Skip to main content
SpringerLink
Log in

A Novel Bioactive Antimicrobial Film Based on Polyvinyl Alcohol-Protocatechuic Acid: Mechanism and Characterization of Biofilm Inhibition and its Application in Pork Preservation

  • RESEARCH
  • Published:
Food and Bioprocess Technology Aims and scope Submit manuscript

Abstract

Biofilms in food processing environments pose a potential risk of contamination by pathogenic and spoilage microorganisms, and Yersinia enterocolitica, known for its wide temperature adaptation, is the third most common zoonotic pathogen in the European Union. This study investigates the inhibitory effects of protocatechuic acid (PCA) at sub-inhibitory concentrations on various stages of Y. enterocolitica biofilm formation. Core genes are identified through transcriptome data and weighted gene co-expression network analysis (WGCNA), and the potential binding sites are predicted using molecular docking. Additionally, polyvinyl alcohol (PVA) films containing PCA are prepared to assess their antibacterial and mechanical properties. PCA is found to inhibit biofilm formation by up to 50.5% without affecting bacterial growth, reducing flagella-mediated motility, hydrophobicity, cohesion, and extracellular polysaccharides (EPS) content, and inhibiting the production of acyl-homoserine lactones (AHLs). Transcriptome data reveal that PCA inhibits biofilm formation by suppressing the quorum sensing system and reducing the expression of genes such as CsrD, yenR, FlhD, and FlhC. The PVA-PCA antimicrobial film exhibits robust mechanical properties, effectively reducing total colonies in pork and slowing down the deterioration rate. This study enhances our understanding of PCA’s inhibitory effects on Y. enterocolitica and suggests its potential application as a quorum-sensing inhibitor in antimicrobial films for the food industry.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

Data sharing is not applicable to this article as no new data were created or analyzed in this study.

References

  • Amjadi, S., Emaminia, S., Nazari, M., Davudian, S. H., Roufegarinejad, L., & Hamishehkar, H. (2019). Application of reinforced ZnO nanoparticle-incorporated gelatin bionanocomposite film with chitosan nanofiber for packaging of chicken fillet and cheese as food models. Food and Bioprocess Technology, 12(7), 1205–1219.

    Article  CAS  Google Scholar 

  • Araújo, E. A., de Andrade, N. J., da Silva, L. H. M., de Carvalho, A. F., de Sá Silva, C. A., & Ramos, A. M. (2010). Control of microbial adhesion as a strategy for food and bioprocess technology. Food and Bioprocess Technology, 3(3), 321–332. https://doi.org/10.1007/s11947-009-0290-z

  • Bowen, W. H., Burne, R. A., Hui, W., & Koo, H. (2018). Oral biofilms: Pathogens, matrix, and polymicrobial interactions in microenvironments. Trends in Microbiology, 26(3), 229–242.

  • Bridier, A., Sanchez-Vizuete, P., Guilbaud, M., Piard, J. C., Naietali, M., & Briandet, R. (2015). Biofilm-associated persistence of food-borne pathogens. Food Microbiology, 45(feb.pt.b), 167–178.

  • Chaichi, M., Badii, F., Mohammadi, A., & Hashemi, M. (2023). Novel bioactive composite films based on pectin-nanocellulose-synergistic triple essential oils: Development and characterization. Food and Bioprocess Technology, 16(8), 1794–1805.

    Article  CAS  Google Scholar 

  • Demuth, D. R., Lamont, R. J., James, D., & Shao, H. (2006). The Actinobacillus actinomycetemcomitans ribose binding protein RbsB interacts with cognate and heterologous autoinducer 2 signals. Infection & Immunity, 74(7), 4021–4029.

    Article  Google Scholar 

  • Felipe, V., Breser, M. L., Bohl, L. P., Rodrigues da Silva, E., Morgante, C. A., Correa, S. G., & Porporatto, C. (2019). Chitosan disrupts biofilm formation and promotes biofilm eradication in Staphylococcus species isolated from bovine mastitis. International Journal of Biological Macromolecules, 126, 60–67.

    Article  CAS  PubMed  Google Scholar 

  • Gao, C., Tian, L., Lu, J., Zhang, S., Wu, D., Xaio, P., & Gong, G. (2023). Cinnamaldehyde reduces Yersinia enterocolitica activity and biofilm formation by altering membrane permeability and signalling. Food Bioscience, 53, 102791. https://doi.org/10.1016/j.fbio.2023.102791

  • Gupta, P., Sarkar, S., Das, B., Bhattacharjee, S., & Tribedi, P. (2016). Biofilm, pathogenesis and prevention–a journey to break the wall: A review. Archives of Microbiology, 198(1), 1–15.

    Article  CAS  PubMed  Google Scholar 

  • Jamal, M., Ahmad, W., Andleeb, S., Jalil, F., Imran, M., Nawaz, M. A., Hussain, T., Ali, M., Rafiq, M., & Kamil, M. A. (2018). Bacterial biofilm and associated infections. Journal of the Chinese Medical Association: JCMA, 81(1), 7–11.

    Article  PubMed  Google Scholar 

  • Jenal, U., Reinders, A., & Lori, C. (2017). Cyclic di-GMP: Second messenger extraordinaire. Nature Reviews. Microbiology, 15(5), 271–284.

    Article  CAS  Google Scholar 

  • Klug, T. V., Novello, J., Laranja, D. C., Aguirre, T. A. S., de Oliveira Rios, A., Tondo, E. C., dos Santos, R. P., & Bender, R. J. (2017). Effect of tannin extracts on biofilms and attachment of Escherichia coli on lettuce leaves. Food and Bioprocess Technology, 10(2), 275–283.

    Article  CAS  Google Scholar 

  • Kolonas, A., Vareltzis, P., Kiroglou, S., Goutzourelas, N., Stagos, D., Trachana, V., Tsadila, C., Mossialos, D., Mourtakos, S., & Gortzi, O. (2023). Antioxidant and antibacterial properties of a functional sports beverage formulation. International Journal of Molecular Sciences, 24(4), 3558. https://doi.org/10.3390/ijms24043558

  • Lee, J., Hiibel, S. R., Reardon, K. F., & Wood, T. K. (2010). Identification of stress-related proteins in Escherichia coli using the pollutant cis-dichloroethylene. Journal of Applied Microbiology, 108, 2088–2102.

    CAS  PubMed  Google Scholar 

  • Li, R., Du, W., Yang, J., Liu, Z., & Yousef, A. E. (2018). Control of Listeria monocytogenes biofilm by paenibacterin, a natural antimicrobial lipopeptide. Food Control, 84, 529–535.

    Article  CAS  Google Scholar 

  • Li, S., Liang, H., Wei, Z., Bai, H., Li, M., Li, Q., Qu, M., Shen, X., Wang, Y., & Zhang, L. (2019). An osmoregulatory mechanism operating through OmpR and LrhA controls the motile-sessile switch in the plant growth-promoting bacterium pantoea alhagi. Applied and Environmental Microbiology, 85(10), e00077-e119.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Massimiliano, M., Visscher, P. T., & Lilliam, C. M. (2010). Exopolymeric substances (EPS) from Bacillus subtilis: Polymers and genes encoding their synthesis. FEMS Microbiology Letters, 1, 1–9.

    Google Scholar 

  • McClean, K. H., Winson, M. K., Fish, L., Taylor, A., Chhabra, S. R., Camara, M., Daykin, M., Lamb, J. H., Swift, S., Bycroft, B. W., Stewart, G. S. A. B., & Williams, P. (1997). Quorum sensing and Chromobacterium violaceum: Exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology, 143, 3703–3711.

    Article  CAS  PubMed  Google Scholar 

  • Meng, C. (2019). Differential regulation of physiological activities by RcsB and OmpR in Yersinia enterocolitica. FEMS Microbiology Letters, 366(17).

  • Messinese, E., Pitirollo, O., Grimaldi, M., Milanese, D., Sciancalepore, C., & Cavazza, A. (2023). By-products as sustainable source of bioactive compounds for potential application in the field of food and new materials for packaging development. Food and Bioprocess Technology, 127, 338–348.

    Google Scholar 

  • Miquel, S., Lagrafeuille, R., Souweine, B., & Forestier, C. (2016). Anti-biofilm activity as a health issue. Frontiers in Microbiology, 7, 592.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ng, Y.-K., Grasso, M., Wright, V., Garcia, V., Williams, P., & Atkinson, S. (2018). The quorum sensing system of Yersinia enterocolitica 8081 regulates swimming motility, host cell attachment, and virulence plasmid maintenance. Genes, 9(6), 307.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nicolle, P. (1975). Behavior of Yersinia enterocolitica in Foods. Iranian Journal of Public Health, 2011.11(2011):420732.

  • Palmer, J., Flint, S., & Brooks, J. (2007). Bacterial cell attachment, the beginning of a biofilm. Journal of Industrial Microbiology & Biotechnology, 34(9), 577–588.

    Article  CAS  Google Scholar 

  • Ren, Y., Yu, G., Shi, C., Liu, L., Guo, Q., Han, C., Zhang, D., Zhang, L., Liu, B., Gao, H., Zeng, J., Zhou, Y., Qiu, Y., Wei, J., Luo, Y., Zhu, F., Li, X., Wu, Q., Li, B., Fu, W., Tong, Y., Meng, J., Fang, Y., Dong, J., Feng, Y., Xie, S., Yang, Q., Yang, H., Wang, Y., Zhang, J., Gu, H., Xuan, H., Zou, G., Luo, C., Huang, L., Yang, B., Dong, Y., Zhao, J., Han, J., Zhang, X., & Huang, H. (2022). Majorbio cloud: A one-stop, comprehensive bioinformatic platform for multiomics analyses. iMeta, 1, e12.

  • Shaaban, M., Elgaml, A., & Habib, E.-S.E. (2019). Biotechnological applications of quorum sensing inhibition as novel therapeutic strategies for multidrug resistant pathogens. Microbial Pathogenesis, 127, 138–143.

    Article  CAS  PubMed  Google Scholar 

  • Silva-Rohwer, A. R., Held, K., Sagawa, J., Fernandez, N. L., Waters, C. M., & Vadyvaloo, V. (2021). CsrA enhances cyclic-di-GMP biosynthesis and Yersinia pestis biofilm blockage of the flea foregut by alleviating Hfq-dependent repression of the hmsT mRNA. mBio, 12(4), e0135821.

  • Souza, M. P., Vaz, A. F. M., Silva, H. D., Cerqueira, M. A., Vicente, A. A., & Carneiro-da-Cunha, M. G. (2015). Development and characterization of an active chitosan-based film containing quercetin. Food and Bioprocess Technology, 8(11), 2183–2191.

    Article  CAS  Google Scholar 

  • Toyofuku, M., Inaba, T., Kiyokawa, T., Obana, N., Yawata, Y., & Nomura, N. (2016). Environmental factors that shape biofilm formation. Bioscience, Biotechnology and Biochemistry, 80(1), 7–12. https://doi.org/10.1080/09168451.2015.1058701

  • Verónica, C. M., Julia, T. M., & M., S. A., Carina, A. M., & Alejandra, B. M. (2023). Antibacterial activity of Bacillus Lipopeptides vehiculized and delivered by biopolymeric films. Food and Bioprocess Technology, 110, 291–303.

    Google Scholar 

  • Wang, X., Dubey, A. K., Suzuki, K., Baker, C. S., Babitzke, P., & Romeo, T. (2005). CsrA post-transcriptionally represses pgaABCD, responsible for synthesis of a biofilm polysaccharide adhesin of Escherichia coli. Molecular Microbiology, 56(6), 1648–1663.

    Article  CAS  Google Scholar 

  • Wang, K., Li, W., Cui, H., & Qin, S. (2023). Phylogenetic analysis and characterization of diguanylate cyclase and phosphodiesterase in planktonic filamentous Cyanobacterium Arthrospira sp. International Journal of Molecular Sciences, 24, 15210.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, X., Zeng, Q., Koestler, B. J., Waters, C. M., & Yang, C. H. (2014). Deciphering the components that coordinately regulate virulence factors of the soft rot pathogen Dickeya dadantii. Molecular Plant-Microbe Interactions: MPMI, 27(10), 1119.

    Article  PubMed  Google Scholar 

  • Wu, M., Tian, L., Fu, J., Liao, S., Li, H., Gai, Z., & Gong, G. (2022). Antibacterial mechanism of protocatechuic acid against Yersinia enterocolitica and its application in pork. Food Control, 133, 108573.

    Article  CAS  Google Scholar 

  • Xu, Y., Wen, X., Zhang, D., Schroyen, M., Wang, D., Li, X., & Hou, C. (2023). Changes in the freshness and bacterial community of fresh pork in controlled freezing point storage assisted by different electrostatic field usage frequencies. Food and Bioprocess Technology, 12(5), 852–864.

    Google Scholar 

  • Yang, S., Liu, L., Li, D., Xia, H., Su, X., Peng, L., & Pan, S. (2016). Use of active extracts of poplar buds against Penicillium italicum and possible modes of action. Food Chemistry, 196, 610–618.

    Article  CAS  PubMed  Google Scholar 

  • Zadernowska, A., Chajecka-Wierzchowska, W., & Laniewska-Trokenheim, L. (2014). Yersinia enterocolitica: A dangerous, but often ignored, foodborne pathogen. Food Reviews International, 30(1), 53–70.

    Article  Google Scholar 

  • Zhang, J., Feng, T., Wang, J., Wang, Y., & Zhang, X. H. (2019). The mechanisms and applications of quorum sensing (QS) and quorum quenching (QQ). Journal of Ocean University of China, 18(6), 1427–1442.

    Article  ADS  Google Scholar 

  • Zhao, R., Song, Y., Dai, Q., Kang, Y., Pan, J., Zhu, L., Zhang, L., Wang, Y., & Shen, X. (2017). A starvation-induced regulator, RovM, acts as a switch for planktonic/biofilm state transition in Yersinia pseudotuberculosis. Scientific Reports, 7(1), 639.

    Article  ADS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Special thanks to Jiangnan University for providing the Schrödinger software usage platform.

Funding

This work was financially supported by the National Natural Science Foundation of China (32202007) and Xianyang Qin Chuang Yuan Science and Technology Innovation Project (2021ZDZX-NY-0007).

Author information

Authors and Affiliations

  1. College of Food Science and Engineering, Shaanxi University of Science and Technology, Xian, 710021, Shaanxi, China

    Chang Gao, Lu Tian, Jiaxing Lu & Guoli Gong

Authors
  1. Chang Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lu Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiaxing Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guoli Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

CG: conceptualization, investigation, methodology, validation, writing—original draft; LT: conceptualization, supervision, writing—review and editing, project administration, funding acquisition; JL: validation; GG: conceptualization, supervision, project administration.

Corresponding authors

Correspondence to Lu Tian or Guoli Gong.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gao, C., Tian, L., Lu, J. et al. A Novel Bioactive Antimicrobial Film Based on Polyvinyl Alcohol-Protocatechuic Acid: Mechanism and Characterization of Biofilm Inhibition and its Application in Pork Preservation. Food Bioprocess Technol (2024). https://doi.org/10.1007/s11947-023-03309-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11947-023-03309-5

Keywords

Search

Navigation