Cited by 117Probiotics and Fermented FoodsBacterial Genetics and BiotechnologyGut microbiota and health

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Probiotic Potential and Safety Evaluation of Enterococcus faecalis OB14 and OB15, Isolated From Traditional Tunisian Testouri Cheese and Rigouta, Using Physiological and Genomic Analysis

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Baccouri, Olfa, Boukerb, Amine Mohamed, Farhat, Leila Ben, Zébré, Arthur, Zimmermann, Kurt, Domann, Eugen, Cambronel, Mélyssa, Barreau, Magalie, Maillot, Olivier, Rincé, Isabelle, Muller, Cécile, Marzouki, Mohamed Nejib, Feuilloley, Marc, Abidi, Ferid, Connil, Nathalie·2019·Frontiers in Microbiology

DOI 10.3389/fmicb.2019.00881PMC PMC6491886

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Abstract

Lactic acid bacteria (LAB) strains OB14 and OB15 were isolated from traditional Tunisian fermented dairy products, Testouri cheese and Rigouta, respectively. They were identified as Enterococcus faecalis by the MALDI TOF-MS (matrix assisted laser desorption-ionization time of flight mass spectrometry) biotyper system and molecular assays (species-specific PCR). These new isolates were evaluated for probiotic properties, compared to E. faecalis Symbioflor 1 clone DSM 16431, as probiotic reference. The bacteria were found to be tolerant to the harsh conditions of the gastrointestinal tract (acidity and bile salt). They were low to moderate biofilm producers, can adhere to Caco-2/TC7 intestinal cells and strengthen the intestinal barrier through the increase of the transepithelial electrical resistance (TER). Susceptibility to ampicillin, vancomycin, gentamicin and erythromycin has been tested using the broth microdilutions method. The results demonstrated that E. faecalis OB14 and OB15 were sensitive to the clinically important ampicillin (MIC=1µg/mL) and vancomycin (MIC= 2µg/mL) antibiotics. However, Whole Genome Sequencing (WGS) showed the presence of tetracycline resistance and cytolysin genes in E. faecalis OB14, and this led to high mortality of Galleria Mellonella larvae in the virulence test. Hierarchical cluster analysis by MALDI TOF-MS biotyper showed that E. faecalis OB15 was closely related to the E. faecalis Symbioflor 1 probiotic strain than to OB14, and this has been confirmed by WGS using the Average Nucleotide Identity (ANI) and Genome-to-Genome Hybridization similarity (GGDH) methods. According to these results, E. faecalis OB15 seems to be reliable for future development as probiotic, in food or feed industry.

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Method
Compatibility, Cytotoxicity, and Gastrointestinal Tenacity of Bacteriocin-Producing Bacteria Selected for a Consortium Probiotic Formulation to Be Used in Livestock Feed
Eveno, M., Savard, P., Belguesmia, Y., Bazinet, L., Gancel, F., Drider, D., & Fliss, I. (2020) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-020-09687-y · Cited by 13
“The key criteria for selecting a microbial strain as a probiotic are safety, survival under gastrointestinal conditions, and ability to inhibit pathogens [6].”
Background
Systematic approach to select lactic acid bacteria from spontaneously fermented milk able to fight Listeria monocytogenes and Staphylococcus aureus
Mkadem, W., Belguith, K., Oussaief, O., El‐Hatmi, H., Indio, V., Savini, F., Cesare, A. D., & Boudhrioua, N. M. (2022) · Food Bioscience · doi:10.1016/j.fbio.2022.102275 · Cited by 11
Probiotic potential and safety assessment of bacteriocinogenic Enterococcus faecalis CAUM157
Elnar, A. G., & Kim, G. (2025) · Frontiers in Microbiology · doi:10.3389/fmicb.2025.1563444 · Cited by 11
Effect of fermented milk Pediococcus acidilactici BK01 on cholesterol and microbiota in Wistar mice intestine
Melia, S., Juliyarsi, I., Kurnia, Y. F., Aritonang, S. N., Purwati, E., Sukma, A., Fitria, N., Susmiati, S., Meinapuri, M., Pratama, Y. E., et al. (2023) · Journal of Advanced Veterinary and Animal Research · doi:10.5455/javar.2023.j653 · Cited by 11
“[30] explained that the peptidoglycan cell wall of probiotic bacteria binds the cholesterol even to dead bacteria to decrease the levels.”
Background
Serotonin Exposure Improves Stress Resistance, Aggregation, and Biofilm Formation in the Probiotic Enterococcus faecium NCIMB10415
Scardaci, R., Manfredi, M., Barberis, E., Scutera, S., Marengo, E., & Pessione, E. (2021) · Microbiology Research · doi:10.3390/microbiolres12030043 · Cited by 10
Correlation between metabolites of lactic acid bacteria isolated from dairy traditional fermented Tunisian products and antifungal and antioxidant activities
Farhat, L. B., Aissaoui, N., Torrijos, R., Luz, C., Meca, G., & Abidi, F. (2022) · Journal of Applied Microbiology · doi:10.1111/jam.15763 · Cited by 10
“9% NaCl (w/v)] and 100 μl of each dilution was inoculated on Man Rogosa Sharpe (MRS) agar and M17 agar and all plates were incubated for 48 h at 30°C under anaerobic conditions (Baccouri et al., 2019).”
MethodInfluential
The Gill Microbiota of Argopecten purpuratus Scallop Is Dominated by Symbiotic Campylobacterota and Upwelling Intensification Differentially Affects Their Abundance
González, R. C., Henríquez‐Castillo, C., Lohrmann, K. B., Romero, M. S., Ramajo, L., Schmitt, P., & Brokordt, K. (2022) · Microorganisms · doi:10.3390/microorganisms10122330 · Cited by 9
In vitro evaluation of lactic acid bacteria with probiotic activity isolated from local pickled leaf mustard from Wuwei in Anhui as substitutes for chemical synthetic additives
Wu, C., Lin, X., Lin, T., Dai, C., Lv, H., Zhou, X., & Zhang, J. (2021) · Open Chemistry · doi:10.1515/chem-2021-0054 · Cited by 9
All Driven by Energy Demand? Integrative Comparison of Metabolism of Enterococcus faecalis Wildtype and a Glutamine Synthase Mutant
Loghmani, S. B., Zitzow, E., Koh, C. C., Ulmer, A., Veith, N., Großeholz, R., Rossnagel, M., Loesch, M., Aebersold, R. H., Kreikemeyer, B., et al. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.02400-21 · Cited by 9
Probiotics in milk and dairy foods
da Motta, A. D. S., Nespolo, C. R., & Breyer, G. M. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-85170-1.00004-x · Cited by 8
Enterococci as Intestinal Microbiota: Investigation of Characteristics and Probiotic Potential in Isolates from Adults and Breast-Fed Infants
Rahmani, M., Saffari, F., Domann, E., Zimmermann, K., Langroudi, L., & Mansouri, S. (2022) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-022-09951-3 · Cited by 8
“faecalis Symbioflor 1 was used as positive control [30].”
BackgroundMethodInfluential
Characterization of an Acidogenic Bacterial Consortium as Probiotic and Its Effect on Rumen Fermentation In Vitro and In Vivo
Robles‐Rodríguez, C., Cardoso-Carmona, D., González‐Dávalos, L., Lozano‐Flores, C., Páez-Trejo, A., Shimada, A. S., & Mora, O. (2023) · Ruminants · doi:10.3390/ruminants3040028 · Cited by 8
“Baccouri et al. [35], working with Enterococcus faecalis OB14, reported resistance to gentamicin and erythromycin.”
Background
A native probiotic strain Enterococcus faecalis TMBC 10513 alleviates avian pathogenic Escherichia coli-induced growth impairment and intestinal disruptions in yellow-feathered broilers at the early stage of infection
Ling, C., Yan, F., Lin, K., Ye, H., Cao, Q., Dong, Z., Zhang, C., Zuo, J., & Wang, W. (2025) · Poultry Science · doi:10.1016/j.psj.2025.105725 · Cited by 7
“…and acetic acids) to lower microenvironmental pH value, secrete antibacterial substances (e. g. bacteriocin) to destruct pathogenic bacterial cell membrane (Ladjouzi et al., 2025; Yin et al., 2024), as well as competitively inhibit pathogenic colonization of host intestine (Baccouri et al., 2019).”
Engineered Lactiplantibacillus plantarum and Levilactobacillus brevis utilizing ribonucleoprotein-mediated editing for inactivation of hemolysin gene
Kim, H. J., Kwon, M. Y., Song, S., Cheon, S. W., & Kim, H. J. (2025) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-025-04598-y · Cited by 8
“Streptococcus mutans , ATCC 6538 , and Enterococcus faecalis KCTC 3206 were used as controls for the hemolysis test, as described in previous studies (Baccouri et al. 2019; Wolff and Liljemark 1978 ; Xu et al. 2024).”
Probiotic Characterization of Lactic Acid Bacteria from Donkey Feces in China
Wu, Y., Yue, S., Yu, J., Bian, F., Gao, C., & Zhang, Y. (2025) · Animals · doi:10.3390/ani15020207 · Cited by 6
Hovenia Monofloral Honey can Attenuate Enterococcus faecalis Mediated Biofilm Formation and Inflammation
You, R., Kwon, O. Y., Woo, H. J., & Lee, S. H. (2021) · Food Science of Animal Resources · doi:10.5851/kosfa.2021.e65 · Cited by 6
Assessment of the safety of Levilactobacillus brevis CNCM I-5321, a probiotic candidate strain isolated from pulque with anti-proliferative activities
Torres-Maravilla, E., Boucard, A.-S., Azzaz, J. A., Gontier, S., Kulakauskas, S., Langella, P., & Bermúdez‐Humarán, L. G. (2023) · Beneficial Microbes · doi:10.1163/18762891-20230004 · Cited by 6
Bioprotective potential of lactic acid bacteria
Laslo, É., György, É., & András, C. D. (2020) · Acta Universitatis Sapientiae Alimentaria · doi:10.2478/ausal-2020-0007 · Cited by 6
Probiotic potential of three Enterococcus spp. isolated from raw milk: An in vitro assessment
Acar, B. Ç., Yüksekdağ, Z., & Yılmaz, E. Ş. (2025) · International Dairy Journal · doi:10.1016/j.idairyj.2025.106196 · Cited by 6
Gene Expression, Structural Characterization, and Functional Properties of Exopolysaccharide Produced from Potential Probiotic Enterococcus faecalis NOC219 Strain
Özdemir, N. (2023) · Applied Biochemistry and Biotechnology · doi:10.1007/s12010-023-04393-1 · Cited by 5
“Some strains of this genus, especially some of the Enterococcus faecalis strains, do not show pathogenicity [11].”
Background
Bacillus strains from the ovaries of Swiss albino mice (Mus musculus): deciphering of probiotic potential through an in vitro approach
Chirakkara, S. P., & Abraham, A. (2022) · Biomedicine · doi:10.51248/.v42i6.2302 · Cited by 5
Draft Genome Sequence of Enterococcus faecalis Strain OB15, a Probiotic Strain Recently Isolated from Tunisian Rigouta Cheese
Baccouri, O., Boukerb, A. M., Nilly, F., Cambronel, M., Smaali, I., Feuilloley, M. G. J., Abidi, F., & Connil, N. (2020) · Microbiology Resource Announcements · doi:10.1128/mra.01433-19 · Cited by 5
“faecalis OB15 from rigouta, a popular traditional Tunisian fermented cheese that is often prepared by boiling acidified cheese whey from cow’s milk (7).”
Background
Genomic evaluation of the probiotic and pathogenic features of Enterococcus faecalis from human breast milk and comparison with the isolates from animal milk and clinical specimens
Badr, L., Yasir, M., Alkhaldy, A. A., Soliman, S. A., Ganash, M., Turkistani, S. A., Jiman-Fatani, A. A., Alzahrani, I., & Azhar, E. I. (2024) · PeerJ · doi:10.7717/peerj.18392 · Cited by 4
“Moreover, capsule formation and adhesion–related genes have also been reported in probiotic/starter strains of enterococci ( Baccouri et al., 2019 ).”
Background
Enterococcus faecalis-Induced Biochemical Transformation during Fermentation of Underutilized Solenostemon monostachyus Leaves
Afolabi, I. S., Ahuekwe, E. F., Garuba, P. A., Adigun, A. J., Odutayo, O. E., & Adeyemi, A. O. (2022) · Fermentation · doi:10.3390/fermentation9010033 · Cited by 4
Enterococcus faecalis-Aided Fermentation to Facilitate Edible Properties and Bioactive Transformation of Underutilized Cyathea dregei Leaves
Afolabi, I. S., Adigun, A. J., Garuba, P. A., Ahuekwe, E. F., Odutayo, O. E., & Adeyemi, A. O. (2023) · Fermentation · doi:10.3390/fermentation9080707 · Cited by 4
Understanding the ambiguity behind Enterococcus as a probiotic ally or a pathogenic adversary
Elnar, A. G., & Kim, G. (2025) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2025.2562926 · Cited by 3
“Nevertheless, members of this genus continue to be a key component of various traditional fermented food products, enhancing the sensory properties of food and providing beneficial effects to the consuming host (Baccouri et al. 2019; Dapkevicius et al. 2021; de Melo Pereira et al. 2022).”
Revealing probiotic properties of Lactiplantibacillus plantarum and Enterococcus faecalis in Cornu aspersum animal model
Avgousti, K., Dushku, E., Spyropoulou, A., Kotzamanidis, C., Staikou, A. E., & Yiangou, M. (2025) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2025.105481 · Cited by 3
Gut-Derived Lactic Acid Bacteria from Cotton Bollworm Exhibit Efficient Gossypol Degradation and Probiotic Potential During Solid-State Fermentation of Cottonseed Meal
Li, S., Deng, S., Zhang, P., Lu, Q., Pu, W., Ma, M., Li, S., Zhang, W., & Chen, C. (2025) · Fermentation · doi:10.3390/fermentation11100598 · Cited by 3
“These findings are consistent with previous reports [39,40].”
Optimizing the application strategy of phosphorus fertilizer by Pseudomonas E sp017968885 to increase phosphorus yield of pepper
Hu, Q. C., Wu, H., Yu, M., Song, L., Feng, J., Ma, Y., Ding, F., Guo, L., & Wang, Z. (2025) · Frontiers in Agronomy · doi:10.3389/fagro.2025.1628083 · Cited by 3
Robust Goat-Derived Enterococcus Isolates with Broad-Spectrum Antipathogenic Activity as Next-Generation Probiotic Candidates
Essa, M. O. A., Basher, N. S., Abdelhadi, L. A. M., Ibrahim, N. A., Rehman, S. U., Husien, H. M., Saleh, A. A., & Cheng, D. (2026) · Veterinary Sciences · doi:10.3390/vetsci13020120 · Cited by 4
“Additionally, they can be found in diverse environments such as agro-industrial waste, food, animal feed, soil, plants, and water [41].”
Characterization and safety assessment of promising probiotic lactic acid bacteria from naturally fermented goat milk for use as functional yogurt starters
Billateh, A., Cheirsilp, B., & Suyotha, W. (2026) · Applied Food Research · doi:10.1016/j.afres.2026.102087 · Cited by 3
Traditional Mediterranean cheeses: Lactic acid bacteria populations and functional traits
Laranjo, M., & Potes, M. E. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-89875-1.00011-0 · Cited by 3
Traditionally fermented dairy products harbouring multidrug-resistant bacteria with probiotic-associated characteristics
Nath, S., Paul, M., Paul, P., Chanda, P., Naha, A., Yumnam, H., & Sharma, I. (2025) · International Dairy Journal · doi:10.1016/j.idairyj.2025.106538 · Cited by 2
Selection Criteria for Identifying Putative Probiont
TEZEL, B. U., Şanlıbaba, P., Akçelik, N., & Akçelik, M. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-822909-5.00002-2 · Cited by 4
Probiotic potential and anti-quorum sensing activity of Enterococcus faecalis and Lactobacillus kunkeei isolates from Apis mellifera
Kıymacı, M. E., Şimşek, D., Tok, K. C., Dirican, D., & Gumustas, M. (2023) · Journal of the Hellenic Veterinary Medical Society · doi:10.12681/jhvms.26743 · Cited by 2
Tannin derived from Uncaria gambir Roxb. as potential Enterococcus faecalis UDP-N-Acetylenolpyruvoyl-Glucosamine Reductase (Mur Benzyme) inhibitor: In-silico antibacterial study
Dharsono, H. D. A., Mujahid, M., Apriyanti, E., Adang, R. A. F., Putri, S. A., Satari, M. H., & Kurnia, D. (2023) · Research Journal of Pharmacy and Technology · doi:10.52711/0974-360x.2023.00744 · Cited by 2
Probiotic Dairy Foods
Eminoğlu, G., Akal, C., & Özer, B. (2023) · Wiley eBooks · doi:10.1002/9781119776406.ch3 · Cited by 2
Characterization of novel potential probiotic strains of lactic acid bacteria from rat faeces
Dieudonné, N., Mbugua, A., & Kevin, M. (2024) · African Journal of Microbiology Research · doi:10.5897/ajmr2024.9742 · Cited by 1
“These findings align with previous studies where Enterococcus strains (Baccouri et al., 2019) and L. garvieae strains (Patel et al., 2020) were viable in acidic pH and high bile salt concentrations.”
BackgroundResult
Antimicrobial potential and mechanism of infant feces-derived Enterococcus faecalis in inhibiting Enterotoxigenic Escherichia coli
Lü, X., Sang, W., & Pan, L. (2025) · Journal of Functional Foods · doi:10.1016/j.jff.2025.106659 · Cited by 1
Assessing lactococcal and enterococcal strains derived from traditionally fermented kefir and nabeez for their prospects as probiotics
Aziz, G., & Zaidi, A. (2025) · Microbiology · doi:10.1099/mic.0.001616 · Cited by 1
“Enterococcus species sourced from fermented foods generally lack gelatinase [72], as is the case here.”
Multifactorial Neuroprotective Potential of γ-Aminobutyric acid-Producing Potential Probiotics Against Stress Induced Neuronal Cell Lines
Paul, S., Banerjee, S., Banerjee, S., & Goel, G. (2026) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-026-10941-y · Cited by 1
“The same was determined using free radical scav - enging activity assays [ 59 , 60].”
Evaluation of the topical healing ability of purified exopolysaccharides (EPSs) from Enterococcus faecalis on skin wounds in male albino mice
Abed, S. M., Essa, R. H., & Yaseen, K. H. (2022) · AIP conference proceedings · doi:10.1063/5.0093648 · Cited by 1
Probiotic potential of indigenous Lactobacillus strains isolated from Algerian goatskin bag cheese Bouhezza using physiological and comparative genomic analyses
Sana, M., Zitoun, O. A., Zidoune, M. N., Barreau, M., Boukerb, A. M., & Connil, N. (2025) · International Dairy Journal · doi:10.1016/j.idairyj.2025.106206 · Cited by 2
Indicator Microflora of Ducks and Chickens in Home Farm Conditions
Виговська, Л. М., Ushkalov, А. V., DAVYDOVSKA, L., Melnyk, V. V., Ushkalov, В., & Shevchenko, O. (2025) · Veterinary Sciences and Practices · doi:10.17094/vetsci.1577819 · Cited by 1
Probiotic characterisation of Enterococcus faecalis strain isolated from a household dahi sample of Wayanad district, Kerala
Chandran, A., Beena, A. K., Bhagya, S., Rathish, R. L., & Rahila, M. P. (2022) · Journal of Veterinary and Animal Sciences · doi:10.51966/jvas.2022.53.1.70-78 · Cited by 1
Assessing the Microbial Quality of Commercial Aquaculture Probiotics by Next Generation Sequencing Revealed Faecal Bacteria and Bacteria of Public Health SignificancePreprint
Joseph, T. C., Bibindas, K. S., Lakshmi, T. R., Eltholth, M. M., & Murray, F. J. (2021) · Research Square · doi:10.21203/rs.3.rs-740362/v1 · Cited by 1
Safety and Microbiological Quality
Remize, F., & Montēt, D. (2019) · Fermentation · doi:10.3390/fermentation5020050
A Comparative Transcriptomic Analysis of Human Placental Trophoblasts in Response to Pathogenic and Probiotic Enterococcus faecalis Interaction
Tan, Q., Zeng, Z., Xu, F., & Wei, H. (2021) · Canadian Journal of Infectious Diseases and Medical Microbiology · doi:10.1155/2021/6655414
“faecalis strains are regarded as commensal bacteria or even probiotics for creating a healthy gut environment; however, other strains are considered to be dangerous as they can lead to a variety of nosocomial infections and diseases [2, 3].”
Background

Authors: Baccouri, O., Boukerb, A. M., Farhat, L. B., Zébré, A., Zimmermann, K., Domann, E., Cambronel, M., Barreau, M., Maillot, O., Rincé, I., Muller, C., Marzouki, M. N., Feuilloley, M., Abidi, F., & Connil, N.
Affiliations: University of Carthage (TN)
Normandie Université (FR)
SymbioPharm (Germany) (DE)
Justus-Liebig-Universität Gießen (DE)
Corresponding author: Connil, Nathalie
ORCID: Boukerb, Amine Mohamed
Zébré, Arthur
Zimmermann, Kurt
Cambronel, Mélyssa
Barreau, Magalie
Feuilloley, Marc
Abidi, Ferid
Connil, Nathalie
Venue: Frontiers in Microbiology
Publisher: Frontiers Media SA
Published: 2019-04-24
Volume: 10
Pages: 881-881
ISSN: 1664-302X (ISSN-L)
DOI: 10.3389/fmicb.2019.00881
PMC: PMC6491886
OpenAlex: W2942463136
Cited by: 117
References: 92
Citations by year: 2026: 10 · 2025: 15 · 2024: 9 · 2023: 16 · 2022: 27 · 2021: 23 · 2020: 12 · 2019: 5
FWCI: 12.92
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: Frontiers in Microbiology (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
HAL (submittedVersion, cc-by)
HAL (submittedVersion, other-oa)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: European Commission
Région Normandie
Topics: Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Keywords: Enterococcus faecalis, probiotic potential, probiotic safety, fermented dairy products, gastrointestinal tolerance, bile salt tolerance, biofilm formation, intestinal barrier, antibiotic susceptibility, tetracycline resistance, Galleria mellonella virulence, whole genome sequencing, average nucleotide identity

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Probiotic Potential and Safety Evaluation of Enterococcus faecalis OB14 and OB15, Isolated From Traditional Tunisian Testouri Cheese and Rigouta, Using Physiological and Genomic Analysis

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