Abstract
Over the last decades, much research has focused on lactic acid bacteria (LAB) bacteriocins because of their potential as biopreservatives and their action against the growth of spoilage microbes. Meat and fermented meat products are prone to microbial contamination, causing health risks, as well as economic losses in the meat industry. The use of bacteriocin-producing LAB starter or protective cultures is suitable for fermented meats. However, although bacteriocins can be produced during meat processing, their levels are usually much lower than those achieved during in vitro fermentations under optimal environmental conditions. Thus, the direct addition of a bacteriocin food additive would be desirable. Moreover, safety and technological characteristics of the bacteriocinogenic LAB must be considered before their widespread applications. This review describes the perspectives and challenges toward the complete disclosure of new bacteriocins as effective preservatives in the production of safe and “healthy” fermented meat products.
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References
Hui Y, Astiasaran I, Sebranek J, Talon R, Toldrá F (2014) Handbook of fermented meat and poultry. Wiley
Lücke F-K (2000) Utilization of microbes to process and preserve meat. Meat Sci 56(2):105–115
Ninios RL, Ahomaa MF, Korkeala H (2014) Enteropathogenic Yersinia in the pork production chain: challenges for control. Compr Rev Food Sci Food Saf 13(6):1165–1191
Gram L, Ravn L, Rasch M, Bruhn JB, Christensen AB, Givskov M (2002) Food spoilage—interactions between food spoilage bacteria. Int J Food Microbiol 78(1):79–97
Chen J, Ren Y, Seow J, Liu T, Bang W, Yuk H (2012) Intervention technologies for ensuring microbiological safety of meat: current and future trends. Compr Rev Food Sci Food Saf 11(2):119–132
Ojha KS, Kerry JP, Duffy G, Beresford T, Tiwari BK (2015) Technological advances for enhancing quality and safety of fermented meat products. Trends Food Sci Technol 44(1):105–116
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 120:118–132
Chen H, Hoover D (2003) Bacteriocins and their food applications. Compr Rev Food Sci Food Saf 2(3):82–100
Lucera A, Costa C, Conte A, Del Nobile MA (2012) Food applications of natural antimicrobial compounds. Front Microbiol 3:287
Deshmukh P, Thorat P (2013) Bacteriocins: a new trend in antimicrobial food packaging. Int J Advanced Res Engineering Appl Sci 1:1–12
Food, Administration D (1988) Nisin preparation: affirmation of GRAS status as a direct human food ingredient. Fed Regist 53:11247–11251
Gharsallaoui A, Oulahal N, Joly C, Degraeve P (2016) Nisin as a food preservative: part 1: physicochemical properties, antimicrobial activity, and main uses. Crit Rev Food Sci Nutr 56(8):1262–1274
Cotter PD, Hill C, Ross RP (2005) Bacteriocins: develo** innate immunity for food. Nat Rev Microbiol 3(10):777–788
Riley MA, Wertz JE (2002) Bacteriocins: evolution, ecology, and application. Ann Rev Microbiol 56(1):117–137
Perez RH, Zendo T, Sonomoto K (2014) Novel bacteriocins from lactic acid bacteria (LAB): various structures and applications. Microb Cell Factories 13(1):1
Balciunas EM, Martinez FAC, Todorov SD, Franco BDGM, Converti A, Oliveira RPS (2013) Novel biotechnological applications of bacteriocins: a review. Food Control 32(1):134–142
O’Connor PM, Ross RP, Hill C, Cotter PD (2015) Antimicrobial antagonists against food pathogens: a bacteriocin perspective. Curr Opin Food Sci 2:51–57
Diep DB, Nes IF (2002) Ribosomally synthesized antibacterial peptides in Gram positive bacteria. Curr Drug Targets 3(2):107–122
Gillor O, Etzion A, Riley M (2008) The dual role of bacteriocins as anti- and probiotics. Appl Microbiol Biotechnol 81(4):591–606
Heng NC, Wescombe PA, Burton JP, Jack RW, Tagg JR (2007) The diversity of bacteriocins in Gram-positive bacteria. In: Riley MA, Chavan MA (eds) Bacteriocins. Springer, Berlin, pp 45–92
Klaenhammer TR (1993) Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol Rev 12(1–3):39–85
Rea MC, Ross RP, Cotter PD, Hill C (2011) Classification of bacteriocins from Gram-positive bacteria. In: Prokaryotic antimicrobial peptides. Springer, pp 29–53
McAuliffe O, Ross RP, Hill C (2001) Lantibiotics: structure, biosynthesis and mode of action. FEMS Microbiol Rev 25(3):285–308
Drider D, Fimland G, Héchard Y, McMullen LM, Prévost H (2006) The continuing story of class IIa bacteriocins. Microbiol Mol Biol Rev 70(2):564–582
Nissen-Meyer J, Oppegård C, Rogne P, Haugen HS, Kristiansen PE (2010) Structure and mode-of-action of the two-peptide (class-IIb) bacteriocins. Probiotics Antimicrobial Proteins 2(1):52–60
Maqueda M, Sánchez-Hidalgo M, Fernández M, Montalbán-López M, Valdivia E, Martínez-Bueno M (2008) Genetic features of circular bacteriocins produced by Gram-positive bacteria. FEMS Microbiol Rev 32(1):2–22
Gabrielsen C, Brede DA, Nes IF, Diep DB (2014) Circular bacteriocins: biosynthesis and mode of action. Appl Environ Microbiol 80(22):6854–6862
Sivonen K, Leikoski N, Fewer DP, Jokela J (2010) Cyanobactins—ribosomal cyclic peptides produced by cyanobacteria. Appl Microbiol Biotechnol 86(5):1213–1225
Alvarez-Sieiro P, Montalbán-López M, Mu D, Kuipers OP (2016) Bacteriocins of lactic acid bacteria: extending the family. Appl Microbiol Biotechnol 100(7):2939–2951
Ammor S, Dufour E, Zagorec M, Chaillou S, Chevallier I (2005) Characterization and selection of Lactobacillus sakei strains isolated from traditional dry sausage for their potential use as starter cultures. Food Microbiol 22(6):529–538
Hugas M, Garriga M, Aymerich M (2003) Functionalty of enterococci in meat products. Int J Food Microbiol 88(2):223–233
Hugo CJ, Hugo A (2015) Current trends in natural preservatives for fresh sausage products. Trends Food Sci Technol 45(1):12–23
Ammor MS, Mayo B (2007) Selection criteria for lactic acid bacteria to be used as functional starter cultures in dry sausage production: an update. Meat Sci 76(1):138–146
Hugas M, Monfort JM (1997) Bacterial starter cultures for meat fermentation. Food Chem 59(4):547–554
Rahman U, Khan MI, Sohaib M, Sahar A, Ishaq A (2017) Exploiting microorganisms to develop improved functional meat sausages: a review. Food Reviews Inter 33(2):195–215
Chaillou S, Champomier-Vergès M-C, Cornet M, Crutz-Le Coq A-M, Dudez A-M, Martin V, Beaufils S, Darbon-Rongère E, Bossy R, Loux V (2005) The complete genome sequence of the meat-borne lactic acid bacterium Lactobacillus sakei 23K. Nat Biotechnol 23(12):1527–1533
Koort J, Vandamme P, Schillinger U, Holzapfel W, Björkroth J (2004) Lactobacillus curvatus subsp. melibiosus is a later synonym of Lactobacillus sakei subsp. carnosus. Int J Syst Evol Microbiol 54(5):1621–1626
Papamanoli E, Tzanetakis N, Litopoulou-Tzanetaki E, Kotzekidou P (2003) Characterization of lactic acid bacteria isolated from a Greek dry-fermented sausage in respect of their technological and probiotic properties. Meat Sci 65(2):859–867
Franz CM, Stiles ME, Schleifer KH, Holzapfel WH (2003) Enterococci in foods-a conundrum for food safety. Int J Food Microbiol 88(2):105–122
Todorov SD, Favaro L, Gibbs P, Vaz-Velho M (2012) Enterococcus faecium isolated from Lombo, a Portuguese traditional meat product: characterisation of antibacterial compounds and factors affecting bacteriocin production. Benefic Microbes 3(4):319–330
Leroy F, Verluyten J, De Vuyst L (2006) Functional meat starter cultures for improved sausage fermentation. Int J Food Microbiol 106(3):270–285
Andrade MJ, Córdoba JJ, Casado EM, Córdoba MG, Rodríguez M (2010) Effect of selected strains of Debaryomyces hansenii on the volatile compound production of dry fermented sausage “salchichón”. Meat Sci 85(2):256–264
Cano-García L, Flores M, Belloch C (2013) Molecular characterization and aromatic potential of Debaryomyces hansenii strains isolated from naturally fermented sausages. Food Res Int 52(1):42–49
Rodriguez J, Cintas L, Casaus P, Horn N, Dodd H, Hernandez P, Gasson M (1995) Isolation of nisin-producing Lactococcus lactis strains from dry fermented sausages. J Appl Bacteriol 78(2):109–115
Noonpakdee W, Santivarangkna C, Jumriangrit P, Sonomoto K, Panyim S (2003) Isolation of nisin-producing Lactococcus lactis WNC 20 strain from nham, a traditional Thai fermented sausage. Int J Food Microbiol 81(2):137–145
Biscola V, Todorov SD, Capuano V, Abriouel H, Gálvez A, Franco BDGM (2013) Isolation and characterization of a nisin-like bacteriocin produced by a Lactococcus lactis strain isolated from charqui, a Brazilian fermented, salted and dried meat product. Meat Sci 93(3):607–613
Sobrino OJ, Rodríguez JM, Moreira WL, Cintas LM, Fernández MF, Sanz B, Hernández PE (1992) Sakacin M, a bacteriocin-like substance from Lactobacillus sake 148. Int J Food Microbiol 16(3):215–225
Nes IF, Mørtvedt CI, Nissen-Meyer J, Skaugen M (1994) Lactocin S, a lanthionine-containing bacteriocin isolated from Lactobacillus sake L45. In: Vuyst LD, Vandamme EJ (eds) Bacteriocins of lactic acid bacteria. Springer, Heidelberg, pp 435–449
Aymerich M, Garriga M, Monfort J, Nes I, Hugas M (2000) Bacteriocin-producing lactobacilli in Spanish-style fermented sausages: characterization of bacteriocins. Food Microbiol 17(1):33–45
Amadoro C, Rossi F, Piccirilli M, Colavita G (2015) Features of Lactobacillus sakei isolated from Italian sausages: focus on strains from Ventricina del Vastese. Italian J Food Safety 4(4):5449
Todorov SD, Vaz-Velho M, Franco BDGM, Holzapfel WH (2013) Partial characterization of bacteriocins produced by three strains of Lactobacillus sakei, isolated from salpicao, a fermented meat product from north-west of Portugal. Food Control 30(1):111–121
Lewus CB, Kaiser A, Montville TJ (1991) Inhibition of food-borne bacterial pathogens by bacteriocins from lactic acid bacteria isolated from meat. Appl Environ Microbiol 57(6):1683–1688
Benoit V, Mathis R, Lefebvre G (1994) Characterization of brevicin 27, a bacteriocin synthetized byLactobacillus brevis SB27. Curr Microbiol 28(1):53–61
Vignolo GM, Suriani F, APdR H, Oliver G (1993) Antibacterial activity of Lactobacillus strains isolated from dry fermented sausages. J Appl Bacteriol 75(4):344–349
**raphi N, Georgalaki M, Van Driessche G, Devreese B, Van Beeumen J, Tsakalidou E, Metaxopoulos J, Drosinos EH (2006) Purification and characterization of curvaticin L442, a bacteriocin produced by Lactobacillus curvatus L442. Antonie Van Leeuwenhoek 89(1):19–26
Casaburi A, Di Martino V, Ferranti P, Picariello L, Villani F (2016) Technological properties and bacteriocins production by Lactobacillus curvatus 54M16 and its use as starter culture for fermented sausage manufacture. Food Control 59:31–45
Rattanachaikunsopon P, Phumkhachorn P (2006) Isolation and preliminary characterization of a bacteriocin produced by Lactobacillus plantarum N014 isolated from nham, a traditional Thai fermented pork. J Food Prot 69(8):1937–1943
**raphi N, Georgalaki M, Rantsiou K, Cocolin L, Tsakalidou E, Drosinos E (2008) Purification and characterization of a bacteriocin produced by Leuconostoc mesenteroides E131. Meat Sci 80(2):194–203
Wan X, Saris PE, Takala TM (2015) Genetic characterization and expression of leucocin B, a class IId bacteriocin from Leuconostoc carnosum 4010. Res Microbiol 166(6):494–503
Cintas LM, Rodriguez JM, Fernandez MF, Sletten K, Nes IF, Hernandez PE, Holo H (1995) Isolation and characterization of pediocin L50, a new bacteriocin from Pediococcus acidilactici with a broad inhibitory spectrum. Appl Environ Microbiol 61(7):2643–2648
Castellano P, Belfiore C, Fadda S, Vignolo G (2008) A review of bacteriocinogenic lactic acid bacteria used as bioprotective cultures in fresh meat produced in Argentina. Meat Sci 79(3):483–499
Quadri L, Sailer M, Roy KL, Vederas JC, Stiles ME (1994) Chemical and genetic characterization of bacteriocins produced by Carnobacterium piscicola LV17B. J Biol Chem 269(16):12204–12211
Cintas LM, Casaus P, Håvarstein LS, Hernandez PE, Nes IF (1997) Biochemical and genetic characterization of enterocin P, a novel sec-dependent bacteriocin from Enterococcus faecium P13 with a broad antimicrobial spectrum. Appl Environ Microbiol 63(11):4321–4330
Sabia C, Manicardi G, Messi P, De Niederhäusern S, Bondi M (2002) Enterocin 416K1, an antilisterial bacteriocin produced by Enterococcus casseliflavus IM 416K1 isolated from Italian sausages. Int J Food Microbiol 75(1):163–170
Sparo M, Nuñez G, Castro M, Calcagno M, Allende MG, Ceci M, Najle R, Manghi M (2008) Characteristics of an environmental strain, Enterococcus faecalis CECT7121, and its effects as additive on craft dry-fermented sausages. Food Microbiol 25(4):607–615
Castellano P, Vignolo G (2006) Inhibition of Listeria innocua and Brochothrix thermosphacta in vacuum-packaged meat by addition of bacteriocinogenic Lactobacillus curvatus CRL705 and its bacteriocins. Lett Appl Microbiol 43(2):194–199
Aymerich T, Artigas M, Garriga M, Monfort J, Hugas M (2000) Effect of sausage ingredients and additives on the production of enterocin A and B by Enterococcus faecium CTC492. Optimization of in vitro production and anti-listerial effect in dry fermented sausages. J Appl Microbiol 88(4):686–694
Alahakoon AU, Jayasena DD, Ramachandra S, Jo C (2015) Alternatives to nitrite in processed meat: up to date. Trends Food Sci Technol 45(1):37–49
Jayasena DD, Jo C (2013) Essential oils as potential antimicrobial agents in meat and meat products: a review. Trends Food Sci Technol 34(2):96–108
Chen C-M, Sebranek J, Dickson J, Mendonca A (2004) Combining pediocin (ALTA 2341) with postpackaging thermal pasteurization for control of Listeria monocytogenes on frankfurters. J Food Prot 67(9):1855–1865
O’Connor E, Roos R, Hill C (2007) Application of bacteriocins in food industry. Norfolk: Bacteriocins current research and applications:153–176
Pawar D, Malik S, Bhilegaonkar K, Barbuddhe S (2000) Effect of nisin and its combination with sodium chloride on the survival of Listeria monocytogenes added to raw buffalo meat mince. Meat Sci 56(3):215–219
Reunanen J, Saris P (2004) Bioassay for nisin in sausage; a shelf life study of nisin in cooked sausage. Meat Sci 66(3):515–518
Paik H-D, Kim H-J, Nam K-J, Kim C-J, Lee S-E, Lee D-S (2006) Effect of nisin on the storage of sous vide processed Korean seasoned beef. Food Control 17(12):994–1000
Karina P, Julio C, Leda G, Noemi Z (2011) Behavior of Listeria monocytogenes type1 355/98 (85) in meat emulsions as affected by temperature, pH, water activity, fat and microbial preservatives. Food Control 22(10):1573–1581
Mohamed HM, Elnawawi FA, Yousef AE (2011) Nisin treatment to enhance the efficacy of gamma radiation against Listeria monocytogenes on meat. J Food Prot 74(2):193–199
Kalschne DL, Geitenes S, Veit MR, Sarmento CM, Colla E (2014) Growth inhibition of lactic acid bacteria in ham by nisin: a model approach. Meat Sci 98(4):744–752
Tu L, Mustapha A (2002) Reduction of Brochothrix thermosphacta and Salmonella serotype Typhimurium on vacuum-packaged fresh beef treated with nisin and nisin combined with EDTA. J Food Sci 67(1):302–306
Wijnker J, Weerts E, Breukink E, Houben J, Lipman L (2011) Reduction of Clostridium sporogenes spore outgrowth in natural sausage casings using nisin. Food Microbiol 28(5):974–979
Ghabraie M, Vu KD, Tnani S, Lacroix M (2016) Antibacterial effects of 16 formulations and irradiation against Clostridium sporogenes in a sausage model. Food Control 63:21–27
Khan A, Gallah H, Riedl B, Bouchard J, Safrany A, Lacroix M (2016) Genipin cross-linked antimicrobial nanocomposite films and gamma irradiation to prevent the surface growth of bacteria in fresh meats. Innovative Food Sci Emerg Technol 35:96–102
Pattanayaiying R, Aran H, Cutter CN (2015) Incorporation of nisin Z and lauric arginate into pullulan films to inhibit foodborne pathogens associated with fresh and ready-to-eat muscle foods. Int J Food Microbiol 207:77–82
Rose N, Sporns P, Stiles M, McMullen L (1999) Inactivation of nisin by glutathione in fresh meat. J Food Sci 64(5):759–762
Deegan LH, Cotter PD, Hill C, Ross P (2006) Bacteriocins: biological tools for bio-preservation and shelf-life extension. Int Dairy J 16(9):1058–1071
Davies EA, Milne CF, Bevis HE, Potter RW, Harris JM, Williams GC, Thomas LV, Delves-Broughton J (1999) Effective use of nisin to control lactic acid bacterial spoilage in vacuum-packed bologna-type sausage. J Food Prot 62(9):1004–1010
Ravyts F, Barbuti S, Frustoli MA, Parolari G, Saccani G, De Vuyst L, Leroy F (2008) Competitiveness and antibacterial potential of bacteriocin-producing starter cultures in different types of fermented sausages. J Food Prot 71(9):1817–1827
Van Wezemael L, Verbeke W, Kügler JO, Scholderer J (2011) European consumer acceptance of safety—improving interventions in the beef chain. Food Control 22(11):1776–1784
Gálvez A, Abriouel H, López RL, Omar NB (2007) Bacteriocin-based strategies for food biopreservation. Int J Food Microbiol 120(1):51–70
Aasen IM, Markussen S, Møretrø T, Katla T, Axelsson L, Naterstad K (2003) Interactions of the bacteriocins sakacin P and nisin with food constituents. Int J Food Microbiol 87(1):35–43
Dicks LMT, Mellett F, Hoffman L (2004) Use of bacteriocin-producing starter cultures of Lactobacillus plantarum and Lactobacillus curvatus in production of ostrich meat salami. Meat Sci 66(3):703–708
Todorov SD, Koep K, Van Reenen C, Hoffman L, Slinde E, Dicks LMT (2007) Production of salami from beef, horse, mutton, Blesbok (Damaliscus dorcas phillipsi) and Springbok (Antidorcas marsupialis) with bacteriocinogenic strains of Lactobacillus plantarum and Lactobacillus curvatus. Meat Sci 77(3):405–412
Kingcha Y, Tosukhowong A, Zendo T, Roytrakul S, Luxananil P, Chareonpornsook K, Valyasevi R, Sonomoto K, Visessanguan W (2012) Anti-listeria activity of Pediococcus pentosaceus BCC 3772 and application as starter culture for Nham, a traditional fermented pork sausage. Food Control 25(1):190–196
Budde BB, Hornbæk T, Jacobsen T, Barkholt V, Koch AG (2003) Leuconostoc carnosum 4010 has the potential for use as a protective culture for vacuum-packed meats: culture isolation, bacteriocin identification, and meat application experiments. Int J Food Microbiol 83(2):171–184
Castellano P, González C, Carduza F, Vignolo G (2010) Protective action of Lactobacillus curvatus CRL705 on vacuum-packaged raw beef. Effect on sensory and structural characteristics. Meat Sci 85(3):394–401
Kouakou P, Ghalfi H, Destain J, Duboisdauphin R, Evrard P, Thonart P (2008) Enhancing the antilisterial effect of Lactobacillus curvatus CWBI-B28 in pork meat and cocultures by limiting bacteriocin degradation. Meat Sci 80(3):640–648
Jacobsen T, Budde B, Koch A (2003) Application of Leuconostoc carnosum for biopreservation of cooked meat products. J Appl Microbiol 95(2):242–249
Favaro L, Penna ALB, Todorov SD (2015) Bacteriocinogenic LAB from cheeses—application in biopreservation? Trends Food Sci Technol 41(1):37–48
Muthukumarasamy P, Holley RA (2006) Microbiological and sensory quality of dry fermented sausages containing alginate-microencapsulated Lactobacillus reuteri. Int J Food Microbiol 111(2):164–169
Barbosa MS, Todorov SD, Jurkiewicz CH, Franco BDGM (2015) Bacteriocin production by Lactobacillus curvatus MBSa2 entrapped in calcium alginate during ripening of salami for control of Listeria monocytogenes. Food Control 47:147–153
Aymerich T, Garriga M, Ylla J, Vallier J, Monfort J, Hugas M (2000) Application of enterocins as biopreservatives against Listeria innocua in meat products. J Food Prot 63(6):721–726
Nieto-Lozano JC, Reguera-Useros JI, Peláez-Martínez MC, de la Torre AH (2006) Effect of a bacteriocin produced by Pediococcus acidilactici against Listeria monocytogenes and Clostridium perfringens on Spanish raw meat. Meat Sci 72(1):57–61
Mattila K, Saris P, Työppönen S (2003) Survival of Listeria monocytogenes on sliced cooked sausage after treatment with pediocin AcH. Int J Food Microbiol 89(2):281–286
Murray M, Richard JA (1997) Comparative study of the antilisterial activity of nisin A and pediocin AcH in fresh ground pork stored aerobically at 5°C. J Food Prot 60(12):1534–1540
Zhang J, Liu G, Li P, Qu Y (2010) Pentocin 31-1, a novel meat-borne bacteriocin and its application as biopreservative in chill-stored tray-packaged pork meat. Food Control 21(2):198–202
Ananou S, Garriga M, Jofré A, Aymerich T, Gálvez A, Maqueda M, Martínez-Bueno M, Valdivia E (2010) Combined effect of enterocin AS-48 and high hydrostatic pressure to control food-borne pathogens inoculated in low acid fermented sausages. Meat Sci 84(4):594–600
Turgis M, Stotz V, Dupont C, Salmieri S, Khan RA, Lacroix M (2012) Elimination of Listeria monocytogenes in sausage meat by combination treatment: radiation and radiation-resistant bacteriocins. Radiat Phys Chem 81(8):1185–1188
Rivas FP, Castro MP, Vallejo M, Marguet E, Campos CA (2014) Sakacin Q produced by Lactobacillus curvatus ACU-1: functionality characterization and antilisterial activity on cooked meat surface. Meat Sci 97(4):475–479
Barbosa M, Todorov SD, Ivanova I, Chobert J-M, Haertlé T, Franco BDGM (2015) Improving safety of salami by application of bacteriocins produced by an autochthonous Lactobacillus curvatus isolate. Food Microbiol 46:254–262
El-Ziney M, Van Den Tempel T, Debevere J, Jakobsen M (1999) Application of reuterin produced by Lactobacillus reuteri 12002 for meat decontamination and preservation. J Food Prot 62(3):257–261
Koo OK, Kim SM, Kang S-H (2015) Antimicrobial potential of Leuconostoc species against E. coli O157: H7 in ground meat. J Korean Soc Appl Biological Chem 58(6):831–838
Campos C, Castro M, Rivas F, Schelegueda L (2013) Bacteriocins in food: evaluation of the factors affecting their effectiveness. In: Méndez-Vilas A (ed) Microbial pathogens and strategies for combating them: sciences, technology and education. Formatex, Badajoz, pp 994–1004
Chung K-T, Dickson JS, Crouse JD (1989) Effects of nisin on growth of bacteria attached to meat. Appl Environ Microbiol 55(6):1329–1333
Rayman K, Malik N, Hurst A (1983) Failure of nisin to inhibit outgrowth of Clostridium botulinum in a model cured meat system. Appl Environ Microbiol 46(6):1450–1452
Junttila J, Hirn J, Hill P, Nurmi E (1989) Effect of different levels of nitrite and nitrate on the survival of Listeria monocytogenes during the manufacture of fermented sausage. J Food Prot 52(3):158–161
Chumchalová J, Josephsen J, Plocková M (1998) The antimicrobial activity of acidocin CH5 in MRS broth and milk with added NaCl, NaNO3 and lysozyme. Int J Food Microbiol 43(1):33–38
Nilsen T, Nes IF, Holo H (1998) An exported inducer peptide regulates bacteriocin production in Enterococcus faecium CTC492. J Bacteriol 180(7):1848–1854
Schillinger U, Kaya M, Lücke FK (1991) Behaviour of Listeria monocytogenes in meat and its control by a bacteriocin-producing strain of Lactobacillus sake. J Appl Bacteriol 70(6):473–478
Zhu M, Du M, Cordray J, Ahn DU (2005) Control of Listeria monocytogenes contamination in ready-to-eat meat products. Compr Rev Food Sci Food Saf 4(2):34–42
Schirru S, Favaro L, Mangia NP, Basaglia M, Casella S, Comunian R, Fancello F, Franco BDGM, de Souza Oliveira RP, Todorov SD (2014) Comparison of bacteriocins production from Enterococcus faecium strains in cheese whey and optimised commercial MRS medium. Ann Microbiol 64(1):321–331
Todorov SD (2008) Bacteriocin production by Lactobacillus plantarum AMA-K isolated from Amasi, a Zimbabwean fermented milk product and study of the adsorption of bacteriocin AMA-K to Listeria sp. Braz J Microbiol 39(1):178–187
Ünlü G, Nielsen B, Ionita C (2015) Production of antilisterial bacteriocins from lactic acid bacteria in dairy-based media: a comparative study. Probiotics Antimicrobial Proteins 7(4):259–274
Todorov SD, Wachsman M, Tomé E, Dousset X, Destro MT, Dicks LMT, Franco BDGM, Vaz-Velho M, Drider D (2010) Characterisation of an antiviral pediocin-like bacteriocin produced by Enterococcus faecium. Food Microbiol 27(7):869–879
Jones E, Salin V, Williams GW (2005) Nisin and the market for commercial bacteriocins. Consumer and Product Research CP-01-05, Texas Agribusiness Market Research Center, Texas A&M University, College Station, Tex, USA
Bali V, Panesar PS, Bera MB (2016) Trends in utilization of agro-industrial byproducts for production of bacteriocins and their biopreservative applications. Crit Rev Biotechnol 36(2):204–214
Romanelli MG, Povolo S, Favaro L, Fontana F, Basaglia M, Casella S (2014) Engineering Delftia acidovorans DSM39 to produce polyhydroxyalkanoates from slaughterhouse waste. Int J Biol Macromol 71:21–27
Koutinas AA, Vlysidis A, Pleissner D, Kopsahelis N, Garcia IL, Kookos IK, Papanikolaou S, Kwan TH, Lin CSK (2014) Valorization of industrial waste and by-product streams via fermentation for the production of chemicals and biopolymers. Chem Soc Rev 43(8):2587–2627
Cripwell R, Favaro L, Rose SH, Basaglia M, Cagnin L, Casella S, van Zyl W (2015) Utilisation of wheat bran as a substrate for bioethanol production using recombinant cellulases and amylolytic yeast. Appl Energy 160:610–617
Shah A, Favaro L, Alibardi L, Cagnin L, Sandon A, Cossu R, Casella S, Basaglia M (2016) Bacillus sp. strains to produce bio-hydrogen from the organic fraction of municipal solid waste. Appl Energy 176:116–124
Tsapekos P, Kougias P, Treu L, Campanaro S, Angelidaki I (2017) Process performance and comparative metagenomic analysis during co-digestion of manure and lignocellulosic biomass for biogas production. Appl Energy 185:126–135
Alibardi L, Favaro L, Lavagnolo MC, Basaglia M, Casella S (2012) Effects of heat treatment on microbial communities of granular sludge for biological hydrogen production. Water Sci Technol 66(7):1483–1490
Alibardi L, Green K, Favaro L, Vale P, Soares A, Cartmell E, Bajon Fernandez Y (2017) Performance and stability of sewage sludge digestion under CO2 enrichment: a pilot study. Bioresour Technol. https://doi.org/10.1016/j.biortech.2017.08.071
Favaro L, Cagnin L, Basaglia M, Pizzocchero V, van Zyl WH, Casella S (2017) Production of bioethanol from multiple waste streams of rice milling. Bioresour Technol 244:151–159
Chikindas ML, Weeks R, Drider D, Chistyakov VA, Dicks LM (2018) Functions and emerging applications of bacteriocins. Curr Opin Biotechnol 49:23–28
O’Shea EF, O’Connor PM, Cotter PD, Ross RP, Hill C (2010) Synthesis of trypsin-resistant variants of the Listeria-active bacteriocin salivaricin P. Appl Environ Microbiol 76(16):5356–5362
Carmona-Ribeiro AM, de Melo Carrasco LD (2014) Novel formulations for antimicrobial peptides. Int J Mol Sci 15(10):18040–18083
de Abreu LCL, Todaro V, Sathler PC, da Silva LCRP, do Carmo FA, Costa CM, Toma HK, Castro HC, Rodrigues CR, de Sousa VP (2016) Development and characterization of nisin nanoparticles as potential alternative for the recurrent vaginal candidiasis treatment. AAPS PharmSciTech 17(6):1421–1427
Torres NI, Noll KS, Xu S, Li J, Huang Q, Sinko PJ, Wachsman MB, Chikindas ML (2013) Safety, formulation and in vitro antiviral activity of the antimicrobial peptide subtilosin against herpes simplex virus type 1. Probiotics Antimicrobial Proteins 5(1):26–35
Healy B, Field D, O’Connor PM, Hill C, Cotter PD, Ross RP (2013) Intensive mutagenesis of the nisin hinge leads to the rational design of enhanced derivatives. PLoS One 8(11):e79563
Carroll J, Field D, O'connor PM, Cotter PD, Coffey A, Hill C, O’Mahony J (2010) The gene encoded antimicrobial peptides, a template for the design of novel anti-mycobacterial drugs. Bioengineered Bugs 1(6):408–412
Jozala AF, De Andrade MS, De Arauz LJ, Pessoa A, Penna TCV (2007) Nisin production utilizing skimmed milk aiming to reduce process cost. Appl Biochem Biotechnol 137(1–12):515–528
Vaucher RA, Motta SA, Brandelli A (2010) Evaluation of the in vitro cytotoxicity of the antimicrobial peptide P34. Cell Biol Int 34(3):317–323
Carneiro B, Braga A, Batista M, Rahal P, Favaro L, Penna A, Todorov S (2014) Lactobacillus plantarum ST202Ch and Lactobacillus plantarum ST216Ch-what are the limitations for application. J Nutritional Health Food Engineering 1(2):00010
Suwandecha T, Srichana T, Balekar N, Nakpheng T, Pangsomboon K (2015) Novel antimicrobial peptide specifically active against Porphyromonas gingivalis. Arch Microbiol 197(7):899–909
Brogden KA (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3(3):238–250
Das D, Goyal A (2014) Characterization of a noncytotoxic bacteriocin from probiotic Lactobacillus plantarum DM5 with potential as a food preservative. Food Funct 5(10):2453–2462
Settanni L, Guarcello R, Gaglio R, Francesca N, Aleo A, Felis GE, Moschetti G (2014) Production, stability, gene sequencing and in situ anti-Listeria activity of mundticin KS expressed by three Enterococcus mundtii strains. Food Control 35(1):311–322
Götz F, Perconti S, Popella P, Werner R, Schlag M (2014) Epidermin and gallidermin: staphylococcal lantibiotics. Int J Med Microbiol 304(1):63–71
Maher S, McClean S (2006) Investigation of the cytotoxicity of eukaryotic and prokaryotic antimicrobial peptides in intestinal epithelial cells in vitro. Biochem Pharmacol 71(9):1289–1298
Martinez RCR, Wachsman M, Torres NI, LeBlanc JG, Todorov SD, de Melo Franco BDG (2013) Biochemical, antimicrobial and molecular characterization of a noncytotoxic bacteriocin produced by Lactobacillus plantarum ST71KS. Food Microbiol 34(2):376–381
Todorov SD, Wachsman MB, Knoetze H, Meincken M, Dicks LM (2005) An antibacterial and antiviral peptide produced by Enterococcus mundtii ST4V isolated from soya beans. Int J Antimicrob Agents 25(6):508–513
Fisher K, Phillips C (2009) The ecology, epidemiology and virulence of Enterococcus. Microbiology 155(6):1749–1757
Rathnayake I, Hargreaves M, Huygens F (2012) Antibiotic resistance and virulence traits in clinical and environmental Enterococcus faecalis and Enterococcus faecium isolates. Syst Appl Microbiol 35(5):326–333
Belgacem ZB, Abriouel H, Omar NB, Lucas R, Martínez-Canamero M, Gálvez A, Manai M (2010) Antimicrobial activity, safety aspects, and some technological properties of bacteriocinogenic Enterococcus faecium from artisanal Tunisian fermented meat. Food Control 21(4):462–470
Hendrickx AP, Willems RJ, Bonten MJ, van Schaik W (2009) LPxTG surface proteins of enterococci. Trends Microbiol 17(9):423–430
Todorov S, Franco B, Wiid I (2014) In vitro study of beneficial properties and safety of lactic acid bacteria isolated from Portuguese fermented meat products. Benefic Microbes 5(3):351–366
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Favaro, L., Todorov, S.D. Bacteriocinogenic LAB Strains for Fermented Meat Preservation: Perspectives, Challenges, and Limitations. Probiotics & Antimicro. Prot. 9, 444–458 (2017). https://doi.org/10.1007/s12602-017-9330-6
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DOI: https://doi.org/10.1007/s12602-017-9330-6