Tequila vinasse, a by-product generated during agave fermentation, is a wastewater characterized by its dark color and composition, which includes water, alcohol, sugars, phenolic compounds, proteins, among others. Its high chemical oxygen demand (COD) and pH levels classify it as hazardous to the soil, plants, and aquatic organisms, requiring the development of treatment strategies or proper disposal methods. It is worth noting that vinasse contains numerous compounds that can be recovered and valorized. In this study, different concentrations of tequila vinasse (100%, 70%, and 50%) were subjected to a 10-day treatment with Trametes sanguineus. Significant reductions in color, phenolic content, and COD were observed across all conditions, with approximately 70% decolorization and 60% reduction in phenolic content achieved. Among the different conditions tested, the 50% concentration exhibited the highest laccase production, reaching approximately 1,779 U/L on the 5th day of cultivation, while laccases were also detected in the other conditions. Subsequently, the potential of the treated vinasse for germination and seedling growth was assessed. Trametes sanguineus was removed from the vinasse, and the resulting supernatant was applied directly to the seeds. Lettuce and tomato seeds were employed in these assays, both of which demonstrated seed germination rates ranging from 50–80%, respectively. Notably, vinasse without T. sanguineus treatment did not exhibit any germination. Additionally, seedling growth assays were conducted, revealing that the treated vinasse supported the growth of tomato and lettuce plants, with root-related features comparable to the control. Valorization of agroindustrial waste presents a viable approach for obtaining value-added products.
Research Article
Detoxification of tequila vinasse by Trametes sanguineus: a biotechnological approach to laccase production and water reuse in seedling growth
https://doi.org/10.21203/rs.3.rs-3228310/v1
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vinasse
detoxification
basidiomycetes
valorization
laccase
water reuse
Tequila is one of the most important agroindustries in Mexico and it is in continuous growth. According to the Tequila Regulatory Council, approximately 650 million liters of tequila were produced in 2022, representing a 2.4-fold increase in production over the past 5 years. Consequently, the production of tequila generates substantial amounts of waste (agave bagasse and vinasse) at a corresponding rate. Specifically, after agave fermentation, each liter of tequila produced generates approximately 10–13 liters of vinasse (Moran-Salazar et al. 2016; Robles-González et al. 2012). Thus, according to tequila production, approximately 7,000 million liters of vinasse were produced last year, posing challenges related to proper management and disposal.
Although agave vinasse is specific to Mexico, it shares the same challenges in terms of its management and disposal as vinasse derived from other sources (Moran-Salazar et al. 2016).
Vinasse is a black liquid composed of water, alcohol, acids, phenolic compounds, minerals, and nitrogen salts (dosReis et al. 2018). The physicochemical composition of vinasse varies depending on the raw material, harvest season and the specific industrial process employed (Fuess et al. 2018; España-Gamboa et al. 2011).
The significance of this by-product stems from its composition and the volume generated. Vinasse is considered hazardous due to its high levels of chemical oxygen demand (70,000-150,000 mg/L), biological oxygen demand (35,000–50,000 mg O2/L), total solids content (25,000–95,000 mg/L) and low pH (Sánchez-Ureña et al. 2022; Robles-González et al. 2012). In aquatic ecosystems, the discharge of vinasse can contribute to eutrophication, resulting in algae proliferation, reduced photosynthetic activity and decreased dissolved oxygen concentration, negatively impacting the fauna, flora and microbiota of rivers and lagoons (Ahmed et al. 2018; dosReis et al. 2018; Potentini et al. 2006). In soil, the abundance of salts and other compounds present in vinasse can provoke soil salinization, which leads to poor soil quality (Fuess et al. 2018). Furthermore, the phenolic content in vinasse has a detrimental effect on soil microbiota and can inhibit seed germination (Robles-Gonzalez et al. 2012).
Current policies have prioritized strategies to address the adverse effects resulting from anthropogenic activities and promote waste recycling. In Mexico, the circular economy law enacted in 2021, promotes the valorization of agro-industrial wastes as a means to optimize resource utilization and minimize waste generation. However, it is crucial to establish alternatives for the treatment and reuse of vinasse. The valorization of agro-industrial wastewater has gained significant attention in recent years. Vinasse has been used for purposes such as crops irrigation, biofuels production (García-Depraect et al. 2020) as raw material for microbial and algae biomass (Quintero-Dallos et al. 2019), for the production of biopolymers (Trapé et al. 2021), volatile fatty acids (Eng et al. 2022) and enzymes (Junior et al. 2020; Pinheiro et al. 2020).
Bioremediation of agro-industrial effluents has been accomplished through the utilization of Ascomycetes and Basidiomycetes fungi. In particular, white-rot fungi possess a ligninolytic complex comprising peroxidases, tyrosinase and laccases, which enables the reduction of various phenolic compounds, including polyphenols, melanins and melanoidins with the concomitant color reduction of vinasse (Fernandes et al. 2021; Junior et al. 2020). Therefore, this work aims to evaluate a strategy to reuse tequila vinasse, firstly for enzyme production and secondly as water for seedling growth.
Microorganism and vinasse
Trametes sanguineus was generously donated by Dr. Jorge Folch Mallol. The strain was routinely subcultured on potato-dextrose agar (PDA) plates, incubated at 30 ºC for 7 days and stored at 4 ºC. Tequila vinasse was kindly donated by Dr. Luis Arellano (CIATEJ). Tequila vinasse was stored at 4 ºC before use.
Tequila vinasse treatment by T. sanguineus
Vinasse was adjusted to pH 5 and autoclaved at 121 ºC for 15 min (solids were not removed from vinasse). T. sanguineus was grown on PDA plates for 7 days at 30 ºC. One agar plug (2x2 cm diameter) was transferred to 250 mL Erlenmeyer flask containing 50 mL of preculture medium BF (Branflakes 80 g/L, yeast extract 2 g/L, KH₂PO₄ 2 g/L, MgSO₄*7H₂O 0.5 g/L, CaCl₂*2H₂O 0.1 g/L) and grown for 72 h at 30 ºC, 180 rpm. Subsequently, 10% (v/v) of growing cells (pellet) was added to Erlenmeyer flasks 500 mL with 250 mL vinasse at 100, 70 and 50% (v/v) final concentration. Diluted vinasse was carried out with distilled water before sterilization. Cultures were incubated for 10 days at 30 ºC, 180 rpm. Total phenol content, laccase activity, sugar consumption and color reduction were monitored each 48 h and each assay was evaluated in triplicate. Biomass, pH and electric conductivity (EC) were measured at the end of the culture.
Bioassay on lettuce and tomato plants - Germination bioassays
Lettuce (Lactuca sativa) and tomato (Solanum lycopersicum) were used as model seeds since these seeds were widely studied in the literature. Besides, these seeds allow us to compare a plant with fast and low germination. Lettuce and tomato seeds showed > 90% germination efficiency and were purchased in Semillas Fax hortalizas and ITSCO, respectively. Germination assays were performed on sterilized filter paper discs (8 cm diameter) with 7 mL water (control) or vinasse (treated or untreated). Samples of 25 seeds of lettuce or tomato seeds were placed in a recipient containing sterilized paper discs, these seeds were incubated under controlled conditions 16:8 (light:dark) at 25 ºC for 96 h for lettuce and 14 days for tomato seeds, and scored daily for germination (when radicles first became visible).
Different treatments were: 1) vinasses 100%, 2) vinasses 100% treated with T. sanguineus (Ts), 3) vinasses 70%, 4) vinasses 70% treated Ts, 5) vinasses 50%, 6) vinasses 50% treated Ts, and 7) control (distilled water). Additionally, other conditions were evaluated: 8) vinasse 35% treated Ts and 9) vinasse 25% treated and untreated. Each treatment consisted of three replicas.
Bioassay on lettuce and tomato plants - Seedling assays
For the plant growth studies, seeds were planted in nursery trays containing commercial peat moss-based substrate. Every 48 h, 4 mL of water or treated vinasse was supplied to the cultivation soil. The plants were cultivated in a chamber at 25 ºC and 16:8 (L:D). After 25 days for tomato and 21 days for lettuce, parameters such as plant height, chlorophyll, root length, stem diameter, and root/shoot weight were determined. Chlorophyll was measured using a chlorophyll content meter (Opti-sciences, CCM-200 plus).
Analytical methods
Total sugar concentration was determined by the phenol-sulfuric method (DuBois et al., 1956). Dry cell biomass determination was performed at the end of the culture, biomass was recovered by centrifugation and dry at 60 ºC until constant weight. Total phenolic compounds analysis was performed using the Folin-Ciocalteau method, using gallic acid as standard. Determinations were performed on 96-well microplates on a microplate reader (EON Biotek), the assay was performed as follows: 5 uL sample, 103 uL distilled water, 12 uL Folin reagent and after 5 min incubation, 80 uL sodium carbonate (7%) was added and incubated for 2 h. Colorimetric determination was performed at 765 nm in a microplate reader. The laccase activity was determined spectrophotometrically by monitoring the oxidation of ABTS. The reaction mixture contained 1 mM ABTS, 100 mM acetate buffer (pH 4.5) and the enzyme, the change in absorbance was monitored at 436 nm (ε436 nm = 29,300 M⁻¹cm⁻¹) for 2 min. Laccase activity was expressed as units per liter (U/L), one enzyme unit representing the amount of enzyme needed to oxidize 1 µmol of ABTS, per min. The DQO determination was performed using DQO standard vials (HACH, 200 − 15,000 mg/L), 200 uL of 10-fold diluted samples were added to each vial and incubated at 120 ºC for 2h, and measurements were determined by spectrophotometer at 620 nm. Color reduction was calculated from absorbance measurements at 475 nm using a microplate reader, according to the formula:
Color reduction (%) = [(A0 − At)/A0]x 100
Statistical analysis
All samples were analyzed in triplicate (n = 3) and the results were expressed as the mean ± Standard Deviation by using a Microsoft Office Excel 2007 program. One-way ANOVA followed by the Tukey test was applied to evaluate differences in seedlings with water (control) and treated vinasse (50%). Data were considered significantly different if P values < 0.05. Data analysis was performed using Minitab 21.
Tequila vinasse treatment by T. sanguineus
In general, the biological treatment of vinasse using fungi involves the use of diluted vinasse to enhance fungal growth and detoxify the effluent. In this study, the effectiveness of T. sanguineus was evaluated on raw vinasse and diluted vinasse. Initial assays were performed growing T. sanguineus on vinasse agar plates (100% concentration), but the fungal mycelium exhibited slower growth compared to the control medium (potato dextrose agar). However, despite the limited growth on vinasse agar plates, they did exhibit decolorization properties (data no show). As a result, the subsequent step involved assessing the growth and decolorization capabilities of T. sanguineus at different concentrations of vinasse: 100, 70 and 50% (diluted with distilled water). At the end of the culture, a significant reduction in vinasse color, phenolic content, and COD was observed. Table 1presents the physicochemical composition of treated and untreated vinasse.
|
Parameter |
Vinasse 100% |
Vinasse 100% treated |
Vinasse 70% |
Vinasse 70% treated |
Vinasse 50% |
Vinasse 50% treated |
|---|---|---|---|---|---|---|
|
pH (25 ºC) |
4.58 |
4.49 |
4.6 |
4.45 |
4.82 |
4.58 |
|
COD (mg/L) |
55,800 ± 424.3 |
43,350 ± 919.2 |
42,700 ± 1271.8 |
27,700 ± 2545.6 |
29,750 ± 777.8 |
18,900 ± 141.4 |
|
Total sugar content (mg/L) |
14.99 ± 1.51 |
18.25 ± 1.27 |
10.99 ± 0.09 |
10.29 ± 0.49 |
7.44 ± 0.38 |
6.0 ± 0.32 |
|
Electric conductivity (µS/cm) |
107.5 ± 6.08 |
94.8 ± 3.26 |
87.3 ± 5.32 |
82.0 ± 3.14 |
63.9 ± 4.05 |
64.3 ± 2.66 |
|
Phenolic content (mg/L) |
6.89 ± 0.30 |
2.21 ± 0.16 |
5.06 ± 1.22 |
1.50 ± 0.06 |
3.44 ± 0.28 |
1.35 ± 0.40 |
Phenolic content and COD exhibited a noticeable decrease when vinasse was treated with T. sanguineus. Other parameters, such as pH and EC, remained relatively unchanged or showed minimal variation. Ahmed et al. (2022) reported a reduction in COD (60%) and phenolic content (30%) after 21 days of culture of Trametes sp., where they evaluated vinasse at 75 and 50% concentrations with the addition of sugar. Fernandes et al. (2021) also demonstrated a decrease in phenolic content through the action of Phlebia rufa, leading to the complete elimination of compounds such as p-hydroxybenzoic, gallocatechin gallate, chlorogenic acid, p-coumaric acid, m-coumaric acid, and others.
Various organisms have been employed for vinasse detoxification, including yeast (Saccharomyces cerevisiae) and fungi such as Pleurotus ostreatus, Phanaerochaete chrysosporium or Ganoderma sp. However, some authors have reported that fungi growth is inhibited by vinasse at 50 or 100% concentrations in the medium (Ahmed et al. 2018). Herein, T. sanguineus exhibited growth and detoxification capabilities even at high vinasse concentrations. The final biomass achieved was 5.7 g/L at 50% vinasse, 5.4 g/L at 70% vinasse and 5.9 g/L with 100% vinasse.
Furthermore, phenolic content showed a reduction in all three conditions, with the highest phenolic reduction observed at around 70%. As for decolorization, the best condition was found to be 50% vinasse. In terms of COD reduction, both the 50% and 70% vinasse concentrations exhibited a 30% reduction, while a 20% reduction was achieved with 100% vinasse (Fig. 1).
One of the main parameters showing noticeable changes was the color. The production of laccase from the 2nd to the 8th day of T. sanguineus growth indicated its involvement in vinasse decolorization. Previous studies have observed that laccases secreted during fungal growth on vinasses contribute to reducing the color of vinasse (Ferreira et al. 2010; Aguiar et al. 2010). In a study by Ahmed et al. (2018) 51% discoloration and 78% phenolic reduction were observed using 10% vinasse with Pycnoporus sp. after a 12-day culture period
The color of vinasses is generally attributed to the presence of phenolic compounds and melanoidins, which can be effectively removed by ligninolytic fungi (Robles-Gonzalez et al. 2012). Fernandes et al. (2020) observed a correlation between the concentration of phenolic compounds and the color of the vinasse, with vinasse discoloration occurring when the phenolic compound levels were reduced to values lower than 10 mg/L.
T. sanguineus laccase production
Several studies have utilized fungi for the treatment of vinasse and the production of ligninolytic enzymes, primarily focusing on sugarcane vinasse. However, there is a scarcity of research concerning laccase production from tequila vinasse. In this study, T. sanguineus was cultivated under three different conditions of vinasse concentration (100, 70 and 50%), and the laccase activity was monitored throughout the cultivation period (Fig. 2).
Laccase activity was detected as early as day 2 when T. sanguineus was cultivated in vinasse 50%. However, there was a delayed onset of laccase production in other conditions. These findings align with existing literature, as it has been reported that high concentrations of vinasse can adversely affect fungal growth (Ahmed et al. 2018).
In this case, T. sanguineus demonstrated the ability to grow and produce laccase under all the conditions evaluated. The maximum laccase activity was achieved on the 6th day when grown in vinasse with a concentration of 50% and on the 8th day for growth in vinasse with concentrations of 70 and 100%. Interestingly, the maximum volumetric activity was nearly identical between vinasse concentrations of 70% (1808.9 ± 153.8 U/L) and 50% (1775.9 ± 104.6 U/L). On the other hand, raw vinasse (100%) exhibited the lowest laccase activity, although the titers were high compared to previous studies. For instance, España-Gamboa et al. (2011) evaluated the treatment of 10% sugarcane vinasse using Trametes versicolor and observed that the majority of color and phenols were removed when laccase reached its peak at 428 U/L.
Laccase activity in these kinds of materials is associated with the removal of aromatic compounds such as p-hydroxybenzoic acid, p-coumaric acid or ferulic acid (Fernandes et al. 2021; Tapia-Tussell et al. 2015). Laccases, along with other ligninolytic enzymes, are well-known defense mechanisms against xenobiotics. Laccases can be either constitutive or inducible in response to the presence of specific compounds, including phenolic compounds and metals (Ahmed et al. 2018; Bertrand et al. 2013; Collins and Dobson 1997). Their production is triggered in the presence of these compounds found in lignocellulosic materials (Junior et al. 2020; Ahmed et al. 2020). Tapia-Tussell et al. (2015) observed an increase in laccase mRNA gene transcript levels when phenolic compounds typically found in vinasses were present in the culture media, and high laccase activity was observed in vinasse at a 10% concentration.
Various authors have supplemented vinasses to promote fungal growth and enhance laccase activity by adding substances such as glucose or copper. Ferreira et al. (2010) added glucose to raw vinasse and observed that laccase activity remained until the 15th day of culture, compared to raw vinasse (without glucose) where laccase activity declined by the 12th day. On the other hand, copper is commonly used as a laccase inducer, Junior et al. (2020) produced laccase from Pleurotus sajor-caju and achieved a laccase activity of 500 U/L by adding copper sulfate (0.4 mM) in sugarcane vinasse. It is worth noting that no copper was added to the vinasse in this study. However, chemical characterization of agave vinasse has indicated the presence of trace amounts of metals, including copper, at concentrations ranging from 1–3 mg/L (Sánchez-Lizarraga et al. 2018; Lopez-López et al. 2010). As vinasse contains all the nutrients necessary for fungal growth, the utilization of this agro-industrial waste presents a promising approach for the production of ligninolytic enzymes.
Bioassay on lettuce and tomato plants - Germination bioassays
Vinasse has been found to exert strong phytotoxic effects on seed germination and seedling development, primarily due to high concentrations of phenolic compounds and high EC. These negative effects are further exacerbated in the presence of salts or organic compounds, displaying a synergistic effect when these compounds are present in vinasse (Moran-Salazar et al. 2016; Ramana et al. 2002). Moreover, the phenolic compounds commonly found in vinasse have been shown to negatively impact soil microbial activity (Robles-Gonzalez et al. 2012).
To assess the suitability of treated vinasse for irrigation in nursery seedling production, bioassays were conducted. Lettuce and tomato seeds were used to determine the effects of treated and untreated vinasse on seed germination. No germination was observed when raw vinasse at 100, 70 and 50% was added. Additionally, treated vinasse at 100 and 70% exhibited no germination, while treated 50% vinasse showed a germination rate of approximately 50% (data not shown). Consequently, diluted vinasse at concentrations of 25 and 35% were evaluated. All three conditions (25, 35 and 50% treated vinasse) tested showed over 50% germination (Fig. 3), with treated vinasse at 25% showing a germination rate similar to the control (water). However, untreated vinasse at 50% did not exhibit any detectable germination during the evaluated time period.
In addition, tomato germination was evaluated for 14 days (Fig. 4), and the most favorable treatment was found to be treated vinasse at a concentration of 25%. This treatment exhibited an 86% germination rate by the 10th day. On the other hand, untreated vinasse at 25% showed a germination rate of 69% after 12 days. Treated vinasse at 35 and 50% demonstrated the lowest germination percentages, while untreated vinasse at these concentrations failed to show any germination.
Candido et al. (2021) demonstrated the phytotoxicity of vinasse derived from sugarcane bagasse using L. sativa as a bioindicator. On the other hand, Ahmed et al. (2022) reported a reduction in phytotoxicity when vinasse is treated with Trametes sp., the untreated sugarcane vinasse resulted in no germination. Unlike lettuce seeds, the presence of vinasse, whether treated or untreated, exhibited an impact on the germination rate of tomato seeds, causing a noticeable delay in germination. Thus, the negative effect of the vinasse can be stronger in plants with slow germination rate.
Seed germination is a regulated process which is strongly influenced by internal factors such as seed size, seed coat hardness, permeability or seed reserves (Zhang et al. 2020) and external factors such as light, temperature, presence of phytohormones or organic acids and growth media (Arancon, 2012). However, seed genetic factors, environmental conditions, and physicochemical properties of the germination site (porosity, water-holding capacity, aeration, pH, and EC) are determinants of germination success (Haase et al. 2021).
Bioassay on lettuce and tomato plants - Seedling assays
Based on the germination results, seedling assays were conducted to determine whether even treated vinasse could affect key characteristics of seedling development. Two plant species, lettuce and tomato, were selected for evaluation. Lettuce is known for its rapid growth, while tomato exhibits slower germination. Both plants were placed in substrate and watered with either water (control) or treated vinasse at a concentration of 50% every 48 h. Table 2 presents the effects on the main parameters observed in this study.
The addition of vinasse to tomato seeds did not display any significant effects on parameters related to the root, indicating that the roots were not noticeably impacted by the treatment. However, parameters associated with the shoot, such as chlorophyll content, plant height and shoot weight, exhibited significant differences between the control (water) and the treated vinasse.
Similarly, the results with lettuce seeds, as presented in Table 3, demonstrated a comparable pattern to that of tomato seeds. Parameters linked to the root system did not show significant differences between the control and the treated vinasse. On the other hand, chlorophyll, plant height, shoot weight displayed significant differences between the two treatments, suggesting an effect of vinasse treatment on the shoot development of lettuce plants.
Indeed, clear differences were observed in the shoot parameters of both lettuce and tomato plants when treated vinasse are used (Fig. 5). However, no significant differences were found in the root parameters between treatments. Candido et al. 2021 demonstrated that even a 5% concentration of vinasse had a negative impact on lettuce root growth. Sobrero and Ronco (2004) have mentioned that phytotoxicity can be observed directly on root growth, and a delay in root growth can indicate a sublethal response when concentrations are not sufficient to inhibit germination. In this case, since no phytotoxic effect was observed at root level, it suggested that the concentrations of treated vinasse were not inhibitory to root growth.
Considering that seedling production is an essential part of horticultural crop production, stillage treated to a concentration of 50% could be used in the production of tomato and lettuce seedlings. Although some negative effects remain in shoot parameters, the reduction of these effects are noticeable when vinasse is treated with T. sanguineus. Seedling root growth was similar to the control, maintaining seedling quality, a determinant characteristic that can favor early plant establishment and crop uniformity (Vastakaite-Kairiene et al. 2022).
The proper disposal of agroindustry wastewater remains a significant challenge, and while various strategies have been proposed for its treatment, it is important to highlight the potential for recovering or repurposing the valuable compounds present in these effluents. Using vinasse as a culture medium for enzyme production is a viable approach, as demonstrated in this study through the bioremediation of tequila vinasse using T. sanguineus strain. Laccase production was observed in both raw and diluted vinasse. Regarding the bioassays for water reuse, it appears feasible to employ treated vinasse for the initial growth of seedling of economically important high-consumption vegetables such as lettuce and tomato. However, additional analysis and physicochemical steps are required to develop a robust strategy for the reuse of tequila vinasse.
In summary, our results indicate that T. sanguineus can be effectively employed for the treatment of tequila vinasse, as evidenced by the removal of color and phenolic compounds, leading to a significant reduction in the phytotoxicity of the effluent. Therefore, the utilization of agro-industrial waste offers a promising approach to the production of ligninolytic enzymes. Currently, valorizing industrial wastewater has become imperative in order to minimize the quantities to be disposed of and promote their reuse. Moreover, the treatment of vinasse is crucial to prevent environmental contamination.
Acknowledgements
To Jorge Aburto and Instituto Mexicano del Petróleo to authorize the use of the strain. KVTR acknowledges the postdoctoral fellowship (CVU number 558865).
Author contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by KVTR, SGM, OBHF and ICBM. The first draft of the manuscript was written by KVTR and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Funding
The research leading to these results received funding from National Council of Humanities, Science and Technology (CONAHCYT) under grant No. 2095609.
Conflict of interests: The authors have no competing interests to declare that are relevant to the content of this article.
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No competing interests reported.