Antimicrobial activity of bacteriocins of Lactic Acid Bacteria on Listeria monocytogenes, Staphylococcus aureus and Clostridium tyrobutyricum in cheese production

The generally accepted concept of the necessity of producing safe foods has indirectly influenced the decision to replace chemical preservatives with natural ones. Bacteriocins, and in particular those synthesized by lactic acid bacteria (LAB) in the food industry, are considered to be their effective replace-ment. In controlling the growth of microbial pathogens and/or the occurrence of pathogenic bacteria in food, with the permitted nisin and pediocin, a significant antibacterial effect has been shown for most LAB bacteriocins. However, the use of purified bacteriocins as bio preservatives in cheese production is limited. To inhibit the growth of bacteria L. monocytogenes, S. aureus and C. tyrobutyricum in cheese, bacteriocinogenic LAB strains contained in primary, adjunct or protective culture are much more ac-ceptable in cheese production.

[1]  Edward M. Fox,et al.  Staphylococcus aureus – Dairy , 2020 .

[2]  T. Silvetti,et al.  Clostridium spp. , 2020, Reference Module in Food Science.

[3]  S. Yilmaz,et al.  Maldi-tof mass spectrometry for the identification and detection of antimicrobial activity of lactic acid bacteria isolated from local cheeses , 2019 .

[4]  A. D. V. van Staden,et al.  Migration of Bacteriocins Across Gastrointestinal Epithelial and Vascular Endothelial Cells, as Determined Using In Vitro Simulations , 2019, Scientific Reports.

[5]  Jae-Ho Shin,et al.  Ocins for Food Safety , 2019, Front. Microbiol..

[6]  H. Gaudreau,et al.  Bioprotective Culture: A New Generation of Food Additives for the Preservation of Food Quality and Safety , 2019, Industrial Biotechnology.

[7]  Cristóbal N. Aguilar,et al.  Production of Bioactive Peptides from Lactic Acid Bacteria: A Sustainable Approach for Healthier Foods. , 2019, Comprehensive reviews in food science and food safety.

[8]  R. Rahmeh,et al.  Distribution and antimicrobial activity of lactic acid bacteria from raw camel milk , 2019, New microbes and new infections.

[9]  E. Auclair,et al.  Benefits and Inputs From Lactic Acid Bacteria and Their Bacteriocins as Alternatives to Antibiotic Growth Promoters During Food-Animal Production , 2019, Front. Microbiol..

[10]  J. Arqués,et al.  Technological Properties of Bifidobacterial Strains Shared by Mother and Child , 2019, BioMed research international.

[11]  A. Gasbarrini,et al.  Bacteriocins and Bacteriophages: Therapeutic Weapons for Gastrointestinal Diseases? , 2019, International journal of molecular sciences.

[12]  H. Mahboub,et al.  Studies on the effect of Lactococcus garvieae of dairy origin on both cheese and Nile tilapia (O. niloticus) , 2018, International journal of veterinary science and medicine.

[13]  R. Hammami,et al.  The Genus Enterococcus: Between Probiotic Potential and Safety Concerns—An Update , 2018, Front. Microbiol..

[14]  Vanaja Kumar,et al.  Potential applications of lactic acid bacteria and bacteriocins in anti-mycobacterial therapy , 2018 .

[15]  Brendan R. Jackson,et al.  Listeriosis Outbreaks Associated with Soft Cheeses, United States, 1998–2014 , 2018, Emerging infectious diseases.

[16]  T. Møretrø,et al.  Listeria monocytogenes strains show large variations in competitive growth in mixed culture biofilms and suspensions with bacteria from food processing environments. , 2018, International journal of food microbiology.

[17]  Paul D. Cotter,et al.  Sequencing of the Cheese Microbiome and Its Relevance to Industry , 2018, Front. Microbiol..

[18]  S. Ribeiro,et al.  Application of Bacteriocins and Protective Cultures in Dairy Food Preservation , 2018, Front. Microbiol..

[19]  A. Krastanov,et al.  Immobilization of Bacteriocins from Lactic Acid Bacteria and Possibilities for Application in Food Biopreservation , 2018 .

[20]  Gordon Y C Cheung,et al.  Basis of Virulence in Enterotoxin-Mediated Staphylococcal Food Poisoning , 2018, Front. Microbiol..

[21]  M. Bodmer,et al.  Control of Staphylococcus aureus in dairy herds in a region with raw milk cheese production: farmers’ attitudes, knowledge, behaviour and belief in self-efficacy , 2018, BMC Veterinary Research.

[22]  M. Pajic,et al.  Expression of toxic shock syndrome toxin-1 gene of Staphylococcus aureus in milk: Proof of concept , 2018 .

[23]  G. LaPointe,et al.  Symposium review: Interaction of starter cultures and nonstarter lactic acid bacteria in the cheese environment. , 2017, Journal of dairy science.

[24]  V. Kaškonienė,et al.  Characterization and application of newly isolated nisin producing Lactococcus lactis strains for control of Listeria monocytogenes growth in fresh cheese. , 2018 .

[25]  L. Pellegrino,et al.  The late blowing defect of hard cheeses: Behaviour of cells and spores of Clostridium tyrobutyricum throughout the cheese manufacturing and ripening , 2018 .

[26]  R. Du,et al.  Purification and Characterization of Bacteriocin Produced by a Strain of Enterococcus faecalis TG2 , 2018, Applied Biochemistry and Biotechnology.

[27]  K. Nagy,et al.  The European Union summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in 2016 , 2017, EFSA journal. European Food Safety Authority.

[28]  M. B. Habibi Najafi,et al.  The biodiversity of Lactobacillus spp. from Iranian raw milk Motal cheese and antibacterial evaluation based on bacteriocin-encoding genes , 2017, AMB Express.

[29]  M. P. Mokoena Lactic Acid Bacteria and Their Bacteriocins: Classification, Biosynthesis and Applications against Uropathogens: A Mini-Review , 2017, Molecules.

[30]  R. P. Ross,et al.  Characterization and Application of Antilisterial Enterocins on Model Fresh Cheese. , 2017, Journal of food protection.

[31]  S. Knabel,et al.  Identification of a major Listeria monocytogenes outbreak clone linked to soft cheese in Northern Italy – 2009-2011 , 2017, BMC Infectious Diseases.

[32]  R. C. Whiting,et al.  A review of Listeria monocytogenes: An update on outbreaks, virulence, dose-response, ecology, and risk assessments , 2017 .

[33]  S. Chollet,et al.  MALDI-TOF mass spectrometry for the identification of lactic acid bacteria isolated from a French cheese: The Maroilles. , 2017, International journal of food microbiology.

[34]  M. Gottschalk,et al.  Antimicrobial potential of bacteriocins in poultry and swine production , 2017, Veterinary Research.

[35]  R. Gaglio,et al.  Anti-Listeria Activity of Lactic Acid Bacteria in Two Traditional Sicilian Cheeses , 2017, Italian journal of food safety.

[36]  A. Karaduman,et al.  Identification by using MALDI-TOF mass spectrometry of lactic acid bacteria isolated from non-commercial yogurts in southern Anatolia, Turkey. , 2017, International microbiology : the official journal of the Spanish Society for Microbiology.

[37]  H. C. Mantovani,et al.  Bacteriocins from lactic acid bacteria and their potential in the preservation of fruit products , 2017, Critical reviews in biotechnology.

[38]  C. A. Oliveira,et al.  Pathogenic Bacteria in Cheese, Their Implications for Human Health and Prevention Strategies , 2017 .

[39]  M. Sarker,et al.  Inactivation Strategies for Clostridium perfringens Spores and Vegetative Cells , 2016, Applied and Environmental Microbiology.

[40]  R. del Campo,et al.  Evaluation of bacteriocinogenic activity, safety traits and biotechnological potential of fecal lactic acid bacteria (LAB), isolated from Griffon Vultures (Gyps fulvus subsp. fulvus) , 2016, BMC Microbiology.

[41]  N. Chavarría‐Hernández,et al.  LAB bacteriocin applications in the last decade , 2016 .

[42]  R. P. Ross,et al.  Bacteriocins: Novel Solutions to Age Old Spore-Related Problems? , 2016, Front. Microbiol..

[43]  Y. Yoon,et al.  Cheese Microbial Risk Assessments — A Review , 2016, Asian-Australasian journal of animal sciences.

[44]  O. Kuipers,et al.  Bacteriocins of lactic acid bacteria: extending the family , 2016, Applied Microbiology and Biotechnology.

[45]  Raimondo Gaglio,et al.  In Vitro Evaluation of Bacteriocin-Like Inhibitory Substances Produced by Lactic Acid Bacteria Isolated During Traditional Sicilian Cheese Making , 2016, Italian journal of food safety.

[46]  A. Penna,et al.  Bio Preservation of Cheese by Lactic Acid Bacteria , 2016 .

[47]  T. Haertlé,et al.  Screening for antimicrobial and proteolytic activities of lactic acid bacteria isolated from cow, buffalo and goat milk and cheeses marketed in the southeast region of Brazil , 2015, Journal of Dairy Research.

[48]  M. Ávila,et al.  Impact of Clostridium spp. on cheese characteristics: Microbiology, color, formation of volatile compounds and off-flavors , 2015 .

[49]  R. P. Ross,et al.  The sactibiotic subclass of bacteriocins: an update. , 2015, Current protein & peptide science.

[50]  L. Pellegrino,et al.  Mechanisms of Clostridium tyrobutyricum removal through natural creaming of milk: A microscopy study. , 2015, Journal of dairy science.

[51]  C. Lelis,et al.  Effects of nisin on Staphylococcus aureus count and physicochemical properties of Minas Frescal cheese. , 2015, Journal of dairy science.

[52]  R. Fischetti,et al.  A novel bacteriocin produced by Lactobacillus plantarum LpU4 as a valuable candidate for biopreservation in artisanal raw milk cheese , 2015 .

[53]  R. Stephan,et al.  Outbreak of staphylococcal food poisoning among children and staff at a Swiss boarding school due to soft cheese made from raw milk. , 2015, Journal of dairy science.

[54]  T. Zendo,et al.  Purification and characterization of a novel plantaricin, KL-1Y, from Lactobacillus plantarum KL-1 , 2015, World journal of microbiology & biotechnology.

[55]  J. M. Landete,et al.  Antimicrobial Activity of Lactic Acid Bacteria in Dairy Products and Gut: Effect on Pathogens , 2015, BioMed research international.

[56]  L. Favaro,et al.  Bacteriocinogenic LAB from cheeses – Application in biopreservation? , 2015 .

[57]  F. Irlinger,et al.  Cheese rind microbial communities: diversity, composition and origin. , 2015, FEMS microbiology letters.

[58]  T. Zendo,et al.  Novel bacteriocins from lactic acid bacteria (LAB): various structures and applications , 2014, Microbial Cell Factories.

[59]  C. Sung,et al.  Antibacterial activities of bacteriocins: application in foods and pharmaceuticals , 2014, Front. Microbiol..

[60]  M. Basaglia,et al.  Bacteriocinogenic potential and safety evaluation of non-starter Enterococcus faecium strains isolated from home made white brine cheese. , 2014, Food microbiology.

[61]  M. Ávila,et al.  Inhibitory activity of reuterin, nisin, lysozyme and nitrite against vegetative cells and spores of dairy-related Clostridium species. , 2014, International journal of food microbiology.

[62]  R. Konrad,et al.  Send Orders of Reprints at Reprints@benthamscience.net Application of Maldi-tof Ms for the Identification of Food Borne Bacteria , 2022 .

[63]  C. Bonacina,et al.  Detection of Clostridium tyrobutyricum in milk to prevent late blowing in cheese by automated ribosomal intergenic spacer analysis. , 2013, Journal of food science.

[64]  R. P. Ross,et al.  Bacteriocins — a viable alternative to antibiotics? , 2012, Nature Reviews Microbiology.

[65]  M. Lindström,et al.  Clostridium tyrobutyricum strains show wide variation in growth at different NaCl, pH, and temperature conditions. , 2012, Journal of food protection.

[66]  A. Medveďová,et al.  Staphylococcus aureus: Characterisation and Quantitative Growth Description in Milk and Artisanal Raw Milk Cheese Production , 2012 .

[67]  D. Beshkova,et al.  Bacteriocins from lactic acid bacteria: Microorganisms of potential biotechnological importance for the dairy industry , 2012 .

[68]  M. Ayyash,et al.  Inactivation of Listeria innocua in brined white cheese by a combination of nisin and heat , 2012 .

[69]  S. Bhattacharjee,et al.  Structure-activity relationships of an antimicrobial peptide plantaricin s from two-peptide class IIb bacteriocins. , 2011, Journal of medicinal chemistry.

[70]  A. F. Carvalho,et al.  The effects of nisin on Staphylococcus aureus count and the physicochemical properties of Traditional Minas Serro cheese , 2011 .

[71]  L. Cocolin,et al.  Microbial ecology of artisanal products from North West of Italy and antimicrobial activity of the autochthonous populations. , 2010 .

[72]  D. Samaržija,et al.  Methods for Culture-Independent Identification of Lactic Acid Bacteria in Dairy Products , 2010 .

[73]  A. Vicente,et al.  Shelf life extension of ricotta cheese using coatings of galactomannans from nonconventional sources incorporating nisin against Listeria monocytogenes. , 2010, Journal of agricultural and food chemistry.

[74]  L. Vuyst,et al.  Bacteriocins of lactic acid bacteria to combat undesirable bacteria in dairy products. , 2010 .

[75]  D. Bravo,et al.  Nisin and lacticin 481 coproduction by Lactococcus lactis strains isolated from raw ewes' milk. , 2009, Journal of dairy science.

[76]  M. Martínez-Bueno,et al.  Characterization and safety evaluation of enterococci isolated from Spanish goats' milk cheeses. , 2009, International journal of food microbiology.

[77]  Iva Dolenčić Špehar,et al.  Probiotičke bakterije u prevenciji i terapiji dijareje , 2009 .

[78]  E. Marchioni,et al.  Smearing of soft cheese with Enterococcus faecium WHE 81, a multi-bacteriocin producer, against Listeria monocytogenes. , 2009, Food microbiology.

[79]  R. P. Ross,et al.  Controlling Listeria monocytogenes in Cottage cheese through heterologous production of enterocin A by Lactococcus lactis , 2008, Journal of applied microbiology.

[80]  O. Martín‐Belloso,et al.  Use of nisin and other bacteriocins for preservation of dairy products , 2008 .

[81]  F. Leroy,et al.  Bacteriocins from Lactic Acid Bacteria: Production, Purification, and Food Applications , 2007, Journal of Molecular Microbiology and Biotechnology.

[82]  I. Rogelj,et al.  Inhibition of Clostridium tyrobutyricum in cheese by Lactobacillus gasseri , 2007 .

[83]  Y. Seto,et al.  Characterization of a bacteriocin, Thermophilin 1277, produced by Streptococcus thermophilus SBT1277 , 2006, Journal of applied microbiology.

[84]  Dubravka Samar Staphylococcus aureus u siru , 2007 .

[85]  M. Martínez-Bueno,et al.  Control of Listeria monocytogenes in goat's milk and goat's jben by the bacteriocinogenic Enterococcus faecium F58 strain. , 2006, Journal of food protection.

[86]  R. P. Ross,et al.  Evaluation of live‐culture‐producing lacticin 3147 as a treatment for the control of Listeria monocytogenes on the surface of smear‐ripened cheese , 2006, Journal of applied microbiology.

[87]  R. P. Ross,et al.  Food microbiology: Bacteriocins: developing innate immunity for food , 2005, Nature Reviews Microbiology.

[88]  T. Beresford,et al.  Microbiology of Hard Cheese , 2005 .

[89]  J. M. Rodríguez,et al.  Antimicrobial activity of pediocin-producing Lactococcus lactis on Listeria monocytogenes, Staphylococcus aureus and Escherichia coli O157:H7 in cheese , 2005 .

[90]  T. Beresford,et al.  The Microbiology of Cheese Ripening , 2004 .

[91]  A. Mathot,et al.  Streptococcus thermophilus 580 produces a bacteriocin potentially suitable for inhibition of Clostridium tyrobutyricum in hard cheese. , 2003, Journal of dairy science.

[92]  B. Martínez,et al.  Inhibition of Clostridium tyrobutyricum in Vidiago cheese by Lactococcus lactis ssp. lactis IPLA 729, a nisin Z producer. , 2003, International journal of food microbiology.

[93]  C. Hill,et al.  Generation of Food-Grade Lactococcal Starters Which Produce the Lantibiotics Lacticin 3147 and Lacticin 481 , 2003, Applied and Environmental Microbiology.

[94]  S. Scherer,et al.  A Pediocin-Producing Lactobacillus plantarum Strain Inhibits Listeria monocytogenes in a Multispecies Cheese Surface Microbial Ripening Consortium , 2003, Applied and Environmental Microbiology.

[95]  C. Hill,et al.  Evaluation of a spray‐dried lacticin 3147 powder for the control of Listeria monocytogenes and Bacillus cereus in a range of food systems , 2001, Letters in applied microbiology.

[96]  C. Hill,et al.  Development of bioactive food packaging materials using immobilised bacteriocins lacticin 3147 and nisaplin. , 2000, International journal of food microbiology.