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
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Probiotic potential of Enterococcus faecalis strains isolated from meconium
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Background
Functional and health promoting inherent attributes of Enterococcus hirae F2 as a novel probiotic isolated from the digestive tract of the freshwater fish Catla catla
Adnan, M., Patel, M. B., & Hadi, S. S. (2017) · PeerJ · doi:10.7717/peerj.3085 · Cited by 73 · cited 1×
“While the genus Enterococcus includes many species, only few have been studied to be used as probiotics, such as E. faecalis, E. faecium, E. lactis and more recently E. hirae (Adnan et al., 2017) and E. durans (Li et al., 2018).”
Background
Comparative study of normal and sensitive skin aerobic bacterial populations
Hillion, M., Mijouin, L., Jaouen, T., Barreau, M., Meunier, P., Lefeuvre, L., Lati, E., Chevalier, S., & Feuilloley, M. G. J. (2013) · MicrobiologyOpen · doi:10.1002/mbo3.138 · Cited by 70 · cited 1×
“1 system, as previously described (Hillion et al., 2013; Zommiti et al., 2018).”
The genus Enterococcus as probiotic: safety concerns
Araújo, T. F., & Ferreira, C. L. D. L. F. (2013) · Brazilian Archives of Biology and Technology · doi:10.1590/s1516-89132013000300014 · Cited by 70
Technologically important characteristics of Enterococcus isolates from milk and dairy products
Wessels, D., Jooste, P. J., & Mostert, J. F. (1990) · International Journal of Food Microbiology · doi:10.1016/0168-1605(90)90082-g · Cited by 67
Biofilm-Forming Capacity in Biogenic Amine-Producing Bacteria Isolated from Dairy Products
Díaz, M., Ladero, V., del Río, B., Redruello, B., Fernández, M., Martín, M. C., & Álvarez, M. A. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00591 · Cited by 65
Improved Performance of Bacterium and Yeast Identification by a Commercial Matrix-Assisted Laser Desorption Ionization–Time of Flight Mass Spectrometry System in the Clinical Microbiology Laboratory
Haigh, J., Degun, A., Eydmann, M., Millar, M. R., & Wilks, M. (2011) · Journal of Clinical Microbiology · doi:10.1128/jcm.00576-11 · Cited by 63 · cited 1×
“Formic acid was used on the bacterial spots as a quick extraction procedure (Haigh et al., 2011), then the MALDI target plate was introduced in the mass spectrometer for measurement and data acquisition.”
Method
Optimization of processing conditions for the quantification of enterococci biofilms using microtitre-plates
Extremina, C. I., Costa, L., Aguiar, A. I., Peixe, L., & Fonseca, A. P. (2010) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2010.11.007 · Cited by 62
Lactococcus sp. as Potential Probiotic Lactic Acid Bacteria
Kimoto‐Nira, H., Mizumachi, K., Nomura, M., Kobayashi, M., Fujita, Y., Okamoto, T., Suzuki, I., Tsuji, N. M., Kurisaki, J., & Ohmomo, S. (2007) · Japan Agricultural Research Quarterly JARQ · doi:10.6090/jarq.41.181 · Cited by 60 · cited 1×
“It has been reported that the mechanism of adhesion to Caco-2/TC7 cells involves the combinations of carbohydrate and protein factors on the bacterial cell surface (Kimoto-Nira et al., 2007).”
Background
Application of MALDI-TOF MS fingerprinting as a quick tool for identification and clustering of foodborne pathogens isolated from food products.
Elbehiry, A., Marzouk, E., Hamada, M., Aldubaib, M., Alyamani, E. J., Moussa, I. M., AlRowaidhan, A., & Hemeg, H. A. (2017) · PubMed · Cited by 59
Strain‐specific immunomodulatory effects of Lactobacillus plantarum strains on birch‐pollen‐allergic subjects out of season
Snel, J., Vissers, Y. M., Smit, B., Jongen, J. M. J., van der Meulen, E. T., Zwijsen, R. M. L., Ruinemans‐Koerts, J., Jansen, A. P. H., Kleerebezem, M., & Savelkoul, H. F. J. (2010) · Clinical & Experimental Allergy · doi:10.1111/j.1365-2222.2010.03650.x · Cited by 52 · cited 1×
“These differences among bacteria are not surprising since the immunomodulatory effects are often strain-specific (Helwig et al., 2006; Snel et al., 2011).”
Background
Multistep mechanism of probiotic bacterium, the effect on innate immune system
Amit‐Romach, E., Uni, Z., & Reifen, R. M. (2009) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.200800591 · Cited by 43 · cited 1×
“The ability of LAB to modulate cytokines production is considered as another criterion for the selection of beneficial microbes (Amit-Romach et al., 2010).”
Background
Safety characterisation and inhibition of fungi and bacteria by a novel multiple enterocin-producing Enterococcus lactis 4CP3 strain
Braïek, O. B., Cremonesi, P., Morandi, S., Smaoui, S., Hani, K., & Ghrairi, T. (2018) · Microbial Pathogenesis · doi:10.1016/j.micpath.2018.03.005 · Cited by 42
Complete Genome Sequence of the Probiotic Enterococcus faecalis Symbioflor 1 Clone DSM 16431
Fritzenwanker, M., Kuenne, C. T., Billion, A., Hain, T., Zimmermann, K., Goesmann, A., Chakraborty, T., & Domann, E. (2013) · Genome Announcements · doi:10.1128/genomea.00165-12 · Cited by 41
Novel Aggregation Promoting Factor AggE Contributes to the Probiotic Properties of Enterococcus faecium BGGO9-28
Veljović, K., Popović, N., Miljković, M., Tolinački, M., Terzić-Vidojević, A., & Kojić, M. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01843 · Cited by 38
In vitrocomparison of commensal, probiotic and pathogenic strains ofEnterococcus faecalis
Christoffersen, T. E., Jensen, H., Kleiveland, C. R., Dørum, G., Jacobsen, M., & Lea, T. (2012) · British Journal Of Nutrition · doi:10.1017/s0007114512000220 · Cited by 35 · cited 1×
“The complete genome sequence of this strain has been determined and several toxicological studies showed that the strain can be administred safely to humans (Domann et al., 2007; Christoffersen et al., 2012; Fritzenwanker et al., 2013).”
Background
Effects of the ProbioticEnterococcus faeciumand PathogenicEscherichia coliStrains in a Pig and Human Epithelial Intestinal Cell Model
Lodemann, U., Strahlendorf, J., Schierack, P., Klingspor, S., Aschenbach, J. R., & Märtens, H. (2015) · Scientifica · doi:10.1155/2015/235184 · Cited by 32
Does Enterococcus faecalis from Traditional Raw Milk Cheeses Serve as a Reservoir of Antibiotic Resistance and Pathogenic Traits?
Silvetti, T., Morandi, S., & Brasca, M. (2019) · Foodborne Pathogens and Disease · doi:10.1089/fpd.2018.2542 · Cited by 32 · cited 1×
“faecalis isolated from raw milk cheeses does not represent a substantial reservoir of antimicrobial resistance and virulence factors if compared with clinical strains (Silvetti et al., 2019).”
Background
Probiotic Assessment of Lactobacillus plantarum 15HN and Enterococcus mundtii 50H Isolated from Traditional Dairies Microbiota.
Haghshenas, B., Haghshenas, M., Nami, Y., Khosroushahi, A. Y., Abdullah, N., Barzegari, A., Rosli, R., & Hejazi, M. S. (2016) · PubMed Central · doi:10.15171/apb.2016.07 · Cited by 27 · cited 1×
“3% oxgall with a survival rate of 98% after 3 h of incubation (Haghshenas et al., 2016), and E.”
Background
Probiotic Enterococcus faecalis Symbioflor® down regulates virulence genes of EHEC in vitro and decrease pathogenicity in a Caenorhabditis elegans model
Neuhaus, K., Lamparter, M. C., Zölch, B., Landstorfer, R., Simon, S., Spanier, B., Ehrmann, M. A., & Vogel, R. F. (2016) · Archives of Microbiology · doi:10.1007/s00203-016-1291-8 · Cited by 23
Substance P enhances lactic acid and tyramine production in Enterococcus faecalis V583 and promotes its cytotoxic effect on intestinal Caco-2/TC7 cells
Biaggini, K., Borrel, V., Szunerits, S., Boukherroub, R., N’Diaye, A. R., Zébré, A. C., Bonnin-Jusserand, M., Duflos, G., Feuilloley, M. G. J., Drider, D., et al. (2017) · Gut Pathogens · doi:10.1186/s13099-017-0171-3 · Cited by 23
CylA is a sequence-specific protease involved in toxin biosynthesis
Tang, W., Bobeica, S. C., Wang, L., & van der Donk, W. A. (2018) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/s10295-018-2110-9 · Cited by 23 · cited 1×
“faecalis and acute patient mortality in the clinic (Tang et al., 2018).”
Background
Probiotic potential of enterococci isolated from canine feed
Lauková, A., Marciňáková, M., Strompfová, V., & Ouwehand, A. C. (2008) · Folia Microbiologica · doi:10.1007/s12223-008-0012-3 · Cited by 22 · cited 2×
“Some strains of Enterococci, isolated from canine feed, were even found to be able to grow in the presence of 5% Oxgall (Lauková et al., 2008).”
BackgroundInfluential
Development of a Rapid Identification Method for the Differentiation of Enterococcus Species Using a Species-Specific Multiplex PCR Based on Comparative Genomics
Park, J., Jin, G.-D., Pak, J. I., Won, J., & Kim, E. B. (2017) · Current Microbiology · doi:10.1007/s00284-017-1210-5 · Cited by 17
Survival of potentially probiotic enterococci in dairy matrices and in the human gastrointestinal tract
Pimentel, L. L., Mättö, J., Malcata, F. X., Pintado, M., & Saarela, M. (2012) · International Dairy Journal · doi:10.1016/j.idairyj.2012.07.008 · Cited by 10
In Silico and Experimental Data Claiming Safety Aspects and Beneficial Attributes of the Bacteriocinogenic Strain Enterococcus faecalis B3A-B3B
Al-Seraih, A., Belguesmia, Y., Cudennec, B., Baah, J., & Drider, D. (2017) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-017-9357-8 · Cited by 7

Flagged first, then by citations

Research works printed but not linked: 2

Pritchard, 2017, PYANI: Python Module for Average NucleotideIdentity Analyses
Seemann, 2018, abricate: Mass Screening of Contigs for Antimicrobial and Virulence Genes

Sorted by citations

Probiotics Mechanism of Action on Immune Cells and Beneficial Effects on Human Health
Mazziotta, C., Tognon, M., Martini, F., Torreggiani, E., & Rotondo, J. C. (2023) · Cells · doi:10.3390/cells12010184 · Cited by 889
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Krawczyk, B., Wityk, P., Gałęcka, M., & Michalik, M. (2021) · Microorganisms · doi:10.3390/microorganisms9091900 · Cited by 432
Microbial Metabolic Capacity for Intestinal Folate Production and Modulation of Host Folate Receptors
Engevik, M. A., Morra, C. N., Röth, D., Engevik, K. A., Spinler, J. K., Devaraj, S., Crawford, S. E., Estes, M. K., Kalkum, M., & Versalovic, J. A. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.02305 · Cited by 206
“These microbes included three strains which are currently available as probiotics (L. reuteri ATCC PTA 6475, Enterococcus faecalis Symbioflor DSM 16431, and E. coli Nissle 1917) (Gronbach et al., 2010; Mu et al., 2018; Baccouri et al., 2019).”
Background
Advantages and disadvantages of non‐starter lactic acid bacteria from traditional fermented foods: Potential use as starters or probiotics
Grujović, M. Ž., Mladenović, K., Semedo‐Lemsaddek, T., Laranjo, M., Stefanović, O. D., & Kocić‐Tanackov, S. (2022) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.12897 · Cited by 163
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Dapkevicius, M. D. L. E., Sgardioli, B. F., Câmara, S. P. D. A. E., Poeta, P. A. C. Q. D., & Malcata, F. X. (2021) · Foods · doi:10.3390/foods10040821 · Cited by 166
“faecalis strain from traditional Tunisian Rigouta increased by 28% the secretion of interleukin-10 in Caco-2/TC7 cells, an indication of its immunomodulatory potential [235].”
Background

See all 117

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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