Probiotic Potential of Dairy Western Balkan Countries Enterococcus faecium strains

  • Nikola Popović University in Belgrade – Institute of Molecular Genetics and Genetic Engineering
  • Amarela Terzić-Vidojević University in Belgrade – Institute of Molecular Genetics and Genetic Engineering
  • Emilija Brdarić University in Belgrade – Institute of Molecular Genetics and Genetic Engineering
  • Svetlana Soković Bajić University in Belgrade – Institute of Molecular Genetics and Genetic Engineering
  • Jelena Djokić University in Belgrade – Institute of Molecular Genetics and Genetic Engineering
  • Milica Živković University in Belgrade – Institute of Molecular Genetics and Genetic Engineering
  • Katarina Veljović University in Belgrade – Institute of Molecular Genetics and Genetic Engineering
Keywords: enterococci, virulence factors, probiotics, extracellular matrix, adhesion, survival

Abstract


One of the major genera of the lactic acid bacteria family, Enterococcus sp., has a controversial status, reflected in the fact that enterococci are utilized as starter cultures and probiotics, in addition to being known to cause nosocomial infections. The qualified presumption of the safety list and the widely acknowledged safe status for Enterococcus species are absent. Rich sources of Enterococcus faecium species with possible probiotic characteristics can be found in artisanal dairy products, typically made from raw milk. To further understand the probiotic potential and health-promoting effects, this study looked at the presence of virulence factors and adhesion properties of En. faecium isolated from artisanal dairy products from Western Balkan countries.

References

Vandera E, Kakouri A, Koukkou A-I, Samelis J. Major ecological shifts within the dominant nonstarter lactic acid bacteria in mature Greek Graviera cheese as affected by the starter culture type. Int J Food Microbiol. 2019; 290:15–26.

Švec P, and Franz CMAP. The family Enterococcaceae. Lactic Acid Bacteria: Biodiversity and Taxonomy. Wiley 2014; p. 171-173

Hanchi H, Mottawea W, Sebei K, Hammami R. The Genus Enterococcus: Between Probiotic Potential and Safety Concerns-An Update. Front Microbiol. 2018;9:1791.

Leclercq R. Epidemiological and resistance issues in multidrug-resistant staphylococci and enterococci. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis. 2009;15:224–231.

Kiruthiga A, Padmavathy K, Shabana P, Naveenkumar V, Gnanadesikan S, Malaiyan J. Improved detection of esp, hyl, asa1, gelE, cylA virulence genes among clinical isolates of Enterococci. BMC Res Notes. 2020;13:170.

Ramos S, Silva V, Dapkevicius M de LE, Igrejas G, Poeta P. Enterococci, from Harmless Bacteria to a Pathogen. Microorganisms. 2020;8:1118.

Ch’ng J-H, Chong KKL, Lam LN, Wong JJ, Kline KA. Biofilm-associated infection by enterococci. Nat Rev Microbiol. 2019;17:82–94.

Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, et al. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014;11:506–514.

Mitra AK, Rabbani GH. A double-blind, controlled trial of bioflorin (Streptococcus faecium SF68) in adults with acute diarrhea due to Vibrio cholerae and enterotoxigenic Escherichia coli. Gastroenterology. 1990;99:1149–1152.

Bybee SN, Scorza AV, Lappin MR. Effect of the probiotic Enterococcus faecium SF68 on presence of diarrhea in cats and dogs housed in an animal shelter. J Vet Intern Med. 2011;25:856–860.

Franz CMAP, Stiles ME, Schleifer KH, Holzapfel WH. Enterococci in foods conundrum for food safety. Int J Food Microbiol. 2003;88:105–122.

Graham K, Stack H, Rea R. Safety, beneficial and technological properties of enterococci for use in functional food applications - a review. Crit Rev Food Sci Nutr. 2020;60:3836–3861.

Terzić-Vidojević A, Veljović K, Popović N, Tolinački M, Golić N. Enterococci from Raw-Milk Cheeses: Current Knowledge on Safety, Technological, and Probiotic Concerns. Foods Basel Switz. 2021;10:2753.

Popović N, Dinić M, Tolinački M, Mihajlović S, Terzić-Vidojević A, Bojić S, et al. New Insight into Biofilm Formation Ability, the Presence of Virulence Genes and Probiotic Potential of Enterococcus sp. Dairy Isolates. Front Microbiol. 2018;9:78.

Kainulainen V, Korhonen TK. Dancing to another tune-adhesive moonlighting proteins in bacteria. Biology. 2014;3:178–204.

Somarajan SR, La Rosa SL, Singh KV, Roh JH, Höök M, Murray BE. The fibronectin-binding protein Fnm contributes to adherence to extracellular matrix components and virulence of Enterococcus faecium. Infect Immun. 2015;83:4653–4661.

Pinkston KL, Gao P, Diaz-Garcia D, Sillanpää J, Nallapareddy SR, Murray BE, Harvey BR. The Fsr quorum-sensing system of Enterococcus faecalis modulates surface display of the collagen-binding MSCRAMM Ace through regulation of gelE. J Bacteriol. 2011;193:4317–4325.

Garsin DA, Frank KL, Silanpää J, Ausubel FM, Hartke A, Shankar N, Murray BE. Pathogenesis and Models of Enterococcal Infection. In: Gilmore, MS, Clewell, DB, Ike, Y, Shankar, N (eds.), Enterococci: From Commensals to Leading Causes of Drug Resistant Infection. Massachusetts Eye and Ear Infirmary, Boston2014; (internet).

Parish, JH. Genetic manipulation of streptomyces—A laboratory manual: By DA Hopwood, MJ Bibb, KF Chater; T Kieser CJ Bruton, HM Kieser, DJ Lydiate, CP Smith, JM Ward and H Schrempf. pp 356. The John Innes Foundation, Norwich, UK and Cold Spring Harbour Laboratory. 1985. ISBN 0‐7084‐0336‐0. 1986; 196-196.

Lesuffleur T, Barbat A, Dussaulx E, Zweibaum A. 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. 1990;50(19):6334-43.

Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65:55–63.

Popović N, Brdarić E, Đokić J, Dinić M, Veljović K, Golić N, Terzić-Vidojević A. Yogurt Produced by Novel Natural Starter Cultures Improves Gut Epithelial Barrier In Vitro. Microorganisms. 2020;8:1586.

Valeriano VD, Parungao-Balolong MM, Kang D-K. In vitro evaluation of the mucin-adhesion ability and probiotic potential of Lactobacillus mucosae LM1. J Appl Microbiol. 2014;117:485–497.

Živković M, Miljković MS, Ruas-Madiedo P, Markelić MB, Veljović K, Tolinački M, et al. 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. 2016;7:286.

Terzić-Vidojević A, Veljović K, Begović J, Filipić B, Popović D, Tolinački M, et al. Diversity and antibiotic susceptibility of autochthonous dairy enterococci isolates: are they safe candidates for autochthonous starter cultures? Front Microbiol. 2015;6:954.

Anderson AC, Jonas D, Huber I, Karygianni L, Wölber J, Hellwig E, et al. Enterococcus faecalis from Food, Clinical Specimens, and Oral Sites: Prevalence of Virulence Factors in Association with Biofilm Formation. Front Microbiol. 2015;6:1534.

Fisher K, Phillips C. The ecology, epidemiology and virulence of Enterococcus. Microbiol Read Engl. 2009;155:1749–1757.

Marco ML, Pavan S, Kleerebezem M. Towards understanding molecular modes of probiotic action. Curr Opin Biotechnol. 2006;17:204–210.

Revolledo L, Ferreira AJP, Mead GC. Prospects in Salmonella Control: Competitive Exclusion, Probiotics, and Enhancement of Avian Intestinal Immunity. J Appl Poult Res. 2006;15:341–351.

Howarth GS, Wang H. Role of endogenous microbiota, probiotics and their biological products in human health. Nutrients. 2013;5:58–81.

Sánchez J-I, Martínez B, Guillén R, Jiménez-Díaz R, Rodríguez A. Culture conditions determine the balance between two different exopolysaccharides produced by Lactobacillus pentosus LPS26. Appl Environ Microbiol. 2006;72:7495–7502.

Zareba TW, Pascu C, Hryniewicz W, Wadström T. Binding of extracellular matrix proteins by enterococci. Curr Microbiol. 1997;34:6–11.

Miljkovic M, Strahinic I, Tolinacki M, Zivkovic M, Kojic S, Golic N, Kojic M. AggLb Is the Largest Cell-Aggregation Factor from Lactobacillus paracasei сubsp. paracasei BGNJ1-64, Functions in Collagen Adhesion, and Pathogen Exclusion In Vitro. PloS One. 2015;10:e0126387.

Veljović K, Popović N, Miljković M, Tolinački M, Terzić-Vidojević A, Kojić M. Novel Aggregation Promoting Factor AggE Contributes to the Probiotic Properties of Enterococcus faecium BGGO9-28. Front Microbiol. 2017;8:1843.

Probiotics in food: health and nutritional properties and guidelines for evaluation ; report of a Joint FAO/WHO Expert Consultation on Evaluation of Health and Nutritional Properties of Probiotics in Food including Powder Milk with Live Lactic Acid Bacteria, Córdoba, Argentina, 1 - 4 October 2001 ; report of a Joint FAO/WHO Working Group on Drafting Guidelines for the Evaluation of Probiotics in Food, London, Ontario, Canada, 30 April - 1 May 2002. Rome: Food and Agriculture Organization of the United Nations [u.a], 2006.

Nakayama J, Kariyama R, Kumon H. 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. 2002;68:3152–5.

Duprè I, Zanetti S, Schito AM, Fadda G, Sechi LA. Incidence of virulence determinants in clinical Enterococcus faecium and Enterococcus faecalis isolates collected in Sardinia (Italy). J Med Microbiol. 2003;52:491–498.

Vankerckhoven V, Van Autgaerden T, Vael C, Lammens C, Chapelle S, Rossi R, et al. 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. 2004;42:4473–9.

Eaton TJ, Gasson MJ. Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl Environ Microbiol. 2001;67:1628–35.

Published
2023/12/23
Section
Original scientific paper