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. 2024 May 3;61(11):2157–2165. doi: 10.1007/s13197-024-05986-2

Development of biocomposite films incorporated with the extract from pitcher associated bacteria for the postharvest protection from fungi

R Aswani 1,#, Soumya Das 2,#, K S Sebastian 3, Jyothis Mathew 1, E K Radhakrishnan 1,✉
PMCID: PMC11464650  PMID: 39397836

Abstract

Pythium aphanidermatum is known to cause diseases like damping-off, root rot, stem rot and fruit rot in a wide range of plants. Eventhough many chemical methods have been demonstrated to have the potential to manage these diseases, their benefits are being offset equally by the negative side effects. Therefore, the control of Pythium spp. using natural antifungal agents is of immense significance due to its environmental safety. Here, the plant associated microorganisms with antifungal metabolites have significant promises to be explored both as sustainable biocontrol agents and also as active constituents of antifungal materials. Antimicrobial packaging films prepared using such components can have significant applications to meet the requirements to prevent postharvest loss of agricultural produce by inhibiting the fungal growth. Eventhough there are reports on the development of antimicrobial packaging films for such applications, the use of bacterial extracts with antifungal activity for the same is least investigated. Hence, the present study demonstrates the development of biocomposite films prepared using polyvinyl alcohol (PVA) incorporated with the extracts prepared from bacterial isolates (Serratia sp. NhPB1, Kocuria sp. NhPB49, and Pantoea dispersa NhPB54) previously isolated from the pitcher plant. Here, the individual films were prepared by incorporating 1 mL of bacterial extract in 40 mL of 3% PVA solution and the developed films were then subjected to antifungal activity screening against P. aphanidermatum. The antifungal activity analysis of the films prepared with the incorporation of extracts from Serratia sp. NhPB1, Kocuria sp. NhPB49, and Pantoea dispersa NhPB54 showed remarkable activity against the tested pathogen. The application of biocomposite films on Solanum lycopersicum and Capsicum annuum fruits for its protection from P. aphanidermatum by dip coating method further indicates the promises of developed biocomposite films for active packaging applications.

Keywords: Pitcher associated bacteria, Pythium aphanidermatum, Polyvinyl alcohol, Solanum lycopersicum and Capsicum annuum

Introduction

The loss of fresh produce due to microbial attack cause severe challenge to food security. Here, packaging materials play a pivotal role in the preservation and protection of many products including the fresh produce, refrigerated foods and pantry goods. Among these, the application of active packaging material to inhibit the microbial growth that cause losses in the agricultural productivity and yield at the juvenile or postharvest stage is of great importance (Nair et al. 2021). The active packaging materials have been prepared extensively with the incorporation of diverse antimicrobial components into the film forming material which thereby has the promises to be expected to control fungal agents. Eventhough polymeric materials such as polystyrene, polyethylene, and polypropylene are used for the packaging applications, they have significant environmental concern due to non-degradability and toxicity issues (Hahladakis et al. 2018). Here comes, the demand for biodegradable polymers with engineered antimicrobial properties for its use as efficient alternative to the conventional petroleum based films.

Polyvinyl alcohol (PVA) is a hydrophilic, nontoxic, biocompatible and biodegradable environment-friendly polymer and has been widely used for packaging applications (Abdullah and Dong 2019; Nandhavathy et al. 2020; Suganthi et al. 2020). PVA has also been received FDA approval for its close contact with food products and therefore films prepared from this have been recommended for food packaging applications. PVA has also been submitted to FDA approval for its use under the GRAS category and thereby to make use of this as edible film (GRAS Notice no. 676, 2018) (Sapper et al. 2020). The flexibility, transparency, and less toxicity of PVA further indicates its suitability for packaging applications (Cano et al. 2015a). But due to its high versatility, the commercialization of PVA requires the modifications as per their specific applications. This includes the reinforcement of antimicrobial activity through incorporation of antimicrobial agents, improved mechanical and physical properties by nanoparticle fabrication, etc. (Suganthi et al. 2020; Carbone et al. 2016; Olewnik-Kruszkowska et al. 2019). There are many reports on PVA based films incorporated with natural products or biological materials (Suganthi et al. 2020; Panda et al. 2022). In a previous study, development of antimicrobial films based on chitosan-polyvinyl alcohol blend enriched with ethyl lauroyl arginate (LAE) was found to have attractive properties and can be considered as a food packaging material with low environmental impact (Haghighi et al. 2020). This indicates the promises to incorporate antifungal/bacterial agents into PVA to explore its antifungal applications. However in most of the studies, PVA has been modified with different nanomaterials and plant extract to make it antimicrobial. For example, in another study, preparation, and surface characterization of poly (vinyl alcohol)/plant extracts films conferred significant antibacterial activity against both Gram positive and Gram negative bacteria (Barbălată-Mândru et al. 2022). But use of microbial extracts to generate active PVA based materials for packaging applications is highly unique. This is because many microbial metabolites including lipopeptides, phenazine, biosurfactants and others are antifungal in nature. In our previous study, pitcher associated bacteria was found to produce a blend of chemicals including 1-hydroxyphenazine, surfactin, pyocyanin and other bioactive metabolites as the basis of its antifungal property (Ravi et al. 2021; Aswani et al. 2023a). Therefore in the present study, we focused on the development of PVA based biocomposite films to control P. aphanidermatum infections in Solanum lycopersicum and Capsicum annuum fruits. As P. aphanidermatum is a cosmopolitan fungal pathogen affecting a wide range of plants it also cause a huge postharvest loss (Muthukumar et al. 2011; Al-Hussini et al. 2018). The genus Pythium contains members which are cosmopolitan and have diverse biological significance. Most species are soil inhabitants, although some reside in saltwater estuaries and other aquatic environments. Most Pythium spp. are saprophytes or facultative plant pathogens causing a wide variety of diseases, including damping-off and a range of field and post-harvest rots (Lévesque et al. 2010). Pythium spp. are opportunistic plant pathogens that can cause severe damage whenever plants are stressed or at a vulnerable stage.The involvement of multiple Pythium spp. and their ability to disperse through various routes make it difficult to control their spread and infection (Arora et al. 2021). Here, the use of integrated approaches to design and develop biocomposite films expands its agricultural application in an environment friendly manner.

Materials and methods

Selection of bacteria

Three bacterial isolates Serratia sp. NhPB1, Kocuria sp. NhPB49, and P. dispersa NhPB54 isolated and identified with antagonistic potential against P. aphanidermatum in our previous studies (Aswani et al. 2023a; Ravi et al. 2023; Das et al. 2023) were selected for the development of antifungal biocomposite films.

Preparation of bacterial extracts

Extracts were prepared from all the selected bacterial isolates (Serratia sp. NhPB1, Kocuria sp. NhPB49, and P. dispersa NhPB54) using the solvent extraction method. For this, the bacterial cultures were inoculated into 500 mL of Luria Bertani broth followed by incubation at room temperature for 10 days. After that, the supernatant was collected by centrifugation at 10,000 rpm for 10 min at 4 °C. The collected supernatant was further extracted using ethyl acetate and dried using a rotary vaccum evaporator (Aswani et al. 2023a). After this, the dried extracts were reconstituted in 5 mL of methanol and used for film casting. Also, uninoculated LB broth prepared and processed under same condition was extracted using the same protocol for its use as the control.

Preparation of biocomposite films using selected bacterial extracts

Biocomposite films based on PVA incorporated with the extracts from selected bacterial isolates were prepared by solvent casting method (Tampau et al. 2020). For this, 1.2 g of PVA (Himedia, Cat. No. GRM6170) powder was added into 40 mL of distilled water and continuously mixed with a magnetic stirrer at 90 °C for 3 h. The resulting transparent solution was then separately added with 500 and 1000 μL of bacterial extracts and was mixed with a magnetic stirrer for 1 h at room temperature. The film solution was then casted on glass Petridish and dried in a hot air oven at 60 °C for 24 h. Here, the film prepared using the extract from uninoculated LB was kept as the control. The dried film was then peeled off and labelled as PPB1, PPB49, PPB54, and PLB for the films prepared with the extracts from NhPB1, NhPB49, NhPB54, and uninoculated LB broth control respectively.

Fourier transform infrared spectroscopy (FT-IR) analysis

For understanding the interactions among the various chemical groups present within the biocomposite films PPB1, PPB49, PPB54, and PLB, the FT-IR analysis was performed using Shimadzu IR Prestige 2 FTIR Spectroscopy in attenuated total reflectance mode (ATR). The measurements were recorded in the range of 4500–500 cm−1 with a scan rate of 4 cm−1 (Mathew and Mathew 2019).

Activity of developed biocomposite films against Pythium aphanidermatum

The prepared biocomposite films were further analyzed for its activity against P. aphanidermatum as per the method described by Cano et al. (2015b) with some modifications. Here, two, three, and four discs of 2 × 2 cm2 size were cut each from PPB1, PPB49, PPB54, and PLB and all the film samples were UV sterilized for 15 min. The sterilized films were then immersed in 10 mL of potato dextrose broth followed by the inoculation with an agar block of P. aphanidermatum. All the tubes in triplicates were further incubated in an orbital shaker at room temperature for 48 h and observed for fungal growth inhibition.

Microbial barrier properties of the developed biocomposite films

For the determination of microbial barrier properties of the films, McCartney tubes containing 10 mL of potato dextrose broth was aseptically covered with UV sterilized PPB1, PPB49, PPB54, and PLB films. The edges of the films were sealed using parafilm and incubated at room temperature for 7 days. After the incubation, the presence of fungal growth was checked visibly and confirmed by spread plating of 100 μL of potato dextrose broth. Here, all the experiments were conducted in triplicates on PDA (Jose et al. 2021).

Application of developed biocomposite as active antimicrobial packaging material against P. aphanidermatum by dip coating

The potential application of developed biocomposite as active antimicrobial packaging material was finally checked by dip coating method (Joshy et al. 2020). For this, S. lycopersicum and C. annuum fruits were surface sterilized using sodium hypochlorite as per the previously described method (Aswani et al. 2023b). The surface sterilized fruits were then immersed in the PPB1, PPB49, PPB54, and PLB solutions for 2 h and were dried in a laminar airflow up to 24 h. The coated fruits were further inoculated with an agar block of P. aphanidermatum and incubated at room temperature for 10–15 days and observed for mycelial growth inhibition on the fruit surface. All experiments were conducted in triplicates.

Results

Preparation of biocomposite films using selected bacterial extracts

All the prepared films (PPB1, PPB49, PPB54, and PLB) were peeled off from the Petridish with ease and observed to be transparent with slight orange colour for the PPB49 and PPB54 films (Fig. 1). FT-IR analysis of the developed biocomposite film samples was done to identify the interaction among the individual components within the film matrix. For the PVA control films, a very broad and intense peak was observed at 3800–3100 cm−1 and it could be attributed to the stretching vibrations of the strong OH groups present. The peak seen at 2943 cm−1 could be ascribed to the carbonyl C–H stretching vibrations. The peak at 1609 and 1689 cm−1 indicated the presence of C=C and C=O stretching respectively. Also, smaller peaks observed in the range of 1083 cm−1 could be attributed to the vibrational C–O–C stretching. In the case of PVA composite films prepared with the addition of bacterial extracts from NhPB1, NhPB49, and NhPB54, the peaks were observed to have minor shift in its positioning and intensities when compared with the control PVA film (Fig. 2). This indicated the interaction of bacterial extracts with the PVA matrix.

Fig. 1.

Fig. 1

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Transparency image of the developed biocomposite films a PLB film prepared with the extract of uninoculated LB broth control, b PPB1 films prepared with the extract of NhPB1, c PPB49 film prepared with the extract of NhPB49, and d PPB54 film prepared with the extract of NhPB54

Fig. 2.

Fig. 2

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FTIR analysis of PVA biocomposite films. Where a-d are PPB54, PPB49, PPB1, and PLB films

Activity of developed biocomposite films against Pythium aphanidermatum

The activity of the developed films against P. aphanidermatum showed it to have remarkable mycelial growth inhibition especially for the biocomposite films incorporated with 1 mL of the bacterial extracts. Here, the experimental sets with four discs of 2 × 2 cm2 diameter films were found to have higher antifungal activity when compared to two and three discs. Whereas the control films incorporated with 1 mL of extract prepared from the uninoculated LB broth showed visible mycelial growth in the medium (Fig. 3).

Fig. 3.

Fig. 3

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Activity of biocomposite films against P. aphanidermatum. (1)-Activity of PLB film, (2)- Activity of PPB1 film, (3)- Activity of PPB49 film, (4)- Activity of PPB54 film, a activity with two circular discs, b activity with three circular discs of and c activity with four circular discs of respective films

Microbial barrier properties of the developed biocomposite films

The barrier property of the film which prevents microbial entry is one of the desirable features for the packaging applications. Hence, the developed biocomposite films were also analyzed for their ability to prevent the microbial entry. The results revealed the McCartney tubes covered with the PLB films to have dense fungal growth while the other biocomposite films covered tubes (PPB1, PPB49, and PPB54) did not show any visible growth of microorganisms (Fig. 4). By plating the broth, dense mycelial growth could also be observed for samples from PLB film covered tube and one or two colonies were observed for the samples from PPB1 and PPB49 biocomposite films covered broth. However, no fungal growth could be observed for the samples from PPB54 covered films which further confirmed the promises of developed biocomposite films for packaging applications (Fig. 5).

Fig. 4.

Fig. 4

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Microbial barrier properties of the developed biocomposite films, where a-d are the tubes covered with PLB, PPB1, PPB49, and PPB54 films respectively

Fig. 5.

Fig. 5

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Microbial barrier properties of the developed films, where a-d are the spread plated broth samples from McCartney tubes covered with PLB, PPB1, PPB49, and PPB54 films respectively

Application of developed biocomposite as active packaging against P. aphanidermatum by dip coating

For this, S. lycopersicum and C. annuum fruit samples were dipped in biocomposites (PPB1, PPB49, PPB54) and control (PLB) solutions followed by inoculation with P. aphanidermatum and observation for 10 days. From the results, the biocomposite coated fruits were observed to have higher disease protection. In both S. lycopersicum and C. annuum coated with biocomposite films, absence of growth of P. aphanidermatum could be observed on the fruit surface. While the PLB control film coated fruits showed 100% disease incidence with cottony mycelial growth along with lesions on the surface (Fig. 6). This further indicated the promising packaging applications of the developed biocomposite films.

Fig. 6.

Fig. 6

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Protective effect of biocomposite coated fruits against P. aphanidermatum. (1)- Protective effect of composite films coated S. lycopersicum fruits against P. aphanidermatum, (2)- Protective effect of composite films coated C. annuum fruits against P. aphanidermatum, a–d are the fruits coated with PLB, PPB1, PPB49, and PPB54 biocomposite solution

Discussion

The impact of plastic packaging waste and its accumulation is considered to be a global issue due to its environmental toxicity and challenges to humans, animals, and other living systems (Alabi et al. 2019; Shankar and Rhim 2018). Here comes the need for biodegradable packaging materials as an eco-friendly alternative to the synthetic materials. Therefore the present study is focused on the development of a biodegradable PVA-based material with the potential to be used for the packaging applications. PVA is one among the widely used synthetic polymers for the food packaging owing to its biodegradability, non-toxicity and film-forming properties. Interestingly, the development of PVA based materials is mainly based on its use as packaging film, coating agent, pharmaceutical and cosmetic and other medical applications (Tripathi et al. 2009). However, PVA polymers have limitations with its high-water solubility, low tensile strength, and high degree of water absorption. In order to manage the same, PVA has been fabricated by blending with diverse cross-linking materials to improve its properties as per the specific requirements (Suganthi et al. 2020). Here, biodegradable packaging materials reinforced with antimicrobial agents are highly demanding in the agricultural sector to control the diseases caused by fungal pathogens and also to minimize microbial spoilage. Food spoilage is regarded as the major issue for the food industry leading to food waste, substantial economic losses for producers and consumers. Among causes, fungal contamination can be encountered at various stages of the food chain like post-harvest, processing and storage time (Leyva Salas et al. 2017).

Soil-borne pathogens represent a major challenge to the crops worldwide. Diseases and loses caused by soil-borne pathogens vary from one place and crop to another depending on the pathogen, environmental conditions and management strategies (Halo et al. 2019). Pythium spp. are a major problem worldwide especially for the vegetable crops. Pythium-induced damping-off and root diseases of cucurbits and tomatoes can result in up to 100% loss (Halo et al. 2019; Al-Sa’di et al. 2008). Diseases in these crops are caused by various Pythium species and the most common of which is P. aphanidermatum (Kipngeno et al. 2015; Seonghee Lee and Moorman 2010).

P. aphanidermatum is one of the most aggressive species in the genus and has a wide host range, but little is known about its population genetic structure. For the control of Pythium induced diseases, commercial fungicides like metalaxyl have been widely used. But this inturn is harmful to the consumers and environment which thereby demand the need for the development of effective natural antimicrobial solutions (Suasa-ard et al. 2019; Kumar and Kudachikar 2019). Hence in the present study, the selected bacterial isolates with antagonistic activity against P. aphanidermatum were used for the preparation of biocomposite films to develop active packaging materials. Antimicrobial packaging is an innovative form of packaging and has gained much importance as it involves higher efficiency with lesser toxicity (Perez-Perez et al. 2006). Nithya et al. (2013) and Joshy et al. (2020) have demonstrated the development and application of active films using antibacterial peptide of Bacillus licheniformis Me1 to control the spoilage and pathogenic organisms in food and thereby extending the shelf life of food. However even with many microorganisms having excellent biocontrol applications those used for active packaging is least studied. Hence, the current study has been focused on the development of active films incorporated with extracts prepared from the selected bacteria like Serratia sp. NhPB1, Kocuria sp. NhPB49, and Pantoea dispersa NhPB54 with inherent antifungal potential. As the use of extracts in active packaging materials for postharvest application is an innovative approach, the study highlights immense promises with the development of active packaging materials for applications. Here, the extracts prepared from Serratia sp. NhPB1, Kocuria sp. NhPB49, and Pantoea dispersa NhPB54 were used in different concentrations to prepare active biocomposite films for postharvest protection. The extracts contained diverse bioactive metabolites and hence it was expected to act multimechanistically against fungal pathogens through cell disruption, and inhibition of metabolic functioning. FTIR analysis of the PVA biocomposite film showed a broad band in the range of 3800 to 3100 cm−1 that corresponds to the –OH groups (Paukshtis et al. 2019). Similarly, the peak at 2943 cm−1 attributes to the C-H stretching. Moreover, the peak in the range 1650–1600 cm−1 showed a vibrational C=C groups and at 1710 −1685 cm−1 indicates the C=O stretching. The peak at 1083 cm −1 observed for the PVA film indicates the presence of vibrational C–O–C bending. The result was also in accordance with the previous reports (Jamnongkan et al. 2012). In the case of PVA biocomposite films PPB1, PPB49, and PPB54, all these peaks with minor shifts in peak positioning and intensities could be observed. The variation in the peak shifting might be due to the interaction of bacterial extracts with the PVA matrix without modulating the basic chemical nature of the PVA thin films. From the antifungal activity analysis, the biocomposite films prepared with 1 mL of the extract showed remarkable activity against P. aphanidermatum. The observed antifungal activity of the films against P. aphanidermatum was also in accordance with the reports on the activity of PVA based biocomposite film against the postharvest pathogens Colletotrichum gloeosporioides and Lasiodiplodia theobromae (Nair et al. 2020). Similar studies on the antifungal potential of films incorporated with extract of both A. albida and P. juliflora against C. gloeosporioides and L. theobromae further supports the results of the present study (Nair et al. 2021). In addition to this, these biocomposite films also showed microbial barrier properties as evidenced by the no or minimal microbial growth for the samples from broth covered with the developed biocomposite films. While the control PVA film covered samples showed dense fungal growth. This further indicates the characteristic features of developed packaging material for commercial application. The protective effect of the developed film casting solution on S. lycopersicum and C. annuum fruits against Pythium infection also confirm the application of PVA based biocomposite films for active packaging. Joshy et al. (2023) have described the application of dip coating process as an effective method in the edible coating of fruits and vegetables. From the results, dip coating using PVA based coating solution thus could be an environment friendly approach to manage postharvest loss.

Conclusion

The loss of agricultural products due to microbial attack is a major issue in the food sector. Recent advances in active packaging application showed promises of biocomposite films with inherent antimicrobial activities. PVA based active packaging materials have gained much interest due to its biocompatibility, biodegradability and eco-friendly nature. Hence, the present study has focused on the development of PVA based biocomposite films to act against Pythium attack on S. lycopersicum and C. annuum fruits as it causes a huge reduction at the postharvest stage. Here, the biocomposite films prepared by incorporating the extracts from selected bacterial isolates revealed it to have inhibitory activity against P. aphanidermatum than the PVA control film. Also, the biocomposite film forming solution was found to provide antifungal protection to S. lycopersicum and C. annuum by dip coating process which further confirmed the antimicrobial efficacy of the developed biocomposite films.

Author contributions

RA: Conceptualization, methodology, data curation, original draft preparation. SD: Conceptualization, data curation. KSS: Data curation, JM: data analysis and EKR: Supervision, Conceptualization, methodology, validation, reviewing and editing.

Funding

Kerala state plan fund, KSCSTE-SRS, DST-SERB-SURE project for the instrumental support.

Data availability

All data generated or analyzed during this study are included in this published article [and its supplementary information files].

Declarations

Conflict of interest

The authors declares that they have no conflict of interest.

Ethical approval

This is not applicable because this study does not involve human participants, cell lines, microorganisms, and antibodies.

Consent to participate

This is not applicable because this study does not involve human participants.

Consent to publish

This is not applicable because this study does not involve human participants.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

R. Aswani and Soumya Das have equally contributed to this work.

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Data Availability Statement

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