Marine-derived fungus Paramarasmius palmivorus CBMAI 1062 applied to sulphur indigo blue decolorization, degradation and detoxification

Abstract

The use of marine microorganisms in the treatment of dyes and textile effluents is promising in view of their tolerance to salinity, a characteristic found in this kind of effluent. In this study, different culture conditions were applied to evaluate the decolorization, degradation, and detoxification of Sulphur Indigo Blue (SIB) by the marine-derived basidiomycete Paramarasmius palmivorus CBMAI 1062. Low salt concentration (SLS) and high salt concentration (SMASHS) media were used. P. palmivorus decolorized 100 % and 91.38 % of SIB after 120 h of growth in the SLS medium and after 168 h of growth in the SMASHS medium, respectively. Laccase activity was detected only in the SLS bioassay. UV-Vis, FT-IR, and GC-MS analyses indicated the occurrence of dye biosorption and biotransformation. In the SLS medium metabolites associated with SIB biotransformation (e.g. aldehyde, alkanes, and phenols) were detected. The toxicity measured by Cucumis sativus decreased from 45.41 % to 24.11 % in the SLS bioassay, while in SMASHS medium there was no change in toxicity. The efficiency for decolorization and detoxification of SIB indicates that microorganisms from the marine environment can be a source for biotechnological application in bioremediation processes carried out under saline conditions, adding value to blue biotechnology.

Key words bioremediation; environmental biotechnology; marine mycology; phytotoxicity; textile dyes

INTRODUCTION

The textile industry produces large amounts of effluents composed of dyes, salts, surfactants, chlorine compounds, and suspended solids. Although all these substances are potentially toxic to the environment, dyes are considered the main environmental pollutants, partially because dyes can affect water transparency, even at small concentrations (Khandegar & Saroha 2013, Sharma et al. 2021). Consequently, photosynthetic organisms in water bodies do not receive adequate light and are detrimental to the entire food chain. In addition, some dyes are toxic and mutagenic and may affect water quality for consumption, irrigation, and recreation. Furthermore, they cause deleterious effects on fauna, flora, and microbiome when in contact with polluted water (Hubbe et al. 2012, Przystaś et al. 2012, Tkaczyk et al. 2020).

Sulfur Indigo Blue dye, analogous to indigo carmine, is applied to dye cotton yarns used mainly to manufacture denim fabric. About 5 % to 20 % of the dye is lost during dyeing. Direct wastewater discharge in the environment can cause severe problems to aquatic biological processes (Sousa et al. 2008, Berradi et al. 2019). To avoid the environmental damage caused by indigo carmine, many studies have focused on the use of physicochemical techniques, including adsorption (Ahmed et al. 2017, Harrache et al. 2019), photodegradation (Güy & Özacar 2018, Prado et al. 2008), ozonation (Qu et al. 2015), electrochemical oxidation (Labiadh et al. 2017), and heterogeneous Fenton system (Zhou et al. 2016). Although the application of these approaches can achieve high decolorization rates of indigo carmine, physicochemical techniques should not be preferred since they can result in secondary pollution (Chowdhury et al. 2020).

Previous studies related to biological treatments of indigo carmine reported the potential of microorganisms for the degradation of this textile dye, including the bacteria Stenotrophomonas sp. CFB-09 (Olajuyigbe et al. 2022) and Bacillus sp. MZS10 (Li et al. 2015b), the yeast Diutina rugosa (Bankole et al. 2017), the filamentous fungus Ganoderma sp. En3 (Lu et al. 2016) and the white rot fungus Cyathus bulleri Brodie DAOMC 195062 (Ahlawat et al. 2022). Despite being capable of degrading the indigo carmine dye molecule, most of these and other microorganisms have been in a non-saline condition. Since many microorganisms have no adaptation to salinity and considering that textile effluents have a variety of dissolved salts (Tomei et al. 2016, Yaseen & Scholz 2019), studies aiming at the decolorization of textile dyes and/or effluent under saline conditions are relevant. Additionally, halophile microorganisms have advantages for industrial biotechnology mainly due to low energy and less fresh water consumption in bioprocessing (Yin et al. 2015, Kalpana et al. 2020, Fontes et al. 2021).

White rot fungi basidiomycetes are highly efficient in environmental pollutant degradation. The non-specific mechanisms used by these fungi to degrade lignin enable them to act also in the degradation of other molecules composed of aromatic rings, such as textile dyes (Bazanella et al. 2014, Dharajiya et al. 2016, Kurade et al. 2017, Moreira-Neto et al. 2013). In this sense, white rot fungi of marine origin have advantages in saline processes in relation to their terrestrial counterparts (Dash et al. 2013, Bonugli-Santos et al. 2015, Fontes et al. 2021) being the subject of studies focused on the production of ligninolytic enzymes and bioremediation of environmental pollutants under saline conditions (Bonugli-Santos et al. 2010a, b, 2012, Vieira et al. 2021, Yuan et al. 2021, Hadibarata et al. 2022).

Manganese peroxidase (MnP) and laccase (Lac) are the main ligninolytic enzymes applied for indigo carmine degradation. Li et al. (2015a) and Zhang et al. (2016) used the MnP produced by Phanerochaete chrysosporium CICC 40719 and Trametes sp. 48424, respectively, to decolorize indigo carmine. On the other hand, Campos et al. (2001), Jasińska et al. (2018) and He et al. (2015) used Lac from Trametes hirsuta (THL1 and THL2) and Sclerotium rolfsii SRL1, Mirothecium roridum IM 6482 and Ganoderma sp. En3, respectively, to this same dye decolorization.

Considering that the production of ligninolytic enzymes varies according to the microbial culture conditions and that microorganisms with an enzymatic apparatus capable of degrading pollutants under saline conditions represent a promising alternative for the bioremediation of textile dyes and effluents, this study aimed to apply the marine-derived white rot fungus P. palmivorus CBMAI 1062 for the decolorization, degradation, and detoxification of Sulphur Indigo Blue (SIB) textile dye under different culture and saline conditions.

MATERIALS AND METHODS

Microorganism

Paramarasmius palmivorus CBMAI 1062 (former Marasmius palmivorus > former Marasmiellus palmivorus) was isolated by Menezes et al. (2010) from the marine sponge Amphimedon viridis, collected at São Sebastião city, northern coast of São Paulo state, Brazil. The fungus was previously identified as reported by Bonugli-Santos et al. (2010a) and is deposited in the following microbial culture collections: Brazilian Collection of Environmental and Industrial Microorganisms (CBMAI) (CPQBA, Campinas State University – UNICAMP, Campinas, SP, Brazil) under the acronym CBMAI 1062 and UNESP’s Central of Microbial Resource (CRM-UNESP) (Biosciences Institute, São Paulo State University – UNESP, Rio Claro, SP, Brazil) under the acronym CRM 593.

Culture conditions for textile dye decolorization, degradation, and detoxification

Considering that culture conditions directly affect microbial performance in the degradative process, two different media were used to evaluate the dye decolorization, degradation, and detoxification by the marine-derived fungus P. palmivorus CBMAI 1062: a simple medium (SLS) and a more complex medium (SMASHS). At first, the fungus was cultivated in malt extract agar (20 g L^-1 malt extract, 20 g L^-1 agar) for seven days at 28 °C. Three fungal culture discs (0.5 cm diameter) from the edge of the colony were transferred to 50 mL conical tubes containing 15 mL of malt extract 1.5 % at 28 °C and 140 rpm. After 48 h, the growth colony (inoculum) was transferred aseptically to 125 mL Erlenmeyer flasks containing 50 mL of the two different media: i) SLS (sucrose and low salt concentration) broth medium: composed of 400 mg L^-1 SIB, 10 g L^-1 sucrose, and 5 g L^-1 NaCl (lower salt condition), and ii) SMASHS (sucrose, malt extract, ammonium sulfate, and higher salt concentration) broth medium: composed of 400 mg L^-1 SIB, 6 g L^-1 sucrose, 6 g L^-1 malt extract, 1 g L^-1 (NH4)₂SO₄, and 30 g L^-1 NaCl (higher salt condition). Both media were autoclaved at 1 atm for 15 min. After inoculation, the flasks were incubated at 28 °C and 140 rpm for 12, 24, 72, and 120 h. Bioassay conducted with the SMASHS medium was also analyzed after 168 h of incubation. All experiments were carried out in triplicate. Flasks cultured under the same conditions without the fungus addition were considered as control (time zero: 0 h). The composition of SLS and SMASHS were defined after a previous study of SIB decolorization using different concentrations of nutrients (sucrose, malt, and (NH₄)₂SO₄) and salinity (NaCl) (data not shown).

Sulphur Indigo Blue dye

Sulphur Indigo Blue (SIB) dye was provided by Texpal Química Ltda (Valinhos, SP, Brazil) and used to prepare the standard stock solution (see Fig. 1).

Figure 1
Molecular structure of Sulphur Indigo Blue dye.

Dry biomass

At the final stage of the experiments, the samples were filtered in qualitative filter paper (previously dried) to separate the fungal biomass. The supernatant was used for the remaining analyses. Fungal biomass was dried at 105 °C and measured until constant mass. The difference between the final mass (dry mycelium + filter paper) and initial mass (filter paper) was the fungal biomass value.

Decolorization assay

The supernatants were diluted tenfold with distilled water and the decolorization was analyzed on UV-Vis spectrophotometer (Shimadzu UV-1240, Kyoto, Japan), according to Bonugli-Santos et al. (2012). The absorbance was measured at the maximum absorption peak obtained through the supernatant scanning on the spectrophotometer. Equation 1 was applied to obtain the decolorization ratio.

$$\text{Decolorizatio}(\mathrm{\%})=100\times (A_0-A_t)/A_0$$ (Equation 1)

A₀ absorbance value of the initial dye solution

A_t absorbance value of the final dye solution in samples

Enzymatic assay

The enzymatic assay was performed using the samples supernatants. Enzyme activities were measured spectrophotometrically (Shimadzu UV-1240, Kyoto, Japan) in triplicate and laccase (Lac) activity was determined using 2.2’-azinobis-(3-ethylbenzothiazoline – ABTS (ε = 36000 M^-1 cm^-1) according to Buswell et al. (1995). The assay was composed of 0.3 mL sodium acetate buffer (0.1 M pH 5.0), 0.1 mL ABTS solution (0.5 mM), and 0.6 mL sample supernatant. ABTS oxidation was measured by monitoring the increase in absorbance at 420 nm. MnP activity was determined using manganese sulfate as substrate (Wariishi et al. 1992). The reaction mixture contained 0.05 mL manganese sulfate (10 mM), 0.05 mL hydrogen peroxide (2 mM), 0.8 mL sodium malonate buffer (60 mM pH 4.5), and 0.1 mL sample supernatant. Oxidation of Mn²⁺ to Mn³⁺ was checked by absorbance increase at 270 nm due to the formation of the malonate-Mn³⁺ complex (ε = 11590 M^-1 cm^-1). LiP activity was determined by veratryl alcohol oxidation according to Tien and Kirk (1984). The mixture reaction included 1 mL sodium tartrate buffer (125 mM pH 3.0), 0.5 mL veratryl alcohol (10 mM), 0.5 mL hydrogen peroxide (2 mM), and 0.5 mL sample supernatant. The reaction was initiated with hydrogen peroxide with the appearance of veratraldehyde (ε = 9300M^-1 cm^-1) measured at 310 nm. One enzyme unit was defined as 1 μmol of product formed per minute under the assay conditions through equation 2, derived from the Beer-Lambert Law:

$$U{L}^{-1}=∆A\times V\times {10}^6/\varepsilon \times R\times t$$ (Equation 2)

ΔA Difference between the final and initial absorbance

V Reaction volume (total assay volume)

10⁶ Conversion of moles from ɛ to μmols

ɛ Extinction coefficient (M−¹ cm−¹)

R Amount of enzyme in the broth (L)

t Reaction time (min)

FT-IR analysis

The SIB biotransformation was studied by using FT-IR spectroscopy (Shimadzu IR Prestige 21), a useful tool to analyze metabolites formed from the biotransformation of dye molecules. A 15 mL aliquot of the sample supernatants was heat evaporated at 60 ^oC to subsequently remain in a vacuum desiccator for two days in order to concentrate metabolites and reduce the volume. It was followed by the preparation of KBr discs at a ratio of 10 mg of sample: 140 mg of KBr placed on suitable holders to have their readings performed at the mid-infrared region (400–4000 cm−¹) with 32 scans at a resolution of 4 cm−¹.

Metabolites extraction

To extract metabolites, ethyl acetate (Purity: > 99.5 %, Sigma-Aldrich) was used. A 20 mL aliquot of the sample supernatants was added to 10 mL of ethyl acetate. This mixture was vortexed for 5 min to obtain the metabolites. After this step, the tube contents were transferred to a separation funnel, where they remained for 5 min, until the complete formation of the interface between the solvent and the assay supernatant. The supernatant was then removed and the process was repeated, obtaining 20 mL of ethyl acetate extract, stored in Falcon-type tubes. To the ethyl acetate containing the metabolites was added 1.5 g of sodium sulfate (Na₂SO₄) to absorb any remaining aqueous solution. Subsequently, the samples were centrifuged for 3 min at 25 °C and 5000 rpm, the solvent was filtered in Nylon syringe filters with a diameter of 25 mm and pores of 0.20 µm (Analytical) and transferred to 15 mL tubes. Finally, the samples were concentrated in a sample concentrator at 30 °C until complete evaporation of the solvent. The metabolites present at the bottom of the tube were suspended in 1 mL of ethyl acetate and stored at -20 °C in appropriate glass vials for injection and subsequent analysis in GC-MS.

GC-MS analysis

Metabolites were evaluated on the GC-MS-QP2010 Ultra (Shimadzu, Japan). The separation was performed in an Rtx-5MS column (0.25mm, 30m – Restek, United States), with 2 µL of sample injected at 275 °C, with column temperature starting at 100 °C for 3 min increasing linearly at 9.5 °C per minute to 280 °C. The eluent gas was helium with a flow of 2 mL min^-1. The mass analysis was performed in scan mode, with a quadrupole analyzer, the ionization voltage was 70 eV, full scan.

Detoxification assay using Cucumis sativus

To evaluate the phytotoxicity of SIB degradation intermediates, the test using C. sativus seeds (TopSeed® Garden), with no pesticides, was carried out based on the study of Wang et al. (2001). The samples supernatants from the SLS medium were not diluted, while those from the SMASHS bioassay were diluted (25 %) in distilled water. The pH was adjusted to 7.0 for all samples before the phytotoxicity test. Fifteen C. sativus seeds were placed on Petri dishes (8 cm diameter) above the filter papers and moistened with 2.5 mL of each sample. The plates remained at 24 °C in the dark for five days. The positive control consisted of ZnSO₄ 0.05 M and the negative control was distilled water. The toxicity effects were recorded in terms of radical length and the root growth inhibition percentage was calculated according to equation 3:

Radical growth inhibition (%) = 100 x (W-S)/W (Equation 3)

S radical length of the sample and

W radical length of the negative control (distilled water)

Statistical analysis

Results are presented as mean ± standard deviation. Values were submitted to Anderson-Darling normality test and assessed the statistical significance of the data through one-way analysis of variance (ANOVA) with Tukey’s test (p < 0.05) using Minitab 1.2.

RESULTS

The time course of decolorization, dry biomass, and enzymatic activity of the marine-derived basidiomycete P. palmivorus CBMAI 1062 in media SLS (sucrose and lower salt concentration) and SMASHS (sucrose, malt extract, ammonium sulfate, and higher salt concentration) are displayed in Fig. 2a and b, respectively. In the first 12 h, 50 % of dye decolorization was achieved in both bioassays. The parameters assessed increased continuously until the end of the experiment, reaching 100 % and 81.47 % of SIB decolorization after 120 h in the SLS and SMASHS bioassays, respectively. The fungal biomass was approximately twice higher in the SMASHS bioassay than for the SLS (Fig. 2a and b) after 120 h of incubation. Neither of the conditions studied showed the presence of MnP nor LiP activities. However, Lac activity was detected in the SLS bioassay. Considering that after 120 h the dye was completely removed only for the SLS medium, an additional 48 h was considered for the SMASHS condition. After 168 h of incubation, the fungus decolorized 91.38 % of the SIB, with dry biomass of 2.194 g L^-1.

Figure 2
Dry biomass, decolorization and laccase activity after P. palmivorus CBMAI 1062 incubation in SLS (a) and SMASHS (b) media at 28 °C and 140 rpm. The vertical lines represent the standard deviation of the mean.

The SLS bioassay led to a decrease in the absorbance peak of the dye (601 nm) during the treatment and changes occurred in the UV-Vis spectrum after 72 h (Fig. 3a). Visible spectra scanning of the time course in the SMASHS bioassay (Fig. 3b) showed that the absorption peaks decreased over time, especially after the first 12 h of incubation, when the decolorization reached 50 %. Nevertheless, no changes occurred in the UV-Vis spectrum during the time course. In both conditions, the pH at 0 h was 8.0 and at the end of the bioassay 6.30 ± 0.03 for the SLS bioassay and 2.64 ± 0.06 for the SMASHS bioassay (data not shown).

Figure 3
Time course UV-Vis spectrum of the Sulphur Indigo Blue textile dye after P. palmivorus CBMAI 1062 incubation in SLS (a) and SMASHS (b) media at 28 °C and 140 rpm.

The FT-IR spectra of SIB show the functional groups found in the molecular structure of the dye (Fig. 4a). The bands observed at 3425 cm^-1 and 3370 cm^-1 would represent the –NH group. The bands at 3072 cm^-1, 2923 cm^-1 and 1387 cm^-1 were attributed to a stretching of –CH bond. A characteristic band at 1653 cm^-1 also appeared, indicating a carbon-carbon double bond (C=C), part of the dye’s chromophore region. The bands at 1610 cm^-1 and 1456 cm^-1 were attributed to the vibration of aromatic rings. The fingerprint region of the indigo dye is represented in the peaks between 1350-400 cm^-1 (Kushch et al. 2019). The bands in this region indicate the stretching vibration of single bonds involving C-C, C-N, and C-S. In addition, the band observed at 1150 cm–¹ was assigned to the sulfonate group (S=O), which is the part of the dye that is adsorbed (Vautier et al. 2001).

Figure 4
FT-IR spectra of (a) Sulphur Indigo Blue dye, (b) SLS medium at 0 h (control) and (c) after 120 h of P. palmivorus CBMAI 1062 incubation at 28 °C and 140 rpm.

Fig. 4b illustrates the spectra of the control at 0 h (SIB, sucrose and NaCl). The band observed at 1642 cm–¹ was considered a junction of the bands 1653 cm–¹ and 1610 cm–¹ found on the SIB spectra (Fig 4a). The band at 1420 cm–¹ was attributed to an angular deformation of adjacent -CH found in aromatic rings and sucrose. The FT-IR spectroscopic analysis of SIB and the metabolites generated by the fungus metabolism revealed sharp spectral changes after 120 h of incubation for the SLS bioassay (Fig. 4c). The changes indicate the occurrence of biodegradation of the dye molecule. In contrast, no significant changes appeared in the experiments with SMASHS medium (Fig. 5). Comparing the spectra of the control (0 h) and after the bioassay, the bands and their intensity are similar, suggesting the absence of biodegradation.

Figure 5
FT-IR spectra of SMASHS medium (a) at 0 h (control) and (b) after 168 h of P. palmivorus CBMAI 1062 incubation at 28 °C and 140 rpm.

Table I shows the compounds found in the GC-MS analysis of the SLS bioassay. Despite some listed compounds being the same at time 0 h and after 120 h, there were variations in the sizes of the peaks. They can be seen in Fig. 6, where the chromatogram before and after the bioassay is shown. Peaks with the alkanes tetradecane (B), hexadecane (E) and octadecane (C and F) increased after the bioassay. An increase in the amide compound 9-Octadecenamide (N) was also observed. On the other hand, there was a decrease in the aromatic compound Phenol, 2,4-bis(1,1-dimethylethyl) (D) and the ester Hexadecanoic acid, 2-hydroxy-1-(hydroxymethyl)ethyl ester (O). The other peaks listed in Table I showed no change after the bioassay. In addition to the listed peaks, it is possible to observe the formation of four new peaks after 120 h (indicated by the arrows in Fig. 6). In the retention time (RT) 14.034 there was the formation of the aldehyde Octadecal (I) and in the RT 14.652 of the alcohol n-Nonadecanol-1 (J). In the other two RT (15.936 and 16.005) the Octadecanoic acid, 2,3-dihydroxypropyl ester (L and M) was detected.

Figure 6
GC-MS spectra after P. palmivorus CBMAI 1062 incubation in SLS medium at 28 °C and 140 rpm. The above line indicates 0 h (control) and the bottom line 120 h of incubation. The arrows indicate the peaks detected only after 120 h.

Table I
Compounds identified by GC-MS at 0 h (control) and after 120 h of P. palmivorus CBMAI 1062 incubation in SLS medium at 28 °C and 140 rpm.

Peak	Retention Time (min)	Similarity (%)	Compound
A	3.822	91 %	Triethyl phosphate
B	6.909	94 %	Tetradecane
C	7.686	90 %	Octadecane
D	8.382	95 %	Phenol, 2,4-bis(1,1-dimethylethyl)
E	9.354	93 %	Hexadecane
F	10.527	91 %	Octadecane
G	11.262	94 %	Tetradecanoic acid
H	13.413	93 %	n-Hexadecanoic acid
I	14.034	91 %	Octadecala
J	14.652	90 %	n-Nonadecanol-1a
K	15.399	93 %	Octadecanoic acid
L	15.936	93 %	Octadecanoic acid, 2,3-dihydroxypropyl estera
M	16.005	94 %	Octadecanoic acid, 2,3-dihydroxypropyl estera
N	17.295	90 %	9-Octadecenamide, (Z)
O	18.537	90 %	Hexadecanoic acid, 2-hydroxy-1-(hydroxymethyl)ethyl ester

• ^aOnly detected at 120 h.

The compounds identified in the SMASHS bioassay (Table II) also showed variations in the sizes of the peaks at 0 h and after 168 h of bioassay. In Fig. 7 it is possible to verify the decrease in the peak of the compound 5-Hydroxymethylfurfural (A’) after the bioassay. There was an increase in the peak of the alkane Tetradecane (B’) and of the aromatic compound Phenol, 2,4-bis(1,1-dimethylethyl) (C’). The compounds carboxylic acids, tetradecanoic acid (F’), hexadecanoic acid (H’) and octadecanoic acid (I’) and amide 9-Octadecenamide (L’) also had the highest peaks after 168 h of incubation. In addition, four new peaks J’, K’, M’ and N’ were detected but could not be identified. The retention times of the compounds were not the same for the bioassays (Fig. 6), which suggests the formation of different compounds in the two bioassays. Additionally, in the SMASHS condition the compound identified as Pyrrolo[1,2-a] pyrazine-1,4-dione, hexahydro-3-(2-methylpropyl (G’) disappeared after 168 h of incubation.

Figure 7
GC-MS spectra after P. palmivorus CBMAI 1062 incubation in SMASHS medium at 28 °C and 140 rpm. The above line indicates 0 h (control) and the bottom line 168 h of incubation. The arrows indicate the peaks detected only after 168 h.

Table II
Compounds identified by GC-MS at 0 h (control) and after 168 h of P. palmivorus CBMAI 1062 incubation in SMASHS medium at 28 °C and 140 rpm.

Peak	Retention Time (min)	Similarity (%)	Compound
A’	4.920	93 %	5-Hydroxymethylfurfural
B’	6.909	90 %	Tetradecane
C’	8.379	95 %	Phenol, 2,4-bis(1,1-dimethylethyl)
D’	9.351	91 %	Hexadecane
E’	10.524	90 %	Octadecane
F’	11.250	94 %	Tetradecanoic acid
G’	13.284	89 %	Pyrrolo[1,2-a] pyrazine-1,4-dione, hexahydro-3-(2-methylpropyl)a
H’	13.419	93 %	Hexadecanoic acid
I’	15.399	93 %	Octadecanoic acid
J’	16.719	52 %	Non-identifiedb
K’	17.049	62 %	Non-identifiedb
L’	17.292	92 %	9-Octadecenamide, (Z)
M’	17.778	72 %	Non-identifiedb
N’	18,126	52 %	Non-identifiedb
O’	18.618	91 %	Hexadecanoic acid, 2-hydroxy-1-(hydroxymethyl)ethyl ester

• ^aOnly detected at 0 h. ^bOnly detected at 168 h.

Data related to the toxicity using C. sativus seeds as bioindicator revealed a reduction in the inhibition of root growth in both bioassays (Fig. 8). For the SLS bioassay (Fig. 8a) the results showed a significant decrease in phytotoxicity (from 45.41 % to 24.11 % of root inhibition growth). However, there was no significant difference before and after the SMASHS bioassay (Fig. 8b).

Figure 8
Cucumis sativus radical inhibition growth after P. palmivorus CBMAI 1062 incubation in SLS (a) and SMASHS (b) media at 28 °C and 140 rpm. Different letters indicate that values are significantly different from each other by Tukey (p< 0.05). The vertical lines represent the standard deviation of the mean.

DISCUSSION

Results from the present study revealed that the white rot fungus P. palmivorus CBMAI 1062 isolated from a marine sponge was able to highly decolorize the SIB textile dye in both conditions (SLS and SMASHS media) (Fig. 2a and b). After 120 h of incubation in the less nutritive and saline medium (SLS) SIB textile dye was completely decolorized, while in the more nutritive and saline medium (SMASHS) the decolorization was about 80 %. The fungal biomass was twice higher in the SMASHS than in the SLS bioassay (Fig. 2a and b). These results suggest that P. palmivorus CBMAI 1062 would rather use the enriched medium (SMASHS) as carbon and nitrogen sources than the dye itself.

The initial decolorization for both conditions (50 % after 12 h) probably occurred due to biosorption of the dye by the fungus mycelium, which visually became blue (data not shown). Cantele et al. (2017) reported that the rates of decolorization of different textile dyes (anthraquinone and azo groups) by the fungus Marasmiellus palmivorus VE-111 after 24 h of incubation probably occurred mainly by biosorption rather than degradation by extracellular enzymes. However, a 100 % decolorization of the dye was observed in the bioassay in SLS medium, after 120 h and Lac activity of 20 U L^-1, which suggests the influence of the laccase enzyme in the decolorization process.

The less nutritious medium (SLS), containing only the SIB dye, sucrose and NaCl favored the production of Lac. On the other hand, as mentioned earlier, the more nutritious medium (SMASHS) may have favored the growth of the mycelium rather than the production of ligninolytic enzymes. Placido et al. (2016) reported that the use of glucose as a carbon source favored the production of ligninolytic enzymes and promoted the decolorization of real textile effluent. Schneider et al. (2018) reported the production of Lac in a bioreactor condition by Marasmiellus palmivorus VE111 (current name Paramarasmius palmivorus) at low glucose concentrations (5 and 10 g L^-1). In previous studies, the marine-derived fungus P. palmivorus (former Marasmiellus sp.) CBMAI 1062 produced great amounts of Lac after 21 days of incubation in a medium composed of malt extract and artificial seawater (Bonugli-Santos et al. 2010a, 2012). Furthermore, the higher concentration of NaCl (30 g L^-1) in the SMASHS medium may also have inhibited the activity of Lac (Moreira et al. 2014). These findings demonstrate that the production of ligninolytic enzymes used in bioremediation processes of environmental pollutants is indeed related to microorganisms and cultivation conditions.

The increase in the decolorization rate was accompanied by the increase in Lac production, with the decrease of the chromophore peak of the dye (601 nm) and the appearance of a new peak (235 nm) in the UV-Vis spectra (Fig. 3a). The new peak is probably related to isatin sulfonic acid and isatin, intermediate compounds of indigo carmine degradation. Several studies have already correlated the appearance of this peak in UV-Vis spectra with the detection of these compounds in LC-MS (Wang et al. 2017), HPLC (Flox et al. 2006), electrospray time-of-flight mass spectrometer (Qu et al. 2015) and HPLC-MS (Zaied et al. 2011). Campos et al. (2001) reported that several types of laccases are capable of oxidizing the indigo dye, resulting in the compound isatin. In the study carried out by Lu et al. (2016) the increase in the decolorization of indigo dye by the white rot fungus Ganoderma sp. En3 was also accompanied by an increase in Lac production. Previous studies showed satisfactory decolorization rates of Indigo using purified laccases, indicating that these enzymes are important in dye molecule degradation (Campos et al. 2001, He et al. 2015, Kushch et al. 2019).

A comparison of the FT-IR spectra obtained after 0 h (Fig. 4b) and 120 h (Fig. 4c) of incubation in the SLS condition revealed that the band at 1642 cm^-1 had reduced intensity, suggesting the disruption of C=C double bond (chromophore region). This result is in accordance with the 100 % decolorization found after 120 h. Moreover, the lower intensity at 1642 cm^-1 and the sharp decrease in 1456 cm^-1 and 1420 cm^-1 suggest the breakdown of aromatic rings (Li et al. 2015b). The reduced intensity of the bands in the fingerprinting region indicates the occurrence of changes in the dye molecule. The prominent band observed at 1150 cm^-1 (S=O) in the control experiments (Fig. 4a and b) decreased after 120 h of the treatment, probably resulting from dissulfonation and biosorption by the fungus mycelium. The biotransformation of the dye molecule (verified by UV-Vis and FT-RI spectra) suggests possible mineralization of part of the dye molecules. Moreover, as mentioned before, biosorption was also responsible for the bioremediation of the dye. According to Huang et al. (2014) both processes (biosorption and biodegradation) occurred in the decolorization of the Remazol Brilliant Blue R (RBBR) dye by the fungus Myrothecium sp. IMER1.

New peaks of alkane compounds were detected in GC-MS chromatograms of the SLS bioassay after 120 h of incubation. Olajuyigbe et al. (2022) also observed the formation of several peaks of alkane compounds such as Hexadecane and 3-Methyl hexadecane during the degradation of Indigo carmine dye by the ligninolytic bacterium Stenotrophomonas sp. CFB-09. Similarly, Rajendran et al. (2015) verified the presence of octadecane after the treatment of textile effluent, containing indigo carmine, by a consortium of immobilized bacteria. In the present study, the formation of aldehyde octadecanal was also detected in the medium containing sucrose as the only additional carbon source, indicating that these compounds (alkanes and aldehyde) may be related to SIB metabolism. The decrease in the peak of the aromatic compound Phenol, 2,4-bis(1,1-dimethylethyl) in the SLS bioassay is in agreement with the sharp decrease found in the FT-IR spectrum. Phenol, 2,4-bis(1,1-dimethylethyl) is an alkyl phenol and is considered a persistent organic pollutant used in agriculture as a fungicide, herbicide and insecticide (Kee et al. 2015, Devi et al. 2021). This same compound was also found in the degradation of the Mordant Black 11 dye by the bacterium Klebsiella pneumoniae MB398 (Tahir & Yasmin 2021). Alkyl phenols affect the functioning of sexual hormones in humans and other animals, which can lead to sterility (Michalowicz & Duda 2007). The reduction in toxicity evidenced in the experiments with C. sativus (Fig. 7a) can be related to the decrease in the peak of this compound. In the SLS condition it was possible to observe a higher peak of 9-Octadecenamide (Z) after the conduction of the bioassay. This molecule was also seen as a product of the degradation of the textile dye Congo Red by Lac. The possible mechanism may have been the cleavage of the C–N bond, removing the nitrogen attached to the aromatic ring and leading to several intermediate products, such as 9-Octadecenamide (Z) (Liu et al. 2020).

Considering the results of complete decolorization (100 %) and dye transformation (based on UV-Vis, FT-IR, and GC-MS analyses), Lac production, and detoxification (using C. sativus as bioindicator) in the less nutritive and saline condition (SLS medium), it is reasonable to believe that other enzymes could have participated in the biodegradation and detoxification processes, including those from the cytochrome P-450 system and epoxide hydrolases. Some studies have reported the presence of these enzymes in the degradation of dyes and other organic pollutants by fungi (Bezalel et al. 1996, Cha et al. 2001, Zhang et al. 2015).

In the experiments using a more nutritive and saline condition (SMASHS medium) results related to biomass production, UV-Vis spectrum, ligninolytic enzymes, and toxicity indicate that the decolorization occurred mainly by biosorption. Since the SIB dye is anionic, the positive charge in the fungus mycelium could have promoted interaction with the SO₃ groups of the dye. Moreover, the acidification of the medium could have favored biosorption. According to Iscen et al. (2007), the fungus mycelium is protonated and when the pH decreases the positive charges increase on the surface. Consequently, a low pH in the medium can favor biosorption (Karthik et al. 2019, Karatay et al. 2021). Although the absorbance peaks decreased over time, as shown in the UV-Vis spectrum, no other peak was detected in SMASHS bioassay (Fig. 3b). In this condition, the spectrum maintained the same topography, indicating the absence of significant structural changes in the dye molecule during the bioassay.

The FT-IR spectra (Fig. 5) showed no spectral differences between 0 h and 168 h after the bioassay. The concentration of SIB was much lower, but there were still whole molecules of the dye, which reinforces the biosorption hypothesis previously discussed since no biotransformation occurred in the dye molecule.

Data from GC-MS analysis (Fig. 7) revealed that the peak of the compound Pyrrolo[1,2-a] pyrazine-1,4-dione, hexahydro-3-(2-methylpropyl) disappeared after 168 h of incubation. A similar compound (Pyrrolo[1,2-a]pyrazine-1,4-dione, hexahydro-3-[phenylmethyl]) was already observed in the study related to indigo carmine degradation (Olajuyigbe et al. 2022) and congo red dye degradation (Liu et al. 2020). However, the compound was seen as the final metabolite in both studies. The disappearance of the peak in the present study suggests that this compound was bioabsorbed and/or degraded. In this SMASHS bioassay, the peak of the aromatic compound Phenol, 2,4-bis(1,1-dimethylethyl) was higher after 168 h of bioassay. This result is probably related to the absence of detoxification observed in the experiments using C. sativus as a bioindicator. Additionally, a higher peak of carboxylic acids, including octadecanoic acid, was seen in SMASHS bioassay after 168 h of incubation. This compound has already been detected as a residue in cassava fermentation by the basidiomycete Trametes sp. SYBC-L4 (Li et al. 2014), which may indicate a natural compound of the metabolism of P. palmivorus CBMAI 1062. The increase of this compound was not detected in the SLS bioassay, reinforcing the hypothesis that the most nutritive medium stimulated the fungal metabolism related to the use of other nutrient sources instead of the dye molecule, being the dye probably removed from the medium mainly by biosorption. The non-identified new peaks (Table II) detected in the GC-MS spectra in different RT from the SLS bioassay can be related to the metabolisms of the medium nutrients by the fungus or compounds from the degradation of the dye molecule. However, additional analyzes are necessary to elucidate the compounds and the sources, thus building possible metabolic pathways.

Biosorption is also considered a great microbial strategy for the treatment of dyes, given the cost, ease of operation, and no need for specific equipment (Sintakindi & Ankamwar 2021). Bonugli-Santos et al. (2012) reported that most of the decolorization of the RBBR dye by the fungus P. palmivorus (former Marasmiellus sp.) CBMAI 1062 occurred by adsorption by the mycelium in a medium composed of 2 % malt extract (complex medium) and without NaCl. Several studies have been carried out evaluating the adsorption of various textile dyes by filamentous fungi (Li et al. 2019, Karthik et al. 2019, Karatay et al. 2021). However, more studies are necessary to evaluate biosorption in saline processes (Wang et al. 2015, Nouri et al. 2021).

CONCLUSIONS

The textile dye SIB was completely decolorized by the marine-derived fungus P. palmivorus CBMAI 1062 at the less nutritive and saline medium through biotransformation and biosorption processes with a significant decrease in toxicity. High percentage of SIB decolorization (91.38 %) was also achieved at the more nutritive and saline medium in an extended period of time, but with no significant alteration in toxicity. Biosorption was probably the main process in this condition.

Taking into account the high standard of governmental legislation applied to textile industries, in which color removal is one of the main aspects, the discovery of microorganisms adapted to the salinity of the textile effluents able to decolorize/detoxify the dyes is a great achievement. In this sense, to prevent or mitigate the deleterious effects of spilling textile effluents into the environment, biological systems containing microorganisms of marine origin can be applied or be associated with other remediation processes.

ACKNOWLEDGMENTS

This study was financed by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (grants #2018/12098-9 and #2016/07957-7). EPP thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for her Master scholarship (#130364/2017-7). LDS thanks the CNPq for her Productivity Fellowships (#303145/2016-1 and #305173/2023-5).

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Publication Dates

• Publication in this collection
  28 Oct 2024
• Date of issue
  2024

History

• Received
  20 Mar 2023
• Accepted
  06 July 2024