Biopreservation strategies using bacteriocins to control meat spoilage and foodborne outbreaks

Submitted: 11 April 2024
Accepted: 9 July 2024
Published: 17 October 2024
Abstract Views: 124
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Fresh meat is highly perishable, presenting challenges in spoilage mitigation and waste reduction globally. Despite the efforts, foodborne outbreaks from meat consumption persist. Biopreservation offers a natural solution to extend shelf life by managing microbial communities. However, challenges include the effective diffusion of bacteriocins through the meat matrix and the potential inhibition of starter cultures by bacteriocins targeting closely related lactic acid bacteria (LAB). LAB, predominant in meat, produce bacteriocins – small, stable peptides with broad antimicrobial properties effective across varying pH and temperature conditions. This review highlights the recent advances in the optimization of bacteriocin use, considering its structure and mode of action. Moreover, the strengths and weaknesses of different techniques for bacteriocin screening, including novel bioengineering methods, are described. Finally, we discuss the advantages and limitations of the modes of application of bacteriocins toward the preservation of fresh, cured, and novel meat products.

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Achemchem F, Martínez-Bueno M, Abrini J, Valdivia E, Maqueda M, 2005. Enterococcus faecium F58, a bacteriocinogenic strain naturally occurring in Jben, a soft, farmhouse goat’s cheese made in Morocco. J Appl Microbiol 99:141-50. DOI: https://doi.org/10.1111/j.1365-2672.2005.02586.x
Aljohani AB, Al-Hejin AM, Shori AB, 2023. Bacteriocins as promising antimicrobial peptides, definition, classification, and their potential applications in cheeses. Food Sci Technol 43:e118021. DOI: https://doi.org/10.1590/fst.118021
Almeida-Santos AC, Novais C, Peixe L, Freitas AR, 2021. Enterococcus spp. as a producer and target of bacteriocins: a double-edged sword in the antimicrobial resistance crisis context. Antibiotics 10:1215. DOI: https://doi.org/10.3390/antibiotics10101215
Amarh MA, Laryea MK, Borquaye LS, 2023. De novo peptides as potential antimicrobial agents. Heliyon 9:e19641. DOI: https://doi.org/10.1016/j.heliyon.2023.e19641
Ayrapetyan M, Oliver JD, 2016. The viable but non-culturable state and its relevance in food safety. Curr Opin Food Sci 8:127-33. DOI: https://doi.org/10.1016/j.cofs.2016.04.010
Baillo AA, Cisneros L, Villena J, Vignolo G, Fadda S, 2023. Bioprotective lactic acid bacteria and lactic acid as a sustainable strategy to combat Escherichia coli O157:H7 in meat. Foods 12:231. DOI: https://doi.org/10.3390/foods12020231
Balouiri M, Sadiki M, Ibnsouda SK, 2016. Methods for in vitro evaluating antimicrobial activity: a review. J Pharm Anal 6:71-9. DOI: https://doi.org/10.1016/j.jpha.2015.11.005
Balutis AM, 2014. Quantification of bacteriocin gene expression in Carnobacterium maltaromaticum ATCC PTA-5313. Available from: https://era.library.ualberta.ca/items/294af8ad-8bbe-4ae5-95dd-680c22caf4df.
Barcenilla C, Puente A, Cobo-Díaz JF, Alexa EA, Garcia-Gutierrez E, O’Connor PM, Cotter PD, González-Raurich M, López M, Prieto M, Álvarez-Ordóñez A, 2023. Selection of lactic acid bacteria as biopreservation agents and optimization of their mode of application for the control of Listeria monocytogenes in ready-to-eat cooked meat products. Int J Food Microbiol 403:110341. DOI: https://doi.org/10.1016/j.ijfoodmicro.2023.110341
Bastos MCF, Coelho MLV, Santos OCS, 2015. Resistance to bacteriocins produced by Gram-positive bacteria. Microbiology 161:683-700. DOI: https://doi.org/10.1099/mic.0.082289-0
Ben Braïek O, Smaoui S, Ennouri K, Ben Ayed R, Hani K, Mastouri M, Ghrairi T, 2020. In situ Listeria monocytogenes biocontrol and sensory attributes enhancement in raw beef meat by Enterococcus lactis. J Food Process Preserv 44:e14633. DOI: https://doi.org/10.1111/jfpp.14633
Beristain-Bauza SC, Mani-López E, Palou E, López-Malo A, 2017. Antimicrobial activity of whey protein films supplemented with Lactobacillus sakei cell-free supernatant on fresh beef. Food Microbiol 62:207-11. DOI: https://doi.org/10.1016/j.fm.2016.10.024
Bindu A, Lakshmidevi N, 2021. In vitro and in silico approach for characterization of antimicrobial peptides from potential probiotic cultures against Staphylococcus aureus and Escherichia coli. World J Microbiol Biotechnol 37:172. DOI: https://doi.org/10.1007/s11274-021-03135-x
Bromberg R, Moreno I, Zaganini CL, Delboni RR, de Oliveira, J, 2004. Isolation of bacteriocin-producing lactic acid bacteria from meat and meat products and its spectrum of inhibitory activity. Braz J Microbiol 35:137-44. DOI: https://doi.org/10.1590/S1517-83822004000100023
Broucke K, Van Pamel E, Van Coillie E, Herman L, Van Royen G, 2023. Cultured meat and challenges ahead: a review on nutritional, technofunctional and sensorial properties, safety and legislation. Meat Sci 195:109006. DOI: https://doi.org/10.1016/j.meatsci.2022.109006
Bungenstock L, Abdulmawjood A, Reich F, 2020. Evaluation of antibacterial properties of lactic acid bacteria from traditionally and industrially produced fermented sausages from Germany. PLoS One 15:e0230345. DOI: https://doi.org/10.1371/journal.pone.0230345
Casaus P, Nilsen T, Cintas LM, Nes IF, Hernández PE, Holo H, 1997. Enterocin B, a new bacteriocin from Enterococcus faecium T136 which can act synergistically with enterocin A. Microbiology 143:2287-94. DOI: https://doi.org/10.1099/00221287-143-7-2287
Carrión MG, Corripio MAR, Contreras JVH, Marrón MR, Olán GM, Cázares ASH, 2023. Optimization and characterization of taro starch, nisin, and sodium alginate-based biodegradable films: antimicrobial effect in chicken meat. Poul Sci 102:103100. DOI: https://doi.org/10.1016/j.psj.2023.103100
Chen H, Ma L, Dai H, Fu Y, Wang H, Zhang Y, 2022. Advances in rational protein engineering toward functional architectures and their applications in food science. J Agric Food Chem 70:4522-33. DOI: https://doi.org/10.1021/acs.jafc.2c00232
Choi GH, Holzapfel WH, Todorov SD, 2023. Diversity of the bacteriocins, their classification and potential applications in combat of antibiotic resistant and clinically relevant pathogens. Crit Rev Microbiol 49:578-97. DOI: https://doi.org/10.1080/1040841X.2022.2090227
Crandall AD, Montville TJ, 1998. Nisin resistance in Listeria monocytogenes ATCC 700302 is a complex phenotype. Appl Environ Microbiol 64:231-7. DOI: https://doi.org/10.1128/AEM.64.1.231-237.1998
Cui Y, Zhang C, Wang Y, Shi J, Zhang L, Ding Z, Qu X, Cui H, 2012. Class IIa bacteriocins: diversity and new developments. Int J Mol Sci 13:16668-707. DOI: https://doi.org/10.3390/ijms131216668
da Costa RJ, Voloski FLS, Mondadori RG, Duval EH, Fiorentini ÂM, 2019. Preservation of meat products with bacteriocins produced by lactic acid bacteria isolated from meat. J Food Qual 2019:e4726510. DOI: https://doi.org/10.1155/2019/4726510
Dallagnol AM, Barrio Y, Cap M, Szerman N, Castellano P, Vaudagna SR, Vignolo G, 2017. Listeria inactivation by the combination of high hydrostatic pressure and lactocin AL705 on cured-cooked pork loin slices. Food Bioprocess Technol 10:1824-33. DOI: https://doi.org/10.1007/s11947-017-1956-6
Darbandi A, Asadi A, Mahdizade Ari M, Ohadi E, Talebi M, Halaj Zadeh M, Darb Emamie A, Ghanavati R, Kakanj M, 2021. Bacteriocins: properties and potential use as antimicrobials. J Clin Lab Anal 36:e24093. DOI: https://doi.org/10.1002/jcla.24093
Das P, Sercu T, Wadhawan K, Padhi I, Gehrmann S, Cipcigan F, Chenthamarakshan V, Strobelt H, Dos Santos C, Chen PY, Yang YY, Tan JPK, Hedrick J, Crain J, Mojsilovic A, 2021. Accelerated antimicrobial discovery via deep generative models and molecular dynamics simulations. Nat Biomed Eng 5:613-23. DOI: https://doi.org/10.1038/s41551-021-00689-x
Davidson AL, Dassa E, Orelle C, Chen J, 2008. Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72:317-64. DOI: https://doi.org/10.1128/MMBR.00031-07
de Souza Barbosa M, Todorov SD, Ivanova I, Chobert JM, Haertlé T, de Melo Franco BDG, 2015. Improving safety of salami by application of bacteriocins produced by an autochthonous Lactobacillus curvatus isolate. Food Microbiol 46:254-62. DOI: https://doi.org/10.1016/j.fm.2014.08.004
Deegan LH, Cotter PD, Hill C, Ross P, 2006. Bacteriocins: biological tools for bio-preservation and shelf-life extension. Int Dairy J 16:1058-71. DOI: https://doi.org/10.1016/j.idairyj.2005.10.026
Deo S, Turton KL, Kainth T, Kumar A, Wieden HJ, 2022. Strategies for improving antimicrobial peptide production. Biotechnol Adv 59:107968. DOI: https://doi.org/10.1016/j.biotechadv.2022.107968
Diep DB, Skaugen M, Salehian Z, Holo H, Nes IF, 2007. Common mechanisms of target cell recognition and immunity for class II bacteriocins. Proc Natl Acad Sci U S A 104:2384-9. DOI: https://doi.org/10.1073/pnas.0608775104
Diep DB, Straume D, Kjos M, Torres C, Nes IF, 2009. An overview of the mosaic bacteriocin pln loci from Lactobacillus plantarum. Peptides 30:1562-74. DOI: https://doi.org/10.1016/j.peptides.2009.05.014
Dorn-In S, Mang S, Cosentino RO, Schwaiger K, 2024. Changes in the microbiota from fresh to spoiled meat, determined by culture and 16S rRNA analysis. J Food Prot 87:100212. DOI: https://doi.org/10.1016/j.jfp.2023.100212
Dortu C, Fickers P, Franz CMAP, Ndagano D, Huch M, Holzapfel WH, Joris B, Thonart P, 2009. Characterisation of an antilisterial bacteriocin produced by Lactobacillus sakei CWBI-B1365 isolated from raw poultry meat and determination of factors controlling its production. Probiotics Antimicrobial Proteins 1:75-84. DOI: https://doi.org/10.1007/s12602-008-9000-9
Drider D, Fimland G, Héchard Y, McMullen LM, Prévost H, 2006. The continuing story of class IIa bacteriocins. Microbiol Mol Biol Rev 70:564-82. DOI: https://doi.org/10.1128/MMBR.00016-05
EFSA, ECDC, 2023. The European Union one health 2022 zoonoses report. EFSA J 21:e8442. DOI: https://doi.org/10.2903/j.efsa.2023.8442
Enan G, 2006. Nature and phenotypic characterization of plantaricin UG1 resistance in Listeria monocytogenes LMG 10470. J Food Agric Environ 4:105-8.
European Commission, 2005. Commission Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. In: Official Journal, L338/1, 22/12/2005.
Frederix PWJM, Patmanidis I, Marrink SJ, 2018. Molecular simulations of self-assembling bio-inspired supramolecular systems and their connection to experiments. Chem Soc Rev 47:3470-89. DOI: https://doi.org/10.1039/C8CS00040A
Gálvez A, Abriouel H, López RL, Omar NB, 2007. Bacteriocin-based strategies for food biopreservation. Int J Food Microbiol 120:51-70. DOI: https://doi.org/10.1016/j.ijfoodmicro.2007.06.001
García-López JD, Barbieri F, Baños A, Madero JMG, Gardini F, Montanari C, Tabanelli G, 2023. Use of two autochthonous bacteriocinogenic strains as starter cultures in the production of salchichónes, a type of Spanish fermented sausages. Curr Res Food Sci 7:100615. DOI: https://doi.org/10.1016/j.crfs.2023.100615
Geiker NRW, Bertram HC, Mejborn H, Dragsted LO, Kristensen L, Carrascal JR, Bügel S, Astrup A, 2021. Meat and human health—current knowledge and research gaps. Foods 10:1556. DOI: https://doi.org/10.3390/foods10071556
Ghalfi H, Benkerroum N, Doguiet DDK, Bensaid M, Thonart P, 2007. Effectiveness of cell‐adsorbed bacteriocin produced by Lactobacillus curvatus CWBI‐B28 and selected essential oils to control Listeria monocytogenes in pork meat during cold storage. Lett Appl Microbiol 44:268-73. DOI: https://doi.org/10.1111/j.1472-765X.2006.02077.x
Gillor O, Etzion A, Riley MA, 2008. The dual role of bacteriocins as anti- and probiotics. Appl Microbiol Biotechnol 81:591-606. DOI: https://doi.org/10.1007/s00253-008-1726-5
González JE, Keshavan ND, 2006. Messing with bacterial quorum sensing. Microbiol Mol Biol Rev 70:859-75. DOI: https://doi.org/10.1128/MMBR.00002-06
Guerra NP, Macías CL, Agrasar AT, Castro LP, 2005. Development of a bioactive packaging cellophane using Nisaplin as biopreservative agent. Lett Appl Microbiol 40:106-10. DOI: https://doi.org/10.1111/j.1472-765X.2004.01649.x
Hammami R, Zouhir A, Le Lay C, Ben Hamida J, Fliss I, 2010. BACTIBASE second release: a database and tool platform for bacteriocin characterization. BMC Microbiol 10:22. DOI: https://doi.org/10.1186/1471-2180-10-22
Hastings JW, Sailer M, Johnson K, Roy KL, Vederas JC, Stiles ME, 1991. Characterization of leucocin A-UAL 187 and cloning of the bacteriocin gene from Leuconostoc gelidum. J Bacteriol 173:7491-500. DOI: https://doi.org/10.1128/jb.173.23.7491-7500.1991
Heilbronner S, Krismer B, Brötz-Oesterhelt H, Peschel A, 2021. The microbiome-shaping roles of bacteriocins. Nat Rev Microbiol 19:726-39. DOI: https://doi.org/10.1038/s41579-021-00569-w
Holck AL, Axelsson L, Hühne K, Kröckel L, 1994. Purification and cloning of sakacin 674, a bacteriocin from Lactobacillus sake Lb674. FEMS Microbiol Lett 115:143-9. DOI: https://doi.org/10.1016/0378-1097(94)90005-1
Hossain TJ, 2024. Methods for screening and evaluation of antimicrobial activity: a review of protocols, advantages, and limitations. Eur J Microbiol Immunol 14:97-115. DOI: https://doi.org/10.1556/1886.2024.00035
Hsu STD, Breukink E, Tischenko E, Lutters MAG, de Kruijff B, Kaptein R, Bonvin AMJJ, van Nuland NAJ, 2004. The nisin–lipid II complex reveals a pyrophosphate cage that provides a blueprint for novel antibiotics. Nat Struct Mol Biol 11:963-7. DOI: https://doi.org/10.1038/nsmb830
Ibrahim SA, Ayivi RD, Zimmerman T, Siddiqui SA, Altemimi AB, Fidan H, Esatbeyoglu T, Bakhshayesh RV, 2021. Lactic acid bacteria as antimicrobial agents: food safety and microbial food spoilage prevention. Foods 10:3131. DOI: https://doi.org/10.3390/foods10123131
Imanian B, Donaghy J, Jackson T, Gummalla S, Ganesan B, Baker RC, Henderson M, Butler EK, Hong Y, Ring B, Thorp C, Khaksar R, Samadpour M, Lawless KA, MacLaren-Lee I, Carleton HA, Tian R, Zhang W, Wan J, 2022. The power, potential, benefits, and challenges of implementing high-throughput sequencing in food safety systems. Npj Sci Food 6:35. DOI: https://doi.org/10.1038/s41538-022-00150-6
Iwatani S, Zendo T, Sonomoto K, 2011. Class IId or linear and non-pediocin-like bacteriocins. In: Drider D, Rebuffat S (eds.), Prokaryotic antimicrobial peptides: from genes to applications (pp. 237–252). Springer, New York, USA. DOI: https://doi.org/10.1007/978-1-4419-7692-5_13
Jack RW, Wan J, Gordon J, Harmark K, Davidson BE, Hillier AJ, Wettenhall RE, Hickey MW, Coventry MJ, 1996. Characterization of the chemical and antimicrobial properties of piscicolin 126, a bacteriocin produced by Carnobacterium piscicola JG126. Appl Environ Microbiol 62:2897-903. DOI: https://doi.org/10.1128/aem.62.8.2897-2903.1996
Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, Tunyasuvunakool K, Bates R, Žídek A, Potapenko A, Bridgland A, Meyer C, Kohl SAA, Ballard AJ, Cowie A, Romera-Paredes B, Nikolov S, Jain R, Adler J, Back T, Petersen S, Reiman D, Clancy E, Zielinski M, Steinegger M, Pacholska M, Berghammer T, Bodenstein S, Silver D, Vinyals O, Senior AW, Kavukcuoglu K, Kohli P, Hassabis D, 2021. Highly accurate protein structure prediction with AlphaFold. Nature 596:583-9. DOI: https://doi.org/10.1038/s41586-021-03819-2
Karwowska M, Łaba S, Szczepański K, 2021. Food loss and waste in meat sector—why the consumption stage generates the most losses? Sustainability 13:6227. DOI: https://doi.org/10.3390/su13116227
Kassaa IA, Rafei R, Moukhtar M, Zaylaa M, Gharsallaoui A, Asehraou A, Omari KE, Shahin A, Hamze M, Chihib NE, 2019. LABiocin database: a new database designed specifically for lactic acid bacteria bacteriocins. Int J Antimicrob Agents 54:771-9. DOI: https://doi.org/10.1016/j.ijantimicag.2019.07.012
Kaur G, Singh TP, Malik RK, 2013. Antibacterial efficacy of Nisin, Pediocin 34 and Enterocin FH99 against Listeria monocytogenes and cross resistance of its bacteriocin resistant variants to common food preservatives. Braz J Microbiol 44:63-71. DOI: https://doi.org/10.1590/S1517-83822013005000025
Kiran F, Osmanagaoglu O, 2014. Inhibition of Listeria monocytogenes in chicken meat by pediocin AcH/PA-1 produced by Pediococcus pentosaceus OZF. Agro Food Industry Hi-Tech, 25:66-9.
Kolodkin-Gal I, Dash O, Rak R, 2024. Probiotic cultivated meat: bacterial-based scaffolds and products to improve cultivated meat. Trends Biotechnol 42:269-81. DOI: https://doi.org/10.1016/j.tibtech.2023.09.002
Komora N, Maciel C, Isidro J, Pinto CA, Fortunato G, Saraiva JMA, Teixeira P, 2023. The impact of HPP-assisted biocontrol approach on the bacterial communities’ dynamics and quality parameters of a fermented meat sausage model. Biology 12:1212. DOI: https://doi.org/10.3390/biology12091212
Kordi M, Talkhounche PG, Vahedi H, Farrokhi N, Tabarzad M, 2024. Heterologous production of antimicrobial peptides: notes to consider. Protein J 129-58. DOI: https://doi.org/10.1007/s10930-023-10174-w
Krishnamoorthi R, Srinivash M, Mahalingam PU, Malaikozhundan B, Suganya P, Gurushankar K, 2022. Antimicrobial, anti-biofilm, antioxidant and cytotoxic effects of bacteriocin by Lactococcus lactis strain CH3 isolated from fermented dairy products—an in vitro and in silico approach. Int J Biol Macromol 220:291-306. DOI: https://doi.org/10.1016/j.ijbiomac.2022.08.087
Lahiri D, Nag M, Dutta B, Sarkar T, Pati S, Basu D, Abdul Kari Z, Wei LS, Smaoui S, Wen Goh K, Ray RR, 2022. Bacteriocin: a natural approach for food safety and food security. Front Bioeng Biotechnol 10:1005918. DOI: https://doi.org/10.3389/fbioe.2022.1005918
Lee H, Kim HY, 2011. Lantibiotics, class I bacteriocins from the genus Bacillus. J Microbiol Biotechnol 21:229-35. DOI: https://doi.org/10.4014/jmb.1010.10017
Lei J, Sun L, Huang S, Zhu C, Li P, He J, Mackey V, Coy DH, He Q, 2019. The antimicrobial peptides and their potential clinical applications. Am J Transl Res 11:3919-31.
Luong NDM, Coroller L, Zagorec M, Membré JM, Guillou S, 2020. Spoilage of chilled fresh meat products during storage: a quantitative analysis of literature data. Microorganisms 8:1198. DOI: https://doi.org/10.3390/microorganisms8081198
Marques PH, Jaiswal AK, de Almeida FA, Pinto UM, Ferreira-Machado AB, Tiwari S, de Castro Soares S, Paiva AD, 2023. Lactic acid bacteria secreted proteins as potential Listeria monocytogenes quorum sensing inhibitors. Mol Divers doi: 10.1007/s11030-023-10722-7. DOI: https://doi.org/10.1007/s11030-023-10722-7
Martínez JM, Martínez MI, Herranz C, Suárez AM, Cintas LM, Fernández MF, Rodríguez JM, Hernández PE, 2000. Use of genetic and immunological probes for pediocin PA-1 gene detection and quantification of bacteriocin production in Pediococcus acidilactici strains of meat origin. Food Agric Immunol 12:299-310. DOI: https://doi.org/10.1080/09540100020008164
Mauriello G, Ercolini D, La Storia A, Casaburi A, Villani F, 2004. Development of polythene films for food packaging activated with an antilisterial bacteriocin from Lactobacillus curvatus 32Y. J Appl Microbiol 97:314-22. DOI: https://doi.org/10.1111/j.1365-2672.2004.02299.x
McGinnis S, Madden TL, 2004. BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res 32:W20-5. DOI: https://doi.org/10.1093/nar/gkh435
Meng EC, Goddard TD, Pettersen EF, Couch GS, Pearson ZJ, Morris JH, Ferrin TE, 2023. UCSF ChimeraX: tools for structure building and analysis. Protein Sci 32:e4792. DOI: https://doi.org/10.1002/pro.4792
Moraes PM, Perin LM, Tassinari Ortolani MB, Yamazi AK, Viçosa GN, Nero LA, 2010. Protocols for the isolation and detection of lactic acid bacteria with bacteriocinogenic potential. LWT - Food Sci Technol 43:1320-4. DOI: https://doi.org/10.1016/j.lwt.2010.05.005
Morata A, 2015. Nuevas Tecnologías de Conservación de Alimentos 2010 2Ed-Resumen. Available from: https://doi.org/10.13140/RG.2.1.4187.6641.
Mørtvedt CI, Nes IF, 1990. Plasmid-associated bacteriocin production by a Lactobacillus sake strain. Microbiology 136:1601-7. DOI: https://doi.org/10.1099/00221287-136-8-1601
Nain Z, Adhikari UK, Abdulla F, Hossain N, Barman NC, Mansur FJ, Azakami H, Karim MM, 2020. Computational prediction of active sites and ligands in different AHL quorum quenching lactonases and acylases. J Biosci 45:26. DOI: https://doi.org/10.1007/s12038-020-0005-1
Nedyalkova M, Paluch AS, Potes Vecini D, Lattuada M, 2024. Progress and future of the computational design of antimicrobial peptides (AMPs): bio-inspired functional molecules. Digital Discovery 3:9-22. DOI: https://doi.org/10.1039/D3DD00186E
Negash AW, Tsehai BA, 2020. Current applications of bacteriocin. Int J Microbiol 2020:4374891. DOI: https://doi.org/10.1155/2020/4374891
Nauman K, Jaspal MH, Asghar B, Manzoor A, Akhtar KH, Ali U, Ali S, Nasir J, Sohaib M, Badar IH, 2022. Effect of different packaging atmosphere on microbiological shelf life, physicochemical attributes, and sensory characteristics of chilled poultry fillets. Food Sci Anim Resour 42:153-74. DOI: https://doi.org/10.5851/kosfa.2021.e71
Ng WL, Bassler BL, 2009. Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197-222. DOI: https://doi.org/10.1146/annurev-genet-102108-134304
Nissen-Meyer J, Oppegård C, Rogne P, Haugen HS, Kristiansen PE, 2011. The two-peptide (class-iib) bacteriocins: genetics, biosynthesis, structure, and mode of action. In: Drider D, Rebuffat S (eds.), Prokaryotic antimicrobial peptides: from genes to applications.. Springer, New York, USA; pp 197-212. DOI: https://doi.org/10.1007/978-1-4419-7692-5_11
Noda M, Miyauchi R, Danshiitsoodol N, Matoba Y, Kumagai T, Sugiyama M, 2018. Expression of genes involved in bacteriocin production and self-resistance in lactobacillus brevis 174A is mediated by two regulatory proteins. Appl Environ Microbiol 84:e02707-17. DOI: https://doi.org/10.1128/AEM.02707-17
Odeyemi OA, Alegbeleye OO, Strateva M, Stratev D, 2020. Understanding spoilage microbial community and spoilage mechanisms in foods of animal origin. Compr Rev Food Sci Food Saf 19:311-31. DOI: https://doi.org/10.1111/1541-4337.12526
Oftedal TF, 2023. Bacteriocins: from discovery to characterization and applications. Available from: https://nmbu.brage.unit.no/nmbu-xmlui/handle/11250/3098644.
Ortiz S, López V, Garriga M, Martínez-Suárez JV, 2014. Antilisterial effect of two bioprotective cultures in a model system of Iberian chorizo fermentation. Int J Food Sci Technol 49:753-8. DOI: https://doi.org/10.1111/ijfs.12362
Palmer N, Maasch JRMA, Torres MDT, de la Fuente-Nunez C, 2021. Molecular dynamics for antimicrobial peptide discovery. Infect Immun 89:e00703-20. DOI: https://doi.org/10.1128/IAI.00703-20
Perez RH, Zendo T, Sonomoto K, 2014. Novel bacteriocins from lactic acid bacteria (LAB): Various structures and applications. Microb Cell Fact 13:S3. DOI: https://doi.org/10.1186/1475-2859-13-S1-S3
Piazentin ACM, Mendonça CMN, Vallejo M, Mussatto SI, de Souza Oliveira RP, 2022. Bacteriocin-like inhibitory substances production by Enterococcus faecium 135 in co-culture with Ligilactobacillus salivarius and Limosilactobacillus reuteri. Braz J Microbiol 53:131-41. DOI: https://doi.org/10.1007/s42770-021-00661-6
Proutière A, du Merle L, Garcia-Lopez M, Léger C, Voegele A, Chenal A, Harrington A, Tal-Gan Y, Cokelaer T, Trieu-Cuot P, Dramsi S, 2023. Gallocin A, an atypical two-peptide bacteriocin with intramolecular disulfide bonds required for activity. Microbiol Spectr 11:e0508522. DOI: https://doi.org/10.1128/spectrum.05085-22
Quadri LE, Sailer M, Roy KL, Vederas JC, Stiles ME, 1994. Chemical and genetic characterization of bacteriocins produced by Carnobacterium piscicola LV17B. J Biol Chem 269:12204-11. DOI: https://doi.org/10.1016/S0021-9258(17)32702-3
Raimondi S, Spampinato G, Candeliere F, Amaretti A, Brun P, Castagliuolo I, Rossi M, 2021. Phenotypic traits and immunomodulatory properties of leuconostoc carnosum isolated from meat products. Front Microbiol 12:730827. DOI: https://doi.org/10.3389/fmicb.2021.730827
Ramani S, Ko D, Kim B, Cho C, Kim W, Jo C, Lee CK, Kang J, Hur S, Park S, 2021. Technical requirements for cultured meat production: a review. J Anim Sci Technol 63:681-92. DOI: https://doi.org/10.5187/jast.2021.e45
Rashid M, Sharma S, Kaur A, Kaur A, Kaur S, 2023. Biopreservative efficacy of Enterococcus faecium-immobilised film and its enterocin against Salmonella enterica. AMB Express 13:11. DOI: https://doi.org/10.1186/s13568-023-01516-z
Rodrigues Blanco I, Luduverio Pizauro LJ, dos Anjos Almeida JV, Nóbrega Mendonça CM, de Mello Varani A, Pinheiro de Souza Oliveira R, 2022. Pan-genomic and comparative analysis of Pediococcus pentosaceus focused on the in silico assessment of pediocin-like bacteriocins. Comput Struct Biotechnol J 20:5595-606. DOI: https://doi.org/10.1016/j.csbj.2022.09.041
Rose NL, Palcic MM, Sporns P, McMullen LM, 2002. Nisin: a novel substrate for glutathione S-transferase isolated from fresh beef. J Food Sci 67:2288-93. DOI: https://doi.org/10.1111/j.1365-2621.2002.tb09542.x
Ross AC, McKinnie SMK, Vederas JC, 2012. The synthesis of active and stable diaminopimelate analogues of the lantibiotic peptide lactocin S. J Am Chem Soc 134:2008-11. DOI: https://doi.org/10.1021/ja211088m
Ruiz Puentes P, Henao MC, Cifuentes J, Muñoz-Camargo C, Reyes LH, Cruz JC, Arbeláez P, 2022. Rational discovery of antimicrobial peptides by means of artificial intelligence. Membranes 12:708. DOI: https://doi.org/10.3390/membranes12070708
Sarmast E, Foudjing GGD, Salmieri S, Lacroix M, 2023. Application of combined essential oils and bacteriocins encapsulated in gelatin for bio-preservation of meatballs. J Food Saf 43:e13080. DOI: https://doi.org/10.1111/jfs.13080
Scharff RL, 2020. Food attribution and economic cost estimates for meat- and poultry-related illnesses. J Food Prot 83:959-67. DOI: https://doi.org/10.4315/JFP-19-548
Selman HM, Mahdi AA, Rofaei NAE, Mutwali, EM, Selman HM, Mahdi AA, Rofaei NAE, Mutwali EM, 2021. Antibacterial activity of the bacteriocins producing- lactic acid bacteria isolated from some processed meat products against selected indicator bacterial strains. World J Adv Res Rev 12:640-5. DOI: https://doi.org/10.30574/wjarr.2021.12.2.0643
Simons A, Alhanout K, Duval RE, 2020. Bacteriocins, antimicrobial peptides from bacterial origin: overview of their biology and their impact against multidrug-resistant bacteria. Microorganisms 8:639. DOI: https://doi.org/10.3390/microorganisms8050639
Sionek B, Szydłowska A, Trząskowska M, Kołożyn-Krajewska D, 2024. The impact of physicochemical conditions on lactic acid bacteria survival in food products. Fermentation 10:298. DOI: https://doi.org/10.3390/fermentation10060298
Srinivas M, O’Sullivan O, Cotter PD, van Sinderen D, Kenny JG, 2022. The application of metagenomics to study microbial communities and develop desirable traits in fermented foods. Foods 11:3297. DOI: https://doi.org/10.3390/foods11203297
Soltani S, Hammami R, Cotter PD, Rebuffat S, Said LB, Gaudreau H, Bédard F, Biron E, Drider D, Fliss I, 2021. Bacteriocins as a new generation of antimicrobials: toxicity aspects and regulations. FEMS Microbiol Rev 45:fuaa039. DOI: https://doi.org/10.1093/femsre/fuaa039
Sowers A, Wang G, Xing M, Li B, 2023. Advances in antimicrobial peptide discovery via machine learning and delivery via nanotechnology. Microorganisms 11:1129. DOI: https://doi.org/10.3390/microorganisms11051129
Surati S, 2020. Bacteriocin, antimicrobial as a new natural food preservative: its potential and challenges. ERUDITIO Indonesia J Food Drug Saf 1:63-82. DOI: https://doi.org/10.54384/eruditio.v1i1.34
Szilágyi A, Závodszky P, 2000. Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey. Structure 8:493-504. DOI: https://doi.org/10.1016/S0969-2126(00)00133-7
Thompson JD, Higgins DG, Gibson TJ, 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-80. DOI: https://doi.org/10.1093/nar/22.22.4673
Tsukano C, Uchino A, Irie K, 2024. Synthesis and applications of symmetric amino acid derivatives. Org Biomol Chem 22:411-28. DOI: https://doi.org/10.1039/D3OB01379K
Umu ÖCO, Rudi K, Diep DB, 2017. Modulation of the gut microbiota by prebiotic fibres and bacteriocins. Microb Ecol Health Dis 28:1348886. DOI: https://doi.org/10.1080/16512235.2017.1348886
Urso R, Rantsiou K, Cantoni C, Comi G, Cocolin L, 2006. Technological characterization of a bacteriocin-producing Lactobacillus sakei and its use in fermented sausages production. Int J Food Microbiol 110:232-9. DOI: https://doi.org/10.1016/j.ijfoodmicro.2006.04.015
V A L, Alarjani KM, Malaisamy A, Balasubramanian B, 2021. Bacteriocin producing microbes with bactericidal activity against multidrug resistant pathogens. J Infect Public Health 14:1802-9. DOI: https://doi.org/10.1016/j.jiph.2021.09.029
van Heel AJ, de Jong A, Song C, Viel JH, Kok J, Kuipers OP, 2018. BAGEL4: A user-friendly web server to thoroughly mine RiPPs and bacteriocins. Nucleic Acids Res 46:W278-81. DOI: https://doi.org/10.1093/nar/gky383
Varadi M, Anyango S, Deshpande M, Nair S, Natassia C, Yordanova G, Yuan D, Stroe O, Wood G, Laydon A, Žídek A, Green T, Tunyasuvunakool K, Petersen S, Jumper J, Clancy E, Green R, Vora A, Lutfi M, Figurnov M, Cowie A, Hobbs N, Kohli P, Kleywegt G, Birney E, Hassabis D, Velankar S, 2022. AlphaFold protein structure database: massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Res 50:D439-44. DOI: https://doi.org/10.1093/nar/gkab1061
Walsh C, 2017. An in silico analysis of bacteriocin production in the human microbiota. PhD Thesis, University College Cork.
Wan X, Saris PEJ, Takala TM, 2015. Genetic characterization and expression of leucocin B, a class IId bacteriocin from Leuconostoc carnosum 4010. Res Microbiol 166:494-503. DOI: https://doi.org/10.1016/j.resmic.2015.04.003
Wang D, Cui F, Ren L, Li J, Li T, 2023. Quorum-quenching enzymes: promising bioresources and their opportunities and challenges as alternative bacteriostatic agents in food industry. Compr Rev Food Sci Food Saf 22:1104-27. DOI: https://doi.org/10.1111/1541-4337.13104
Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ, 2009. Jalview version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189-91. DOI: https://doi.org/10.1093/bioinformatics/btp033
Woraprayote W, Kingcha Y, Amonphanpokin P, Kruenate J, Zendo T, Sonomoto K, Benjakul S, Visessanguan W, 2013. Anti-listeria activity of poly(lactic acid)/sawdust particle biocomposite film impregnated with pediocin PA-1/AcH and its use in raw sliced pork. Int J Food Microbiol 167:229-35. DOI: https://doi.org/10.1016/j.ijfoodmicro.2013.09.009
Woraprayote W, Malila Y, Sorapukdee S, Swetwiwathana A, Benjakul S, Visessanguan W, 2016. Bacteriocins from lactic acid bacteria and their applications in meat and meat products. Meat Sci 120:118-32. DOI: https://doi.org/10.1016/j.meatsci.2016.04.004
Wosinska L, Walsh CJ, O’Connor PM, Lawton EM, Cotter PD, Guinane CM, O’Sullivan O, 2022. In vitro and in silico based approaches to identify potential novel bacteriocins from the athlete gut microbiome of an elite athlete cohort. Microorganisms 10:701. DOI: https://doi.org/10.3390/microorganisms10040701
Xie Y, Zhang M, Gao X, Shao Y, Liu H, Jin J, Yang W, Zhang H, 2018. Development and antimicrobial application of plantaricin BM‐1 incorporating a PVDC film on fresh pork meat during cold storage. J Appl Microbiol 125:1108-16. DOI: https://doi.org/10.1111/jam.13912
Xin B, Liu H, Zheng J, Xie C, Gao Y, Dai D, Peng D, Ruan L, Chen H, Sun M, 2020. In silico analysis highlights the diversity and novelty of circular bacteriocins in sequenced microbial genomes. mSystems 5:00047-20. DOI: https://doi.org/10.1128/msystems.00047-20
Xin WG, Wu G, Ying JP, Xiang YZ, Jiang YH, Deng XY, Lin LB, Zhang QL, 2023. Antibacterial activity and mechanism of action of bacteriocin LFX01 against Staphylococcus aureus and Escherichia coli and its application on pork model. Meat Sci 196:109045. DOI: https://doi.org/10.1016/j.meatsci.2022.109045
Yang E, Fan L, Yan J, Jiang Y, Doucette C, Fillmore S, Walker B, 2018. Influence of culture media, pH and temperature on growth and bacteriocin production of bacteriocinogenic lactic acid bacteria. AMB Express 8:10. DOI: https://doi.org/10.1186/s13568-018-0536-0
Yang X, Peng Z, He M, Li Z, Fu G, Li S, Zhang J, 2024. Screening, probiotic properties, and inhibition mechanism of a Lactobacillus antagonistic to Listeria monocytogenes. Sci Total Environ 906:167587. 167587. DOI: https://doi.org/10.1016/j.scitotenv.2023.167587
Yoo JM, Song JH, Vasquez R, Hwang IC, Lee JS, Kang DK, 2023. Characterization of novel amylase-sensitive, anti-listerial class IId bacteriocin, agilicin C7 produced by Ligilactobacillus agilis C7. Food Sci Animal Resour 43:625-38. DOI: https://doi.org/10.5851/kosfa.2023.e24
Yu W, Guo J, Liu Y, Xue X, Wang X, Wei L, Ma J, 2023. potential impact of combined inhibition by bacteriocins and chemical substances of foodborne pathogenic and spoilage bacteria: a review. Foods 12:3128. DOI: https://doi.org/10.3390/foods12163128
Zacharof MP, Lovitt RW, 2012. Bacteriocins produced by lactic acid bacteria a review article. APCBEE Procedia 2:50-6. DOI: https://doi.org/10.1016/j.apcbee.2012.06.010
Zhang M, Gao X, Zhang H, Liu H, Jin J, Yang W, Xie Y, 2017. Development and antilisterial activity of PE-based biological preservative films incorporating plantaricin BM-1. FEMS Microbiol Lett 364. doi: 10.1093/femsle/fnw283. DOI: https://doi.org/10.1093/femsle/fnw283
Zhang P, Gänzle M, Yang X, 2019. Complementary antibacterial effects of bacteriocins and organic acids as revealed by comparative analysis of Carnobacterium spp. from meat. Appl Environ Microbiol 85:e01227-19. DOI: https://doi.org/10.1128/AEM.01227-19
Zhu L, Zeng J, Wang C, Wang J, 2022. Structural basis of pore formation in the mannose phosphotransferase system by pediocin PA-1. Appl Environ Microbiol 88:e0199221. DOI: https://doi.org/10.1128/AEM.01992-21

How to Cite

1.
Fernandes N, Achemchem F, Gonzales-Barron U, Cadavez V. Biopreservation strategies using bacteriocins to control meat spoilage and foodborne outbreaks. Ital J Food Safety [Internet]. 2024 Oct. 17 [cited 2024 Oct. 28];. Available from: https://www.pagepressjournals.org/ijfs/article/view/12558