Biodegradation and reduction of toxicity of Azo Trypan Blue dye by Amazonian strains of gasteroid fungi (Basidiomycota)

Biodegradação e redução da toxicidade do corante Azo Trypan Blue por Cepas amazônicas de fungos gasteroides (Basidiomycota)

Abstract

Amazonian strains of Cyathus spp. and Geastrum spp. were studied for the ability to discolor the trypan blue azo dye and reduce its toxicity. Discoloration of trypan blue dye (0.05%) was evaluated in solid and aqueous medium over different periods. The reduction of dye toxicity after treatment was assessed by seed germination and the development of lettuce seedlings (Lactuca sativa L.) and toxicity test in Artemia salina (L.) larvae. All evaluated strains showed the potential to reduce the color intensity of trypan blue dye. Cyathus strains reached 96% discoloration, and C. albinus and C. limbatus also reduced dye toxicity. Geastrum strains showed a high efficiency degree in color reduction, reaching 98% discoloration, however, the by-products generated during the process presented toxicity and require further investigation. For the first time, Amazonian strains of gasteroid fungi degrading trypan blue are reported, some even reducing its toxicity. Thus, making them promising sources of enzymes of interest to bioremediation scenarios involving synthetic dyes.

Keywords:
bird's nest fungi; Cyathus; dye discoloration; earthstars fungi; Geastrum

Resumo

Cepas amazônicas de Cyathus spp. e Geastrum spp. foram estudadas quanto a capacidade de descolorir o corante azo Azul de tripano e reduzir sua toxicidade. Foi avaliada a descoloração do corante Azul de tripano (0,05%) em meio sólido e aquoso sob diferentes períodos de tempo. A redução da toxicidade do corante após o tratamento foi avaliada através da germinação de sementes e do desenvolvimento de plântulas de alface (Lactuca sativa L.), além do teste de toxicidade em larvas de Artemia salina (L.). Todas as cepas avaliadas apresentaram potencial de reduzir a intensidade da coloração do corante azul de tripano. As cepas de Cyathus alcançaram 96% de descoloração, sendo que C. albinus e C. limbatus também reduziram a toxicidade do corante. As cepas de Geastrum apresentaram alto grau de eficiência na redução de cor, alcançando 98% de descoloração, porém, os subprodutos gerados durante o processo apresentaram toxicidade e necessitam de maior atenção. Pela primeira vez se relata cepas amazônicas de fungos gasteroides degradando o Azul de tripano, algumas ainda reduzindo sua toxicidade, tornando-as fontes promissoras de enzimas de interesse em cenários de biorremediação envolvendo corantes sintéticos.

Palavras-chave:
fungos ninho-de-pássaro; Cyathus; descoloração de corante; fungos estrela-da-terra; Geastrum

1. Introduction

The disposal of contaminated textile effluents in ecosystems is one of the critical environmental issues (Ceretta et al., 2021; Wang et al., 2021). Most of these effluents are from azo dyes, the largest and most versatile class of synthetic dyes (Lee et al., 2017), which represents approximately 70% of the weight of all dyes used worldwide (Kanagaraj et al., 2015). These dyes cause environmental impacts (Hassaan and Nemr, 2017; Mourid et al., 2017) and are considered recalcitrant, non-biodegradable, persistent (Saratale et al., 2009a, b), stable in light and difficult to remove from water by conventional wastewater treatment methods (Islam et al., 2011).

Among these dyes, we highlight the trypan blue (C34H28N6O14S4), widely used in medical histology (study of biological tissues) to analyze the viability of cell death (Keogh et al., 1980; Cooksey, 2014), in yeast viability tests (Liesche et al., 2015), in the detection of dead plant tissue and in the staining technique of arbuscular mycorrhizal fungi (Phillips and Hayman, 1970). Although versatile in application, this dye has been widely questioned because it is harmful to human health with teratogenic, oncogenic, carcinogenic and mutagenic effects (Weisburger & Weisburger, 1966; Chung, 2016; Field et al., 1977; Brown et al., 1978; Robertson et al., 1982; Nadaroglu et al., 2017; Tang et al., 2021), in addition to chronic cytotoxic effects (Kodjikian et al., 2005).

In an attempt to reduce its use, some substitutes were proposed (Santana et al., 2020a; Silva et al., 2015; Vierheilig et al., 2005), but when indispensable, it is necessary to think about alternatives for the treatment of effluents to reduce the impacts on the environment. One option is biodegradation performed by basidiomycete fungi and, even if other trypan blue discoloration techniques have been proposed (Nadaroglu et al., 2017; Ghime and Ghosh, 2020; Aljadaani et al., 2021), biological discoloration by fungi has many advantages in view of the enormous enzymatic potential proven useful in the treatment of synthetic azo dyes (Nozaki et al., 2008; Ali et al., 2010; Gregorio et al., 2010).

A portion of the basidiomycetes corresponds to gasteroid fungi, widely distributed in the tropics (Mueller et al., 2007), mainly in Brazil, where the diversity of the group increases every year (Accioly et al., 2019; Assis et al., 2022; Ferreira-Sá et al., 2021; Freitas et al., 2023; Santana & Couceiro, 2023). Studies with this group revealed the production of important substances with proven biological activity (Liu & Zhang, 2004; Dore et al., 2007; Coetze and Van Wyk, 2009), but there is a study gap regarding the discoloration of synthetic dyes. The genera Cyathus Haller and Geastrum Pers., common taxa in forests are known to be producers of bioactive compounds useful for bioremediation and discoloration of some synthetic dyes (Vasdev and Kuhad, 1994; Vasdev et al., 1995; Mishra and Bisaria, 2006; Santana et al., 2016), but there is no information on these genera regarding the discoloration of trypan blue.

Thus, given the need to study other fungal species and increase treatment options for synthetic dyes and encourage enzymatic studies of gasteroid fungi, the aims of this study were to investigate the ability of Amazonian strains of Cyathus and Geastrum species to discolor the synthetic dye trypan blue and to analyze the toxicity of the dye after the fungal treatment.

2. Materials and Methods

2.1. Sampling and identification of fungi

Fresh and mature specimens of Cyathus and Geastrum were collected manually (Lodge et al., 2004) in a fragment of the Amazon rain forest (dense rainforest) in the vicinity of the Sílvio Braga Hydroelectric Power Plant (2°48'44.45”S, 54°17'56.23”W), Western Pará, Brazil. The identification of the material was performed based on morphological characters following the descriptions in the specialized literature (Sunhede, 1989; Calonge et al., 2005; Silva et al., 2013; Sousa et al., 2014; Accioly et al., 2018, 2019; Góis et al., 2021). Part of the samples was used to obtain the strains and the other part was assembled in vouchers in the fungi collection of the Herbarium HSTM (HSTM-Fungos) (JBRJ, 2023) of the Federal University of Western Pará (Table 1).

Table 1
Species used to obtain Amazonian strains of gasteroid fungi.

Family	Species	Voucher
Agaricaceae	Cyathus albinus Accioly, R. Cruz & Baseia	14790
	C. limbatus Tul. & C. Tul.	14883
	C. setosus H.J. Brodie	14957
Geastraceae	G. echinulatum T.S. Cabral, B.D.B. Silva & Baseia	14901
	Geastrum hirsutum Baseia & Calonge	14865
	G. schweinitzii (Berk. & M.A. Curtis) Zeller	14896

2.2. Fungal strains

The strains of Geastrum were obtained from sections removed from the pseudoparenchyma layer of fresh basidiome exoperidium and inoculated in a 90 mm diameter Petri dish containing 15 mL of potato dextrose agar (PDA, Difco^®) culture medium®. The strains of Cyathus were obtained from sections of the peridioles inoculated in a 90 mm diameter Petri dish containing 15 mL PDA culture medium. After growth, fragments of 3 × 3 mm from the edge of the cultures were inoculated in the center of new Petri dishes with equal volume and content. Then they were incubated under the conditions suggested by Santana et al. (2020b) to obtain the pure culture. Thus, each species was considered a treatment, totaling six treatments.

2.3. Trypan blue dye discoloration in solid culture medium

For the discoloration test of the blue trypan dye in solid medium, a 3 × 3 mm block was used, containing mycelium removed from the edge of the pure strain of each species and transferred to the centre of a Petri dish (90 mm in diameter) containing 15 mL of the homogeneous mixture of PDA plus trypan blue (0.05%). Petri dishes were incubated according to the indications of Santana et al. (2020b), and each plate was considered a replicate. Every three days, from the beginning of the experiment, for a period of 21 d of incubation, the dye discoloration halo was evaluated by measuring the diameter with a ruler (orthogonal directions). The PDA culture medium containing the dye, but in the absence of fungi was used as the control treatment of the experiment.

2.4. Trypan blue dye discoloration in aqueous culture medium

For the dye degradation test in aqueous medium, three blocks containing 3 × 3 mm mycelium were removed from the edge of each pure strain and transferred to 250 mL Erlenmeyer bottles with 50 mL of dextrose potato medium (DP) plus trypan blue (0.05%). The mixture was homogenized and sterilized in autoclave at 121 °C for 15 min. The vials were incubated at 25 ± 2 °C according to the indications for cultivation of Santana et al. (2020b), and each bottle was considered a replicate. Dye discoloration was analyzed every 20 days from the beginning of the experiment, for a period of 60 days. The mycelium was separated from the culture medium by filtration. The DP medium containing the dye, but without fungi, was used as control of the experiment.

The trypan blue dye discoloration in the aqueous medium was monitored recording the changes of absorbance of the filtrate at different times. The dye discoloration supernatant in aqueous medium was obtained by centrifugation at 10,000 rpm for 5 min, and the record was taken in the maximum spectral range of 590 nm using a visible UV spectrophotometer. The same procedure was performed for the control treatment. The supernatant resulting from this experiment was used in dye toxicity tests.

Discoloration of trypan blue dye was evaluated according to the Formula 1 below:

$$D\left(\%\right)=\left[\left(Af-Ai\right)/Ai\right)*100]$$ (1)

Where Af is the absorbance of the dye treated by the strains of the gasteroid fungi and Ai is the absorbance of the untreated dye.

Culture medium supplementation (DP) was used because it made discoloration more efficient (Chang et al., 2000; Bardi and Marzona, 2010), since azo dyes, in general, have carbon and nitrogen deficiency (Stolz, 2001), elements of great relevance in the development of fungal cultures. Furthermore, supplementation has positive results in the development of Geastrum strains (Santana et al., 2020b).

2.5. Dye phytotoxicity to lettuce after discoloration

The phytotoxicity of the dye trypan blue after the discoloration process by the strains of gasteroid fungi was evaluated in lettuce (Lactuca sativa L.) from the percentage of seed germination and the early development of seedlings. All seeds were sterilized by immersion in 98.2% alcohol, sodium hypochlorite 2% and rinsed abundantly with sterile water five times. Subsequently, four replicates of 25 seeds, totaling 100 seeds per treatment, were packed on a layer of Whatman filter paper in Petri dishes (90 mm diameter) and kept at 25 ± 2 °C.

The seeds received daily waterings of 1 mL of the dye treated by the strains of gasteroid fungi for seven days, when observations were made to calculate the germination percentage and measure the length of the hypocotyl and radicle with a digital caliper. Seeds watered with sterilized distilled water were used as positive control and seeds watered with untreated dye were used as negative control.

2.6. Dye toxicity to Artemia salina after discoloration

Dye toxicity after treatment with gasteroid fungal strains was tested on Artemia salina L larvae. Thus, 0.1 g of A. salina eggs were hatched in 100 mL artificial marine water solution (NaCl 77.23%, MgSO4 9.62%, MgCl 7.13%, CaCl23.32%, KCl 2.11% and NaHCO3 0.59%) in a 500 mL Erlenmayer at 27 ± 2 °C in static mode and under constant illumination.

The test was performed in 1 mL of A. salina larvae of (about 100 individuals per treatment) transferred to test tubes (10 × 200 mm) containing 300 μL of the dye treated by fungal strains. In the positive control, the larvae were submitted only to artificial seawater solution without dye and in the negative control, the larvae were submitted to artificial seawater solution with 300 μL of pure dye. The tubes were kept at 25 ± 2 °C for 24 hours and under constant illumination. After this period, the live larvae were counted with a stereomicroscope to determine the degree of toxicity (GT) of the dye (Harwig and Scott 1971) using the Formula 2 below:

$$GT\left(\%\right)=\left[\left(NIM-TI\right)/TI\right)*100]$$ (2)

Where NIM is the number of individuals killed and TI is the total of individuals in the tube.

The toxicity classification of trypan blue treated by the fungal strains was based on the mortality percentage of the A. salina larvae (Teixeira et al. 2011). Thus, between 0 and 9% mortality, the dye is not considered toxic; between 10 and 49% mortality, the dye is considered slightly toxic; between 50 and 89% mortality, the dye is considered toxic; between 90 and 100% mortality, the dye is considered highly toxic.

2.7. Statistical analysis

The experiments were conducted in a completely randomized design. For the experiments in solid culture medium, the experimental unit consisted of a Petri dish, with five replicates per treatment and for the experiments in aqueous culture medium, the experimental unit was an Erlenmeyer bottle, also with five replicates per treatment. To evaluate the discoloration of the trypan blue and its toxicity after treatment by fungal strains, the means of the experiments were submitted to an analysis of variance (ANOVA) and compared by the Tukey test at the level of 5% significance using the software BioEstat 5.0.

3. Results

The strains of gasteroid fungi developed in the presence of trypan blue surviving toits toxicity and causing its discoloration, even at different intensities. In solid culture medium, after 21 days of observation, Cyathus strains showed the highest discoloration halos of the dye, especially C. albinus strains that reached the edge of the Petri dish in nine days and presented the highest contrast in discoloration (Figure 1A). Among the Geastrum strains, none reached the edge of the Petri dish within the observed period, although the G. hirsutum strains presented the highest halo of discoloration (Figure 1D).

Figure 1
Discoloration halo of trypan blue dye by Amazonian gasteroid fungi after 21 days of observation. A: Cyathus albinus; B: C. limbatus; C. setosus; D: Geastrum hirsutum; E: G. schweinitzii; F: G. echinulatum.

The visual result of dye discoloration by the strains of gasteroid fungi in aqueous medium over time can be seen in Figure 2.

Figure 2
Discoloration aspect of trypan blue dye performed by Amazonian strains of gasteroid fungi in different time periods. CT: Control; A: Cyathus albinus; B: C. setosus; C: C. limbatus; D: Geastrum schweinitzii; E: G. hirsutum; F: G. echinulatum.

Figure 3 shows the performance of gasteroid fungi strains in the discoloration of trypan blue dye in aqueous culture medium over time. The percentage of discoloration varied between the two genera and Cyathus strains presented dye discoloration higher than 90% in the first 20 days of incubation, reaching 96 ± 0.06% (mean ± standard deviation) at the end of 60 days. Likewise, the Geastrum strains differed at 20 days, with the best result observed for G. schweinitzii with 84.7 ± 0.04% (mean ± standard deviation) dye discoloration and the lowest percentage for G. hirsutum with 41.9 ± 0.41% (mean ± standard deviation). At 40 days, the results of G. schweinitzii and G. echinulatum strains were equal to Cyathus strains for dye discoloration. At the end of the 60 days of incubation, all strains of gasteroid fungi showed results above 96% discoloration, especially G. echinulatum which almost completely discolored the dye (98.6 ± 0.08%, mean ± standard deviation).

Figure 3
Discoloration of trypan blue dye in aqueous culture medium by Amazonian gasteroid fungi over time. ■ A: Geastrum hirsutum; ▲ B: Cyathus limbatus; ● C: C. setosus; ■ D: C. albinus; × E: G. schweinitzii; ♦ F: G. echinulatum; + G: Control.

Table 2 presents the dye toxicity after treatment by strains of gasteroid fungi tested on the germination of lettuce seeds, in the early development of seedlings and in the mortality of Artemia salina larvae. At 20 days of incubation, the dye treated by Cyathus strains maintained toxicity similar to untreated dye on seed germination. However, regarding the early development of seedlings, those watered with the dye treated by C. albinus and C. limbatus strains had a higher development when compared to the negative control and were equal to the positive control. Larvae mortality remained the same as negative control for all strains. In the same period, the dye treated by Geastrum strains did not overcome negative control in any toxicity analysis.

Table 2
Trypan blue dye toxicity for seed germination rate (SGR), lettuce seedling development (HL = hypocotyl length and RL = radicle length) and mortality rate of Artemia salina (MRA) larvae after the discoloration treatment by Amazonian strains of gasteroid fungi over time. Data are shown as mean ± standard deviation.

Species	20 days				40 days				60 days
	SGR (%)	HL (mm)	RL (mm)	MRA (%)	SGR (%)	HL (mm)	RL (mm)	MRA (%)	SGR (%)	HL (mm)	RL (mm)	MRA (%)
Positive control1	89a	10.7 ± 3.2b	4.7 ± 2.1b	0a	90a	10.5 ± 3.1c	4.6 ± 2.1c	0a	89a	10.8 ± 3.5c	4.5 ± 2.4c	0a
Negative control2	41b	7.9 ± 4.3c	1,9 ± 0.9d	100b	40b	7.2 ± 3.3d	1,2 ± 0.7f	100d	40d	7.0 ± 4.1d	1.7 ± 0.8e	100d
Cyathus albinus	41b	10.3 ± 1.7b	4.8 ± 0.7b	100b	42b	20.3 ± 2.5a	9.2 ± 1.5a	71.8c	79b	20.1 ± 3.4a	9.5 ± 2.3a	54.8c
C. setosus	40b	3.7 ± 0.5d	3.6 ± 0.5c	100b	40b	7.4 ± 1.9d	4.5 ± 1.1c	100d	42d	18.1 ± 2.2b	8.8 ± 0.7ab	100d
C. limbatus	40b	18.7 ± 0.8a	8.6 ± 3.0a	100b	41b	13.1 ± 2.0b	7.5 ± 1.4b	77b	64c	18.7 ± 0.8b	8.6 ± 3.0b	65b
Geastrum schweinitzii	36c	*	*	100b	37c	6.2 ± 0.9e	3.5 ± 0.5d	100d	41d	7.6 ± 0.7d	3.9 ± 0.6cd	100d
G. hirsutum	25e	*	*	100b	29d	*	*	100d	36e	6.2 ± 1.1d	3.3 ± 0.8d	100d
G. echinulatum	33d	*	*	100b	40b	5.3 ± 0.5f	2.3 ± 0.5e	100d	36e	6.1 ± 2.8d	3.4 ± 1.1d	100d
CV (%)	5.25	22.41	21.84	0.76	5.13	13.12	20.12	1.96	5.13	17.41	21.14	2.54

• ¹
  Watered with distilled water;
• ²
  Watered with untreated trypan blue dye;
• ^*
  Germinated seed without seedling development. CV: Coefficient of Variation; Different letters indicate statistical difference between treatments at 5% significance according to Tukey test.

At 40 days, the germination rate of seeds watered with the dye treated by Cyathus strains remained the same as the negative control. However, seedlings watered with dye treated by C. albinus and C. limbatus strains were twice as effective as positive control and the mortality rate of A. salina larvae was reduced by 29 and 23% respectively. Geastrum strains were not efficient in decreasing the toxicity of the treated dye, since they provided toxicity data similar to the negative control.

At 60 days, the germination rate watered with the dye treated by Cyathus strains was higher than the negative control, except for those watered with the dye treated by C. setosus, which remained equal to the negative control. However, regarding the early development of seedlings, all strains presented higher values than the positive control and the mortality rate of A. salina larvae submitted to the dye treated by C. albinus and C. limbatus was reduced by 46 and 35% respectively. For Geastrum strains, the results of the treated dye toxicity were not satisfactory when compared to the positive control.

4. Discussion

The search for fungi capable of biodegrading synthetic dyes has attracted more attention, especially by the extracellular enzymes that lignin degrading species produce (Ambrosio et al., 2012). Fungi that produce these enzymes can degrade recalcitrant compounds, such as synthetic dyes (Sen et al., 2016), making the species of this study, degrading lignocellulosic substrates, advantageous targets in bioremediation studies. Furthermore, they are widespread, which facilitates the availability of material for future studies. This is the first report on these species with proven activity in the discoloration of trypan blue.

Cyathus strains were the most efficient time-wise, reaching above 90% in the discoloration first analysis, possibly due to the high rates of extracellular enzymes they produced, such as lacase (Pointing, 2001), one of the most widely used in bioprospecting studies involving Cyathus. The production of this enzyme is related to proven activity of dye degradation in C. striatus (Huds.) Willd. (Vasdev et al., 1995), C. stercoreus (Schwein.) De Toni and C. bulleri (Vasdev and Kuhad, 1994; Vasdev et al., 1995; Mishra and Bisaria, 2006) and in some species its production is directly related to mycelial growth (Vasdev and Kuhad, 1994; Sethuraman et al., 1999), similar to other Basidiomycota (Wood, 1980; Rehman and Thurston, 1992).

The performance of Geastrum strains in dye discoloration, although low in the first analyses, increased to the detriment of incubation time and strain development, reaching 98% discoloration at the end of the analyses. This result also suggests that mycelial growth provides greater availability of enzymes capable of degrading dyes. Among these enzymes, Kuhar et al. (2016) observed that the lacaseis produced in greater quantity in Geastrum cultures and its production varies among the species. Santana et al. (2016) reported that the intensity of phenoloxidase production, a group comprising the lacases and other enzymes, in strains of G. lloydianum and G. subculosum was directly related to the type of substrate they degraded, and the higher the enzyme expression, the greater the discoloration halo of the textile dye Remazol Brilliant Blue R (RBBR).

The difference between the two genera regarding time and intensity of discoloration is due to the ecophysiological differences of the species, the preference for substrates (Wicklow et al., 1984), and the conditions of mycelial growth in vitro. For this study Cyathus strains were obtained from basidiomes decomcomposing trunks and branches, which stimulates higher production of lignocellulosic enzymes (Sen et al., 2016), while the Geastrum strains were isolated from basidiomes that grew on leaf litter (personal observations), where the need for enzyme production that degrades lignin is reduced (Wesenberg et al., 2003). In vitro, Cyathus strains showed rapid growth compared to those of Geastrum, as described in the literature (Sunhede, 1989; Zamora et al., 2014).

The difference between the species regarding dye discoloration also reflected in the final result of toxicity. The strains of C. albinus and C. limbatus were efficient in reducing toxicity, proven by increased seed germination and lettuce seedling development. Furthermore, there was a decrease in mortality of A. salina larvae over the analyzed period. For Geastrum strains, the post-treatment result showed that the toxicity remained similar to the untreated dye, both for seed germination and seedling development, although they stimulated the length of the radicle and the mortality of A. salina larvae. This difference is related to the products derived from the degradation process that each species performs (Singh, 2006) and to the incomplete mineralization of the dye (Wang and Hu, 2008).

Strains of Penicillium simplicissimum (Oudem.) have the ability to discolor textile dyes and reduce their toxicity (Bergsten-Torralba et al., 2009), as observed for other fungal species (Martins et al., 2002; Anastasi et al., 2010; Ashrafi et al., 2013). However, Aspergillus niger Tiegh., A. terreus Thom and Rhizopus oligosporus Saito, although quite efficient in discoloration of dyes, produce by-products with high toxicological potential (Almeida and Corso, 2019). These species may produce similar enzymes that act on the discoloration of dyes, like lacase, but other products are also generated during this process (Novotny et al., 2004) in response to the complexity of industrial effluents that, in addition to the dye, contain salts, very high ionic forces or extreme pH values, which may be precursors of toxic by-products for some species (Wesenberg et al., 2003).

Although the lacase enzyme is likely responsible for degrading trypan blue dye, as it was for other synthetic dyes, studies should consider that fungi secrete several other enzymes that together can be even more efficient in the degradation of this dye than purified enzymes (Camarero et al., 2005). The combined effect of the enzymatic system of gasteroid fungi, combined with the cultivation conditions to which the strains were submitted (Santana et al., 2020b), may have occurred in this study, resulting in the different outcomes of the degradation and toxicity of the trypan blue dye. It is possible that other variables, such as supplementation of culture medium, pH, temperature and agitation, may increase or accelerate the enzymatic activity of these species, as reported for other fungi (Asgher et al., 2008; Anastasi et al., 2010; Bibi and Bhatti, 2012).

5. Conclusion

The discovery of new species capable of degrading dyes is relevant as it fosters new perspectives to develop efficient, accessible and safe biotechnologies. Amazonian species of gasteroid fungi, including litter colonizers, have great potential for degradation of azo dye, such as trypan blue. Among them, Cyathus albinus and C. limbatus are promising due to rapid mycelial growth, reduced time to start dye degradation, and the ability to decrease dye toxicity. The Geastrum strains also showed a high degree of efficiency regarding dye discoloration, but require greater attention due to the toxic by-products they produced. Hence, endorsing the need for toxicological tests associated with synthetic dye discoloration experiments. Therefore, there is a need to biotechnologically explore the enzymatic activity of these and other species of gasteroid fungi.

Acknowledgements

The authors thank Universidade Federal do Oeste do Pará (UFOPA) for the logistical support.

References

• ACCIOLY, T., CRUZ, R.H.S.F., ASSIS, N.M., ISHIKAWA, N.K., HOSAKA, K., MARTÍN, M.P. and BASEIA, I.G., 2018. Amazonian bird's nest fungi (Basidiomycota): current knowledge and novelties on Cyathus species. Mycoscience, vol. 59, no. 5, pp. 331-342. http://dx.doi.org/10.1016/j.myc.2017.11.006
  » http://dx.doi.org/10.1016/j.myc.2017.11.006
• ACCIOLY, T., SOUSA, J.O., MOREAU, P.A., LÉCURU, C., SILVA, B.D.B., ROY, M., GARDES, M., BASEIA, I.G. and MARTÍN, M.P., 2019. Hidden fungal diversity from the Neotropics: Geastrum hirsutum, G. schweinitzii (Basidiomycota, Geastrales) and their allies. PLoS One, vol. 14, no. 2, pp. e0211388. http://dx.doi.org/10.1371/journal.pone.0211388 PMid:30726262.
  » http://dx.doi.org/10.1371/journal.pone.0211388
• ALI, N., HAMEED, A. and AHMED, S., 2010. Role of brown-rot fungi in the bioremoval of azo dyes under different conditions. Brazilian Journal of Microbiology, vol. 41, no. 4, pp. 907-915. http://dx.doi.org/10.1590/S1517-83822010000400009 PMid:24031570.
  » http://dx.doi.org/10.1590/S1517-83822010000400009
• ALJADAANI, A.H.A., AHMAD AL-THABAITI, S. and KHAN, Z., 2021. SDS capped Cu nanorods: photosynthesis, stability, and their catalytic activity for trypan blue oxidative degradation. Journal of Materials Research and Technology, vol. 15, pp. 6841-6854. http://dx.doi.org/10.1016/j.jmrt.2021.10.143
  » http://dx.doi.org/10.1016/j.jmrt.2021.10.143
• ALMEIDA, E.J.R. and CORSO, C.R., 2019. Decolorization and removal of toxicity of textile azo dyes using fungal biomass pelletized. International Journal of Environmental Science and Technology, vol. 16, no. 3, pp. 1319-1328. http://dx.doi.org/10.1007/s13762-018-1728-5
  » http://dx.doi.org/10.1007/s13762-018-1728-5
• AMBROSIO, S.T., VILAR-JR, J.C., SILVA, C.A.A., OKADA, K., NASCIMENTO, A.E., LONGO, R.L. and CAMPOS-TAKAKI, G.M., 2012. A biosorption isotherm model for the removal of reactive azo dyes by inactivated mycelia of Cunninghamella elegans UCP542. Molecules (Basel, Switzerland), vol. 17, no. 1, pp. 452-462. http://dx.doi.org/10.3390/molecules17010452 PMid:22217557.
  » http://dx.doi.org/10.3390/molecules17010452
• ANASTASI, A., SPINA, F., PRIGIONE, V., TIGINI, V., GIANSANTI, P. and VARESE, G.C., 2010. Scale-up of a bioprocess for textile wastewater treatment using Bjerkandera adusta. Bioresource Technology, vol. 101, no. 9, pp. 3067-3075. http://dx.doi.org/10.1016/j.biortech.2009.12.067 PMid:20071167.
  » http://dx.doi.org/10.1016/j.biortech.2009.12.067
• ASGHER, M., BHATTI, H.N., ASHRAF, M. and LEGGE, R.L., 2008. Recent developments in biodegradation of industrial pollutants by white rot fungi and their enzyme system. Biodegradation, vol. 19, no. 6, pp. 771-783. http://dx.doi.org/10.1007/s10532-008-9185-3 PMid:18373237.
  » http://dx.doi.org/10.1007/s10532-008-9185-3
• ASHRAFI, S.D., REZAEI, S., FOROOTANFAR, H., MAHVI, A.H. and FARAMARZI, M.A., 2013. The enzymatic decolorization and detoxification of synthetic dyes by the laccase from a soil-isolated ascomycete, Paraconiothyrium variabile. International Biodeterioration & Biodegradation, vol. 85, pp. 173-181. http://dx.doi.org/10.1016/j.ibiod.2013.07.006
  » http://dx.doi.org/10.1016/j.ibiod.2013.07.006
• ASSIS, N.M., GÓIS, J.S., FREITAS-NETO, F.J., BARBOSA, F.R. and BASEIA, I.G., 2022. Checklist of Amazonian gasteroid fungi (Agaricomycetidae, Phallomycetidae, Basidiomycota). Acta Amazonica, vol. 52, no. 2, pp. 131-141. http://dx.doi.org/10.1590/1809-4392202101730
  » http://dx.doi.org/10.1590/1809-4392202101730
• BARDI, L. and MARZONA, M., 2010. Factors affecting the complete mineralization of azo dyes. In H. ATACAG ERKURT, ed. Biodegradation of azo dyes. The Handbook of Environmental Chemistry Berlin: Springer-Verlag, pp. 195-210. http://dx.doi.org/10.1007/698_2009_50
  » http://dx.doi.org/10.1007/698_2009_50
• BERGSTEN-TORRALBA, L.R., NISHIKAWA, M.M., BAPTISTA, D.F., MAGALHÃES, D.P. and DA SILVA, M., 2009. Decolorization of different textile dyes by Penicillium simplicissimum and toxicity evaluation after fungal treatment. Brazilian Journal of Microbiology, vol. 40, no. 4, pp. 808-817. http://dx.doi.org/10.1590/S1517-83822009000400011 PMid:24031428.
  » http://dx.doi.org/10.1590/S1517-83822009000400011
• BIBI, I. and BHATTI, H.N., 2012. Enhanced biodecolorization of reactive dyes by basidiomycetes under static conditions. Applied Biochemistry and Biotechnology, vol. 166, no. 8, pp. 2078-2090. http://dx.doi.org/10.1007/s12010-012-9635-6 PMid:22437723.
  » http://dx.doi.org/10.1007/s12010-012-9635-6
• BROWN, J.P., ROEHM, G.W. and BROWN, R.J., 1978. Mutagenicity testing of certified food colors and related azo, xanthene and triphenylmethane dyes with the Salmonella/microsome system. Mutation Research, vol. 56, no. 3, pp. 249-271. http://dx.doi.org/10.1016/0027-5107(78)90192-6 PMid:342943.
  » http://dx.doi.org/10.1016/0027-5107(78)90192-6
• CALONGE, F.D., MATA, M. and CARRANZA, J., 2005. Contribución al catálogo de los Gasteromycetes (Basidiomycotina, Fungi) de Costa Rica. Anales del Jardin Botanico de Madrid, vol. 62, no. 1, pp. 23-45. http://dx.doi.org/10.3989/ajbm.2005.v62.i1.26
  » http://dx.doi.org/10.3989/ajbm.2005.v62.i1.26
• CAMARERO, S., IBARRA, D., MARTÍNEZ, J.M. and MARTÍNEZ, T.A., 2005. Lignin-derived compounds as efficient laccase mediators for decolorization of different types of recalcitrant dyes. Applied and Environmental Microbiology, vol. 71, no. 4, pp. 1775-1784. http://dx.doi.org/10.1128/AEM.71.4.1775-1784.2005 PMid:15812000.
  » http://dx.doi.org/10.1128/AEM.71.4.1775-1784.2005
• CERETTA, M.B., NERCESSIAN, D. and WOLSKI, E.A., 2021. Current trends on role of biological treatment in integrated treatment technologies of textile Wastewater. Frontiers in Microbiology, vol. 12, pp. 651025. http://dx.doi.org/10.3389/fmicb.2021.651025 PMid:33841377.
  » http://dx.doi.org/10.3389/fmicb.2021.651025
• CHANG, I.S., SHIN, P.K. and KIM, B.H., 2000. Biological treatment of acid mine drainage under sulphate-reducing conditions with solid waste materials as substrate. Water Research, vol. 34, no. 4, pp. 1269-1277. http://dx.doi.org/10.1016/S0043-1354(99)00268-7
  » http://dx.doi.org/10.1016/S0043-1354(99)00268-7
• CHUNG, K.T., 2016. Azo dyes and human health: a review. Journal of Environmental Science and Health. Part C, Environmental Carcinogenesis & Ecotoxicology Reviews, vol. 34, no. 4, pp. 233-261. http://dx.doi.org/10.1080/10590501.2016.1236602 PMid:27635691.
  » http://dx.doi.org/10.1080/10590501.2016.1236602
• COETZE, J.C. and VAN WYK, A.E., 2009. The genus Calvatia (‘Gasteromycetes’, Lycoperdaceae): a review of its ethnomycology and biotechnological potential. African Journal of Biotechnology, vol. 8, no. 22, pp. 6007-6015.
• COOKSEY, C.J., 2014. Quirks of dye nomenclature. 2. Congo red. Biotechnic & Histochemistry, vol. 89, no. 5, pp. 384-387. http://dx.doi.org/10.3109/10520295.2014.880513
  » http://dx.doi.org/10.3109/10520295.2014.880513
• DORE, C.M.G., AZEVEDO, T.C., DE SOUZA, M.C., REGO, L.A., DE DANTAS, J.C., SILVA, F.R., ROCHA, H.A.O., BASEIA, I.G. and LEITE, E.L., 2007. Antiinflammatory, antioxidant and cytotoxic actions of β-glucan-rich extract from Geastrum saccatum mushroom. International Immunopharmacology, vol. 7, no. 9, pp. 1160-1169. http://dx.doi.org/10.1016/j.intimp.2007.04.010 PMid:17630194.
  » http://dx.doi.org/10.1016/j.intimp.2007.04.010
• FERREIRA-SÁ, A.S., LEONARDO-SILVA, L., CORTEZ, V.G. and XAVIER-SANTOS, S., 2021. Second world record for two Calvatia species (Agaricaceae: basidiomycota). Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 83, pp. e247840. http://dx.doi.org/10.1590/1519-6984.247840 PMid:34190767.
  » http://dx.doi.org/10.1590/1519-6984.247840
• FIELD, F.E., ROBERTS, G., HALLOWES, R.C., PALMER, A.K., WILLIAMS, K.E. and ELOYD, J.B., 1977. Trypan blue: identification and teratogenic and oncogenic activities of its coloured constituents. Chemico-Biological Interactions, vol. 16, no. 1, pp. 69-88. http://dx.doi.org/10.1016/0009-2797(77)90154-5 PMid:837466.
  » http://dx.doi.org/10.1016/0009-2797(77)90154-5
• FREITAS, I.L.F.S., GÓIS, J.S., FREITAS-NETO, J.F., ASSIS, N.M., BARBOSA, F.R. and BASEIA, I.G., 2023. New records of Geastrum (Geastrales, Basidiomycota) for the Amazon. Acta Amazonica, vol. 53, no. 1, pp. 56-60. http://dx.doi.org/10.1590/1809-4392202201541
  » http://dx.doi.org/10.1590/1809-4392202201541
• GHIME, D. and GHOSH, P., 2020. Decolorization of diazo dye trypan blue by electrochemical oxidation: kinetics with a model based on the Fermi’s equation. Journal of Environmental Chemical Engineering, vol. 8, no. 1, pp. 102792. http://dx.doi.org/10.1016/j.jece.2018.11.037
  » http://dx.doi.org/10.1016/j.jece.2018.11.037
• GÓIS, J.S., CRUZ, R.H.S.F. and BASEIA, I.G., 2021. Taxonomic review and updates of the genus Cyathus (Agaricales, Basidiomycota) from Brazil. The Journal of the Torrey Botanical Society, vol. 148, no. 3, pp. 155-196.
• GREGORIO, S.D., BALESTRI, F., BASILE, M., MATTEINI, V., GINI, F., GIANSANTI, S., TOZZI, M.G., BASOSI, R. and LORENZI, R., 2010. Sustainable discoloration of textile chromo-baths by spent mushroom substrate from the industrial cultivation of Pleurotus ostreatus. Journal of Environmental Protection, vol. 1, no. 2, pp. 85-94. http://dx.doi.org/10.4236/jep.2010.12011
  » http://dx.doi.org/10.4236/jep.2010.12011
• HARWIG, J. and SCOTT, P.M., 1971. Brine Shrimp (Artemia salina L.) larvae as a screening system for fungal toxins. Applied Microbiology, vol. 21, no. 6, pp. 1011-1016. http://dx.doi.org/10.1128/am.21.6.1011-1016.1971
  » http://dx.doi.org/10.1128/am.21.6.1011-1016.1971
• HASSAAN, M.A. and NEMR, A.E., 2017. Health and environmental impacts of dyes: mini review. American Journal of Environmental Science and Engineering, vol. 1, pp. 64-67. http://dx.doi.org/10.11648/j.ajese.20170103.11
  » http://dx.doi.org/10.11648/j.ajese.20170103.11
• ISLAM, M.M., MAHMUD, K., FARUK, O. and BILLAH, S., 2011. Assessment of environmental impacts for textile dyeing industries in Bangladesh. In: International Conference on Green Technology and Environmental Conservation, 2011, Chennai, India. USA: IEEE, pp. 173-181. http://dx.doi.org/10.1109/GTEC.2011.6167665
  » http://dx.doi.org/10.1109/GTEC.2011.6167665
• JARDIM BOTÂNICO DO RIO DE JANEIRO – JBRJ, 2023 [viewed 2 April 2023]. JABOT [online]. Available from: http://hstm.jbrj.gov.br/v2/consulta.php
  » http://hstm.jbrj.gov.br/v2/consulta.php
• KANAGARAJ, J., SENTHILVELAN, T. and PANDA, R.C., 2015. Degradation of azo dyes by laccase: biological method to reduce pollution load in dye wastewater. Clean Technologies and Environmental Policy, vol. 17, no. 6, pp. 1443-1456. http://dx.doi.org/10.1007/s10098-014-0869-6
  » http://dx.doi.org/10.1007/s10098-014-0869-6
• KEOGH, R.C., DEVERALL, B.J. and MCLEOD, S., 1980. Comparison of histological and physiological responses to Phakopsora pachyrhizi in resistant and susceptible soybean. Transactions of the British Mycological Society, vol. 74, no. 2, pp. 329-333. http://dx.doi.org/10.1016/S0007-1536(80)80163-X
  » http://dx.doi.org/10.1016/S0007-1536(80)80163-X
• KODJIKIAN, L., RICHTER, T., HALBERSTADT, M., BEBY, F., FLUECKIGER, F., BOEHNKE, M. and GARWEG, J.G., 2005. Toxic effects of indocyanine green, infracyanine green, and trypan blue on the human retinal pigmented epithelium. Graefes Archive for Clinical and Experimental Ophthalmology, vol. 243, no. 9, pp. 917-925. http://dx.doi.org/10.1007/s00417-004-1121-6 PMid:15834606.
  » http://dx.doi.org/10.1007/s00417-004-1121-6
• KUHAR, F., CASTIGLIA, V.C. and ZAMORA, J.C., 2016. Detection of manganese peroxidase and other exoenzymes in four isolates of Geastrum (Geastrales) in pure culture. Revista Argentina de Microbiologia, vol. 48, no. 4, pp. 274-278. http://dx.doi.org/10.1016/j.ram.2016.09.002 PMid:27916329.
  » http://dx.doi.org/10.1016/j.ram.2016.09.002
• LEE, W.P.C., WONG, F.H., ATTENBOROUGH, N.K., KONG, X.Y., TAN, L.L., SUMATHI, S. and CHAI, S.P., 2017. Two-dimensional bismuth oxybromide coupled with molybdenum disulphide for enhanced dye degradation using low power energy-saving light bulb. Journal of Environmental Management, vol. 197, pp. 63-69. http://dx.doi.org/10.1016/j.jenvman.2017.03.027 PMid:28324782.
  » http://dx.doi.org/10.1016/j.jenvman.2017.03.027
• LIESCHE, J., MAREK, M. and GÜNTHER-POMORSKI, T., 2015. Cell wall staining with trypan blue enables quantitative analysis of morphological changes in yeast cells. Frontiers in Microbiology, vol. 6, pp. 107. http://dx.doi.org/10.3389/fmicb.2015.00107 PMid:25717323.
  » http://dx.doi.org/10.3389/fmicb.2015.00107
• LIU, Y.J. and ZHANG, K.Q., 2004. Antimicrobial activities of selected Cyathus species. Mycopathologia, vol. 157, no. 2, pp. 185-189. http://dx.doi.org/10.1023/B:MYCO.0000020598.91469.d1 PMid:15119855.
  » http://dx.doi.org/10.1023/B:MYCO.0000020598.91469.d1
• LODGE, D.J., AMMIRATI, J.F., O’DELL, T.E. and MUELLER, G.M., 2004. Collecting and describing macrofungi. In: G.M. MUELLER, G.F. BILLS and M.S. FOSTER, eds. Biodiversity of fungi: inventory and monitoring methods Cambridge: Academic Press, pp. 128-158.
• MARTINS, M.A.M., QUEIROZ, M.J., SILVESTRE, A.J.D. and LIMA, N., 2002. Relationship of chemical structures of textile dyes on the pre-adaptation medium and the potentialities of their biodegradation by Phanerochaete chrysosporium. Research in Microbiology, vol. 153, no. 6, pp. 361-368. http://dx.doi.org/10.1016/S0923-2508(02)01332-3 PMid:12234010.
  » http://dx.doi.org/10.1016/S0923-2508(02)01332-3
• MISHRA, S.S. and BISARIA, V.S., 2006. Production and characterization of laccase from Cyathus bulleri and its use in decolourization of recalcitrant textile dyes. Applied Microbiology and Biotechnology, vol. 71, no. 5, pp. 646-653. http://dx.doi.org/10.1007/s00253-005-0206-4 PMid:16261367.
  » http://dx.doi.org/10.1007/s00253-005-0206-4
• MOURID, E., LAKRAIMIL, M., KHATTABI, E., EL-BENAZIZ, L. and BERRAHO, M., 2017. Removal of remazol brilliant blue R from aqueous solution by adsorption using a calcined layered double hydroxides [Zn2-Al-CO3]. Journal of Materials and Environmental Sciences, vol. 8, pp. 921-930.
• MUELLER, G.M., SCHMIT, J.P., LEACOCK, P.R., BUYCK, B., CIFUENTES, J., DESJARDIN, D.E., HALLING, R.E., HJORTSTAM, K., ITURRIAGA, T., LARSSON, K.H., LODGE, D.J., MAY, T.W., MINTER, D., RAJCHENBERG, M., REDHEAD, S.A., RYVARDEN, L., TRAPPE, J.M., WATLING, R. and WU, Q., 2007. Global diversity and distribution of macrofungi. Biodiversity and Conservation, vol. 16, no. 1, pp. 37-48. http://dx.doi.org/10.1007/s10531-006-9108-8
  » http://dx.doi.org/10.1007/s10531-006-9108-8
• NADAROGLU, H., CICEK, S. and GUNGOR, A.A., 2017. Removing Trypan blue dye using nano-Zn modified Luffa sponge. Spectrochimica Acta. Part A: Molecular and Biomolecular Spectroscopy, vol. 172, pp. 2-8. http://dx.doi.org/10.1016/j.saa.2016.08.052 PMid:27592334.
  » http://dx.doi.org/10.1016/j.saa.2016.08.052
• NOVOTNÝ, Č., SVOBODOVÁ, K., KASINATH, A. and ERBANOVÁ, P., 2004. Biodegradation of synthetic dyes by Irpex lacteus under various growth conditions. International Biodeterioration & Biodegradation, vol. 54, no. 2-3, pp. 215-223. http://dx.doi.org/10.1016/j.ibiod.2004.06.003
  » http://dx.doi.org/10.1016/j.ibiod.2004.06.003
• NOZAKI, K., BEH, C.H., MIZUNO, M., ISOBE, T., SHIROISHI, M., KANDA, T. and AMANO, Y., 2008. Screening and investigation of dye decolorization activities of basidiomycetes. Journal of Bioscience and Bioengineering, vol. 105, no. 1, pp. 69-72. http://dx.doi.org/10.1263/jbb.105.69 PMid:18295724.
  » http://dx.doi.org/10.1263/jbb.105.69
• PHILLIPS, J.M. and HAYMAN, D.S., 1970. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society, vol. 55, no. 1, pp. 158-161. https://dx.doi.org/10.1016/S0007-1536(70)80110-3.
• POINTING, S.B., 2001. Feasibility of bioremediation by white-rot fungi. Applied Microbiology and Biotechnology, vol. 57, no. 1-2, pp. 20-33. http://dx.doi.org/10.1007/s002530100745 PMid:11693920.
  » http://dx.doi.org/10.1007/s002530100745
• REHMAN, A.U. and THURSTON, C.F., 1992. Purification of laccase I from Armillaria mellea. Journal of General Microbiology, vol. 138, no. 6, pp. 1251-1257. http://dx.doi.org/10.1099/00221287-138-6-1251
  » http://dx.doi.org/10.1099/00221287-138-6-1251
• ROBERTSON, J.A., HARRIS, W.J. and MCGREGOR, D.B., 1982. Mutagenicity of azo dyes in the Salmonella/activation test. Carcinogenesis, vol. 3, no. 1, pp. 21-23. http://dx.doi.org/10.1093/carcin/3.1.21 PMid:7039853.
  » http://dx.doi.org/10.1093/carcin/3.1.21
• SANTANA, M.D.F. and COUCEIRO, S.R.M., 2023. First record of Sphaerobolus stellatus Tode (Basidiomycota, Geastraceae) from the Amazon, Brazil. Acta Brasiliensis, vol. 7, no. 1, pp. 31-32. http://dx.doi.org/10.22571/2526-4338617
  » http://dx.doi.org/10.22571/2526-4338617
• SANTANA, M.D.F., LARA, T.S. and COUCEIRO, S.R.M., 2020a. Alternative and safe dyes for staining Arbuscular Mycorrhizal fungi. Revista Ibero Americana de Ciências Ambientais, vol. 11, no. 7, pp. 400-408. http://dx.doi.org/10.6008/CBPC2179-6858.2020.007.0032
  » http://dx.doi.org/10.6008/CBPC2179-6858.2020.007.0032
• SANTANA, M.D.F., RODRIGUES, L.D.S.I., AMARAL, T.S. and PINHEIRO, Y.G., 2016. Fenoloxidase e biodegradação do corante têxtil Azul Brilhante de Remazol R (RBBR) para três espécies de macrofungos coletadas na Amazônia. SaBios-Revista de Saúde e Biologia, vol. 11, pp. 53-60.
• SANTANA, M.D.F., VARGAS-ISLA, R., NOGUEIRA, J.C., ACCIOLY, T., SILVA, B.D.B., COUCEIRO, S.R.M., BASEIA, I.G. and ISHIKAWA, N.K., 2020b. Obtaining monokaryotic and dikaryotic mycelial cultures of two Amazonian strains of Geastrum (Geastraceae, Basidiomycota). Acta Amazonica, vol. 50, no. 1, pp. 61-67. http://dx.doi.org/10.1590/1809-4392201901341
  » http://dx.doi.org/10.1590/1809-4392201901341
• SARATALE, R.G., SARATALE, G.D., KALYANI, D.C., CHANG, J.S. and GOVINDWAR, S.P., 2009a. Enhanced decolorization and biodegradation of textile azo dye Scarlet R by using developed microbial consortium-GR. Bioresource Technology, vol. 100, no. 9, pp. 2493-2500. http://dx.doi.org/10.1016/j.biortech.2008.12.013 PMid:19157864.
  » http://dx.doi.org/10.1016/j.biortech.2008.12.013
• SARATALE, R.G., SARATALE, G.D., PARSHETTI, G.K., CHANG, J.S. and GOVINDWAR, S.P., 2009b. Bacterial decolorization and degradation of Azo Dyes: a review. Journal of the Taiwan Institute of Chemical Engineers, vol. 42, no. 1, pp. 138-157. http://dx.doi.org/10.1016/j.jtice.2010.06.006
  » http://dx.doi.org/10.1016/j.jtice.2010.06.006
• SEN, S.K., RAUT, S., BANDYOPADHYAY, P. and RAUT, S., 2016. Fungal decolouration and degradation of azo dyes: a review. Fungal Biology Reviews, vol. 30, no. 3, pp. 112-133. http://dx.doi.org/10.1016/j.fbr.2016.06.003
  » http://dx.doi.org/10.1016/j.fbr.2016.06.003
• SETHURAMAN, A., AKIN, D.E. and ERIKSSON, K.E.L., 1999. Production of ligninolytic enzymes and synthetic lignin mineralization by the bird’s nest fungus Cyathus stercoreus. Applied Microbiology and Biotechnology, vol. 52, no. 5, pp. 689-697. http://dx.doi.org/10.1007/s002530051580 PMid:10570816.
  » http://dx.doi.org/10.1007/s002530051580
• SILVA, A.L.M., SANTANA, M.D.F., PEREIRA, J.C.J., RAIMAM, M.P. and ALBINO, U.B., 2015. Amazonian açai and food dyes for staining arbuscular-micorrhizal fungi. Pesquisa Florestal Brasileira, vol. 35, no. 84, pp. 475-479. http://dx.doi.org/10.4336/2015.pfb.35.84.798
  » http://dx.doi.org/10.4336/2015.pfb.35.84.798
• SILVA, B.D.B., CABRAL, T.S., MARINHO, P., ISHIKAWA, N.K. and BASEIA, I.G., 2013. Two new species of Geastrum (Geastraceae, Basidiomycota) found in Brazil. Nova Hedwigia, vol. 96, no. 3-4, pp. 445-456. http://dx.doi.org/10.1127/0029-5035/2013/0089
  » http://dx.doi.org/10.1127/0029-5035/2013/0089
• SINGH, H., 2006. Mycoremediation: fungal bioremediation Hoboken: Wiley, 616 p. http://dx.doi.org/10.1002/0470050594
  » http://dx.doi.org/10.1002/0470050594
• SOUSA, J.O., MORAIS, L.A., NASCIMENTO, Y.M. and BASEIA, I.G., 2014. Updates on the geographic distribution of three Geastrum species from Brazilian semi-arid region. Mycosphere: Journal of Fungal Biology, vol. 5, no. 3, pp. 467-474. http://dx.doi.org/10.5943/mycosphere/5/3/9
  » http://dx.doi.org/10.5943/mycosphere/5/3/9
• STOLZ, A., 2001. Basic and applied aspects in the microbial degradation of azo dyes. Applied Microbiology and Biotechnology, vol. 56, no. 1-2, pp. 69-80. http://dx.doi.org/10.1007/s002530100686 PMid:11499949.
  » http://dx.doi.org/10.1007/s002530100686
• SUNHEDE, S., 1989. Geastraceae (Basidiomycotina): morphology, ecology and systematics with special emphasis on the North European species Oslo: Fungiflora, 534 p. Synopsis Fungorum, no. 1.
• TANG, A.Y.L., LO, C.K.Y. and KAN, C.W., 2021. Textile dyes and human health: a systematic and citation network analysis review. Coloration Technology, vol. 134, no. 4, pp. 245-257. http://dx.doi.org/10.1111/cote.12331
  » http://dx.doi.org/10.1111/cote.12331
• TEIXEIRA, M.F.S., SILVA, T.A., PALHETA, R.A., CARNEIRO, L.B. and ATAYDE, H.M., eds., 2011. Fungos da Amazônia: uma riqueza inexplorada. Aplicações biotecnológicas. Manaus: Editora da Universidade Federal do Amazonas, 255 p.
• VASDEV, K. and KUHAD, R.C., 1994. Decolorization of PolyR-478 (polyvinylamine sulfonate anthrapyridone) by Cyathus bullen. Folia Microbiologica, vol. 39, no. 1, pp. 61-64. http://dx.doi.org/10.1007/BF02814532
  » http://dx.doi.org/10.1007/BF02814532
• VASDEV, K., KUHAD, R.C. and SAXENA, R.K., 1995. Decolorization of triphenylmethane dyes by the bird’s nest fungus Cyathus bulleri. Current Microbiology, vol. 30, no. 5, pp. 269-272. http://dx.doi.org/10.1007/BF00295500
  » http://dx.doi.org/10.1007/BF00295500
• VIERHEILIG, H., SCHWEIGER, P. and BRUNDRETT, M., 2005. An overview of methods for the detection and observation of arbuscular mycorrhizal fungi in roots. Physiologia Plantarum, vol. 125, no. 4, pp. 393-404. http://dx.doi.org/10.1111/j.1399-3054.2005.00564.x
  » http://dx.doi.org/10.1111/j.1399-3054.2005.00564.x
• WANG, B.E. and HU, Y.Y., 2008. Bioaccumulation versus adsorption of reactive dye by immobilized growing Aspergillus fumigatus beads. Journal of Hazardous Materials, vol. 157, no. 1, pp. 1-7. http://dx.doi.org/10.1016/j.jhazmat.2007.12.069 PMid:18242834.
  » http://dx.doi.org/10.1016/j.jhazmat.2007.12.069
• WANG, Y., SUN, X., HAN, Q., JAMES, T.D. and WANG, X., 2021. Highly sensitive and selective water-soluble fluorescent probe for the alternative detections of formaldehyde in Leather Products. Dyes and Pigments, vol. 188, pp. 109175. http://dx.doi.org/10.1016/j.dyepig.2021.109175
  » http://dx.doi.org/10.1016/j.dyepig.2021.109175
• WEISBURGER, J.J. and WEISBURGER, E.K., 1966. Chemicals as cause of cancer. Chemical and Engineering News, vol. 44, no. 6, pp. 124-142. http://dx.doi.org/10.1021/cen-v044n006.p124
  » http://dx.doi.org/10.1021/cen-v044n006.p124
• WESENBERG, D., KYRIAKIDES, I. and AGATHOS, S.N., 2003. White-rot fungi and their enzymes for the treatment of industrial dye effluents. Biotechnology Advances, vol. 22, no. 1-2, pp. 161-187. http://dx.doi.org/10.1016/j.biotechadv.2003.08.011 PMid:14623049.
  » http://dx.doi.org/10.1016/j.biotechadv.2003.08.011
• WICKLOW, D.T., LANGIE, R., CRABTREE, S. and DETROY, R.W., 1984. Degradation of lignocellulose in wheat straw versus hardwood by Cyathus and related species (Nidulariaceae). Canadian Journal of Microbiology, vol. 30, no. 5, pp. 632-636. http://dx.doi.org/10.1139/m84-093
  » http://dx.doi.org/10.1139/m84-093
• WOOD, D.A., 1980. Production, purification and properties of extracellular laccase of Agariczis bisporzds. Microbiology, vol. 117, no. 2, pp. 327-338. http://dx.doi.org/10.1099/00221287-117-2-327
  » http://dx.doi.org/10.1099/00221287-117-2-327
• ZAMORA, J.C., CALONGE, F.D., HOSAKA, K. and MARTIN, M.P., 2014. Systematics of the genus Geastrum (Fungi: Basidiomycota) revisited. Taxon, vol. 63, no. 3, pp. 477-497. http://dx.doi.org/10.12705/633.36
  » http://dx.doi.org/10.12705/633.36

Publication Dates

• Publication in this collection
  20 Nov 2023
• Date of issue
  2023

History

• Received
  14 Aug 2023
• Accepted
  22 Sept 2023