New insight into biofilm formation ability, the presence of virulence genes and probiotic potential of Enterococcus sp. dairy isolates

Frontiers in Microbiology

Volumn 9, Issue JAN, 2018, Pages

  Popovic, Nikola ^a   Dinic, Miroslav ^a   Tolinacki, Maja ^a   Mihajlovic, Sanja ^a   Terzic Vidojevic, Amarela ^a   Bojic, Svetlana ^b   Djokic, Jelena ^a   Golic, Nataša ^a   Veljovic, Katarina ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

^b HITTest Doo ^*  (Serbia)

Author keywords

Adhesion; Antibiotic resistance; Biofilm formation; Dairy isolates; Enterococcus sp.; Pathogen exclusion; Virulence

Indexed keywords

BACTERIAL TOXIN; CELL SURFACE PROTEIN; CIPROFLOXACIN; DNA 16S; GELATINASE;

ANTIBIOTIC SENSITIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIUM ISOLATE; BIOFILM; CELL ADHESION ASSAY; CYTOTOXICITY; DAIRY PRODUCT; ENTEROCOCCUS AVIUM; ENTEROCOCCUS DURANS; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ENTEROCOCCUS HIRAE; ENTEROCOCCUS ITALICUS; GASTROINTESTINAL TRACT; HEMOLYSIS ASSAY; LACTOBACILLUS; MICROFLORA; MINIMUM INHIBITORY CONCENTRATION; MTT ASSAY; NONHUMAN; OPTICAL DENSITY; PHYLOGENY; POLYMERASE CHAIN REACTION; SALMONELLA ENTERICA SEROVAR ENTERITIDIS; VIRULENCE;

EID: 85041631915     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2018.00078     Document Type: Article

References (49)

1. Anderson, A. C., Jonas, D., Huber, I., Karygianni, L., Wölber, J., Hellwig, E., et al. (2015). Enterococcus faecalis from food, clinical specimens, and oral sites: prevalence of virulence factors in association with biofilm formation. Front. Microbiol. 6:1534. doi: 10.3389/fmicb.2015.01534
2. Banwo, K., Sanni, A., and Tan, H. (2013). Technological properties and probiotic potential of Enterococcus faecium strains isolated from cow milk. J. Appl. Microbiol. 114, 229-241. doi: 10.1111/jam.12031
3. CLSI (2015). M100-S25 Performance Standards For Antimicrobial Susceptibility Testing; Twenty-Fifth Informational Supplement. Wayne, PA: Clinical and Laboratory Standards Institute.
4. du Toit, M., Franz, C. M. A. P., Dicks, L. M. T., and Holzapfel, W. H. (2000). Preliminary characterization of bacteriocins produced by Enterococcus faecium and Enterococcus faecalis isolated from pig faeces. J. Appl. Microbiol. 88, 482-494. doi: 10.1046/j.1365-2672.2000.00986.x
5. Duprè, I., Zanetti, S., Schito, A. M., Fadda, G., and Sechi, L. A. (2003). Incidence of virulence determinants in clinical Enterococcus faecium and Enterococcus faecalis isolates collected in Sardinia (Italy). J. Med. Microbiol. 52, 491-498. doi: 10.1099/jmm.0.05038-0
6. Eaton, T. J., and Gasson, M. J. (2001). Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl. Environ. Microbiol. 67, 1628-1635. doi: 10.1128/AEM.67.4.1628-1635.2001
7. Elhadidy, M., and Zahran, E. (2014). Biofilm mediates Enterococcus faecalis adhesion, invasion and survival into bovine mammary epithelial cells. Lett. Appl. Microbiol. 58, 248-254. doi: 10.1111/lam.12184
8. FAO-WHO (2016). Probiotics In Food. Health and Nutritional Properties and Guidelines for Evaluation. Rome: FAO-WHO.
9. Fisher, K., and Phillips, C. (2009). The ecology, epidemiology and virulence of Enterococcus. Microbiology 155, 1749-1757. doi: 10.1099/mic.0.026385-0
10. Franz, C. M., Huch, M., Abriouel, H., Holzapfel, W., and Gálvez, A. (2011). Enterococci as probiotics and their implications in food safety. Int. J. Food Microbiol. 151, 125-140. doi: 10.1016/j.ijfoodmicro.2011.08.014
11. Franz, C. M., Muscholl-Silberhorn, A. B., Yousif, N. M., Vancanneyt, M., Swings, J., and Holzapfel, W. H. (2001). Incidence of virulence factors and antibiotic resistance among enterococci isolated from food. Appl. Environ. Microbiol. 67, 4385-4389. doi: 10.1128/AEM.67.9.4385-4389.2001
12. Galili, T. (2015). dendextend: an R package for visualizing, adjusting and comparing trees of hierarchical clustering. Bioinformatics 31, 3718-3720. doi: 10.1093/bioinformatics/btv428
13. Giraffa, G. (2003). Functionality of enterococci in dairy products. Int. J. Food Microbiol. 88, 215-222. doi: 10.1016/S0168-1605(03)00183-1
14. Golic, N., Strahinic, I., Terzic-Vidojevic, A., Begovic, J., Nikolic, M., Tolinacki, M., et al. (2012). Molecular diversity among natural populations of Lactobacillus paracasei and Lactobacillus plantarum/paraplantarum strains isolated from autochthonous dairy products. Eur. Food Res. Technol. 234, 627-638. doi: 10.1007/s00217-012-1670-6
15. Hahsler, M., Chelluboina, S., Hornik, K., and Buchta, C. (2011). The arules R-package ecosystem: analyzing interesting patterns from large transaction datasets. J. Mach. Learn. Res. 12, 1977-1981.
16. Hahsler, M., Gruen, B., and Hornik, K. (2005). arules-A computational environment for mining association rules and frequent item sets. J. Stat. Soft. 14:15. doi: 10.18637/jss.v014.i15
17. Howarth, G. S., and Wang, H. (2013). Role of endogenous microbiota, probiotics and their biological products in human health. Nutrients 5, 58-81. doi: 10.3390/nu5010058
18. Hummel, A., Holzapfel, W. H., and Franz, C. M. (2007). Characterisation and transfer of antibiotic resistance genes from enterococci isolated from food. Syst. Appl. Microbiol. 30, 1-7. doi: 10.1016/j.syapm.2006.02.004
19. Johansson, D., and Rasmussen, M. (2013). Virulence factors in isolates of Enterococcus faecalis from infective endocarditis and from the normal flora. Microb. Pathog. 55, 28-31. doi: 10.1016/j.micpath.2012.09.009
20. Koch, S., Hufnagel, M., Theilacker, C., and Huebner, J. (2004). Enterococcal infections: host response, therapeutic, and prophylactic possibilities. Vaccine 22, 822-830. doi: 10.1016/j.vaccine.2003.11.027
21. Kreuzer, S., Machnowska, P., Aßmus, J., Sieber, M., Pieper, R., Schmidt, M. F. G., et al. (2012). Feeding of the probiotic bacterium Enterococcus faecium NCIMB 10415 differentially affects shedding of enteric viruses in pigs. Vet. Res. 43:58. doi: 10.1186/1297-9716-43-58
22. Lesuffleur, T., Barbat, A., Dussaulx, E., and Zweibaum, A. (1990). Growth adaptation to methotrexate of HT-29 human colon carcinoma cells is associated with their ability to differentiate into columnar absorptive and mucus-secreting cells. Cancer Res. 50, 6334-6343.
23. Lopes, Mde. F., Simões, A. P., Tenreiro, R., Marques, J. J. F., and Crespo, M. T. B. (2006). Activity and expression of a virulence factor, gelatinase, in dairy enterococci. Int. J. Food Microbiol. 112, 208-214. doi: 10.1016/j.ijfoodmicro.2006.09.004
24. Lozo, J., Vuksanovic, M., Strahinic, I., and Topisirovic, L. (2004). Characterization and antimicrobial activity of bacteriocin 217 produced by natural isolate Lactobacillus paracasei subsp. paracasei BGBUK2-16. J. Food Prot. 67, 2727-2734. doi: 10.4315/0362-028X-67.12.2727
25. Macovei, L., Ghosh, A., Thomas, V. C., Hancock, L. E., Mahmood, S., and Zurek, L. (2009). Enterococcus faecalis with the gelatinase phenotype regulated by the fsr operon and with biofilm-forming capacity are common in the agricultural environment. Environ. Microbiol. 11, 1540-1547. doi: 10.1111/j.1462-2920.2009.01881.x
26. McWilliam, H., Li, W., Uludag, M., Squizzato, S., Park, Y. M., Buso, N., et al. (2013). Analysis tool web services from the EMBL-EBI. Nucleic Acids Res. 41, W597-600. doi: 10.1093/nar/gkt376
27. Medeiros, A. W., Pereira, R. I., Oliveira, D. V., Martins, P. D., d'Azevedo, P. A., Van der Sand, S., et al. (2014). Molecular detection of virulence factors among food and clinical Enterococcus faecalis strains in South Brazil. Brazilian J. Microbiol. 45, 327-332. doi: 10.1590/S1517-83822014005000031
28. Mohamed, J., and Huang, D. B. (2007). Biofilm formation by enterococci. J. Med. Microbiol. 56, 1581-1588. doi: 10.1099/jmm.0.47331-0
29. Moraes, P. M., Perin, L. M., Todorov, S. D., Silva, A., Franco, B. D., and Nero, L. A. (2012). Bacteriocinogenic and virulence potential of Enterococcus isolates obtained from raw milk and cheese. J. Appl. Microbiol. 113, 318-328. doi: 10.1111/j.1365-2672.2012.05341.x
30. Mosmann, T. (1983). Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63. doi: 10.1016/0022-1759(83)90303-4
31. Nakayama, J., Kariyama, R., and Kumon, H. (2002). Description of a 23.9-kilobase chromosomal deletion containing a region encoding fsr genes which mainly determines the gelatinase-negative phenotype of clinical isolates of Enterococcus faecalis in urine. Appl. Environ. Microbiol. 68, 3152-3155. doi: 10.1128/AEM.68.6.3152-3155.2002
32. Nilsen, T., Nes, I. F., and Holo, H. (2003). Enterolysin A, a cell wall-degrading bacteriocin from Enterococcus faecalis LMG 2333. Appl. Environ. Microbiol. 69, 2975-2984. doi: 10.1128/AEM.69.5.2975-2984.2003
33. Nishiyama, K., Sugiyama, M., and Mukai, T. (2016). Adhesion properties of lactic acid bacteria on intestinal mucin. Microorganisms 20:4. doi: 10.3390/microorganisms4030034
34. Omar, N., Ben, C., Astro, A., Lucas, R., Abriouel, H., Yousif, N. M. K., et al. (2004). Functional and safety aspects of enterococci isolated from different Spanish foods. Syst. Appl. Microbiol. 27, 118-130 doi: 10.1078/0723-2020-00248
35. Panel, E. F. (2012). Guidance on the assessment of bacterial susceptibility to antimicrobials of human and veterinary importance. EFSA J. 10:2740. doi: 10.2903/j.efsa.2012.2740
36. Paradis, E., Claude, J., and Strimmer, K. (2004). APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289-290. doi: 10.1093/bioinformatics/btg412
37. Pieniz, S., de Moura, T. M., Cassenego, A. P. V., Andreazza, R., Frazzon, A. P. G., Camargo, F. A., et al. (2015). Evaluation of resistance genes and virulence factors in a food isolated Enterococcus durans with potential probiotic effect. Food Control 51, 49-54. doi: 10.1016/j.foodcont.2014.11.012
38. Rinkinen, M., Jalava, K., Westermarck, E., Salminen, S., and Ouwehand, A. C. (2003). Interaction between probiotic lactic acid bacteria and canine enteric pathogens: a risk factor for intestinal Enterococcus faecium colonization? Vet. Microbiol. 92, 111-119. doi: 10.1016/S0378-1135(02)00356-5
39. Sánchez, B., Fernández-García, M., Margolles, A., de los Reyes-Gavilán, C. G., and Ruas-Madiedo, P. (2010). Technological and probiotic selection criteria of a bile-adapted Bifidobacterium animalis subsp. Lactis Strain. Int. Dairy J. 20, 800-805. doi: 10.1016/j.idairyj.2010.06.004
40. Soares, R., Fedi, A. C., Reiter, K., Caierão, J., and D'Azevedo, P. (2014). Correlation between biofilm formation and gelE, esp, and agg genes in Enterococcus spp. clinical isolates. Virulence 5, 634-637. doi: 10.4161/viru.28998
41. Terzic-Vidojevic, A., Veljovic, K., Begovic, J., Filipic, B., Popovic, D., Tolinacki, M., et al. (2015). Diversity and antibiotic susceptibility of autochthonous dairy enterococci isolates: are they safe candidates for autochthonous starter cultures? Front. Microbiol. 6:954. doi: 10.3389/fmicb.2015.00954
42. Uroic, K., Nikolic, M., Kos, B., Pavunc, A. L., Beganovic, J., Lukic, J., et al. (2014). Probiotic properties of lactic acid bacteria isolated from Croatian fresh soft cheese and Serbian white pickled cheese. Food Technol. Biotechnol. 52, 232-241.
43. Valenzuela, A. S., Omar, N. B., Abriouel, H., López, R. L., Veljovic, K., Ca-amero, M. M., et al. (2009). Virulence factors, antibiotic resistance, and bacteriocins in enterococci from artisan foods of animal origin. Food Control 20, 381-385. doi: 10.1016/j.foodcont.2008.06.004
44. Valeriano, V. D., Parungao-Balolong, M. M., and Kang, D. K. (2014). In vitro evaluation of the mucin-adhesion ability and probiotic potential of Lactobacillus mucosae LM1. J. Appl. Microbiol. 117, 485-497. doi: 10.1111/jam.12539
45. Vankerckhoven, V., Van Autgaerden, T., Vael, C., Lammens, C., Chapelle, S., Rossi, R., et al. (2004). Development of a multiplex PCR for the detection of asa1, gelE, cylA, esp, and hyl genes in enterococci and survey for virulence determinants among European hospital isolates of Enterococcus faecium. J. Clin. Microbiol. 42, 4473-4479. doi: 10.1128/JCM.42.10.4473-4479.2004
46. Van Tyne, D., and Gilmore, M. S. (2017). Raising the alarmone: within-host evolution of antibiotic-tolerant Enterococcus faecium. MBio 8, e00066-e00017. doi: 10.1128/mBio.00066-17
47. Veljovic, K., Fira, D., Terzic-Vidojevic, A., Abriouel, H., Galvez, A., and Topisirovic, L. (2009). Evaluation of antimicrobial and proteolytic activity of enterococci isolated from fermented products. Eur. Food Res. Technol. 230:63. doi: 10.1007/s00217-009-1137-6
48. Veljovic, K., Popovic, N., Vidojevic, A. T., Tolinacki, M., Mihajlovic, S., Jovcic, B., et al. (2015). Environmental waters as a source of antibiotic-resistant Enterococcus species in Belgrade, Serbia. Environ. Monit. Assess. 187:599. doi: 10.1007/s10661-015-4814-x
49. Živkovic, M., Miljkovic, M. S., Ruas-Madiedo, P., Markelic, M. B., Veljovic, K., Tolinacki, M., et al. (2016). EPS-SJ exopolisaccharide produced by the strain Lactobacillus paracasei subsp. paracasei BGSJ2-8 is involved in adhesion to epithelial intestinal cells and decrease on E. coli association to Caco-2 cells. Front. Microbiol. 7:286. doi: 10.3389/fmicb.2016.00286