Antimicrobial activity of cell-free supernatant of lactic acid bacteria on spoilage bacteria of vacuum-packed sliced emulsion-type sausages

Document Type : Full paper (Original article)

Authors

1 Ph.D. Student in Food Hygiene, Department of Food Hygiene and Public Health, School of Veterinary Medicine, Shiraz University, Shiraz, Iran

2 Department of Food Science and Technology, School of Agriculture, Shiraz University, Shiraz, Iran

3 Department of Food Hygiene and Public Health, School of Veterinary Medicine, Shiraz University, Shiraz, Iran

Abstract

Background: Spoilage is very common in vacuum-packed sliced emulsion-type sausages during refrigerated storage. Aims: This study aimed to investigate the inhibitory effects of cell-free supernatant (CFS) of lactic acid bacteria (LAB) on the spoilage bacteria isolated from vacuum-packed sliced emulsion-type sausages as biological preservatives. Methods: These products from various companies were examined to find the spoilage bacteria. A total of 43 LABs were screened for inhibitory activity against the spoilage bacteria. The MIC90 of protective bacteria and the inhibitory effect of different components obtained from these bacteria was investigated. Results: Four LAB were confirmed as the predominant spoilage bacteria, including Enterococcus mundtii, Latilactobacillus sakei, Latilactobacillus curvatus, and Weissella viridescens. Six strains, including Lactobacillus acidophilus ATCC 4356, Lactobacillus helveticus PTCC 1332, Lactiplantibacillus plantarum CEC 17484, Lactiplantibacillus plantarum LL441, Lacticaseibacillus rhamnosus ATCC 53103, and Pediococcus acidilactici DSM 20284 were able to produce proteinaceous antimicrobial metabolites against the four spoilage agents, which were selected as protective bacteria. CFS of the protective bacteria inhibited four spoilage bacteria by more than 88%. The MIC90 of all protective bacteria was less than 10 mg/ml against E. mandetii and L. sakei. After neutralizing acid and H2O2 of the CFS of P. acidilactici, it was still quite effective against E. mandetii and L. sakei. The sausage’s pasteurization temperature did not affect the bacteria’s active metabolites. Conclusion: The substances derived from these bacteria can be applied as biopreservatives in sliced sausage, even in the pre-pasteurization stage of these products.

Keywords

Main Subjects

References

Abhari, K; Jafarpour, D and Shekarforoush, SS (2018). Effects of in-package pasteurization on preventing spoilage in emulsion vacuum packaged sausages during refrigerated storage. Foods Raw Mater., 6: 40-46.
Albano, H; Todorov, SD; van Reenen, CA; Hogg, T; Dicks, LM and Teixeira, P (2007). Characterization of two bacteriocins produced by Pediococcus acidilactici isolated from “Alheira”, a fermented sausage traditionally produced in Portugal. Int. J. Food Microbiol., 116: 239-247.
Ammor, S; Rachman, C; Chaillou, S; Prévost, H; Dousset, X; Zagorec, M; Dufour, E and Chevallier, I (2005). Phenotypic and genotypic identification of lactic acid bacteria isolated from a small-scale facility producing traditional dry sausages. Food Microbiol., 22: 373-382.
Aymerich, MT; Garriga, M; Costa, S; Monfort, JM and Hugas, M (2002). Prevention of ropiness in cooked pork by bacteriocinogenic cultures. Int. Dairy J., 12: 239-246.
Barcenilla, C; Ducic, M; López, M; Prieto, M and Álvarez-Ordónez, A (2022). Application of lactic acid bacteria for the biopreservation of meat products: A systematic review. Meat Sci., 183: 108661.
Beristain-Bauza, SC; Mani-López, E; Palou, E and López-Malo, A (2016). Antimicrobial activity and physical properties of protein films added with cell-free supernatant of Lactobacillus rhamnosus. Food Control. 62: 44-51.
Bungenstock, L; Abdulmawjood, A and Reich, F (2021). Suitability of lactic acid bacteria and deriving antibacterial preparations to enhance shelf-life and consumer safety of emulsion type sausages. Food Microbiol., 94: 103673.
Chaillou, S; Christieans, S; Rivollier, M; Lucquin, I; Champomier-Verges, MC and Zagorec, M (2014). Quantification and efficiency of Lactobacillus sakei strain mixtures used as protective cultures in ground beef. Meat Sci., 97: 332-338.
Comi, G; Andyanto, D; Manzano, M and Iacumin, L (2016). Lactococcus lactis and Lactobacillus sakei as bio-protective culture to eliminate Leuconostoc mesenteroides spoilage and improve the shelf life and sensorial characteristics of commercial cooked bacon. Food Microbiol., 58: 16-22.
Davies, EA; Milne, CF; Bevis, HE; Potter, RW; Harris, JM; Williams, GC; Thomas, LV and Delves-Broughton, J (1999). Effective use of nisin to control lactic acid bacterial spoilage in vacuum-packed bologna-type sausage. J. Food Prot., 62: 1004-1010.
Devlieghere, F; Vermeiren, L and Debevere, J (2004). New preservation technologies: possibilities and limitations. Int. Dairy J., 14: 273-285.
Dokka, A; Reddy, YK; Spoorthy, GS and Reddy, IS (2018). Protective cultures -A review. IJCMAS., 7: 228-238.
Dos Santos, HRM; Argolo, CS; Argôlo-Filho, RC and Loguercio, LL (2019). A 16S rDNA PCR-based theoretical to actual delta approach on culturable mock communities revealed severe losses of diversity information. BMC Microbiol., 19: 1-14.
Drumond, MM; Tapia-Costa, AP; Neumann, E; Nunes, ÁC; Barbosa, JW; Kassuha, DE and Mancha-Agresti, P (2023). Cell-free supernatant of probiotic bacteria exerted antibiofilm and antibacterial activities against Pseudo-monas aeruginosa: A novel biotic therapy. Front. Pharmacol., 14: 1152588.
Dušková, M; Kameník, J and Karpíšková, R (2013). Weissella viridescens in meat products–a review. Acta Vet. Brno., 82: 237-241.
Flórez, AB and Mayo, B (2018). Genome analysis of Lactobacillus plantarum LL441 and genetic characterisa-tion of the locus for the lantibiotic plantaricin C. Front. Microbiol., 9: 01916.
Frank, JA; Reich, CI; Sharma, S; Weisbaum, JS; Wilson, BA and Olsen, GJ (2008). Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl. Environ. Microbiol., 74: 2461-2470.
Han, Y; Jiang, Y; Xu, X; Sun, X; Xu, B and Zhou, G (2011). Effect of high pressure treatment on microbial populations of sliced vacuum-packed cooked ham. Meat Sci., 88: 682-688.
Hu, P; Xu, XL; Zhou, GH; Han, YQ; Xu, BC and Liu, JC (2008). Study of the Lactobacillus sakei protective effect towards spoilage bacteria in vacuum packed cooked ham analyzed by PCR–DGGE. Meat Sci., 80: 462-469.
Hu, P; Zhou, G; Xu, X; Li, C and Han, Y (2009). Characterization of the predominant spoilage bacteria in sliced vacuum-packed cooked ham based on 16S rDNA-DGGE. Food Control. 20: 99-104.
Iacumin, L; Andyanto, D; Manzano, M; Comuzzo, P and Comi, G (2014). A case of spoilage in wurstel sold in an Italian supermarket. Food Control. 43: 245-250.
İncili, GK; Akgöl, M; Karatepe, P; Üner, S; Tekin, A; Kanmaz, H; Kaya, B; Çalicioğlu, M and Hayaloğlu, AA (2023). Quantification of bioactive metabolites derived from cell-free supernatant of Pediococcus acidilactici and screening their protective properties in frankfurters. Probiotics Antimicrob. Proteins. 4: 1-18.
Islam, KN; Akbar, T; Akther, F and Islam, NN (2016). Characterization and confirmation of Lactobacillus spp. from selective regional yoghurts for probiotic and interference with pathogenic bacterial growth. Asian J. Biol. Sci., 9: 1-9.
Iulietto, MF; Sechi, P; Borgogni, E and Cenci-Goga, BT (2015). Meat spoilage: a critical review of a neglected alteration due to ropy slime producing bacteria. Ital. J. Anim. Sci., 14: 4011.
Jalaei, J; Fazeli, M; Rajaian, H and Shekarforoush, SS (2014). In vitro antibacterial effect of wasp (Vespa orientalis) venom. JVATiTD., 20: 01-06.
Kalschne, DL; Geitenes, S; Veit, MR; Sarmento, CM and Colla, E (2014). Growth inhibition of lactic acid bacteria in ham by nisin: A model approach. Meat Sci., 98: 744-752.
Kalschne, DL; Womer, R; Mattana, A; Sarmento, CMP; Colla, LM and Colla, E (2015). Characterization of the spoilage lactic acid bacteria in “sliced vacuum-packed cooked ham”. Braz. J. Microbiol., 46: 173-181.
Kaya, Hİ and Şimşek, Ö (2020). Characterization of Pediococcus acidilactici PFC69 and Lactococcus lactis PFC77 bacteriocins and their antimicrobial activities in tarhana fermentation. Microorganisms. 8: 1083.
Khorsandi, A; Eskandari, MH; Aminlari, M; Shekarforoush, SS and Golmakani, MT (2019). Shelf-life extension of vacuum packed emulsion-type sausage using combination of natural antimicrobials. Food Control. 104: 139-146.
Lambert, RJW and Pearson, J (2000). Susceptibility testing: accurate and reproducible minimum inhibitory con-centration (MIC) and non-inhibitory concentration (NIC) values. J. Appl. Microbiol., 88: 784-790.
Lim, ES (2016). Inhibitory effect of bacteriocin-producing lactic acid bacteria against histamine-forming bacteria isolated from Myeolchi-jeot. Fish Aquatic Sci., 19: 1-10.
Mani-López, E; Arrioja-Bretón, D and López-Malo, A (2022). The impacts of antimicrobial and antifungal activity of cell-free supernatants from lactic acid bacteria in vitro and foods. Compr. Rev. Food Sci. Food Saf., 21: 604-641.
Ouwehand, AC and Vesterlund, S (2004). Antimicrobial components from lactic acid bacteria. In: Salminen, S; Wright, A and Ouwehand, A (Eds.), Lactic acid bacteria, microbiological and functional aspects. (3rd Edn.), New York, Marcel Dekker Inc., PP: 375-395.
Penderup Jensen, M; Braun, A; Vogensen, FK and Ardö, Y (2009). Study of antimicrobial activity among Lacto-bacillus helveticus strains using three different assays. Ann. Microbiol., 59: 187-190.
Rivas, FP; Castro, MP; Vallejo, M; Marguet, E and Campos, CA (2014). Sakacin Q produced by Lactobacillus curvatus ACU-1: functionality characterization and
antilisterial activity on cooked meat surface. Meat Sci., 97: 475-479.
Saelim, K; Jampaphaeng, K and Maneerat, S (2017). Functional properties of Lactobacillus plantarum S0/7 isolated fermented stinky bean (Sa Taw Dong) and its use as a starter culture. J. Funct. Foods. 38: 370-377.
Salehi, TZ; Mahzounieh, M and Saeedzadeh, A (2005). Detection of invA gene in isolated Salmonella from broilers by PCR method. Int. J. Poult. Sci., 4: 557-559.
Sanni, A; Franz, C; Schillinger, U; Huch, M; Guigas, C and Holzapfel, W (2013). Characterization and technological properties of lactic acid bacteria in the production of “Sorghurt,” a cereal-based product. Food Biotechnol., 27: 178-198.
Turgis, M; Stotz, V; Dupont, C; Salmieri, S; Khan, RA and Lacroix, M (2012). Elimination of Listeria monocytogenes in sausage meat by combination treatment: Radiation and radiation-resistant bacteriocins. Radiat. Phys. Chem., 81: 1185-1188.
Zhang, J; Yang, Y; Yang, H; Bu, Y; Yi, H; Zhang, L; Han, X and Ai, L (2018). Purification and partial characteriza-tion of bacteriocin Lac-B23, a novel bacteriocin production by Lactobacillus plantarum J23, isolated from Chinese traditional fermented milk. Front. Microbiol., 9: 2165.

Files

Share

How to cite

Statistics