Virulence, antibiotic resistance and biogenic amines of bacteriocinogenic lactococci and enterococci isolated from goat milk

International Journal of Food Microbiology

Volumn 185, Issue , 2014, Pages 121-126

  Perin, Luana Martins ^a   Miranda, Rodrigo Otávio ^a   Todorov, Svetoslav Dimitrov ^b   Franco, Bernadette Dora Gombossy de Melo ^b   Nero, Luís Augusto ^a  

^a FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Antibiotic resistance; Bacteriocins; Biogenic amines; Goat milk; Lactic acid bacteria; Virulence

Indexed keywords

ADHESION OF COLLAGEN; AGGREGATION SUBSTANCE; AMPICILLIN; BACTERIAL PROTEIN; BIOGENIC AMINE; CHLORAMPHENICOL; CYTOLYSIN; DEOXYRIBONUCLEASE; ENDOCARDITIS ANTIGEN; ENTEROCOCCAL SURFACE PROTEIN; GELATINASE; GENTAMICIN; GLYCEROL; HISTAMINE; HISTIDINE DECARBOXYLASE; HISTIDINE DECARBOXYLASE 1; HISTIDINE DECARBOXYLASE 2; HYALURONIDASE; MEMBRANE PROTEIN; ORNITHINE DECARBOXYLASE; PUTRESCINE; RIFAMPICIN; TRIACYLGLYCEROL LIPASE; TYRAMINE; TYROSINE DECARBOXYLASE; UNCLASSIFIED DRUG; VANCOMYCIN; VIRULENCE FACTOR;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; ENTEROCOCCUS; ENTEROCOCCUS DURANS; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ENTEROCOCCUS HIRAE; EPSILOMETER TEST; GENE EXPRESSION; GOAT MILK; HEMOLYSIS; HORIZONTAL GENE TRANSFER; INCUBATION TEMPERATURE; LACTOCOCCUS; LACTOCOCCUS LACTIS; LOW TEMPERATURE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; QUORUM SENSING; STARTER CULTURE;

ANTIBIOTIC RESISTANCE; BACTERIOCINS; BIOGENIC AMINES; GOAT MILK; LACTIC ACID BACTERIA; VIRULENCE;

ANIMALS; BIOGENIC AMINES; DRUG RESISTANCE, MICROBIAL; ENTEROCOCCUS; GENE EXPRESSION PROFILING; GOATS; LACTOCOCCUS; MILK; POLYMERASE CHAIN REACTION; VIRULENCE FACTORS;

EID: 84904708793     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2014.06.001     Document Type: Article

References (46)

1. Ammor M.S., Flórez A.B., Mayo B. Antibiotic resistance in non-enterococcal lactic acid bacteria and bifidobacteria. Food Microbiol. 2007, 24:559-570.
2. Badis A., Guetarni D., Moussa Boudjema B., Henni D., Kihal M. Identification and technological properties of lactic acid bacteria isolated from raw goat milk of four Algerian races. Food Microbiol. 2004, 21:579-588.
3. Barbosa J., Gibbs P.A., Teixeira P. Virulence factors among enterococci isolated from traditional fermented meat products produced in the North of Portugal. Food Control 2010, 21:651-656.
4. Bover-Cid S., Holzapfel W.H. Improved screening procedure for biogenic amine production by lactic acid bacteria. Int. J. Food Microbiol. 1999, 53:33-41.
5. Buckenhüskes H.J. Selection criteria for lactic acid bacteria to be used as starter cultures for various food commodities. FEMS Microbiol. Rev. 1993, 12:253-271.
6. Casalta E., Montel M.-C. Safety assessment of dairy microorganisms: the Lactococcus genus. Int. J. Food Microbiol. 2008, 126:271-273.
7. Castellano P., Belfiore C., Fadda S., Vignolo G. A review of bacteriocinogenic lactic acid bacteria used as bioprotective cultures in fresh meat produced in Argentina. Meat Sci. 2008, 79:483-499.
8. Coton M., Romano A., Spano G., Ziegler K., Vetrana C., Desmarais C., Lonvaud-Funel A., Lucas P., Coton E. Occurrence of biogenic amine-forming lactic acid bacteria in wine and cider. Food Microbiol. 2010, 27:1078-1085.
9. Cotter P.D., Hill C., Ross P.R. Bacteriocins: developing innate immunity for food. Nat. Rev. Microbiol. 2005, 3:777-788.
10. Courvalin P. Vancomycin resistance in Gram-positive cocci. Clin. Infect. Dis. 2006, 42:S25-S34.
11. Cox C.R., Coburn P.S., Gilmore M.S. Enterococcal cytolysin: a novel two component peptide system that serves as a bacterial defense against eukaryotic and prokaryotic cells. Curr. Protein Pept. Sci. 2005, 6:77-84.
12. Donabedian S.M., Thal L.A., Hershberger E., Perri M.B., Chow J.W., Bartlett P., Jones R., Joyce K., Rossiter S., Gay K. Molecular characterization of gentamicin-resistant enterococci in the United States: evidence of spread from animals to humans through food. J. Clin. Microbiol. 2003, 41:1109-1113.
13. Eaton T.J., Gasson M.J. Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl. Environ. Microbiol. 2001, 67:1628-1635.
14. EUCAST Clinical Breakpoints. European Committee on Antimicrobial Susceptibility Testing, Växjö, Sweden 2014.
15. Fernández M., Linares D.M., Alvarez M.A. Sequencing of the tyrosine decarboxylase cluster of Lactococcus lactis IPLA 655 and the development of a PCR method for detecting tyrosine decarboxylating lactic acid bacteria. J. Food Prot. 2004, 67:2521-2529.
16. Fernández E., Alegría Á., Delgado S., Mayo B. Phenotypic, genetic and technological characterization of Lactococcus garvieae strains isolated from a raw milk cheese. Int. Dairy J. 2010, 20:142-148.
17. Florez A.B., Delgado S., Mayo B. Antimicrobial susceptibility of lactic acid bacteria isolated from a cheese environment. Can. J. Microbiol. 2005, 51:51-58.
18. Giraffa G., Pepe G., Locci F., Neviani E., Carminati D. Hemolytic activity, production of thermonuclease and biogenic amines by dairy enterococci. Ital. J. Food Sci. 1995, 7:341-349.
19. Girish K.S., Kemparaju K. The magic glue hyaluronan and its eraser hyaluronidase: a biological overview. Life Sci. 2007, 80:1921-1943.
20. Gomes B.C., Esteves C.T., Palazzo I.C.V., Darini A.L.C., Felis G.E., Sechi L.A., Franco B.D.G.M., de Martinis E.C.P. Prevalence and characterization of Enterococcus spp. isolated from Brazilian foods. Food Microbiol. 2008, 25:668-675.
21. Haas W., Shepard B.D., Gilmore M.S. Two-component regulator of Enterococcus faecalis cytolysin responds to quorum-sensing autoinduction. Nature 2002, 415:84-87.
22. Herreros M.A., Sandoval H., González L., Castro J.M., Fresno J.M., Tornadijo M.E. Antimicrobial activity and antibiotic resistance of lactic acid bacteria isolated from Armada cheese (a Spanish goats' milk cheese). Food Microbiol. 2005, 22:455-459.
23. Hummel A., Holzapfel W.H., Franz C.M.A.P. Characterisation and transfer of antibiotic resistance genes from enterococci isolated from food. Syst. Appl. Microbiol. 2007, 30:1-7.
24. Joosten H.M.L.J., Northolt M.D. Detection, growth, and amine-producing capacity of lactobacilli in cheese. Appl. Environ. Microbiol. 1989, 55:2356-2359.
25. Khan S.A., Nawaz M.S., Khan A.A., Hopper S.L., Jones R.A., Cerniglia C.E. Molecular characterization of multidrug-resistant Enterococcus spp. from poultry and dairy farms: detection of virulence and vancomycin resistance gene markers by PCR. Mol. Cell. Probes 2005, 19:27-34.
26. Levy S.B., Marshall B. Antibacterial resistance worldwide: causes, challenges and responses. Nat. Med. 2004, 10:S122-S129.
27. Lopes M.F.S., Simões A.P., Terneiro R., Marques J.J.F., Crespo M.T.B. Activity and expression of a virulence factor, gelatinase, in dairy enterococci. Int. J. Food Microbiol. 2006, 112:208-214.
28. Majhenič A.Č., Rogelj I., Perko B. Enterococci from Tolminc cheese: population structure, antibiotic susceptibility and incidence of virulence determinants. Int. J. Food Microbiol. 2005, 102:239-244.
29. Martín-Platero A.M., Valdivia E., Maqueda M., Martínez-Bueno M. Characterization and safety evaluation of enterococci isolated from Spanish goats' milk cheeses. Int. J. Food Microbiol. 2009, 132:24-32.
30. Mathur S., Singh R. Antibiotic resistance in food lactic acid bacteria - a review. Int. J. Food Microbiol. 2005, 105:281-295.
31. Moraes P.M., Perin L.M., Todorov S.D., Silva A., Franco B.D.G.M., Nero L.A. Bacteriocinogenic and virulence potential of Enterococcus isolates obtained from raw milk and cheese. J. Appl. Microbiol. 2012, 113:318-328.
32. Nieto-Arribas P., Seseña S., Poveda J.M., Chicón R., Cabezas L., Palop L. Enterococcus populations in artisanal Manchego cheese: biodiversity, technological and safety aspects. Food Microbiol. 2011, 28:891-899.
33. Perin L.M., Nero L.A. Antagonistic lactic acid bacteria isolated from goat milk and identification of a novel nisin variant Lactococcus lactis. BMC Microbiol. 2014, 14:36.
34. Perreten V., Schwarz F., Cresta L., Boeglin M., Dasen G., Teuber M. Antibiotic resistance spread in food. Nature 1997, 389:801-802.
35. Ribeiro T., Abrantes M., Lopes M.F.S., Crespo M.T.B. Vancomycin-susceptible dairy and clinical enterococcal isolates carry vanA and vanB genes. Int. J. Food Microbiol. 2007, 113:289-295.
36. Rivas B., Marcobal Á., Muñoz R. Improved multiplex-PCR method for the simultaneous detection of food bacteria producing biogenic amines. FEMS Microbiol. Lett. 2005, 244:367-372.
37. Santos M.H.S. Biogenic amines: their importance in foods. Int. J. Food Microbiol. 1996, 29:213-231.
38. Schirru S., Todorov S.D., Favaro L., Mangia N.P., Basaglia M., Casella S., Comunian R., Franco B.D.G.M., Deiana P. Sardinian goat's milk as source of bacteriocinogenic potential protective cultures. Food Control 2012, 25:309-320.
39. Semedo T., Santos M.A., Lopes M.F.S., Marques J.J.F., Crespo M.T.B., Tenreiro R. Virulence factors in food, clinical and reference enterococci: a common trait in the genus?. Syst. Appl. Microbiol. 2003, 26:13-22.
40. Shankar V., Baghdayan A.S., Huycke M.M., Lindahl G., Gilmore M.S. Infection-derived Enterococcus faecalis strains are enriched in esp, a gene encoding a novel surface protein. Infect. Immun. 1999, 67:193-200.
41. Sousa C.P. Pathogenicity mechanisms of prokaryotic cells: an evolutionary view. Braz. J. Infect. Dis. 2003, 7:23-31.
42. Toomey N., Bolton D., Fanning S. Characterisation and transferability of antibiotic resistance genes from lactic acid bacteria isolated from Irish pork and beef abattoirs. Res. Microbiol. 2010, 161:127-135.
43. Valenzuela A.S., Omar N.b, Abriouel H., López R.L., Veljovic K., Cañamero M.M., Topisirovic M.K.L., Gálvez A. Virulence factors, antibiotic resistance, and bacteriocins in enterococci from artisan foods of animal origin. Food Control 2009, 20:381-385.
44. Van Tyne D., Martin M.J., Gilmore M.S. Structure, function, and biology of the Enterococcus faecalis cytolysin. Toxins 2013, 5:895-911.
45. Van Veen H.W., Konings W.N. The ABC family of multidrug transporters in microorganisms. Biochim. Biophys. Acta Bioenerg. 1998, 1365:31-36.
46. Vankerckhoven V., Van Autgaerden T., Vael C., Lammens C., Chapelle S., Rossi R., Jabes D., Goossens H. 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, 42:4473-4479.