Skip to main content
SpringerLink
Log in

Beet (Beta vulgaris) and Leek (Allium porrum) Leaves as a Source of Bioactive Compounds with Anti-quorum Sensing and Anti-biofilm Activity

  • Original Paper
  • Published:
Waste and Biomass Valorization Aims and scope Submit manuscript

Abstract

The by-products resulted from the processing of raw vegetables contain sometimes appreciable amounts of bioactive compounds can be extracted, purified, concentrated and reused as antipathogenic agents. By altering the pathogenicity of microorganisms, the virulence of the pathogen is attenuated. The objective of this work is to analyze the antibacterial, anti-quorum sensing, anti-biofilm and antioxidant activity of Beta vulgaris (beet) and Allium porrum (leek) leaves as possible antipathogenic agents. The ethanolic extracts of dehydrated beet leaves (EEDBL) showed greater antioxidant activity and a higher concentration of polyphenols than those of ethanolic extract of dehydrated leek leaves (EEDLL). The EEDLL showed major antibacterial activity with a minimal inhibitory concentration (MIC) of 358.33 mg mL−1 and anti-quorum sensing activity at 53.75 mg mL−1 than the EEDBL. Moreover, the EEDLL showed anti-biofilm activity at 268.75 mg mL−1. The use of bioactives extracted from unused portions of different vegetables as antipathogenic substances it is proposed as an alternative to the use of traditional antibacterials.

Graphic Abstract

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

Similar content being viewed by others

References

  1. Socaci, S.A., Fărcaş, A.C., Vodnar, D.C., Tofană, M.: Food Wastes as Valuable Sources of Bioactive Molecules. In: N Shiomi, V. Waisundara (eds) Superfood and Functional Food-The Development of Superfoods and Their Roles as Medicine. IntechOpen, Rijeka, (2017)

    Google Scholar 

  2. Řezbová, H., Belova, A., Škubna, O.: Sugar beet production in the European Union and their future trends. Agris On-line Pap. Econ. Inform. 5, 165–178 (2013)

    Google Scholar 

  3. Cowan, M.M.: Plant products as antimicrobial agents. Clin. Microbiol. Rev. 12(4), 564–582 (1999). https://doi.org/10.1128/cmr.12.4.564

    Article  Google Scholar 

  4. Haddad-Kashani, H., Seyed-Hosseini, E., Nikzad, H., Aarabi, M.H.: Pharmacological properties of medicinal herbs by focus on secondary metabolites. Life Sci. J. 9(1), 509–520 (2012)

    Google Scholar 

  5. Figuerola, F., Hurtado, M.A.L., Estévez, A.M.A., Chiffelle, I., Asenjo, F.: Fibre concentrates from apple pomace and citrus peel as potential fibre sources for food enrichment. Food Chem. 91(3), 395–401 (2005).

    Google Scholar 

  6. Goyeneche, R., Roura, S., Ponce, A., Vega-Gálvez, A., Quispe-Fuentes, I., Uribe, E., Di Scala, K.: Chemical characterization and antioxidant capacity of red radish (Raphanus sativus L.) leaves and roots. J Funct Foods 16, 256–264 (2015).

    Google Scholar 

  7. Vulić, J.J., Ćebović, T.N., Čanadanović-Brunet, J.M., Ćetković, G.S., Čanadanović, V.M., Djilas, S.M., Tumbas Šaponjac, V.T.: In vivo and in vitro antioxidant effects of beetroot pomace extracts. J. Funct. Foods 6, 168–175 (2014). https://doi.org/10.1016/j.jff.2013.10.003

    Article  Google Scholar 

  8. Mohamed, S.M., Jaleel, G.A., Abdallah, H.M.I., Bashandy, S.A.E., Salama, A.B., Mahmoud, A.H.: Hypoglycemic, hypolipidemic and antioxidant activities of Allium porrum leaves extract in streptozotocin-induced diabetic rats. Int. J. PharmTech Res. 9(11), 187–200 (2016).

    Google Scholar 

  9. Velarde, E.D.A., Martínez, D.L.P., Salem, A.Z.M., García, P.G.M., Mariezcurrena Berasain, M.D.: Antioxidant and antimicrobial capacity of three agroindustrial residues as animal feeds. Agrofor. Syst. (2019). https://doi.org/10.1007/s10457-018-00343-7.

    Article  Google Scholar 

  10. Gullón, B., Gullón, P., Eibes, G., Cara, C., De Torres, A., López-Linares, J.C., Ruiz, E., Castro, E.: Valorisation of olive agro-industrial by-products as a source of bioactive compounds. Sci. Total Environ. 645, 533–542 (2018). https://doi.org/10.1016/j.scitotenv.2018.07.155.

    Article  Google Scholar 

  11. Lee, E.H., Jang, K.I., Bae, I.Y., Lee, H.G.: Antibacterial effects of leek and garlic juice and powder in a mixed strains system. Korean J. Food Sci. Technol. 43(4), 518–523 (2011). https://doi.org/10.9721/kjfst.2011.43.4.518

    Article  Google Scholar 

  12. Tankeo, S.B., Lacmata, S.T., Noumedem, J.A.K., Dzoyem, J.P., Kuiate, J.R., Kuete, V.: Antibacterial and antibiotic-potentiation activities of some Cameroonian food plants against multi-drug resistant gram-negative bacteria. Chin. J. Integr. Med. 20(7), 546–554 (2014). https://doi.org/10.1007/s11655-014-1866-7

    Article  Google Scholar 

  13. Fuqua, W.C., Winans, S.C., Greenberg, E.P.: Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 176(2), 269 (1994)

    Google Scholar 

  14. Tang, K., Zhang, X.-H.: Quorum quenching agents: resources for antivirulence therapy. Mar. Drugs 12(6), 3245–3282 (2014)

    Google Scholar 

  15. Gala, V., Desai, K.: Plant based quorum sensing inhibitors of Pseudomonas aeruginosa. Int. J. Pharm. Pharm. Sci. 6, 20–25 (2014)

    Google Scholar 

  16. Ghosh, R., Tiwary, B.K., Kumar, A., Chakraborty, R.: Guava leaf extract inhibits quorum-sensing and Chromobacterium violaceum induced lysis of human hepatoma cells: whole transcriptome analysis reveals differential gene expression. PLoS ONE 9(9), e107703 (2014)

    Google Scholar 

  17. Khan, M.S.A., Zahin, M., Hasan, S., Husain, F.M., Ahmad, I.: Inhibition of quorum sensing regulated bacterial functions by plant essential oils with special reference to clove oil. Lett. Appl. Microbiol. 49(3), 354–360 (2009)

    Google Scholar 

  18. Chu, Y.-Y., Nega, M., Wölfle, M., Plener, L., Grond, S., Jung, K., Götz, F.: A new class of quorum quenching molecules from Staphylococcus species affects communication and growth of gram-negative bacteria. PLoS Pathog. 9(9), e1003654 (2013)

    Google Scholar 

  19. Bhardwaj, A., Vinothkumar, K., Rajpara, N.: Bacterial quorum sensing inhibitors: attractive alternatives for control of infectious pathogens showing multiple drug resistance. Recent Patents Anti-Infect. Drug Discov. 8(1), 68–83 (2013)

    Google Scholar 

  20. Davey, M.E., O'toole, G.A.: Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 64(4), 847–867 (2000).

    Google Scholar 

  21. Costerton, J.W., Stewart, P.S., Greenberg, E.P.: Bacterial biofilms: a common cause of persistent infections. Science 284(5418), 1318–1322 (1999). https://doi.org/10.1126/science.284.5418.1318

    Article  Google Scholar 

  22. Donlan, R.M.: Biofilms: microbial life on surfaces. Emerg. Infect. Dis. 8(9), 881 (2002)

    Google Scholar 

  23. Oral, N.B., Vatansever, L., Aydin, B.D., Sezer, Ç., Guven, A., Gulmez, M., Baser, K.H.C., Kürkçüoğlu, M.: Effect of oregano essential oil on biofilms formed by Staphylococci and Escherichia coli. Kafkas Üniversitesi Veteriner Fakültesi Dergisi 16, S23-S29 (2010).

    Google Scholar 

  24. Kim, Y.-G., Lee, J.-H., Gwon, G., Kim, S.-I., Park, J.G., Lee, J.: Essential oils and eugenols inhibit biofilm formation and the virulence of Escherichia coli O157: H7. Sci. Rep. 6, 36377 (2016)

    Google Scholar 

  25. Niu, C., Gilbert, E.: Colorimetric method for identifying plant essential oil components that affect biofilm formation and structure. Appl. Environ. Microbiol. 70(12), 6951–6956 (2004)

    Google Scholar 

  26. Otero Casal, A., Muñoz Crego, A., Bernárdez Hermida, M., Fábregas Casal, J.: Quorum sensing: el lenguaje de las bacterias. Zaragoza, Acribia, SA (2005)

    Google Scholar 

  27. Turkmen, N., Sari, F., Velioglu, Y.S.: The effect of cooking methods on total phenolics and antioxidant activity of selected green vegetables. Food Chem. 93(4), 713–718 (2005). https://doi.org/10.1016/j.foodchem.2004.12.038

    Article  Google Scholar 

  28. Singleton, V.L., Orthofer, R., Lamuela-Raventós, R.M.: Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. In: Abelson, J, (eds) Methods in Enzymology, vol. 299. pp. 152–178. Academic Press, Cambridge (1999)

    Google Scholar 

  29. Pellegrini, M., Alvarez, M., Ponce, A., Cugnata, N., De Piano, F., Fuselli, S.: Anti-quorum sensing and antimicrobial activity of aromatic species from South America. J. Essent. Oil Res. 26(6), 458–465 (2014)

    Google Scholar 

  30. Hammer, K.A., Carson, C.F., Riley, T.V.: Susceptibility of transient and commensal skin flora to the essential oil of Melaleuca alternifolia (tea tree oil). Am. J. Infect. Control 24(3), 186–189 (1996)

    Google Scholar 

  31. Choo, J., Rukayadi, Y., Hwang, J.K.: Inhibition of bacterial quorum sensing by vanilla extract. Lett. Appl. Microbiol. 42(6), 637–641 (2006)

    Google Scholar 

  32. Fang, K., Jin, X., Hong, S.H.: Probiotic Escherichia coli inhibits biofilm formation of pathogenic E coli via extracellular activity of DegP. Sci. Rep. (2018). https://doi.org/10.1038/s41598-018-23180-1

    Article  Google Scholar 

  33. Čanadanović-Brunet, J.M., Savatović, S.S., Ćetković, G.S., Vulić, J.J., Djilas, S.M., Markov, S.L., Cvetković, D.D.: Antioxidant and antimicrobial activities of beet root pomace extracts. Czech J. Food Sci. 29(6), 575–585 (2011)

    Google Scholar 

  34. Soquetta, M.B., Stefanello, F.S., Huerta, K.d.M., Monteiro, S.S., da Rosa, C.S., Terra, N.N.: Characterization of physiochemical and microbiological properties, and bioactive compounds, of flour made from the skin and bagasse of kiwi fruit (Actinidia deliciosa). Food Chem. 199, 471–478 (2016). https://doi.org/10.1016/j.foodchem.2015.12.022.

    Article  Google Scholar 

  35. Pedreño, M.A., Escribano, J.: Correlation between antiradical activity and stability of betanine from Beta vulgaris L roots under different pH, temperature and light conditions. J. Sci. Food Agric. 81(7), 627–631 (2001)

    Google Scholar 

  36. Fernández, M.V., Jagus, R., Agüero, M.: Evaluation and characterization of nutritional, microbiological and sensory properties of beet greens. Acta Sci. Nutr. Health 1(3), 37–45 (2017)

    Google Scholar 

  37. Biondo, P.B.F., Boeing, J.S., Barizão, É.O., Souza, N.E.d., Matsushita, M., Oliveira, C.C.d., Boroski, M., Visentainer, J.V.: Evaluation of beetroot (Beta vulgaris L.) leaves during its developmental stages: a chemical composition study. Food Sci. Technol. 34, 94–101 (2014).

    Google Scholar 

  38. Kumar, S., Brooks, M.S.-L.: Use of red beet (Beta vulgaris L.) for antimicrobial applications—a critical review. Food Bioprocess Technol., 11, 1–26 (2017).

    Google Scholar 

  39. Kovarovič, J., Bystrická, J., Fehér, A., Lenková, M.: Evaluation and comparison of bioactive substances in selected species of the genus Allium. Potravinarstvo Slovak J. Food Sci. 11(1), 702–708 (2017). https://doi.org/10.5219/833

    Article  Google Scholar 

  40. Radovanović, B., Mladenović, J., Radovanović, A., Pavlović, R., Nikolić, V.: Phenolic composition, antioxidant, antimicrobial and cytotoxic activites of allium porrum L(Serbia) extracts. J. Food Nutr. Res. 3(9), 564–569 (2015)

    Google Scholar 

  41. Lee, S.K., Kader, A.A.: Preharvest and postharvest factors influencing vitamin C content of horticultural crops. Postharvest Biol. Technol. 20(3), 207–220 (2000)

    Google Scholar 

  42. Michiels, J.A., Kevers, C., Pincemail, J., Defraigne, J.O., Dommes, J.: Extraction conditions can greatly influence antioxidant capacity assays in plant food matrices. Food Chem. 130(4), 986–993 (2012)

    Google Scholar 

  43. Beretta, H.V., Bannoud, F., Insani, M., Berli, F., Hirschegger, P., Galmarini, C.R., Cavagnaro, P.F.: Relationships between bioactive compound content and the antiplatelet and antioxidant activities of six allium vegetable species. Food Technol. Biotechnol. 55(2), 266 (2017)

    Google Scholar 

  44. Maidment, D.C.J., Dembny, Z., Watts, D.I.: The anti-bacterial activity of 12 Alliums against Escherichia coli. Nutr. Food Sci. 31(5), 238–241 (2001). https://doi.org/10.1108/eum0000000005614

    Article  Google Scholar 

  45. Lanzotti, V., Scala, F., Bonanomi, G.: Compounds from Allium species with cytotoxic and antimicrobial activity. Phytochem. Rev. 13(4), 769–791 (2014)

    Google Scholar 

  46. Bodini, S., Manfredini, S., Epp, M., Valentini, S., Santori, F.: Quorum sensing inhibition activity of garlic extract and p-coumaric acid. Lett. Appl. Microbiol. 49(5), 551–555 (2009)

    Google Scholar 

  47. Kalia, V.C.: Quorum sensing inhibitors: an overview. Biotechnol. Adv. 31(2), 224–245 (2013)

    Google Scholar 

  48. Truchado, P., Tomás-Barberán, F.A., Allende, A., Ponce, A.: Selected phytochemical bioactive compounds as quorum sensing inhibitors. Acta Hort. 939, 93–97 (2012)

    Google Scholar 

  49. González-Rivas, F., Ripolles-Avila, C., Fontecha-Umaña, F., Ríos-Castillo, A.G., Rodríguez-Jerez, J.J.: Biofilms in the spotlight: detection, quantification, and removal methods. Compr. Rev. Food Sci. Food Saf. 17(5), 1261–1276 (2018)

    Google Scholar 

  50. Husain, F.M., Ahmad, I., Al-thubiani, A.S., Abulreesh, H.H., AlHazza, I.M., Aqil, F.: Leaf extracts of Mangifera indica L. Inhibit quorum sensing–regulated production of virulence factors and biofilm in test bacteria. Front Microbiol 8, 727 (2017).

    Google Scholar 

  51. Lee, J.-H., Kim, Y.-G., Ryu, S.Y., Cho, M.H., Lee, J.: Ginkgolic acids and Ginkgo biloba extract inhibit Escherichia coli O157: H7 and Staphylococcus aureus biofilm formation. Int. J. Food Microbiol. 174, 47–55 (2014)

    Google Scholar 

  52. Mani, A., Mahalingam, G.: Effect of anti-biofilm of different medicinal plants. Asian J. Pharm. Clin. Res. 10(2), 24–32 (2017)

    Google Scholar 

  53. Zhang, J., Rui, X., Wang, L., Guan, Y., Sun, X., Dong, M.: Polyphenolic extract from Rosa rugosa tea inhibits bacterial quorum sensing and biofilm formation. Food Control 42, 125–131 (2014)

    Google Scholar 

  54. Thakur, P., Chawla, R., Tanwar, A., Chakotiya, A.S., Narula, A., Goel, R., Arora, R., Sharma, R.K.: Attenuation of adhesion, quorum sensing and biofilm mediated virulence of carbapenem resistant Escherichia coli by selected natural plant products. Microb. Pathog. 92, 76–85 (2016). https://doi.org/10.1016/j.micpath.2016.01.001

    Article  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the Consejo Nacional de Investigaciones Científicas y Técnicas (PIP 0019 CONICET) and Universidad Nacional de Mar del Plata (UNMDP). The authors thank the members of Grupo de Investigación de Ingeniería en Alimentos, FI, UNMDP. MCP thanks CONICET for her postdoctoral Grant.

Author information

Authors and Affiliations

  1. Grupo de Investigación en Ingeniería en Alimentos (GIIA), Instituto de Ciencia Y Tecnología de Alimentos Y Ambiente (INCITAA-CIC-UNMDP), Facultad de Ingeniería, Universidad Nacional de Mar del Plata, Av. Juan B. Justo 4302, 7600, Mar del Plata, Argentina

    María Celeste Pellegrini & Alejandra Graciela Ponce

  2. Consejo Nacional de Investigaciones Científicas Y Técnicas (CONICET), Godoy Cruz 2290, 1425, Buenos Aires, Argentina

    María Celeste Pellegrini & Alejandra Graciela Ponce

Authors
  1. María Celeste Pellegrini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alejandra Graciela Ponce
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to María Celeste Pellegrini.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pellegrini, M.C., Ponce, A.G. Beet (Beta vulgaris) and Leek (Allium porrum) Leaves as a Source of Bioactive Compounds with Anti-quorum Sensing and Anti-biofilm Activity. Waste Biomass Valor 11, 4305–4313 (2020). https://doi.org/10.1007/s12649-019-00775-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12649-019-00775-x

Keywords

Search

Navigation