Anti-Listeria activity of postbiotics of Lactiplantibacillus sakei in beef fillet using aerosolization technique

Document Type : Original Article

Authors

1 PhD Candidate of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran

2 Department of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran

3 Urmia University

4 Graduate of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran

Abstract
In recent years, the use of probiotics and their metabolites, known as postbiotics as natural preservatives has received increasing attention in the food industry. This study aimed to prepare and characterize postbiotics of Lactiplantibacillus sakei and to investigate its application as an anti-Listeria solution on beef fillets using an aerosolization technique. The functional groups, including organic acids, polysaccharides and other minor metabolites, were identified by Fourier transform infrared (FTIR) in the postbiotics. The 2, 2′-diphenyl-1-picrylhydrazyl radical scavenging activity of the postbiotics was reported as 0.82 mg mL-1. The antimicrobial test using the agar well diffusion method revealed a zone of inhibition of 27.00 ± 1.20 mm. Application of an aerosolized postbiotics solution resulted in a significant reduction in Listeria monocytogenes counts on beef fillets, reaching 3.30 log10 CFU g-1 over a 15-day storage period at 4.00 ± 1.00 ˚C. The results of this study revealed that the postbiotics of L. sakei was an effective antimicrobial additive for controlling foodborne pathogens in beef fillets and aerosolization is a promising method for developing an antimicrobial coating on meat to enhance meat safety.

Keywords

Subjects


  1. Ghorbani M, Moradi M, Tajik H, et al. Carbon dots embedded bacterial cellulose membrane as active packaging: toxicity, in vitro release and application in minced beef packaging. Food Chem 2024; 433: 137311. doi: 10.1016/j.foodchem.2023.137311.
  2. Barcenilla C, Ducic M, López M, et al. Application of lactic acid bacteria for the biopreservation of meat products: A systematic review. Meat Sci 2022; 183: 108661. doi: 10.1016/j.meatsci.2021.108661.
  3. Mohammadi R, Moradi M, Tajik H, et al. Potential application of postbiotics metabolites from bio-protective culture to fabricate bacterial nanocellulose based antimicrobial packaging material. Int J Biol Macromol 2022; 220: 528-536.
  4. Pisoschi AM, Pop A, Georgescu C, et al. An overview of natural antimicrobials role in food. Eur J Med Chem 2018; 143: 922-935.
  5. Rasouli Y, Moradi M, Tajik H, et al. Fabrication of anti-Listeria film based on bacterial cellulose and Lactobacillus sakei-derived bioactive metabolites; application in meat packaging. Food Biosci 2021; 42: 101218. doi: 10.1016/j.fbio.2021.101218.
  6. Zheng J, Wittouck S, Salvetti E, et al. A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int J Syst Evol Microbiol 2020; 70(4): 2782-2858.
  7. Amiri S, Kazemi S. Concept and potential applications of postbiotics in the food industry [Persian]. J Food Sci Technol 2022; 19(126): 87-101.
  8. İncili GK, Akgöl M, Karatepe P, et al. Quantification of bioactive metabolites derived from cell-free super-natant of Pediococcus acidilactici and screening their protective properties in frankfurters. Probiotics Anti-microb Proteins 2023. doi: 10.1007/s12602-023-10147-6.
  9. de Toledo Guimarães J, Barros C, Sharafi H, et al. Postbiotics preparation for use in food and beverages. In: da Cruz AG, Silva MC, Pimentel TC, et al (Eds). Probiotic foods and beverages. 1st Berlin, Germany: Springer Nature 2023; 223-242.
  10. Sharafi H, Divsalar E, Rezaei Z, et al. The potential of postbiotics as a novel approach in food packaging and biopreservation: a systematic review of the latest developments. Crit Rev Food Sci Nutr 2023. doi: 10.1080/10408398.2023.2253909.
  11. İncili GK, Karatepe P, Akgöl M, et al. Impact of chitosan embedded with postbiotics from Pediococcus acidilactici against emerging foodborne pathogens in vacuum-packaged frankfurters during refrigerated storage. Meat Sci 2022; 188: 108786. doi: 10.1016/ j.meatsci.2022.108786.
  12. Da Costa RJ, da Silva AP, da Fonseca RN, et al. Characterization of Enterococcus faecium EO1 isolated from mutton and activity of bacteriocin-like substances in the control of Listeria monocytogenes in fresh mutton sausage. LWT 2021; 141: 110954. doi: 10.1016/j.lwt.2021.110954.
  13. De Lima AL, Guerra CA, Costa LM, et al. A natural technology for vacuum-packaged cooked sausage preservation with potentially postbiotic-containing preservative. Fermentation 2022; 8(3): 106. doi: 10.3390/fermentation8030106.
  14. İncili GK, Karatepe P, Akgöl M, et al. Characterization of lactic acid bacteria postbiotics, evaluation in-vitro antibacterial effect, microbial and chemical quality on chicken drumsticks. Food Microbiol 2022; 104: 104001. doi: 10.1016/j.fm.2022.104001.
  15. Moradi M, Tajik H, Mardani K, et al. Efficacy of lyophilized cell-free supernatant of Lactobacillus salivarius (Ls-BU2) on Escherichia coli and shelf life of ground beef. Vet Res Forum 2019; 10(3): 193-198.
  16. Sullivan DJ, Cruz-Romero MC, Hernandez AB, et al. A novel method to deliver natural antimicrobial coating materials to extend the shelf-life of European hake (Merluccius merluccius) fillets. Food Packag Shelf Life 2020; 25: 100522. doi: 10.1016/ j.fpsl.2020.100522.
  17. Jiang Y, Fan X, Li X, et al. Inactivation of Salmonella Typhimurium and quality presevation of cherry tomatoes by in-package aerosolization of anti-microbials. Food Control 2017; 73: 411-420.
  18. İncili GK, Akgöl M, Karatepe P, et al. Inhibitory effect of bioactive compounds de­rived from freeze-dried paraprobiotic of Pediococcus acidilactici against food-borne pathogens: In-vitro and food model studies. Food Res Int 2023; 170: 113045. doi: 10.1016/j.foodres. 2023.113045.
  19. İncili GK, Akgöl M, Karatepe P, et al. Whole-cell postbiotics: an innovative ap­proach for extending the shelf life and controlling major foodborne pathogens in chicken breast fillets. Food Bioprocess Tech 2023; 16: 1502-1524.
  20. Chakchouk-Mtibaa A, Smaoui S, Ktari N, et al. Biopreservative efficacy of bacteriocin bacFL31 in raw ground turkey meat in terms of microbiological, physicochemical, and sensory qualities. Biocontrol Sci 2017; 22(2): 67-77.
  21. Zagorec M, Champomier-Vergès M-C. Lactobacillus sakei: A starter for sausage fermentation, a protective culture for meat products. Microorganisms 2017; 5(3): 56. doi: 10.3390/microorganisms5030056.
  22. Beristain-Bauza SDC, Mani-López E, Palou E, et al. Antimicrobial activity of whey protein films supplemented with Lactobacillus sakei cell-free supernatant on fresh beef. Food Microbiol 2017; 62: 207-211.
  23. N Kocabey, M Yılmaztekin, Hayaloglu AA. Effect of maceration duration on physicochemical characteristics, organic acid, phenolic compounds and antioxidant activity of red wine from Vitis vinifera Karaoglan. J Food Sci Technol 2016; 53(9): 3557-3565.
  24. Arrioja-Bretón D, Mani-López E, Palou E, et al. Antimicrobial activity and storage stability of cell-free supernatants from lactic acid bacteria and their applications with fresh beef. Food Control 2020; 115: 107286. doi: 10.1016/j.foodcont.2020.107286.
  25. Shen C, Lemonakis L, Etienne X, et al. Evaluation of commercial antimicrobials against stress-adapted Campylobacter jejuni on broiler wings by using immersion and electrostatic spray and an economic feasibility analysis. Food Control 2019; 103: 161-166.
  26. Shafipour Yordshahi A, Moradi M, Tajik H, et al. Design and preparation of antimicrobial meat wrapping nanopaper with bacterial cellulose and postbiotics of lactic acid bacteria. Int J Food Microbiol 2020; 321: 108561. doi: 10.1016/j.ijfoodmicro.2020.108561.
  27. Moradi M, Molaei R, Guimarães JT. A review on preparation and chemical analysis of postbiotics from lactic acid bacteria. Enzyme Microb Technol 2021; 143: 109722. doi: 10.1016/j.enzmictec.2020.109722.
  28. Trabelsi I, Ben Slima S, Chaabane H, et al. Purification and caracterization of a novel exopolysaccharides produced by Lactobacillus sp, Ca6. Int J Biol Macromol 2015; 74: 541-546.
  29. Satpute SK, Kulkarni GR, Banpurker AG, et al. Biosurfactant/s from Lactobacilli species: prpoperties, challenges and potential biomedical application. J Basic Microbiol 2016; 56(11): 1140-1158.
  30. Chang HM, Foo HL, Loh TC, et al. Comparative studies of inhibitory and antioxidant activities, and organic acids compositions of postbiotics produced by probiotic Lactiplantibacillus plantarum strains isolated from malaysian foods. Front Vet Sci 2021; 7: 602280. doi: 10.3389/fvets.2020.602280.
  31. Šebek J, Knaanie R, Albee B, et al. Spectroscopy of the C-H stretching vibrational band in selected organic molecules. J Phys Chem A 2013; 117(32): 7442-7452.
  32. Martinez-Morales F, Alonso-Castro AJ, Zapata-Morales JR, et al. Use of standardized units for a correct interpretation of IC50 values obtained from the inhibition of the DPPH radical by natural antioxidants. Chem Pap 2020; 74: 3325-3334.
  33. İncili GK, Karatepe P, Akgöl M, et al. Characterization of Pediococcus acidilactici postbiotic and impact of postbiotic-fortified chitosan coating on the microbial and chemical quality of chicken breast fillets. Int J Biol Macromol 2021; 184: 429-437.
  34. Hamad GM, Abdelmotilib NM, Darwish AMG, et al. Commercial probiotic cell-free supernatants for inhibition of Clostridium perfringens poultry meat infection in Egypt. Anaerob 2020; 62: 102181. doi: 10.1016/j.anaerobe.2020.102181.
  35. Diop MB, Alvarez VB, Guiro AT, et al. Efficiency of neutralized antibacterial culture supernatant from bacteriocinogenic lactic acid bacteria supplemented with salt in control of microorganisms present in senegalese artisanally handled fish by immersion preservative technology during guedj seafood processing at 10°C and 30°C. J Food Microbiol Saf Hyg 2016; 1: 102. doi: 10.4172/2476-2059.1000102.
  36. Wang B, Song Q, Zhao F, et al. Production optimization, partial characterization and properties of an exopolysaccharide from Lactobacillus sakei L3. Int J Biol Macromol 2019; 141: 21-28.
  37. Bajpai VK, Han JH, Rather IA, et al. characterization and antibacterial potential of lactic acid bacterium Pedioccoccus pentosaceus 4I1 isolated from freshwater fish Zacco koreanus. Front Microbiol 2016; 7: 2037. doi: 10.3389/fmicb.2016.02037.
  38. National Advisory Committee on Microbiological Criteria for Foods. Parameters for determining inoculated pack/challenge study protocols. J Food Prot 2010; 73(1): 140-202.
  39. Hartmann HA, Wilke T, Erdmann R. Efficacy of bacteriocin-containing cell-free culture supernatants from lactic acid bacteria to control Listeria monocytogenes in food. Int J Food Microbiol 2011; 146(2): 192-199.
  40. Ünlü G, Nielsen B, Ionita C. Inhibition of Listeria monocytogenes in hot dogs by surface application of freeze-dried bacteriocin-containing powders from lactic acid bacteria. Probiotics Antimicrob Proteins 2016; 8(2): 102-110.
Volume 15, Issue 5
May 2024
Pages 223-229

  • Receive Date 25 October 2023
  • Revise Date 25 November 2023
  • Accept Date 02 December 2023