–reduction reaction, and thereby generating H2O or H2O2 as products. The oxidases typically contain metal or Flavin coenzyme on their active site (Phale et al. 2019). It was reported that the biodegradation of synthetic dyes by yeast cells can be accomplished through lignin-modifying enzymes, particularly phenoloxidase like Laccase (Lac) and tyrosinase (Tyr) as well as peroxidase such as manganese peroxidase (MnP) and lignin peroxidase (LiP) (Martorell et al. 2012; Solís et al. 2012). Laccase (EC 1.10.3.2) Lac is a benzenediol oxygen reductase that can be expressed in different species including lichens, bacteria and fungi. In fact, this enzyme belongs to the classes of urushiol and P-diphenol oxidase, distinguished by a multicopper atoms in their catalytic center (Arregui et al. 2019). A high redox potential (780 mV) allows these enzymes to oxidize many organic compounds, such as polyphenols, methoxy-substituted phenols, aromatic diamines, and several organic pollutants inclining dyes (Upadhyay et al. 2016). The fungal Lac was found present in Ascomycetes, Deuteromycetes, Basidiomycetes species, but is particularly abundant in white-rot fungi that degrade lignin (Brijwani et al. 2010). In addition, fungal Lac is an extracellular enzyme, this peculiarity facilitates their isolation and purification compared to Lac from other organisms. Therefore, they have gained particular commercial interest in organic syntheses, pulp/textile bleaching, bioremediation, chemical grafting, and surface modification of polymers (Jeon et al. 2012; Viswanath et al. 2014). As shown in the Table 1, a number of studies have documented the role of Lac in yeast cells in the biodegradation of synthetic dye. The use of Lac for the biodegradation of dyes does not require cofactors, since 13 it directly breaks azo dyes via non-specific free radical mechanisms, which does not create toxic by-products, such as aromatic amines, typically produced after the specific cleavage of the azo bond of azo dye (Dave et al. 2015). Tyrosinase (E.C. 1.14.18.1) Try is a copper-containing enzyme, known as polyphenol oxidase or monophenol mono-oxygenase. It has been found in plants, filamentous fungi, bacteria, and some yeast strains. This enzyme has a range of industrial interests, for example in the biosynthesis of melanin, the manufacture of L-dihydroxy phenylalanine, as well as several environmental biotechnologies like the detoxification of phenol-containing wastewater (Ates et al. 2007; Kim and Uyama 2005; Zaidi et al. 2014). With regard to the involvement of Try in the decolorization of synthetic dyes in yeast cells, only a few species revealed their role, notably Galactomyces geotrichum MTCC (Waghmode et al. 2012a, b), S. cerevisiae MTCC 463 (Jadhav et al. 2007) and Candida krusei strains (Charumathi and Das 2011). The catalytic reaction of dyes with Try is performed in two steps: The primary reaction catalyzing the o-hydroxylation of monophenols to the corresponding catechols (monophenolase activity), followed by the second oxidizing monophenols to the corresponding o-quinones (Diphenolase activity) (Duckworth and Coleman 1970). Lignin peroxidase (EC 1.11.1.14) LiP is a glycosylated enzyme that belongs to the oxidoreductase family that acts on peroxide as an acceptor. This ligninolytic enzyme has a high redox potential (700–1400 mV), with optimum activity at acidic range (pH 3–4.5). Lip is a non-specific substrate enzyme, which means that this characteristic confers it the ability to catalyze the degradation of different phenolic and non-phenolic aromatic compounds, including β-O-4 linkagetype arylglycerol-aryl ethers with a redox potential of up to 1.4 V (in comparison with the normal hydrogen electrode) (Choinowski et al. 1999; Chowdhary et al. 2018). For example, the biodegradation mechanism of sulphonated azo Dyes Conditions D (%)/Time Enzymatic activity Sterigmatomyces halophilus SSA-1575 Reactive Black 5 98/24 h G. geotrichum GG Acid Scarlet GR P. occidentalis G1 Acid Red B G. geotrichum MTCC 1360 Methyl Red S. cerevisiae MTCC 463 Methy Red 50 mg L−1 30 °C/0 rpm pH 5.0 100 mg L−1 30 °C /180 rpm pH 7.0–8.0 50 mg L−1 30 °C/160 rpm pH 5.0 100 mg L−1 30 °C/150 rpm pH 3.0 100 mg L−1 30 °C/0 rpm pH 6.5–9.0 G. geotrichum MTCC 1360 Remazol Red Rubine GFL 50 mg L−1 30 °C /0 rpm pH 7.0 96/36 h 87/96 h S. cerevisiae MTCC 463 Malachite Green 95/23 h S. cerevisiae Malachite Green C. krusei Basic Violet 3 D. rugosa Indigo C. samutprakarnensis Acid Red B Candida sp VITJASS Reactive Green 100 mg L−1 33 °C/150 rpm pH 7.2 100 mg L−1 30 °C/150 rpm pH 7.2 10 mg L−1 28 °C/120 rpm pH 6.5 10 mg L−1 30 °C/0 rpm pH 2.0 50 mg L−1 30 °C/160 rpm pH 6.0 100 mg L−1 30 °C/120 rpm pH 5.0–6.0 Al-Tohamy et al. (2020) Oxidase: LiP, MnP and Lac Reductase NADH-DCIP reductase Guo et al. (2019) Oxidase: LiP and Lac Reductase: NADH-DCIP reductase Song et al. (2018a, b) Oxidase: LiP, MnP and Lac Reductase: NADH-DCIP reductase Jadhav et al. (2008b) Oxidase: LiP and Lac Reductase: NADH–DCIP reductase, MG-reductase Jadhav et al. (2007) Oxidase: LiP, Tyr, Lac and Aminopyrine N-demethylase Reductase: NADH-DCIP reductase, AzoR Waghmode et al. (2012a, b) Oxidase: Tyr and Lac Reductase: NADH-DCIP reductase, AzoR, and Riboflavin reductase Jadhav and Govindwar (2006) Oxidase: LiP and Lac Reductase: NADH-DCIP reductase, MG-reductase Biradar et al. (2016) Oxidase: LiP and Lac Reductase: NADH-DCIP reductase, MG-reductase Charumathi and Das (2011) Oxidase: LiP, Tyr and Lac Reductase: NADH-DCIP reductase, MG-reductase and AzoR Bankole et al. (2017) Oxidase: LiP Reductase: NADH-DCIP reductase Song et al. (2018a, b) Oxidase: LiP Reductase: NADH-DCIP reductase Sinha et al. (2018) Oxidase: Lac Reductase: NADH-DCIP reductase, AzoR 92/10 h 98/16 h 100/1 h 100/16 min 99/2 h 100/24 h 99.9/5 5 d 97/18 h 84/96 h References Author's personal copy Yeasts species Environmental Sustainability Table 1 Studies on the biodegradation of dyes by yeasts species 13 13 Table 1 (continued) Conditions D (%)/Time Enzymatic activity References Candida sp MM 4035 T. porosum MM 4037 C. satwnus MM 4034 Barnettozyma californica MM 4018 D. polymorphus C. tropicalis Yellow 4R-HE Black B-V Blue RR-BB Red 7B-HE 200 mg L−1 25 °C/250 rpm pH 4.0 64–96/24 h Oxidase: LiP, MnP, Tyr, Lac and N-demethylase Martorell et al. (2012) Reactive Black 5 100/18–24 h Oxidase: MnP Yang et al. (2008) T. multisporum T. laibachii 63–98/36–72 h Oxidase: LiP, MnP and Lac Pajot et al. (2007) C. boidinii MM 4035 Yellow 4R-HE Red 7B-HE Blue RR-BB Green RR-4B Reactive Black 5 200 mg L−1 28 °C/200 rpm pH 5.0–6.0 200 mg L−1 26 °C/200 rpm pH 4.5 100/24 h Oxidase: MnP, Lac and peroxidase Martorell et al. (2017a) T. akiyoshidainum HP2023 Reactive Black 5 100/12 h Oxidase: phenol oxidase and peroxidase enzymes Martorell et al. (2018) T. beigelii NCIM-3326 Reactive Blue 171 95/24 h Reductase: NADH-DCIP reduc-Saratale et al. (2009a) tase and AzoR P. kudriavzevii CR-Y103 Reactive Orange 16 95/72 h Reductase: NADH-DCIP reduc-Rosu et al. (2018) tase and AzoR C. oleophila Reactive Black 5 100/24 h Reductase: AzoR-like Lucas et al. (2006) I. occidentalis Methyl Orange Orange II 80/15 h Reductase: AzoR Ramalho et al. (2004) G. geotrichum KL20A Methylene Blue 70/48 h Biodegradation Contreras et al. (2019) C. tropicalis TL-F1 Acid Brilliant Red GR 95/24 h Biodegradation Tan et al. (2013) P. rugulosa Y48 C. kruseia Gl Reactive Brilliant Red K-2BP 99/24 h Biodegradation Yu and Wen (2005) 200 mg L−1 25 °C/250 rpm pH 4.0 200 mg L−1 25 ºC/250 rpm pH 7.0 50 mg L−1 37 °C/0 rpm pH 6.6 400 mg L−1 30 °C/120 rpm pH 6.0 200 mg L−1 26 °C/120 rpm pH 7.6 0.2 mM dye 26 °C/120 rpm Acidic pH 50 mg L−1 35 °C pH 7.0 100 mg L−1 35 °C/160 rpm pH 5.0–6.0 200 mg L−1 28 °C/200 rpm pH 5.0–6.0 Author's personal copy Dyes Environmental Sustainability Yeasts species Author's personal copy Tan et al. (2014b) Biodegradation 98/10 h 50 mg L 30 °C/200 rpm pH 6.0 D (%) percentage of decolorization Magnusiomyces ingens LH-F1 Acid Red B Enzymatic activity D (%)/Time Conditions Dyes Yeasts species Table 1 (continued) −1 References Environmental Sustainability dyes by LiP may involve two consecutive one-electron oxidations of the H2O2-oxidized forms of LiP in the phenolic ring, where the corresponding carbonium ion carrying the azo link contributes to the formation of quinone and phenyldiazine through a nucleophilic attack by H2O. The phenyldiazine product is then oxidized by O2 to a phenyl radical and the azo bond is removed as N2, and the phenyl radical extracts hydrogen from its environment to produce a stable aromatic compound (Chivukula et al. 1995). LiP activity was detected during the biodegradation of various dyes using Ascomycota yeast strains of Pichia occidentalis (Song et al. 2018a, b), G. geotrichum (Guo et al. 2019), S. cerevisiae (Jadhav et al. 2007), C. krusei (Charumathi and Das 2011), Diutina rugosa (Bankole et al. 2017), Cyberlindnera samutprakarnensis (Song et al. 2018a, b), as well as strains belonging to the Basidiomycota phylum like Trichosporon laibachii and Trichosporon multisporum (Pajot et al. 2007). Manganese peroxidase (EC 1.11.1.13) MnP is a glycoprotein enzyme belonging to the oxidoreductase’s family, having a molecular weight ranging from 38 to 62.5 kDa (~ 350 amino acid residue). It is a substrate specific enzyme that oxidizes Mn2+ to Mn3+, which diffuses from the enzyme surface and in turn oxidizes the phenolic substrate, such as lignin model compounds or other organic contaminants (Zhou et al. 2013). It was reported by Hofrichter (2002), that MnP production is limited to certain soil litter decomposing and wood-decaying fungus. But some research on the biodegradation of synthetic dyes using yeast reported the involvement of MnP in yeast strains of P. occidentalis (L. Song et al. 2018a, b), Debaryomyces polymorphus, Candida tropicalis (Yang et al. 2008), T. multisporum, and T. laibachii (Pajot et al. 2007). Reductases They are enzyme classes that catalyze the reduction of the azo bonds (–N=N–) of azo dyes to produce a colorless aromatic amine. The involvement of such enzymes in the biodegradation of dyes was mainly recorded in bacteria (Hu 2001). However, other studies demonstrated the biodegradation activity of this enzyme in microalgae (Sinha et al. 2016), filamentous fungi (Bankole et al. 2018) and yeast (Lucas et al. 2006). The main reductase enzymes described in yeast strains are: Azoreductase (EC 1.7.1.6) AzoR is present in diverse microorganisms and higher eukaryotes. Although their structure and function are diverse, they have a common ability to reduce azo bonds of organic compounds including azo dyes, nitroaromatic and azoic drugs (Misal and Gawai 2018). The AzoR classification is primarily based on their secondary and tertiary structures. Thus, they can be divided into two classes: Flavin dependent and independent AzoR. The flavin-dependent AzoR can also be classified according to the required co-enzymes NADH, NADPH, or both (Saratale et al. 2011; Solís et al. 2012). Breaking the azo bond by AzoR act as a critical step in the dye biotransformation 13 Author's personal copy Environmental Sustainability Fig. 2 Suggested azo bond cleavage via a reduction and oxidation, adapted from Kandelbauer and Guebitz (2005) Fig. 3 Reactions catalyzed by NADH-DCIP reductase (a) and MG- reductase (b) mechanisms (Elfarash et al. 2017). The involvement of AzoR during the dye biodegradation was detected in yeast strains of S. cerevisiae MTCC 463 (Jadhav et al. 2007), C. krusei (Charumathi and Das 2011), Issatchenkia occidentalis (Ramalho et al. 2004), Trichosporon beigelii NCIM-3326 (Saratale et al. 2009a). NADH-DCIP reductase (EC 1.6.99.3) The NADH-preferring 2,6-dichloroindophenol reductase is an oxidoreductase that reduces 2,6-dichloroindo-phenol (DCIP) using NADH as an electron donor. DCIP is blue in its oxidized state and becomes colorless after reduction with reductase. This feature confers to this enzyme the ability to be useful in many clinical settings such as the determination of NADH and other dehydrogenases with a colorimetric reaction, when coupled to formazan dye-forming chromogens that act as hydrogen acceptors (Nishiya and Yamamoto 2007). Some studies have shown a significant increase in the activities of NADH-DCIP reductase, during the decolorization of azo dyes by yeast cells (Bankole et al. 2017; Rosu et al. 2018; Saratale et al. 2009a; Song et al. 2018a, b). Malachite green reductase It is an enzyme that also uses NADH as an electron donor to convert green malachite to green Leucomalachite. Only few researchers reported (MG)reductase as a marker enzyme for the reduction of synthetic dyes. The first study showing the role of (MG)-reductase in the biodegradation of green malachite dye was discovered in a yeast strain of S. cerevisiae MTCC 463 (Jadhav and Govindwar 2006). Two years later, Jadhav et al. (2008b) demonstrated that the biodegradation of methyl red by G. geotrichum MTCC 1360 strain involved also the (MG)reductase. Thereafter, Charumathi and Das (2011), reported 13 that (MG)-reductase activity was increased in C. krusei cells following the biodegradation of Basic Violet 3. Biradar et al. (2016) also, reported that the biodegradation of Malachite green by the S. cerevisiae yeast strain involved an increase in the enzymatic activity of (MG)-reductase. The reactions catalyzed by MG-reductase (B) and DCIP-reductase (A) are reflected in Fig. 3. The enzymatic biodegradation of dyes using yeast cells can be improved through omics approaches, especially protein engineering, which would pave the way for further studies. In addition, the exploitation of enzymes from yeast cells after the dye mycoremediation process may be another form of valorization of the resulting biomass. Factors affecting the biodegradation of dyes by yeast The effective biodegradation of dye contaminants in wastewater remains a challenging process, due to many factors that influence this bioprocess. Therefore, it is important to evaluate and optimize the effect of physicochemical operating conditions, in order to make the process faster, more efficient and suitable for large-scale applications. Effects of temperature In the microbial environment, temperature is a critical factor that plays several roles in cell viability, physiological status and metabolic performance. Optimal temperature for yeast growth is typically between 25 °C and 37 °C (Fu and Viraraghavan 2001). In fact, the optimum temperature for dye decolorization using yeast cells, is often correlated with the optimum growth temperature. Changes Author's personal copy Environmental Sustainability in temperature can affect the biological response of yeast cells, especially enzyme activities (Ali 2010). Numerous studies (Table 1) have reported that the decolorization rate increases with increasing temperatures (from low to optimum temperature). However, a decolorization decline was noted at high temperatures (Tan et al. 2013, 2014b, 2016), which can be attributed to the loss of cell viability, or the denaturation of enzymes (Saratale et al. 2009b). Effects of pH It’s known that fungi, including yeast species show greater biodegradation behaviors in acidic or neutral mediums (Ali 2010). As showed in Table 1, almost all yeast decolorization studies demonstrated that the bioremoval of dyes is higher at optimum pH between 4 and 7 (Bankole et al. 2017; Jadhav et al. 2008b; Ramalho et al. 2004), and tended to decrease significantly when the pH of the medium was within the alkaline range. The pH effects are also related to cell viability, as shown by Peña et al. (2015), where the cell cycle of S. cerevisiae was interrupted at pH 9.0. This growth inhibition might be attributed to the decrease in cell transport of amino acids or the incorporation of proteins. On the other hand, the change in pH of the medium could also inhibit the transport of dye molecules through the cell membrane, which is considered as a limiting step for intracellular decolorization (Khan et al. 2013). Effects of dye structure and concentration The chemical structure and concentration of dyes are among the influencing factors of decolonization efficiency. Research studies have suggested that increasing dye concentration gradually reduces their decolorization (Aksu 2003; Jadhav et al. 2007; Martorell et al. 2018), which could be attributed to an increase in dye toxicity. Moreover, at high concentrations, dyes can bind to the active site of enzymes mainly of AzoR, thereby preventing their activity (Jadhav et al. 2008a; Saratale et al. 2009a). Meanwhile, the chemical structure of dyes could also influence their degradation. In a comparative study on monoazo, diazo or triazo dyes, Franciscon et al. (2012) reported that simple-structured azo dyes with low molecular weight were easily biodegradable. Additionally, the azo bond is more susceptible to be broken when the substituent is in the para position of the phenyl ring relative to the ortho and meta position (Hsueh et al. 2009). For example, the substitution of electron withdrawal groups (-SO3H) by (-SO2NH2) in the phenyl ring para position relative to the azo bond, increases the rate of reduction (Walker and Ryan 1971). Also, amino and hydroxyl-based dyes are more resistant to degradation than dyes with nitro, methyl, sulpho, and methoxy groups. This can be explained by the reduction mechanism that is conducted in two steps: a fast one-electron transfer reaction occurs to the radical anion, followed by a second, slower electron transfer process to create a stable dianion. The functional group of azo bond with a higher electronic density may not be suitable for this second electron transfer forming the dianion (Pearce et al. 2003; Rau et al. 2002). Metal-complex dyes might also have an adverse effect on the decolorization efficiency (Chen et al. 2003; Libra et al. 2004). Effects of oxygen and shaking There are differing views on the effect of agitation on decolorization efficiency. According to results of several studies, the highest decolorization efficiency was observed in agitated cultures compared to static cultures. Shaking allows aeration to the medium, and equal distribution of nutrients, it also facilitates the exchange of gas formed by yeasts during the degradation of dyes (Martorell et al. 2017b; Pajot et al. 2007; Yang et al. 2008; Yu and Wen 2005). As mentioned above, several oxidative enzymes require oxygen (Shahid et al. 2015). Meanwhile, some researchers obtained the best decolorization results under static conditions (Table 1). The negative effect of medium agitation on the decolorization efficiency was attributed to the fact that oxygen acts as an electron acceptor with high redox potential, thereby preventing dye reduction (Li et al. 2004; Kalyani et al. 2008; Al-Tohamy et al. 2020). Effect of carbon and nitrogen sources Despite the presence of dyes and other organic compounds in textile wastewater, no yeast strain can achieve an effective decolorization via the biodegradation mechanisms with dyes as the only carbon source, unless bioremoval is based on biosorption mechanisms with non-viable yeast biomass (Mahmoud 2016). It was mentioned that the addition of glucose to yeast culture medium stimulates the biodegradation of dyes (Chang et al. 2000; Waghmode et al. 2011). Other studies also showed a strong correlation between glucose depletion and the rate of dye removal (Lucas et al. 2006; Yang et al. 2008). Glucose can play many roles in metabolic pathways, including its role as regenerator of the redox mediators like NADH and FADH, that act as substrates for the production of H2O2, through an enzymatic reaction by glucose1oxidase and glucose-2-oxidase (Jafari et al. 2014). In turn, H2O2 acts as a co-substrate for extracellular peroxidase activity (Swamy and Ramsay 1999). Meanwhile, decolorization in a medium containing high carbon source concentrations appears to be less effective. In this case, the yeast cells prefer to use readily available carbon sources instead of using dyes as a carbon source (Saratale et al. 2009b). On the other hand, the supplementation of nitrogen sources to the medium (peptone, yeast extract, urea), can also regenerate NADH (Bras et al. 2001). However, similarly to carbon, high nitrogen concentrations may influence the decolorization efficiency. Tatarko and Bumpus (1998) reported that supplementation of high nitrogen concentrations to the medium inhibited Congo red decolorization. Conformingly, a study by Kaushik and Malik (2009), demonstrated that higher nitrogen concentrations (25–60 mM), suppressed ligninolytic enzyme 13 Author's personal copy Environmental Sustainability activity. It is therefore important to determine the appropriate concentration of carbon and nitrogen sources that improve the decolorization process (Pearce et al. 2003; Van der Zee et al. 2001). Since several factors can influence the process of biodegradation of dyes by yeast cells, optimizing these factors is essential to limit losses, whether related to chemicals, growing conditions, or process time. Applying the design of the experiment can be a promising solution that can reduce treatment costs and time, making, therefore, the use of yeast more competitive than the other treatment processes. Chemical characterization and toxicity assessment of dye biodegradation by‑products Irrespective of the technique used (physical, chemical, or biological) in the treatment of textile wastewater, the main concern is not only the dye removal, but mainly the guarantee of its effective detoxification after treatment. Hence, the ecotoxicological evaluation of post-treatment is crucial. The oxidation processes of synthetic dye using Fenton reactions, non-metallic oxidation catalysts based on hydroxyl radicals, and other chemical techniques, can ensure a successful decolorization (Javaid and Qazi 2019). However, these techniques can produce various oxidation by-products that may be more toxic than the original dye molecules (dos Santos et al. 2007; Sun et al. 2009). In order to highlight the biodegradation efficiency of dyes from a toxicological point of view, a detailed characterization of the metabolites produced during and after complete decolorization must be assessed. Particularly, the colorless aromatic amines resulting from the reduction of the cleavage of chromophore azo-bonds, because they are classified among the most hazardous compounds (Forss and Welander 2009; Puvaneswari et al. 2006). Based on the available literature, detailed characterization of dye by-product degradation can be carried out with different chromatography techniques such as thin-layer chromatography (TLC), high performance liquid chromatography (HPLC), high performance thin layer chromatography (HPTLC), liquid chromatography–mass spectrometry (LC–MS), gas chromatographymass spectrometry (GC–MS), and spectroscopy techniques such as ultraviolet–visible spectroscopy (UV–VIS), Fourier transform infrared spectroscopy (FTIR) and nuclear magnetic resonance (NMR) spectroscopy. In addition, some studies (Saratale et al. 2009a, b; Tan et al. 2014b) reported that biodegradation could also be calculated by measuring the level of mineralization using total organic carbon (TOC), chemical oxygen demand (COD) and biochemical oxygen demand (BOD). Table 2 summarizes the analytical technique used for the identification of the by-products of 13 dye biodegradation by yeast species. As showed in Fig. 4 and Table 2, the degradation of the same dye by different yeast strains produces different by-products. This suggests the need for ecotoxicological analyzes to ensure the safety of these metabolites. Indeed, a variety of ecotoxicological approaches can be used. Among the existing ecotoxicological bioassays, phytotoxicity tests are the most commonly used, because of their high sensitivity, low cost and easy use. Saratale et al. (2009a) studied the phytotoxicity of Navy Blue HER dye and its biodegradation by-products on two plant models, Sorghum vulgare and Phaseolus mungo. The results showed a higher germination percentage and significant growth of the plumule and radical in seedlings treated with degradation by-products compared to those treated with the original dye, confirming thus the detoxification of HER by T. beigelii. Similarly, Waghmode et al. (2012a) assessed the phytotoxicity of Remazol Red and its by-products on S. vulgare and P. mungo seeds, and demonstrated that the by-products produced were less toxic compared to the original dye. Likewise, Tan et al. (2014a) reported that the investigation of metabolites derived from Acid Orange G decolorization on P. mungo and Oryza sativa seeds, confirmed the biotransformation of this dye into less toxic byproducts after complete decolorization using C. tropicalis TL-F strain. The other common bioassay used to estimate the acute toxicity of the dye and their biodegradation intermediates may be performed using the Microtox test. Tan et al. (2016) assessed the shift in acute toxicity before and after biodegradation of Acid Scarlet 3R using Scheffersomyces spartinae TLHS-SF1 strain, with the Microtox test, at the initial dye concentration of 20 mg L−1and 50 mg L−1. Moderate (IRs 60% within 30 min) and high (IRs 75% within 30 min) toxicity were recorded against Vibrio fischeri. The dye treatment toxicity sharply decreased to non-toxic levels. Similarly, Song et al. (2018a, b) studied the toxic effects of decolorization intermediates of ARB dye using a yeast strain of P. occidentalis G1 through Microtox test. It was shown that the IRs of 20 mg L−1 and 50 mg L−1 were respectively about 68% and 78%. After dye treatment, the toxicity of both dye solutions decreased to non-toxic levels as indicated by the IRs, which decreased to 8% and 11%, respectively. Likewise, Tan et al. (2019) assessed the toxicity of ARB (50 mg L−1) and its decolorization by-products produced by C. tropicalis SYF-1 by using the Microtox test. The IR was about 75.4% after 5 min exposure, suggesting that the initial dye concentration possessed high acute toxicity. After a 6 h treatment, the dye displayed the 5 min IR of about 67.2%, slightly lower than initial IR. However, the 5 min IR of the dye solution sharply decreased to 9.4% after complete decolorization (12 h), suggesting a non-toxic level. Also, the combinations of different bioassays were used to assess the toxicological effects of synthetic dyes or their metabolites. Waghmode et al. (2012b) studied the toxicity of Rubine GFL Author's personal copy Environmental Sustainability Table 2 By-products detected after the biodegradation of some azo dyes by yeast Yeast strain Dye name and chemical structure Analyses C. tropicalis SYF-1 Pichia sp. TCL Acid Red B M. ingens LH-F1. UV–vis HPLCMS P. occidentalis G1 S. cerevisiae ATCC 9763 Acid Scarlet 3R S. spartinae TLHS-SF1 Monoazo disperse dye C. tropicalis HNMR TLC HPLC LC-MS Reactive blue 13 UV-Vis MS/MS GC-MS C. rugopelliculosa HXL-2 Methyl red S. cerevisiae ATCC 9763 UV-Vis FTIR TLC ESI-MS UV-Vis FTIR HPLC Remazol Red UV-Vis FTIR TLC HPTLC G. geotrichum MTCC 1360 Rubine GFL Reactive Black 5 T. akiyoshidainum HPTLC HPLC FTIR GC-MS UV–vis FTIR HPLCGPC GC–MS Reactive green dye Candida sp. VITJASS UV–Vis FTIR HPLC GC–MS Biotransformation products 4-hydrazinylnaphthalene-1- sulfonic acid 4-hydroxynaphthalene-1- sulfonic acid 4-aminonaphthalene-1-sulfonic acid 3,4-dihydroxynaphthalene-1-sulfonic acid 4-hydroxynaphthalene-1,2-dione 4-aminonaphthalene-1-sulfonic acid naphthalene1,2,3,4-tetraol 3-7-dihydroxy-octahydronaphthalene-2,6-dione 4-aminonaphthalene-1-sulfonic acid 3-amino-4-hydroxynaphthalene-1-sulfonic acid naphthalen-1-ol 3,7-dihydroxy-hexahydronaphthalene-2,6 (1H,7H)dione 4-amino-naphthalene-1-sulfonic acid 3,4-dihy droxy-naphthalene-1-sulfonic acid naphthalene-1,2,4-triol 4-Amino-1-naphthalene sulfonic acid sodium salt 3-amino-4-naphthol-1- sulfonic acid sodium salt Disodium 4-hydroxy-2-[(E)-(4-sulfonato-1-naphthyl) diazenyl]naphthalene-1-sulfonate Disodium 4-hydroxy-2-[(E)-(4-sulfonato-1-phenyl) diazenyl]naphthalene-1-sulfonate Disodium 4-hydroxy-2-[(E)-(4-sulfonato-1-naphthyl) diazenyl]benzene-1-sulfonate 4-aminonaphthalene-1-sulfonic acid 7,8-dihydroxynaphthalene-1,3-disulfonic acid, 3,4-dihydroxynaphthalene-1-sulfonic acid naphthalene-1,2,6,8-tetraol naphthalene-1,2,4-triol References (Tan et al. 2019) (Qu et al. 2012) (Tan et al. 2014b) (L. Song et al. 2018) (Kiayi et al. 2019) (Tan et al. 2016) 2-amino-4-methyl- 5-ethoxycarbomylthiazole (Arora et al. 2005) 1-chloro-3- aniline 2,4,6-triazine 2-chloro-1,3,5-triazine Phenol aniline N, N-dimethyl-p-phenylene diamine (DMPD) 2-Aminobenzoic acid. N, N’-dimethyl- p-phenylenediamine 2-authentic 2-aminobenzoic acid 3-amino [4, 5 (6-chloro-1, 3, 5 triazine-2yl) amino] naphthalene 2, 4, 7 benzene trisulfonic acid. 2[(3-aminophenyl) sulfonyl] ethane sulfonic acid. 2- amino naphthalene N-phenyl-1, 3, 5 triazine 2[(3-aminophenyl) sulfonyl] ethane sulfonic acid ethylsulfonyl-benzene 2-ethylphenyl sulfone 2-(aminomethyl)-4-nitroaniline 1-(3-nitrophenyl)methana- mine N-(3-aminopropyl)benzene-1,4-diamine 4-((chlorodifluoromethyl)sulfonyl) aniline 4- ((diazenilfenil) sulfonyl) methyl hydrogen sulfate 5,7-dimethoxy-1-naphthol 5-amino-4-hydroxy-3,6-dioxo-2,3, 5,6tetrahydronaphthalene2,7-sodium disulfonate. sodium 3-[(dichloro-1,3,5-triazin-2-yl) amino] benzene-1-sulfonate sodium 1-amino-4-[(4-aminophenyl) amino]-9,10dioxo-9,10- dihydroanthracene-2-sulfonate 2-chloro-1,1-diphenyethane Diphenylmethane (Liu et al. 2011) (Vatandoostar ani et al. 2017) (Jadhav et al. 2008b) (Waghmode et al. 2012a) (Waghmode et al. 2012b) (Martorell et al. 2017b) (Sinha et al. 2018) 13 Author's personal copy Environmental Sustainability C.tropicalis SYF-1 (Tan et al. 2019) 4-hydrazinylnaphthalene-1- sulfonicacid 4-hydroxynaphthalene-1- sulfonicacid 4-aminonaphthalene-1-sulfonic acid 3,4-dihydroxynaphthalene-1-sulfonic acid 4-hydroxynaphthalene-1,2-dione HPLC-MS C.samutprakarnensisS4 (Song et al., 2018) Acid Red B S. cerevisiae ATCC 9763 (Kiayi et al., 2019) LC-MS HPLC-MS Pichia sp. TCL (Qu et al., 2012) 4-Amino-1-naphthalene sulfonicacid 3-amino-4-naphthol-1- sulfonicacid 4-hydroxy-2-[(E)-(4-sulfonato-1-naphthyl) diazenyl]naphthalene-1-sulfonate 4-hydroxy-2-[(E)-(4-sulfonato-1-phenyl) diazenyl]naphthalene-1-sulfonate 4-hydroxy-2-[(E)-(4-sulfonato-1-naphthyl) diazenyl]benzene-1-sulfonate Fig. 4 Proposed partial biodegradation pathways of ARB by various yeasts using HPLC–MS and LC–MS analysis techniques dye and its by-products produced from the biodegradation by G. geotrichum MTCC 1360 yeast strain. Analytical methods in this study included genotoxicity and cytotoxicity tests, oxidative stress, activity of antioxidant enzymes, lipid peroxidation and protein oxidation on root cells of Allium cepa as well as the phytotoxicity of the dye and dye by-products using P. mungo and S. vulgare. The outcomes showed that Rubine GFL dye exerted oxidative stress and subsequent toxic effects on the root cells, whereas its metabolites were less toxic. Likewise, Roșu et al. (2019) suggested that after treatment of BB41 dye by Pichia kudriavzevii CR-Y103, the degraded metabolites was found to be less toxic than the parent dye compound, by using phytotoxicity, cytotoxicity, and genotoxicity assays on Trifolium pratense and Triticum aestivum seedlings. This indicates the detoxification of this azo dye. The chemical characterization of the by-products of dye biodegradation not only makes it possible to recognize the pathways of their biodegradation, but may also indicate the toxicity of the aromatic compounds formed during biodegradation. This will assess the performance of treatment from a toxicological point of view. 13 Molecular aspects of dye degradation by yeasts In all areas of life sciences, the use of omics methods, namely metagenomics, transcriptomics, proteomics, and metabolomics, has recently become widespread. The integration of these approaches allows a holistic view of the biological systems. Understanding the molecular mechanisms of biodegradation of aromatic compounds such as synthetic dyes is essential for the development of successful bioremediation strategies. Numerous studies have been carried out on the molecular aspects of dye degradation by fungi (Mäkinen et al. 2019; Sun et al. 2015) and bacteria (Joshi et al. 2020; Ma et al. 2019). However, very little research has focused on the molecular mechanisms involved in the enzymatic biodegradation of synthetic dyes by yeast cells. María et al. (2018) unraveled the genetic basis of the enzymatic activities of Mnp, Lac, and Phenoloxidase after complete decolorization of Reactive Black 5 by Trichosporon akiyoshidainum HP-2023, their genome comprises 30 MB with a G + C content of 60.75% and 9019 gene models. Thus, thirty-three putative carbohydrate-active enzymes with auxiliary activity have been identified in the annotated Author's personal copy Environmental Sustainability genome, nineteen hydrogen peroxide-producing enzymes, four benzoquinone oxidoreductases, four extracellular fungal heme-peroxidases, and two Lacs. For the decolorization of ARB at high osmotic environment, Wang et al. (2020) reported that the halotolerance enhancement through the detection of different genes expressed in P. occidentalis used for the decolorization of ARB was related to the upregulated genes encoding the enzymes or functional proteins related to intracellular synthesis of glycerol. Also based on the transcriptome sequencing, Tan et al. (2020) suggested that the halotolerance capacity of C. tropicalis SYF-1 yeast, used for the decolorization of ARB was enhanced by the regulation of the cell wall component. Some recent studies have focused on enhancing the biodegradation of dyes by improving enzyme activity through protein engineering. For example, Zhang et al. (2019) have reported that the recombinant enzyme rMnP3-BBP6 that resulted from cloning of new MnP gene (mnp3) of the white-rot fungus Cerrena unicolor BBP6 in Pichia pastoris, has shown a high decolorization activity of various dyes: Brilliant blue R, Methyl orange, Crystal Violet, Bromophenol Blue, and Remazol Brilliant Blue. Karla et al. (2020) have used saturation mutagenesis to alter two amino acids in the catalytic tryptophan environment positions V160 and A260, of Versatile peroxidase (VP) from Pleurotus eryngii. In order to effectively use VP and its variants for the degradation of azo dyes (Evans Blue, Amido Black 10B, and Guinea Green B), VP was immobilized on S. cerevisiae EBY100 cell surface and cell wall fragments were used after lysis. Thus, the embedded VP retained ∼ 70% of its initial activity after 10 cycles of decolorization. State-of-the-art technology in the biochemical characterization of dye biodegradation pathways coupled with further studies on genomic, proteomic, and metabolomic aspects, could improve fundamental knowledge in the mycoremediation field. This could offer a wide range of possibilities for improving the performance of yeasts or their enzymes for applications in the bioremoval of toxic dyes or other contaminants from wastewater. Future perspectives Despite the scientific and technical advancements that have been developed for the depollution of textile wastewater, there is no universal approach to achieve effective detoxification with low-cost investment. Each technique has its own advantages and limitations. Therefore, the use of hybrid and/or integrated processes may be a promising solution. In fact, mycoremediation can be an efficient approach to be combined with other chemical or physical processes (Akhtar et al. 2020). In order to promote such bioprocesses and make them more attractive, the first crucial concern is related to the choice of tolerant yeast strains. Furthermore, optimizing operating conditions such as agitation, temperature, and the use of low-cost substrates as carbon and nitrogen sources can significantly reduce the processing cost. From the point of view of environmental sustainability, the chemical characterization of the by-products of the enzymatic biodegradation of dyes by yeast cells and the evaluation of their toxicity after complete decolorization will highlight the environmental safety of this bioprocess compared to other chemical dye-degradation processes. Thus, the combination of characterization studies of biodegradation by-products with further studies based on omics approaches, notably transcriptomics, proteomics and metabolomics techniques, will greatly contribute to the understanding of dye biodegradation pathways by yeast cells (Wang et al. 2020; Zheng et al. 2020). Also, the use of yeast oxidoreductive enzymes in the bioremediation of dyes, and the improvement of their performance in terms of stability, selectivity, and catalytic activity, can be carried out with various genetic engineering techniques (Karla et al. 2020). Indeed, over the past decade, research has become increasingly interested in the application of genetic engineering techniques to develop enzyme formulation for bioremediation applications. Meanwhile, the fate of the biomass after the biodegradation of dyes is among the main questions that needs to be solved. The resulting biomass can be valued in several areas, mainly in the energy sector, for the production of biodiesel (Ali et al. 2021). The mycoremediation of synthetic dyes using yeast is simple, reliable, and cost-efficient at laboratory scales, however approval of this approach should be carried out on pilot schemes prior to large-scale industrial operations. Conclusion Based on the studies reviewed in this review, it can be concluded that mycoremediation using yeast cells can be an efficient and eco-friendly strategy for the treatment of toxic dyes. The biodegradation ability of yeasts has been related to the activity of oxidases (Lac, Tyr, LiP, and MnP), and reductases (AzoR, NADH-DCIP reductase and MG-reductase). The operating physicochemical parameters that influence the biodegradation process have to be optimized for successful decolorization. For most yeast strains, the highest bioremoval capacity is achieved at neutral or acidic pH ranges, in shaken cultures at 30 °C. The addition of appropriate supply of nitrogen or carbon sources significantly improves the dye-removal efficiency. Meanwhile, textile dyes can affect the biodegradation capacity of yeast, both by their chemical properties and/or concentration. During the process of dye biotransformation, the chemical characterization of the degradation intermediates using chromatography and spectroscopy techniques enables the identification of the dye degradation pathways. Besides, toxicological bioassays 13 Author's personal copy Environmental Sustainability revealed that the resulting intermediate metabolites of dye biodegradation using yeast are typically less toxic than the initial dye. We can therefore deduce that the biodegradation of synthetic dyes by yeasts does not only allow dye decolorization, but ensures the effective detoxification of these contaminants and their by-products. This makes the use of yeast cells or their enzymes in the biodegradation of synthetic dyes a promising future technology to ensure environmental sustainability. Acknowledgements The authors gratefully acknowledge Moroccan Foundation for Advanced Science, Innovation and Research (MAScIR) for the financial and technical support. Authors wish also to thank Chanda Mutale Joan for reviewing the quality of the English language in this article. Compliance with ethical standards Conflict of interest On behalf of all authors, the corresponding author states that there is no conflict of interest. References Abiri F, Fallah N, Bonakdarpour B (2017) Sequential anaerobic-aerobic biological treatment of colored wastewaters: case study of a textile dyeing factory wastewater. Water Sci Technol 75(6):1261– 1269. https://doi.org/10.2166/wst.2016.531 Akhtar N, Mannan MA (2020) Mycoremediation: Expunging environmental pollutants. 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