In vitro detection of antimicrobial impact, organic acids production and phytochemical screening of Musa acuminata wastes after treatment with fungiAbstract
The current study was performed to evaluate the bioactivity of banana wastes against some bacterial and fungal isolates, organic acids production, antioxidant and to screen the phytochemicals were present in Musa acuminate (M. acuminate) wastes. The waste was processed by some microbial species. The organic acids were evaluated in the yield using HPLC. Antioxidant impact of the yield was tested by DPPH assay. Qualitative analysis for phytochemicals were done after each treatment. M. acuminate (Banana) extracts showed moderate effect against the growth of tested microorganisms while this effect became much better after treated with fungal species (Fusarium moniliform; Rhizopus stolonifer; Aspergillus parasiticus; Alternaria alternate; Penicillium expansum and Aspergillus flavus). The MIC ranging from 6.25 to 100 mg/ml, MBC and MFC ranging from 3.125 to 250 mg/ml. Citric acid was the most produced organic acid obtained from banana wastes and highly increased after treatment with fungal isolates used. The antioxidant potential of M. acuminata leaves and pseudostem wastes enhanced after treatment with fungal extracts relative to butylated hydroxytoluene (BHT). Phytochemical screening confirmed the presence of active compounds like glycosides, tannins, saponnins, phenols, steroids and flavonoids in the M. acuminate extracts. The treated banana wastes using fungi could be used as a source of in citric acid production, antioxidant source and other chemical production to be applied in many applications.
Keywords:
Musa acuminate
; fungi; antimicrobial; antioxidant
Resumo
O presente estudo foi realizado para avaliar a bioatividade dos resíduos de banana contra alguns isolados bacterianos e fúngicos, a produção de ácidos orgânicos, antioxidantes e para rastrear os fitoquímicos presentes nos resíduos de Musa acuminata (M. acuminata). Os resíduos foram processados por algumas espécies de fungos. Os ácidos orgânicos foram avaliados quanto ao rendimento por meio de HPLC. O impacto antioxidante do rendimento foi testado pelo ensaio DPPH. Análises qualitativas de fitoquímicos foram feitas após cada tratamento. Os extratos de M. acuminata (banana) apresentaram efeito moderado contra o crescimento dos microrganismos testados, porém esse efeito tornou-se muito melhor após tratamento com espécies fúngicas (Fusarium moniliforme; Rhizopus stolonifer; Aspergillus parasiticus; Alternaria alterna; Penicillium expansum e Aspergillus flavus). A concentração inibitória mínima (CIM) variou de 6,25 a 100 mg/ml, enquanto a concentração bactericida mínima (CBM) e a concentração fungicida mínima (MFC) variaram de 3,125 a 250 mg/ml. O ácido cítrico foi o ácido orgânico obtido a partir de resíduos de banana mais produzido e aumentou bastante após o tratamento com isolados fúngicos utilizados. O potencial antioxidante das folhas de M. acuminata e resíduos de pseudocaule aumentou após tratamento com extratos fúngicos, em comparação com o hidroxitolueno butilado (BHT). A triagem fitoquímica confirmou a presença de compostos ativos como glicosídeos, taninos, saponinas, fenóis, esteroides e flavonoides nos extratos de M. acuminata. Os resíduos de banana tratados com fungos podem ser utilizados como fonte para a produção de ácido cítrico, de antioxidantes e de outros compostos químicos aplicáveis em diversas áreas.
Palavras-chave:
Musa acuminate
; fungos; antimicrobiano; antioxidante
1. Introduction
Bananas are the biggest herbaceous flowering plant in the globe and are members of the Musaceae family. Bananas are the second most grown fruit worldwide, behind citrus and it is consumed worldwide and accounts for 40% of global fruit trade. The therapeutic and decorative benefits of every component of the banana plant benefit humankind (Nadumane and Timsina, 2014). The bloom of the banana, which is regarded as a vegetable, is prepared in numerous ways to serve as a medicine to cure a number of ailments, including diabetes, asthma, and heart difficulties. Pseudo-stem, leaves, sap, and flowers are among the parts of the banana that have been shown to have therapeutic or medicinal qualities, including anti-gastric ulcer, antimicrobial, antioxidant effect and antidiarrheal (Khamboonruang et al., 2015; Dikshit et al., 2016; Budi et al., 2020). Once the bananas are harvested, dead parts, such as leaves and pseudo-stems, release a significant amount of agro-waste into the environment from banana fields (Gupta et al., 2019). According to earlier research on the phytochemical makeup of banana sap, substances like hydrocinnamic acids, and flavonoids (Gupta et al., 2022).
A banana crop produces about 220 tons of plant residual waste per hectare, the majority of which is made up of lignocellulose. Even though these materials can be turned into compost or biogas, doing so is not financially feasible due to shipping. Farmers dispose of much of the leftover garbage they create on roads, in lakes and rivers close by, and this poses a major environmental risk. The effective use of agro-industrial wastes has attracted a lot of attention lately (Hikal et al., 2022). On the basis of these materials, a number of bioprocesses have been created to produce single-cell protein, organic acids, ethanol, and secondary metabolites that are crucial to biology (Subash and Perumalsamy, 2023).
The disposal of waste is a significant issue for emerging countries' agro-based sectors. Agricultural wastes are frequently disposed of on land and in aquatic bodies, which poses significant ecological risks. Ineffective and inefficient solid waste disposal practices lead to aesthetic blights, major health risks, public problems, and other disruptions to society well-being and growth. The scarcity of natural resources and needless waste are the outcomes of the incapacity or refusal to effectively repurpose these substances (Bhushan et al., 2019).
Fungi are well-known for their ability to break down organic waste and can typically hydrolyze complicated chemical compounds to provide a significant amount of energy. This possibility has been used for the manufacture of biomass, the removal of organic waste, and the transformation of that waste into useful products (Legodi et al., 2021). In the current study, the biological activities of banana waste, such as leaves and pseudostem, were assessed following treatment with five fungal isolates as antimicrobial agents. This included measuring the generation of organic acids and phytochemicals as well as antioxidant capacity.
2. Materials and Methods
2.1. Microorganisms
In order to generate wheat grain-based media and investigate their effects with banana wastes throughout this project, six fungal species were obtained from the culture collection of the Regional Centre for Mycology and Biotechnology (RCMB), Al-Azhar University, Cairo, Egypt. Aside from that, eleven test organism stock cultures were acquired from RCMB and utilized in antimicrobial activity. As per Jain et al. (2020), every type of fungus was cultured on Malt Glucose Agar (MGA) and incubated at 28ºC, whereas all bacteria were kept on Nutrient Agar (NA) and kept at 37 ºC.
2.2. Preparation of Inoculums
On 100 milliliters of cooked (10 g) wheat grains supplemented with 1.2% calcium sulphate and 0.2% calcium carbonate, inoculums for six fungal cultures were generated. After 15 days of incubation at 28°C, the cultures were used to create wheat grain-based fungal inoculums (WGBFI) using these grains with mycelium. On MGA liquid medium, every fungal isolate grows without any stress (Reddy et al., 2003).
2.3. Substrate preparation and culture conditions
The pseudostem and leaf components of the agricultural waste from banana plants were separated and cut into approximately 2-cm pieces. They were then cleaned, dried, and mixed using an electronic blender to create a powdered sample. In 1000 ml conical flasks, 25 grams of each component were added, and 75 ml of distilled water was used to wet the mixture. After two hours of autoclaving at 121°C, each flask was individually injected with WGBFI, with a blank flask containing banana waste left un-inoculated test specimens were taken at day 14, when each extract was filtered. The cultures were kept in an incubator at 25 °C. After being dried at room temperature in a rotary evaporator, the extract was preserved. In a separating funnel, filtrates were combined with methanol and chloroform 1:1. For a full extraction, the residue was extracted twice again. A rotary evaporator was used to concentrate the chloroform-methanol extract after it had been defatted using hexane to create a distinct lipid layer. To conduct more experiments, the leftovers were reconstituted in one milliliter of methanol (Reddy et al., 2003).
2.4. Determination of organic acids by HPLC
Using immunoaffinity columns from Rhône-diagnostics technologies Ltd. (Spain), the samples were analyzed for organic acid content. High-performance liquid chromatography (HPLC) was used for the measurement process, with some adjustments made during the first extraction stage. Rather of water: methanol (8:2, v/v), the solvent mixture was methanol: water (8:2). After being filtered and diluted, the sample extract was put to use in an immunoaffinity column. Sigma-Aldrich (Quimica S.A. Spain) was the source of standard organic acids. The calibration curve, operating standards, and stock solution were established and used (Han et al., 2019).
2.5. Antimicrobial testing
The antimicrobial susceptibility testing was conducted using the disc diffusion method. On the surface media, inoculum suspensions of the fungi and bacteria were applied. The plates were split into four sections for the extracts treatment, two additional controls (fungal on MGA media without any treatment and WGBFI), and the control (banana waste blank). Sterile 6mm discs were put on the plates, and each disc was covered with 20µL of extract (20 mg/ml), 30 mg/ml of miconazole nitrate (30 mg/ml of chloramphenicol), and 100% methanol. For 24 hours, all of the NA plates had been placed at 37ºC, while the MGA plates were kept for 48 hours at 28ºC. For every plate, the zone of inhibition was determined (Salam et al., 2023).
2.6. Determination of minimum inhibitory concentration (MIC)
The broth dilution technique was used to detect the MICs. Methanol was used to dissolve the M. acuminata extracts in order to achieve the starting concentration of 100 mg/ml. After a two-fold dilution from the first test concentration, 500 μL of a suspension containing 104 spore/ml of fungi and 108 CFU/ml of bacteria was added to each tube. The test tube was incubated for 24 hours at 37 ºC for bacteria and 48 hours at 28 ºC for fungi. Based on turbidity, the minimum extract concentration (MIC) was calculated as the amount at which the test cultures in the tubes could not grow visibly (Kowalska-Krochmal and Dudek-Wicher, 2021).
2.7. Determination of minimum bactericidal and/or fungicidal concentration (MBC/MFC)
Doubling dilution containing different concentrations as used in MIC determination was done thus: to a 0.5 ml extract, 0.5 ml of sterile distilled water was added, from this test tube labeled „1‟, 0.5 ml of the mixture was taken and added to a test tube labelled „2‟ containing 0.5 ml sterile distilled water, this was done twice and from the last test tube labelled „4‟, 0.5 ml of the mixture was taken so that the mixture remained as 0.5 ml. The stock solution is 0.5 ml (without any dilution) and to this was incorporated to 0.5 ml of test microorganism (500 μL of suspension containing 108 CFU/ml of bacteria and 104 spore/ ml of fungi). These levels were indicated by failure of the extract to kill the microrganisms (Hernandes et al., 2013).
2.8. DPPH radical scavenging activity
To quantitatively measure the properties of radical scavenging through: 50 µL of the test samples (80% methanol as a blank) and 5 ml of 0.004% 2, 2-diphenyl-1-picrylhydrazyl radical (DPPH) scavenging in methanol were present in the reaction mixture. Butylated hydroxytoluene (BHT, Sigma), a commercial antioxidant, served as the study's benchmark. After 30 minutes of incubation, the optical density (OD) of the bottles was measured at 517 nm (Rahman et al., 2015).
2.9. Qualitative phytochemical screening
All samples were subjected to phytochemical screening using standard phytochemical methods (Nortjie et al., 2022).
Examination for Carbohydrate: Two milliliters of boiling methanolic extract were mixed with two milliliters of Molish's reagent and two milliliters of concentrated sulfuric acid (H2SO4). Carbohydrates are indicated by a reddish ring.
To test for reducing sugar content: boil Fehling's solution for five minutes and then add two milliliters of methanolic extracts. Reducing sugar is indicated by a brick-red precipitate.
To test for tannins: add 1 ml of ferric chloride (FeCl3) to 2 ml of methanolic extract. The presence of tannins is indicated by a blue-black or greenish-black precipitate.
To test for saponins, add 5 milliliters of distilled water to 2 milliliters of methanolic extracts. Shake the mixture vigorously for 30 seconds. A steady, persistent foaming is indicative of saponin. Testing for flavonoids involves adding a few drops of concentrated HCl and magnesium ribbon to two milliliters of methanolic extracts; the presence of flavonoids is indicated by a pink or red hue.
To test for alkaloids, mix 2 milliliters of methanolic extract with 10 milliliters of chloroform solution. After that, the extract was examined using Meyer's reagent and treated with ten drops of 10% sulfuric acid. The appearance of white precipitate signifies the existence of alkaloids.
Phenols are detected: by adding 2 milliliters of 20% Na2CO3, 0.5 milliliters of Folin-Cicocalteau reagent, and 2 milliliters of methanol extracts. The presence of bluish color shows the presence of phenols. To test for anthraquinones: add two milliliters of methanolic extracts and two milliliters of 10% NH4OH. Anthraquinones are indicated by a vibrant pink hue. To test for steroids: add 2 milliliters of methanolic extract, 2 milliliters of chloroform, 1 milliliter of concentrated H2SO4, and acetic acid. Steroids are indicated by a blue-green color.
2.10. Statistical analysis
Minimum inhibitory concentration of M. acuminata extracts as well as minimum bactericidal/fungicidal concentrations were done in triplicates and outcome were represented as means ± SD. The change in levels of organic acids in different treatments was done by one-way ANOVA to determine the significance.
3. Results
3.1. Antimicrobial properties of extracts
Table 1 showed that, in vitro effect of wheat grain based fungal inocula (WGBFI) after inoculated with leaves and pseudostem of banana and extracted with methanol against six of high resistant bacterial isolates and six fungal species. Bacterial isolates are highly susceptible to extracts than fungal isolates. Methanol as control show little effect against all organisms used. However, larger clear zones were observed on the plates with 30µg/ml of chloramphenicol and miconazole nitrate (standard antimicrobial drugs) when compared to the tested extracts R. stolonifer leaves extracts showed the most stronger extract than other whereas high inhibition zones were observed against E. coli; S. aureus; S. typhi; S. racemosum and C. elatum followed by P. expansum leaves extracts where recorded high effect on P. mirabilis; S. aureus and P. variotii growth in addition, F. oxysporum pseudostem extract exhibited high effect against S. aureus. Besides. in vitro effect of wheat grain based fungal inoculum (WGBFI) after inoculated with leaves and pseudostem of banana and extracted with methanol against six of high resistant bacterial isolates and six fungal species could be seen in (Table 1). Bacterial isolates are highly susceptible to extracts than fungal isolates. Methanol as control show little effect against all organisms used. R. stolonifer leaves extracts showed the most stronger extract than other whereas high inhibition zones were observed against E. coli; S. aureus; S. typhi; S. racemosum and C. elatum followed by P. expansum leaves extracts where recorded high effect on P. mirabilis; S. aureus and P. variotii growth in addition, F. oxysporum pseudostem extract exhibited high effect against S. aureus.
Antimicrobial activity (zone of inhibition) of Musa acuminate wastes after treatment with eight fungal isolates.
3.2. Determination of MIC &MBC & MFC
The MIC value of extracts used ranged from 6.25 to 100±0.2 mg/ml for the cultures tested depending on the isolate and type of extracts (Table 2). The extract had the highest antimicrobial activity against S. aureus with the lowest MIC value of 6.25±0.2 mg/ml under effect of three extracts and 12.5±0.1 mg/ml under effect of the fourth extract (Table 2). The minimum bactericidal concentration for wastes of banana by fungal treated were ranged from 3.125 to 250 mg/ml (Table 3). The MBC of R. stolonifer leaves extract and P. expansum leaves extracts had good bactericidal effect on S. aureus and S. typhi, respectively. At the same minimum fungicidal concentration (MFC) of P. variotii was killed by F. oxysporum pseudostem extract. On the other hand, P. expansum leaves extracts was highly effective on most of bacterial species used whereas it had bacteriostatic effect on B. thuringensis (250±1.0 mg/ml), and fungaistatic effect on S. racemosum and P. variotii (200±1.0 and 150±1.7 mg/ml, respectively) (Table 3).
3.3. Organic acid production
A significant of production (P≤0.05) of citric acid was obtained using leaves and pseudostem of banana wastes and four different fungal isolates (Table 4), the marked production of citric acid was observed after fungal isolates and banana waste mixed together while other organic acids obtained at trace concentrations.
HPLC chromatography for various organic acids levels from banana agronomic waste treated by fungi.
3.4. Determination of antioxidant action
The IC50 value exhibited by banana leaves was 9.6±0.2mg/ml higher than BHT which was 6.12±0.4mg/ml while treatment of leaves using R. stolonifer; P. expansum extract showed 8.5±0.1 and 8.0 mg/ml, respectively. The antioxidant activity of pseudomycelium of banana was 7.5±0.2 mg/ml. Beside, treatment of pseudostem by F. oxysporum extract give 6.7±0.3 mg/ml and treatment of pseudostem by extract of A. flavus = 7.0±0.2 mg/ml. From the figure below it is clearly observed that M. acuminata leaves and pseudostem wastes are an equally good antioxidant as the BHT standard used and became much better after treated with extracts fungal isolates thus these are considered as a good source of natural antioxidant (Figure 1).
Scavenging effect (%) of crude extract of M. acuminate wastes versus standard at 1.0mg/ml. Ban.: Banana leaves extract; R.s: R. stolonifera; P.e: P. expansum leaves extracts Ps: Psudostem of Banana; F.o: F. oxysporum pseudostem extract; A.f: A. flavus pseudostem extract; BHT: Butylylated Hydroxytoulene (Standard).
3.5. Phytochemical analysis
The phytochemical analysis of M. acuminate wastes and fungal extract reveals that carbohydrates glycosides, tannins, saponins, steroids, phenols and flavonoids were present in the methanolic crude extract and increased after treatment (Table 5).
4. Discussion
Urbanization and industry are driving more environmental pollution worldwide. Our problems require permanent solutions. Fungi may also be one. The utilization of fungi in disposal offers a novel and cost-effective approach to managing wastes (Yadav et al., 2024). In this study six different fungal culture were applied on leaves and psudostem of banana to help in waste management and try to transfer waste to beneficial products. New disposal procedures are based on non-thermal methods and are designed to reduce energy usage and enable removal without the danger of burning the remaining component (Rifna et al., 2023).
In this work antimicrobial impact of treated waste were tested versus group test microorganisms where the highest results were upon treatment of banana leaves by R. stolonifer and P. expansum as well as banana pseudostem by F. oxysporum and A. flavus.
Herbal medicine frequently employs plant extracts, either singly or in combination, although some of these extracts showed a weak biological activity. In this work, the low concentrations of active ingredients in the crude extract at the dose used might have been responsible for the studied ineffective antimicrobial properties against treated banana by fungi (Barba-Ostria et al., 2022). Many reports showed the antimicrobial action of banana peel (Kapadia et al., 2015; Rita et al., 2020) and little is known about it impact upon treatment by fungi.
The disposal of banana trash is currently a challenge in the tropical regions (Hikal et al., 2022). In this work the utilization of banana wastes for fungal synthesis of citric acid and other organic acids was investigated. Citric acid is a tricarboxylic acid with six carbons which initially discovered in lemon juice. The food and beverage sector uses roughly 70% of the manufactured citric acid for diverse applications, followed by the healthcare sector (12%) and other commercial uses (18%) (Torrado et al., 2011).
Nonvolatile organic acids contribute to the ripening of and involved in numerous other metabolic processes. 30 organic acids, including tartaric, oxalic, and malic acids, were found in alcoholic banana fruit extracts according to earlier research. The other acids were found in negligible levels, with malic and citric acids being the main acids (Auta et al., 2014). A notable production of citric acid could be seen in this work by treatment of banana leaves by R. stolonifer and P. expansum as well as banana pseudostem by F. oxysporum and A. flavus Numerous microorganisms, have been assessed for their ability to produce citric acid. Aspergillus niger continued to be the preferred method for producing citric acid because of their high yields, versatility in fermenting inexpensive starting materials, and ease of handling (Behera, 2020).
In this work treatment of banana leaves and psudostem using R. stolonifera, P. expansum, F. oxysporum and A. flavus enhance its antioxidant activity. In accordance with (Bhavani et al., 2023) who illustrated the antioxidant action of banana peel.
In this work treatment of banana waste by fungi slightly enhance the production of phytochemicals. According to earlier findings, banana peels are a rich source of chemical components including Alkaloids, flavonoids, tannins, and saponins that are responsible for the antioxidant action (Carvalho et al., 2018)
5. Conclusion
The present findings suggest that pseudostem wastes and leaves from M. acuminate are a good natural supply of antioxidants, antimicrobials, and other phytochemicals could be used in industrial and agricultural settings, as well as to cure a variety of microbial pathogens.
Acknowledgements
This work was supported by Research Supporting Project, King Saud University, Riyadh, Saudi Arabia [grant number RSP-2025R439].
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