Agri-industrial wastes of Mexico crops: phytochemical and antimicrobial propertiesABSTRACT
Agricultural production and the food supply chain generate significant amounts of waste biomass, presenting substantial risks to environmental health. This study focuses on the phytochemical and antimicrobial properties of agri-food waste from regional crops in Mexico, including melon, watermelon, jalapeño, and serrano peppers. The waste materials, specifically seeds from melons and watermelons and whole fruits of jalapeño and serrano peppers, were collected, dehydrated, and processed for compound extraction using ethanol. The extracted compounds were analyzed for total phenolic content, flavonoids, antioxidant activity, vitamin E, capsaicin, and ascorbic acid. Additionally, the antimicrobial activity of these extracts was evaluated against Staphylococcus aureus and Klebsiella pneumoniae using the Kirby-Bauer diffusion method. Results indicated that watermelon waste had the highest concentration of flavonoids content with 213.3 mg/g of QE, while serrano pepper waste exhibited superior values in total phenolic compounds (59.54 mg/h of AGE), antioxidant activity (26040.48 μM/g of equivalent Trolox), vitamin E (3457.4 mg/100 g), capsaicin (296 mg/100 g), and ascorbic acid (3724 mg/100 g) compared to jalapeño waste. Antimicrobial activity results showed that S. aureus was more susceptible to the extracts than Klebsiella sp., with jalapeño pepper waste demonstrating the highest inhibition zones against S. aureus. These findings highlight the potential of agri-food waste as a sustainable source of valuable phytochemicals and antimicrobial agents, promoting the repurposing of agricultural residues into beneficial by-products. This study underscores the importance of utilizing agricultural waste to address environmental pollution and enhance the production of nutritionally rich food products.
Keywords:
Antioxidants; bacteria; melon; peppers; watermelon
RESUMO
A produção agrícola e a cadeia de suprimento de alimentos geram quantidades significativas de biomassa residual, apresentando riscos substanciais à saúde ambiental. Este estudo se concentra nas propriedades fitoquímicas e antimicrobianas de resíduos agroalimentares de culturas regionais no México, incluindo melão, melancia, pimentas jalapeño e serrano. Os resíduos, especificamente sementes de melão e melancia e frutos inteiros de pimentas jalapeño e serrano, foram coletados, desidratados e processados para extração de compostos com etanol. Os compostos extraídos foram analisados quanto ao teor total de fenólicos, flavonoides, atividade antioxidante, vitamina E, capsaicina e ácido ascórbico. Além disso, a atividade antimicrobiana desses extratos foi avaliada contra Staphylococcus aureus e Klebsiella pneumoniae pelo método de difusão de Kirby-Bauer. Os resultados indicaram que o resíduo de melancia apresentou a maior concentração de flavonoides com 213,3 mg/g de QE, enquanto o resíduo de pimenta serrano apresentou valores superiores em compostos fenólicos totais (59,54 mg/g de AGE), atividade antioxidante (26040,48 μM/g de equivalente Trolox), vitamina E (3457,4 mg/100 g), capsaicina (296 mg/100 g) e ácido ascórbico (3724 mg/100 g) em comparação ao resíduo de jalapeño. Os resultados da atividade antimicrobiana mostraram que S. aureus foi mais suscetível aos extratos do que Klebsiella sp., com o resíduo de pimenta jalapeño demonstrando as maiores zonas de inibição contra S. aureus. Essas descobertas destacam o potencial do desperdício agroalimentar como uma fonte sustentável de fitoquímicos valiosos e agentes antimicrobianos, promovendo a reutilização de resíduos agrícolas em subprodutos benéficos. Este estudo destaca a importância do aproveitamento de resíduos agrícolas para combater a poluição ambiental e aprimorar a produção de alimentos ricos em nutrientes.
Palavras-chave:
Antioxidantes; bactérias; melão; pimentões; melancia
In 2010, it was estimated that there were 159 million hectares of cultivated land, and this figure is expected to increase, especially in developed countries, due to population growth (Dubois, 2011). The global population is projected to reach between 9,000 and 10,000 million by 2050 (Ramankutty et al., 2018). Therefore, it is crucial that agricultural production also grows sustainably to meet the population's food demand. However, a significant challenge of modern agriculture is the generation of large volumes of organic agricultural residues, such as discarded fruits and vegetables, peels, fruit remnants, stalks, and forestry residues. These residues often accumulate uncontrollably and can cause various environmental problems (He et al., 2019).
Agricultural production and the food supply chain generate significant amounts of waste biomass, presenting a considerable risk to land and water pollution and, ultimately, public health. However, due to their unique composition, agri-food processing residues are also seen as highly potent materials for biorefinery. They offer various opportunities for the sustainable production of food, feed, chemicals, and energy (Makris & Şahin, 2019). It is worth mentioning that agri-industrial waste is a significant concern due to its environmental pollution and economic impact (Bala et al., 2023). Although the literature on waste recovery is expanding, much is still to be done in the detailed characterization of phytochemical and antimicrobial profiles of agri-food residues from regional crops. The present work aims to cover this gap by investigating the existence of bioactive compounds with potential bioactivities in these residues, leading to the valorization of by-products that fulfil environmental concerns and contribute to food and pharmaceutical world. The FAO reports that these by-products are considered losses and waste because they reduce the food production supply chain and result in global economic losses estimated at around 990 billion dollars (Dhen et al., 2017). Recognizing that this biomass, especially pulp, seeds, and peels, is a renewable source of nutritional and therapeutic compounds encourages a paradigm shift from waste disposal to resource utilization (Bala et al., 2023). Over the past decade, this type of waste has attracted more attention due to its phytonutrient content (secondary metabolites) and the numerous health benefits these compounds offer (Dhiman et al., 2018). Research has shown that these fruits possess health-promoting properties, including antidepressant, anti-inflammatory, antidiabetic, anti-obesity, antibacterial, antidiarrheal, anticancer, anticonvulsant, antihistamine, muscle relaxant, anti-ulcer, and nephroprotective effects, among others (Manivannan et al., 2020). These qualities have sparked global interest in these crops, leading to increased consumption for applications in the food and medicinal industries (Armesto et al., 2020).
Polyphenols, found naturally in fruits and vegetables, are integral to our daily diet. They act as free radical scavengers, potentially interacting with biological systems to help prevent neurodegenerative diseases and cardiovascular disorders in humans. In addition to their potent antioxidant properties, polyphenols frequently demonstrate antimicrobial activity (Agourram et al., 2013). Many plant species are believed to possess medicinal value and high antioxidant potential (Asif, 2015). Similarly, numerous fruits and vegetables contain beneficial antioxidants such as beta-carotene, anthocyanins, and tocopherols. Easily grown vegetables can serve as a primary source of natural antioxidants (Munir et al., 2018).
Phenolic compounds (PC) are an extensive group of secondary metabolites produced by all plants as a reaction to various environmental stimuli, aiding in their adaptation. The PC content in plants is significantly influenced by the specific species and a range of biotic factors (such as bacteria and herbivores) as well as abiotic factors (such as location and time of year) (Kessler & Heil, 2011).
Although phenolic compounds (PC) have been utilized since ancient times because of their presence in plants, human understanding of them is relatively recent (Badhani et al., 2015). These compounds did not gain significant attention until the 1990s, when hundreds were identified in various plant matrices. Their properties were then studied, revealing fascinating biological capabilities for both the plants that contain them and the living beings that interact with them (Stander et al., 2019). As a result, these compounds have become highly valuable, with their applications expanding across different fields and showing promising future potential (Ge et al., 2020).
In this sense, reutilization of agri-food waste coming from regional crops as raw material for producing functional by-products represents a good way to solve undernutrition and reduce consumption of synthetic additives. Consequently, in the present work, the phytochemical and antimicrobial activity of these residues were assessed to justify their potential application in high-value added applications while promoting a more sustainable, circular bioeconomy.
MATERIAL AND METHODS
Study area
The plant materials used were residues of melon, watermelon, jalapeño and serrano pepper fruits collected in agricultural areas of the Comarca Lagunera in the state of Durango, Mexico.
The fruit samples were collected in plastic bags and transferred to the Environmental Engineering Laboratory of the Instituto Tecnologico Superior de Lerdo.
Sample preparation
Only the seeds of the watermelon and melon fruits were used; and from the serrano and jalapeño chili pepper fruits, all the discarded fruit with pulp and seeds were used. Subsequently, they were passed through distilled water to eliminate residues that could contaminate. All fruits waste (watermelon, melon seeds and Serrano and jalapeño pepper) were dehydrated at room temperature (27°C) for a period of 10 days. The dehydrated waste was then processed in a blender (Hamilton Beach®). The pulverized samples were placed in falcon tubes and stored until extraction.
Extraction of compounds
Of each stored sample 1000 mg were taken, and 10 mL of 70% ethanol was added. The samples were subjected to a water bath in test tubes for 30 min, at a temperature between 55 and 58°C. The mixture was then centrifuged at 9200 rpm for 3 minutes; the supernatant was removed from the tubes and filtered with a 45 µm pore syringe filter (Ramirez et al., 2024). Extracts were stored in Eppendorf tubes at −20°C until analysis. Each sample was analyzed in triplicate.
Determination of total phenolic compounds
The content of total phenolic compounds (TPC) was quantified using a modification of the Folin-Ciocalteu method (Ainsworth & Gillespie, 2007). Analyzes were performed in triplicate. The total phenolic compounds were calculated based on a calibration curve with gallic acid as a standard. The results are reported in mg/g of AGE.
Quantification of total flavonoids
The Baba & Malik (2015) technique was used to determine the total flavonoid content. Flavonoid quantification was performed by spectrophotometry at an absorbance of 510 nm. The total flavonoid content was expressed in mg/g of QE. Analyzes were performed in triplicate.
Total antioxidant activity
The analysis of the antioxidant capacity was carried out following the modification of the technique proposed by Domínguez & Ordoñez (2013) using ABTS (2,2'-azinobis [3-ethylbenzothiazoline 6-sulfonic acid]-diammonium salt) as radical (Sigma-Aldrich®, USA). The calibration curve was performed using Trolox (6-hydroxy-2,5,7,8-tetramethylchroman-2-carboxylic acid) as an antioxidant agent; the result was expressed as μM/g of equivalent Trolox.
Quantification of vitamin E
The tocopherol composition was evaluated using an HPLC system (Agilent Technology, 1260 infinity series, USA), equipped with a solvent delivery system, manual sampler, pump, and UV-VIS detector at a wavelength of 292 nm, according to the AOCS method (AOCS, 1996). The results were expressed in mg/100 g.
Determination of capsaicin
Capsaicin was determined using a High-Performance Liquid Chromatography (HPLC) system (Agilent Technologies, USA) which included a solvent delivery system, manual sampler, pump, and UV-VIS detector. These compounds were detected at a wavelength of 280 nm. The separation was performed with C18 column at 60°C (Mlivo et al., 2023). Stock solution of capsaicin (Sigma Aldrich) was prepared at a concentration of 0.5 mg/mL, and their combination was created by mixing random amounts of the individual solutions. The results were expressed in mg/100 g.
Determination of Ascorbic Acid
The analysis of ascorbic acid was carried out using a C18 column with gradient elution of 0.01 M KH2PO4 (A) and acetonitrile (B). Standard materials from Sigma-Aldrich were used for the quantitative determination of ascorbic acid (Bakr, 2018). The results were expressed in mg/100 g.
Antimicrobial activity determination
The antimicrobial activity was evaluated using the Kirby-Bauer diffusion technique (Bauer et al., 1966). The microorganisms tested were Sthaphilococcus aureus and Klebsiella sp., collected from patients using selective media for these microorganisms.
Each of the strains was grown in nutrient broth until reaching a concentration of 1x108 colony-forming units (CFU). Once the concentration was reached, they were inoculated onto Petri dishes with Mueller-Hinton agar. Sterile filter paper disks, 6 mm in diameter, were impregnated with the antioxidants to be evaluated and then placed with sterile tweezers onto the Petri dishes containing the agar. The plates were incubated at 37°C for 16 hours. After this time, the diameters of the inhibition zones were measured to determine the areas of inhibition, with one unit of activity defined as 1 mm2 of the inhibition zone of the indicator bacteria (Barboza-Corona et al., 2007). The experiments were performed in triplicate with six disks per plate. Commercial sensi-discs with antibiotics for gram-positive and gram-negative bacteria were used as positive controls, and disks without antibiotics or antioxidants were used as negative controls.
Statistical analysis
For the analysis of phytochemical compounds present in the various samples of agri-food waste, a randomized block design with three repetitions was used. For the microbiological results, a factorial design was used where factor A was the bacteria and factor B was the samples containing the extracted antioxidants. The data were statistically analyzed using ANOVA to compare the means. The LSD test was used to verify statistically significant differences with a confidence level of 95% (p<0.05). The data were analyzed using SAS 9.0 software.
RESULTS AND DISCUSSION
Phytochemicals evaluated in Agri-food waste
For the variable of total phenolic compounds (PC), the results showed a significant difference between melon and watermelon seeds, with watermelon waste containing a higher concentration of these secondary metabolites. This result can be attributed to the differences given by the type of samples analyzed and the composition of the seed matrices, which can influence the phenolic content despite being obtained with the same extraction methodology. However, there was no significant difference between the waste from these two crops for the variables of total flavonoids (FV) and antioxidant activity (AA) (Table 1).
For the phytochemical variables evaluated in the waste of jalapeño and serrano peppers, it was found that the extract with higher values for each analyzed variable was from serrano pepper waste. The significant difference (p<0.05) is shown in Table 2. In the case of jalapeño and serrano pepper residues, the latter consistently presented higher concentrations of all phytochemical variables (PC, FV, AA, capsaicin, and vitamins C and E). This could be related to the pungency and stress-related metabolic responses of chili peppers, which are known to accumulate more secondary metabolites. Extraction methods were performed identically for all samples; however, environmental factors such as maturity, sun exposure, and water stress during cultivation can also significantly affect metabolite concentrations. Regarding the variable of total phenolic compounds, it is observed that the extracts from serrano pepper waste are higher, with a value of 59.5 mg/g of GAE, whereas the extracts with the lowest amount of PC were from melon waste, with a value of 21.2 mg/g of GAE (Tables 1, 2).
Total flavonoids ranged from 52 to 213 mg/g of QE, with watermelon waste reporting the highest content of FV and jalapeño pepper waste the lowest. This result confirms that the phytochemical composition of agri-food waste is both crop- and tissue-specific. As for antioxidant activity, the range of results varied between 25,992 and 26,076 μM/g of equivalent Trolox, with the highest numerical concentration found in watermelon waste extracts and the lowest AA in jalapeño pepper extracts. However, no significant difference (p>0.05) was found among the different samples analyzed (Tables 1, 2); although, the antioxidant activity did not vary significantly between the samples, the presence of high levels of bioactive compounds in watermelon and serrano waste underscores their potential as natural antioxidants for industrial applications.
For the variables of capsaicin, vitamin E, and vitamin C, the results varied between serrano pepper and jalapeño pepper waste extracts by 62%, 17%, and 75%, respectively, with serrano pepper waste showing higher results for these three variables (Table 2). Differences observed in capsaicin and vitamin content between jalapeño and serrano pepper wastes highlight not only genotypic traits but also the role of fruit maturity and growing conditions in bioactive compound accumulation. The higher capsaicin content in serrano waste indicates potential applications in pharmaceutical formulations as analgesics or antimicrobial agents.
Antimicrobial activity
For antimicrobial activity, two factors were evaluated: bacteria (A) (Staphylococcus aureus and Klebsiella sp.) and extracts from agri-food waste (B). The results showed that for factor A, the bacteria S. aureus exhibited a larger inhibition zone compared to Klebsiella sp.; with a significant difference (p>0.05) of 43% observed in the inhibition results (Table 3).
The results obtained for factor B indicated that the extract achieving the highest inhibition was from jalapeño pepper with the highest value 48.11 mm, followed by serrano pepper and watermelon seeds. It is worth noting that no significant difference was found between the inhibition of jalapeño pepper and watermelon seeds extracts. Lastly, the melon waste extract exhibited a 52% lower inhibition compared to the highest value (Table 4).
The results show that Staphylococcus aureus was more susceptible than Klebsiella sp., consistent with the structure of its gram-positive cell wall, which is more permeable to phenolic compounds (Table 3). Among the extracts, jalapeño residue showed the highest zone of inhibition, closely followed by serrano and watermelon seeds, suggesting broad-spectrum antimicrobial potential (Table 4). These differences could be attributed not only to the concentration of bioactive but also to their chemical structure and synergistic interactions.
Upon analyzing the antimicrobial activity of each treatment considering both factors (bacteria and agri-food waste), it was found that the treatment with the highest inhibition was the jalapeño pepper waste extract against Staphylococcus aureus, with an inhibition zone of 81.3 mm, which may reflect the presence of capsaicinoids and flavonoids known to disrupt bacterial membranes and enzymatic systems. The treatments with the lowest inhibition zones were the jalapeño pepper and melon waste extracts, with inhibition zones of 14.8 mm and 14.3 mm, respectively, against Klebsiella sp. (Table 5) highlighting the resistance mechanisms in Gram-negative bacteria and the importance of compound polarity and size.
The results obtained from the various agri-food wastes analyzed showed that they are an important source of phytochemicals, mainly total phenolic compounds, flavonoids, and antioxidant activity. This type of waste has garnered significant interest from researchers, as it has been found to be rich in antioxidant compounds (Ben-Othman et al., 2020). Mahato et al. (2018) reported a phenolic compound content of 276 and 560 mg/kg for lemon and orange peel and pulp waste, respectively, and values of 10,646 and 22,298 mg/kg for flavonoids in the same residues. When comparing the quantities of bioactive compounds with the results obtained in the present study, it can be observed that the phenolic compounds and flavonoids are higher. Another study on mango seed waste reported values ranging from 7,200 to 13,000 mg/kg for flavonoids, showing a higher concentration of flavonoids compared to jalapeño pepper waste in the present study. However, the concentrations of both citrus and mango fruit wastes for phenolic compounds and flavonoids are similar to those found in melon, watermelon, and serrano pepper wastes (Ballesteros et al., 2019). It is worth mentioning that in the study conducted by Mallek-Ayadi et al. (2017), flavonoid values in melon peels ranged between 67 and 293 μg/g of DW. These results, together with the findings of the current study, indicate that melon waste (peels and seeds) contain favorable amounts of antioxidant compounds that could be utilized to develop other food by-products.
Regarding the antioxidant activity of various agri-food wastes, very varied values have been reported depending on the origin of the analyzed wastes. Literature reports values of 10,586 mg/100 g of TE for mango seeds (Mandha et al., 2021), and for pineapple waste (peels and cores), values of 3.19 mg/g of TE of dry extracts were reported (Lasunon et al., 2022). Another study reported values of 27 IC50 μg/mL for coffee pulp extracts (Duangjai et al., 2016). All the results were studies conducted to determine the antioxidant activity of various wastes using the ABTS method, as was done in this study. These results demonstrate that antioxidant activity, phenolic compound content, and flavonoid content depend on the type of waste and on the extraction method, mostly used to obtain these secondary metabolites and that the efficacy of phenolic compounds is influenced by their interaction with bacterial membranes and metabolic enzymes (Enciso-Martinez et al., 2024).
Some authors state that the polarity of ethanol facilitates the extraction of phenolic compounds, which demonstrated strong antioxidant activity (Anaya-Esparza et al., 2021), therefore, the extracts from the various agri-food wastes evaluated in this study were prepared using ethanol at a 70% concentration.
According to Enciso-Martinez et al. (2024), the antimicrobial effects of these compounds arise from multiple mechanisms; for instance, phenolics and flavonoids can disrupt bacterial cell membranes, change their permeability and function, and also inhibit bacterial growth or cause cell lysis. Additionally, these compounds can hinder enzymes critical for microbial replication and metabolism, thereby decreasing pathogen viability. It has been proposed that the antimicrobial effects of phenolic compounds on foodborne pathogens might stem from a mechanism centered on the cytoplasmic membrane. Specifically, the dissociation of phenolic acids could cause hyper-acidification at the plasma membrane interface. This alteration can impact cell membrane potential and enhance permeability. The differing sensitivity of pathogenic microorganisms to phenolic acids may be accounted for by this mechanism (Vodnar et al., 2017).
In a study conducted by Biswas et al. (2021), the antimicrobial activity of various common vegetable wastes was determined. They evaluated the inhibitory effect of extracts from different wastes on the bacteria Staphylococcus aureus and Escherichia coli. They found inhibition zones ranging from 6.3, 6.6, 6.8, 6.5, to 8.3 mm against S. aureus using extracts from potato peel, cucumber peel, banana peel, cauliflower stems, and pumpkin peel, respectively. According to the inhibition zones reported in the present study for the same bacteria and using the same microbiological method, extracts from watermelon seeds, melon seeds, jalapeño pepper, and serrano pepper waste showed greater antimicrobial effects on the S. aureus strain.
The bacteria Klebsiella pneumoniae is a gram-negative opportunistic pathogen that infects critically ill and immunocompromised patients, causing various infectious diseases such as urinary tract infections, bacteremia, pneumonia, and liver abscesses (Wang et al., 2022).
According to literature, pomegranate peel contains secondary metabolites that inhibit the bacteria K. pneumoniae, with reported inhibition zones ranging between 22 and 34 mm on various fruits of the Brassicaceae family (Dawoud et al., 2023). It is noteworthy that few researchers have conducted antimicrobial tests of agri-industrial waste extracts on this bacterium. Nonetheless, the results obtained in this study showed inhibition zones for K. pneumoniae similar to the previously mentioned values and even higher inhibition zones when the extract was from watermelon seed waste.
The results of this study have demonstrated that crop wastes from the Comarca Lagunera region of Mexico are a valuable source of secondary metabolites, such as phenolic compounds and flavonoids, which confer antioxidant and antibacterial properties. The high content of phenolic compounds, flavonoids, and antioxidant activity observed in agri-food waste, particularly from serrano and watermelon seeds, supports their integration into biotechnological platforms for natural additive development. These residues can be valorized as active ingredients in functional food formulations, offering health-promoting effects (anti-inflammatory, antidiabetic, etc.) and antimicrobial extracts in biodegradable packaging or topical formulations.
The antimicrobial activity against S. aureus and K. pneumoniae was positive for all evaluated waste extracts, with watermelon seeds showing the best results. Moreover, the antimicrobial activity shown against S. aureus and K. pneumoniae confirms their potential in pharmaceutical applications, particularly in combating foodborne pathogens and resistant strains.
These findings underscore the value of agri-food waste as a sustainable resource, offering environmental and economic benefits through waste reduction and the development of high-value products. Further studies should explore scaling extraction methods, compound stability, and regulatory frameworks to ensure their safe incorporation into industrial processes.
ACKNOWLEDGMENTS
We thank the Secretaria de Ciencias, Humanidades, Tecnología e Innovacion (Secretary of Science, Humanities, Technology and Innovation; SECIHTI) for the postdoctoral fellowship of RAMG (CVU: 583735).
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