Enhanced control of Listeria monocytogenes by Enterococcus faecium KE82, a multiple enterocin–producing strain, in different milk environments

Vandera, Elpiniki; Lianou, Alexandra; Kakouri, Athanasia; Feng, Jinbo; Koukkou, Anna-Irini; Samelis, John

doi:10.4315/0362-028x.jfp-16-082

Cited by 44Probiotics and Fermented FoodsListeria monocytogenes in Food SafetyInfant Nutrition and Health

Enhanced control of Listeria monocytogenes by Enterococcus faecium KE82, a multiple enterocin–producing strain, in different milk environments

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Vandera, Elpiniki, Lianou, Alexandra, Kakouri, Athanasia, Feng, Jinbo, Koukkou, Anna-Irini, Samelis, John·2017·Journal of Food Protection

DOI 10.4315/0362-028x.jfp-16-082

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Abstract

Enterococcus faecium KE82, isolated from traditional Greek Graviera cheese, was identified in pure broth cultures in vitro as a multiple enterocin-producing bacterial strain possessing the structural entA, entB, and entP enterocin genes. E. faecium KE82 was further assessed for in situ antilisterial activity in raw milk (RM) and commercially thermized milk (TM; 63°C for 30 s) in the presence of the indigenous microbiota and in sterile raw milk (SRM; 121°C for 5 min) with or without the addition of two commercial starter culture (CSC) strains Streptococcus thermophilus and Lactococcus lactis . Growth of Listeria monocytogenes was completely inhibited in RM incubated at 37°C for 6 h, whereas the pathogen was significantly inactivated in RM+KE82 samples during further incubation at 18°C for 66 h. In contrast, L. monocytogenes levels increased by approximately 2 log CFU/ml in TM, but in TM+KE82 samples, pathogen growth was retarded during the first 6 h at 37°C followed by growth cessation and partial inactivation at 18°C. After 48 to 72 h, growth of L. monocytogenes in SRM+CSC samples decreased by 4 to 5 log CFU/ml compared with the SRM control, whereas additional 10-fold decreases in the pathogen were observed in SRM+CSC+KE82 samples. Reverse transcription PCR analysis of SRM+KE82 and SRM+CSC+KE82 samples confirmed that the entA and entB genes were transcribed, but entP gene transcription was not detected. All RM and SRM samples inoculated with E. faecium KE82 displayed strong in situ inhibitory activity against L. monocytogenes in well diffusion bioassays, whereas activity was weaker to undetectable in comparable or additional TM+KE82 samples; no milk sample without E. faecium KE82 had activity against L. monocytogenes . The findings of this study indicate that E. faecium KE82 is an antilisterial agent that could be used in traditional dairy foods because it concomitantly produces enterocins A and B in situ in milk.

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Bacteriocin-producing LAB species such as L. plantarum, Streptococcus spp. and Enterococcus spp. have been shown to reduce L. monocytogenes and S. aureus contamination in various dairy products.
“Such bacteriocin-producing LAB species as L. plantarum, Streptococcus spp. and Enterococcus spp. have been shown to reduce L. monocytogenes and S. aureus contamination in various dairy products [17,128,143,144,145,146].”
From Lactic Acid Bacteria in Raw-Milk Cheeses: From Starter Cultures to Probiotic Functions (2022) · cites this paper as [145]
The Results and Discussion (page unavailable) report that milk cultures containing the enterocin-producing Enterococcus faecium KE82 inhibited L. monocytogenes, though activity varied by milk treatment. This supports the Enterococcus–Listeria part of the multi-cited sentence. The paper does not establish reductions of S. aureus or demonstrate the claimed effects for L. plantarum or Streptococcus spp. (LLM, conf=0.88)
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The Probiotic Enterococcus Lactis SF68 as a Potential Food Fermentation Microorganism for Safe Food Production
Tadesse, B. T., Gu, L., Solem, C., Mijakovic̀, I., & Jers, C. (2024) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.4c03644 · Cited by 15 · see citing works
Growth and Biocontrol of Listeria monocytogenes in Greek Anthotyros Whey Cheese without or with a Crude Enterocin A-B-P Extract: Interactive Effects of the Native Spoilage Microbiota during Vacuum-Packed Storage at 4 °C
Sameli, N., & Samelis, J. (2022) · Foods · doi:10.3390/foods11030334 · Cited by 15 · see citing works
“thermophilus as the primary milk acidifier than in the respective cheese milks without addition of the starter [44].”
Background
Hurdle factors minimizing growth of Listeria monocytogenes while counteracting in situ antilisterial effects of a novel nisin A-producing Lactococcus lactis subsp. cremoris costarter in thermized cheese milks
Samelis, J., & Kakouri, A. (2018) · AIMS Microbiology · doi:10.3934/microbiol.2018.1.19 · Cited by 15 · see citing works
“For inoculation purposes, fresh (24-h) 10-mL BHI cultures of the strains were centrifuged (3,200 × g for 15 min), the cells were washed with 10 mL of quarter-strength Ringer solution (Lab M), resuspended in the same diluent, and suspensions were combined as before [11,44,51].”
BackgroundMethodInfluential
Bacteriocin characterization of Enterococcus faecium isolates and evaluation of their in situ anti-Listerial activity in Beyaz cheese
Aktaş, H. M. (2024) · Food Bioscience · doi:10.1016/j.fbio.2024.104741 · Cited by 13 · see citing works
Behavior of artificial listerial contamination in model Greek Graviera cheeses manufactured with the indigenous nisin A‐producing strain Lactococcus lactis subsp. cremoris M104 as costarter culture
Samelis, J., Giannou, E., Pappa, E. C., Matijašić, B. B., Lianou, A., Parapouli, M., & Drainas, C. (2016) · Journal of Food Safety · doi:10.1111/jfs.12326 · Cited by 12 · see citing works
Antibiotic Resistant Enterobacteriaceae in Milk Alternatives
Mukuna, W., Mafiz, A. I., Pokharel, B., Aniume, T., & Kilonzo‐Nthenge, A. (2021) · Foods · doi:10.3390/foods10123070 · Cited by 11 · see citing works
Bacteriocins: Applications in Food Preservation and Therapeutics
Thapar, P., & Salooja, M. K. (2022) · IntechOpen eBooks · doi:10.5772/intechopen.106871 · Cited by 11 · see citing works
Assessment of the Spoilage Microbiota and the Growth Potential of Listeria monocytogenes in Minced Free-Range Chicken Meat Stored at 4 °C in Vacuum: Comparison with the Spoilage Community of Resultant Retail Modified Atmosphere Packaged Products
Tsafrakidou, P., Sameli, N., Kakouri, A., Bosnea, L. A., & Samelis, J. (2023) · Applied Microbiology · doi:10.3390/applmicrobiol3040088 · Cited by 10 · see citing works
“…of the above L. monocytogenes strains as inocula in the present study was based on their effective use as target and/or indicator strains in previous challenge studies in respect of their meat origin, serotype, pathogenesis, low or moderate acid sensitivity, and high bacteriocin sensitivity [33].”
Method
Genetic Analysis with Random Amplified Polymorphic DNA of the Multiple Enterocin-Producing Enterococcus lactis 4CP3 Strain and Its Efficient Role in the Growth of Listeria monocytogenes in Raw Beef Meat
Braïek, O. B., Smaoui, S., Ennouri, K., Hani, K., & Ghrairi, T. (2018) · BioMed Research International · doi:10.1155/2018/5827986 · Cited by 10 · see citing works
“Even though enterococci have been found naturally in different types of foods, their use in food products is controversial because they are considered as opportunistic pathogens implicated in several nosocomial infections and constitute a source of multiple antibiotic resistances [16].”
Background
Monitoring Growth Compatibility and Bacteriocin Gene Transcription of Adjunct and Starter Lactic Acid Bacterial Strains in Milk
Asimakoula, S., Giaka, K., Fanitsios, C., Kakouri, A., Vandera, E., Samelis, J., & Koukkou, A. (2020) · Journal of Food Protection · doi:10.4315/jfp-20-317 · Cited by 8 · see citing works
Utilization of Agro-Industrial Byproducts for Bacteriocin Production Using Enterococcus spp. Strains Isolated from Patagonian Marine Invertebrates
Sosa, F. M., Parada, R. B., Marguet, E. R., & Vallejo, M. (2021) · Current Microbiology · doi:10.1007/s00284-021-02712-5 · Cited by 8 · see citing works
Cell Growth Density and Nisin A Activity of the Indigenous Lactococcus lactis subsp. cremoris M78 Costarter Depend Strongly on Inoculation Levels of a Commercial Streptococcus thermophilus Starter in Milk: Practical Aspects for Traditional Greek Cheese Processors
Samelis, J., & Kakouri, A. (2020) · Journal of Food Protection · doi:10.4315/0362-028x.jfp-19-430 · Cited by 8 · see citing works
Perfiles de susceptibilidad antimicrobiana en bacterias aisladas en cultivos agrícolas de la cuenca del río Chambo.
González-Romero, A. C., Guamán-Chabla, M. G., Cordovéz-Martínez, M. D. C., & -Duran, E. E. M. (2022) · Perfiles · doi:10.47187/perf.v1i27.148 · Cited by 7 · see citing works
“Salud Pública [Internet].”
BackgroundInfluential
Application of Bacteriocins in the Food Industry
Gu, Q. (2023) · Springer eBooks · doi:10.1007/978-981-99-2661-9_4 · Cited by 5 · see citing works
Dual Role of Probiotic Lactic Acid Bacteria Cultures for Fermentation and Control Pathogenic Bacteria in Fruit-Enriched Fermented Milk
Borgonovi, T. F., Fugaban, J. I. I., Bucheli, J. E. V., Casarotti, S. N., Holzapfel, W. H., Todorov, S. D., & Penna, A. L. B. (2023) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-023-10135-w · Cited by 5 · see citing works
“Ent. faecium KE82, which produces bacteriocins (entA, entB, and entP), was also able to inhibit List. monocytogenes , and the inhibitory action was observed in heat-treated or non-heat-treated raw milk [73].”
Antilisterial potential of enterocin produced by Enterococcus faecium 3BWK isolated from Minas Frescal cheese
Closs, W. L. C., Costa, G. N., Noriler, S. A., de Oliveira, A. G., Nakazato, G., & Guergoletto, K. B. (2025) · International Dairy Journal · doi:10.1016/j.idairyj.2025.106401 · Cited by 4 · see citing works
Lactobacillus - A Multifunctional Genus
Laranjo, M. (2022) · IntechOpen eBooks · doi:10.5772/intechopen.98170 · Cited by 4 · see citing works
Characterisation of Enterocins Produced by Antilisterial Enterococcus faecium BH04 , BH12 , BH84 , and BH99 and In Vitro/In Situ Inhibition of Listeria monocytogenes
Aktaş, H. (2025) · Food Science & Nutrition · doi:10.1002/fsn3.70142 · Cited by 3 · see citing works
“Furthermore, in the study by Vandera et al. (2017), in skimmed milk (pH decreased from 6.42 to 6.04 during incubation) containing enterocin-producing E. faecium KE82, it was found that the count of L. monocytogenes was suppressed (4.23 log cfu/mL) after 6 h of incubation compared to the con-trol…”
Influential
Antimicrobial Proteins and Peptides as a Promising Weapon to Promote Food Safety Under the One Health Approach
Govari, M., Kafentzi, M.-C., Pavlidis, D., Tsouggou, N., Pemaj, V., Slavko, A., Drosinos, E. H., Koliadima, A., Skandamis, P. N., Kapolos, J., et al. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-822521-9.00160-x · Cited by 3 · see citing works
Antimicrobial Peptides from Lactic Acid Bacteria as a Hurdle Technology Component for Food Preservation: Applications and Safety Considerations
Ruiz-Ramírez, Y., Guadarrama-Mendoza, P. C., Valadez-Blanco, R., & Ponce‐Alquicira, E. (2024) · Springer eBooks · doi:10.1007/978-981-97-3413-9_13 · Cited by 3 · see citing works
Potential and application of tandem mass spectrometry (MS/MS) in the analysis and identification of novel bacteriocins: a review
Kurnianto, M. A., Adesina, P. A., & Rini, D. M. (2024) · International Journal of Food Science & Technology · doi:10.1111/ijfs.17601 · Cited by 2 · see citing works
Inhibition of Listeria Monocytogenes by Human Gut Bacteria
Olesky, P. S. (2018) · Cited by 2 · see citing works
Natural Antimicrobial Compounds in Food Safety
Vesković-Moračanin, S. M. (2025) · Springer eBooks · doi:10.1007/978-3-031-85089-9_4
Exploring the use of Safety-Assessed Bacteriocin-Producing Enterococci as Starters for Production of Soy Yoghurt Analogues
Tadesse, B. T., Molloy, J., Zhao, S., Gu, L., Jers, C., Mijakovic̀, I., & Solem, C. (2026) · Journal of Food Protection · doi:10.1016/j.jfp.2026.100715
Recent advances in bacteriocin research: Synthetic biology approaches for engineering bacteriocins in food industry applications
Gawali, S., Amane, P., Kayalvizhi, N., Muthukalingan, K., Puvaneswari, N., Guldhe, A., Juneja, A., Kumar, A. W. S., & Rameshkumar, N. (2026) · Food Bioscience · doi:10.1016/j.fbio.2026.109686

Application of Enterococcus faecium KE82, an Enterocin A-B-P–Producing Strain, as an Adjunct Culture Enhances Inactivation of Listeria monocytogenes during Traditional Protected Designation of Origin Galotyri Processing
Sameli, N., Skandamis, P. N., & Samelis, J. (2020) · Journal of Food Protection · doi:10.4315/jfp-20-278 · Cited by 18 · see citing works
Control of Listeria monocytogenes in Heat-treated Milks by Enterococcus faecium KE82, a Multiple Enterocin-producing and Potential Probiotic Strain
Kakouri, A. (2016) · IAFP's 12th European Symposium on Food Safety
Inhibition of Listeria monocytogenes by enterocin 4 during the manufacture andripening of Manchego cheese
Núñez, M., Rodríguez, J. L., García, E. F., Gaya, P., & Médina, M. (1997) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.1997.00275.x · Cited by 110 · see citing works
Isolation and characterization from raw milk of Enterocin B-producing Enterococcus faecium: A potential dairy bio-preservative agent
Mancini, L., Carbone, S., Calabrese, F. M., Celano, G., & Angelis, M. D. (2025) · Applied Food Research · doi:10.1016/j.afres.2025.100857 · Cited by 10 · see citing works
Control of Listeria monocytogenes in Goat's Milk and Goat's Jben by the Bacteriocinogenic Enterococcus faecium F58 Strain
Achemchem, F., Abrini, J., Martínez‐Bueno, M., Valdivia, E., & Maqueda, M. (2006) · Journal of Food Protection · doi:10.4315/0362-028x-69.10.2370 · Cited by 51 · see citing works

Authors: Vandera, E., Lianou, A., Kakouri, A., Feng, J., Koukkou, A.-I., & Samelis, J.
Affiliations: University of Ioannina (GR)
Corresponding author: Samelis, John
ORCID: Lianou, Alexandra
Koukkou, Anna-Irini
Samelis, John
Venue: Journal of Food Protection
Publisher: Elsevier BV
Published: 2017-01
Volume: 80
Issue: 1
Pages: 74-85
ISSN: 0362-028X (ISSN-L)
DOI: 10.4315/0362-028x.jfp-16-082
OpenAlex: W2561879314
Cited by: 44
References: 47
Citations by year: 2026: 2 · 2025: 4 · 2024: 6 · 2023: 6 · 2022: 6 · 2021: 4 · 2020: 4 · 2019: 1 · 2018: 8 · 2017: 1 · 2016: 2
FWCI: 5.04
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 2160 d)
Locations: Journal of Food Protection (publishedVersion)
PubMed (publishedVersion)
Funders: European Commission (FOOD-CT-2006-016264)
University of Ioannina
Topics: Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Listeria monocytogenes in Food Safety
Health Sciences › Nursing › Nutrition and Dietetics › Infant Nutrition and Health
Keywords: Listeria monocytogenes, enterocins, antilisterial activity, raw milk, starter cultures, Streptococcus thermophilus, Lactococcus lactis, dairy microbiota, pathogen inactivation
MeSH terms: Animals, Bacteriocins, Bridged-Ring Compounds, Greece, Listeria monocytogenes, Milk, Enterococcus faecium

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Enhanced control of Listeria monocytogenes by Enterococcus faecium KE82, a multiple enterocin–producing strain, in different milk environments

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