Characterization of a wild, novel nisin A-Producing Lactococcus strain with an L. lactis subsp. cremoris genotype and an L. lactis subsp. lactis phenotype, isolated from Greek raw milk

Applied and Environmental Microbiology

Volumn 79, Issue 11, 2013, Pages 3476-3484

  Parapouli, Maria ^a,c   Delbès Paus, Céline ^b   Kakouri, Athanasia ^c   Koukkou, Anna Irini ^a   Montel, Marie Christine ^b   Samelis, John ^c  

^a UNIVERSITY OF IOANNINA   (Greece)

^b Institut National de la Recherche Agronomique   (France)

^c Dairy Research Institute of Ioannina   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

HISTIDINE BIOSYNTHESIS; LACTATE DEHYDROGENASE; LACTOCOCCUS LACTIS; MOLECULAR TOOLS; PROTECTIVE CULTURES; RANDOMLY AMPLIFIED POLYMORPHIC DNA; TAXONOMIC STUDY; WHOLE-CELL PROTEIN;

AMINO ACIDS; ANTIBIOTICS; DAIRIES; ENCODING (SYMBOLS); POLYMERASE CHAIN REACTION; RNA;

GENE ENCODING;

ENDO N ACETYLMURAMIDASE; ENDO-N-ACETYLMURAMIDASE; GLYCOSIDASE; RNA 16S;

ENZYME ACTIVITY; FERMENTATION; GENOTYPE; MICROBIAL COMMUNITY; MILK; PHENOTYPE; RNA; SPECIES DIVERSITY; SUGAR; TAXONOMY;

ANIMAL; ARTICLE; BIOLOGY; CLUSTER ANALYSIS; DNA SEQUENCE; GENETICS; GENOTYPE; GREECE; LACTOCOCCUS LACTIS; MICROBIOLOGY; MILK; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYLOGENY; RANDOM AMPLIFIED POLYMORPHIC DNA; SPECIES DIFFERENCE;

ANIMALS; BASE SEQUENCE; CLONING, MOLECULAR; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; GENOTYPE; GLYCOSIDE HYDROLASES; GREECE; LACTOCOCCUS LACTIS; MILK; MOLECULAR SEQUENCE DATA; PHENOTYPE; PHYLOGENY; RANDOM AMPLIFIED POLYMORPHIC DNA TECHNIQUE; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

GREECE;

EID: 84877108827     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00436-13     Document Type: Article

References (57)

1. Beresford TR, Fitzsimons NA, Brennan NL, Cogan TM. 2001. Recent advances in cheese microbiology. Int. Dairy J. 11:259 -274.
2. Casalta E, Montel MC. 2008. Safety assessment of dairy microorganisms: the Lactococcus genus. Int. J. Food Microbiol. 126:271-273.
3. Fernández E, Alegría A, Delgado S, Cruz Martin M, Mayo B. 2011. Comparative phenotypic and molecular genetic profiling of wild Lactococcus lactis subsp. lactis strains of the L. lactis subsp. lactis and L. lactis subsp. cremoris genotypes, isolated from starter-free cheeses made of raw milk. Appl. Environ. Microbiol. 77:5324 -5335.
4. Weerkamp AH, Klijn N, Neeter R, Smit G. 1996. Properties of mesophilic lactic acid bacteria from raw milk and natually fermented raw milk products. Neth. Milk Dairy J. 50:319 -332.
5. Gaya P, Babin M, Medina M, Nunez M. 1999. Diversity among lactococci isolated from ewes' raw milk and cheese. J. Appl. Microbiol. 87:849- 855.
6. Callon C, Duthoit F, Delbès C, Ferrand M, Le Frileux Y, De Crémoux R, Montel MC. 2007. Stability of microbial communities of goat milk during a lactation year: molecular approaches. Syst. Appl. Microbiol. 30: 547-560.
7. Cogan TM, Barbosa M, Beuvier E, Bianchi-Salvadori B, Cocconcelli PS, Fernandes I, Gomez J, Gomez R, Kalantzopoulos G, Ledda A, Medina M, Rea MC, Rodriguez E. 1997. Characterisation of the lactic acid bacteria in artisanal dairy products. J. Dairy Res. 64:409-421.
8. Mannu L, Paba A, Pes M, Scintu MF. 2000. Genotypic and phenotypic heterogeneity among lactococci isolated from traditional Pecorino Sardo cheese. J. Appl. Microbiol. 89:191-197.
9. Callon C, Millet L, Montel MC. 2004. Diversity of lactic acid bacteria isolated from AOC Salers cheese. J. Dairy Res. 71:231-244.
10. Psoni L, Kotzamanidis C, Yiangou M, Tzanetakis N, Litopoulou-Tzanetaki E. 2007. Genotypic and phenotypic diversity of Lactococcus lactis isolates from Batzos, a Greek PDO raw goat milk cheese. Int. J. Food Microbiol. 114:211-220.
11. Dolci P, Alessandria V, Rantsiou K, Rolle L, Zeppa G, Cocolin L. 2008. Microbial dynamics of Castelmagno PDO, a traditional Italian cheese, with a focus on lactic acid bacteria ecology. Int. J. Food Microbiol. 122: 302-311.
12. Wouters JTM, Ayad EHE, Hugenholtz J, Smit G. 2002. Microbes from raw milk for fermented dairy products. Int. Dairy J. 12:91-109.
13. Samelis J, Kakouri A, Pappa EC, Matijasić BB, Georgalaki MD, Tsakalidou E, Rogelj A. 2010. Microbial stability and safety of traditional Greek Graviera cheese: characterization of the lactic acid bacterial flora and culture-independent detection of bacteriocin genes in the ripened cheeses and their microbial consortia. J. Food Prot. 73:1294 -1303.
14. Roberts RF, Zottola EA, McKay LL. 1992. Use of a nisin-producing starter culture suitable for Cheddar cheese manufacture. J. Dairy Sci. 75: 2353-2363.
15. De Vuyst L. 1994. Nisin production variability between natural Lactococcus lactis subsp. lactis strains. Biotechnol. Lett. 16:287-292.
16. Rodriguez E, Gonzalez B, Gaya P, Nunez M, Medina M. 2000. Diversity of bacteriocins produced by lactic acid bacteria isolated from raw milk. Int. Dairy J. 10:7-15.
17. Galvez A, Lopez RL, Abriouel H, Valdivia E, Ben Omar N. 2008. Application of bacteriocins in the control of foodborne pathogenic and spoilage bacteria. Crit. Rev. Biotechnol. 28:125-152.
18. Delves-Broughton J, Blackburn P, Evans RJ, Hugenholtz J. 1996. Applications of the bacteriocin nisin. Antonie Van Leeuwenhoek 69:193- 202.
19. Samelis J, Kakouri A, Rogga KJ, Savvaidis IN, Kontoninas MG. 2003. Nisin treatments to control Listeria monocytogenes post-processing contamination on Anthotyros, a traditional Greek whey cheese, stored at 4oC in vacuum packages. Food Microbiol. 20:661- 669.
20. Schleifer KH, Kraus J, Dvorak C, Kilpper-Bälz R, Collins MD, Fischer W. 1985. Transfer of Streptococcus lactis and related streptococci to the genus Lactococcus gen. nov. Syst. Appl. Microbiol. 6:183-195.
21. Holt JG. 1994. Gram-positive cocci, p 527-558. In Holt G, Krieg NR, Sneath PHA, Staley JT, Williams ST (ed), Bergey's manual of determinative bacteriology, 9th ed. Williams & Wilkins, Baltimore, MD.
22. Jarvis AW, Jarvis BDW. 1981. Deoxyribonucleic acid homology among lactic streptococci. Appl. Environ. Microbiol. 41:77- 83.
23. Godon JJ, Delorme C, Ehrlich SD, Renault P. 1992. Divergence of genomic sequences between Lactococcus lactis subsp. lactis and Lactococcus lactis subsp. cremoris. Appl. Environ. Microbiol. 58:4045- 4047.
24. Corroler D, Desmasures N, Gueguen M. 1999. Correlation between polymerase chain reaction analysis of the histidine biosynthesis operon, randomly amplified polymorphic DNA analysis and phenotypic characterization of dairy Lactococcus isolates. Appl. Microbiol. Biotechnol. 51: 91-99.
25. Kelly WJ, Ward LJH, Leahy SC. 2010. Chromosomal diversity in Lactococcus lactis and the origin of dairy starter cultures. Genome Biol. Evol. 2:729 -744.
26. Salama M, Sandine W, Giovannoni S. 1991. Development and application of oligonucleotide probes for identification of Lactococcus lactis subsp. cremoris. Appl. Environ. Microbiol. 57:1313-1318.
27. Nomura M, Kobayashi M, Narita T, Kimoto-Nira H, Okamoto T. 2006. Phenotypic and molecular characterization of Lactococcus lactis from milk and plants. J. Appl. Microbiol. 101:396-405.
28. Pu ZY, Dobos M, Limsowtin GKY, Powell IB. 2002. Integrated polymerase chain reaction-based procedures for the detection and identification of species and subspecies of the gram-positive bacterial genus Lactococcus. J. Appl. Microbiol. 93:353-361.
29. Elliott JA, Collins MD, Pigott NE, Facklam RR. 1991. Differentiation of Lactococcus lactis and Lactococcus garvieae from humans by comparison of whole-cell protein patterns. J. Clin. Microbiol. 29:2731-2734.
30. Pot B, Devriese LA, Ursi D, Vandamme P, Haesebrouck F, Kersters K. 1996. Phenotypic identification and differentiation of Lactococcus strains isolated from animals. Syst. Appl. Microbiol. 19:213-222.
31. Buist G, Kok J, Leenhouts KJ, Dabrowska M, Venema G, Haandrikman AJ. 1995. Molecular cloning and nucleotide sequence of the gene encoding the major peptidoglycan hydrolase of Lactococcus lactis, a muramidase needed for cell separation. J. Bacteriol. 177:1554 -1563.
32. Beimfohr C, Ludwig W, Schleifer KH. 1997. Rapid genotypic differentiation of Lactococcus lactis subspecies and biovar. Syst. Appl. Microbiol. 20:216 -221.
33. Urbach E, Daniels B, Salama MS, Sandine WE, Giovannoni SJ. 1997. The ldh phylogeny for environmental isolates of Lactococcus lactis is consistent with rRNA genotypes but not with phenotypes. Appl. Environ. Microbiol. 63:694 -702.
34. Garde S, Babin M, Gaya P, Nunez M, Medina M. 1999. PCR amplification of the gene acmA differentiates Lactococcus lactis subsp. lactis and L. lactis subsp. cremoris. Appl. Environ. Microbiol. 65:5151-5153.
35. Samelis J, Lianou A, Kakouri A, Delbès C, Rogelj I, Bogovic-Matijasić B, Montel MC. 2009. Changes in the microbial composition of raw milk induced by thermization treatments applied prior to traditional Greek hard cheese processing. J. Food Prot. 72:783-790.
36. Trmčić A, Monnet C, Rogelj I, Bogovič Matijašić B. 2011. Expression of nisin genes in cheese-a quantitative real-time polymerase chain reaction approach. J. Dairy Sci. 94:77- 85.
37. Trmčić A, Samelis J, Monnet C, Rogelj I, Matijašic BB. 2011. Complete nisin A gene cluster from Lactococcus lactis M78 (HM219853): obtaining the nucleic acid sequence and comparing it to other published nisin sequences. Genes Genomics 33:217-221.
38. Samelis J, Giannou E, Matijašic BB, Rogelj I. 2009. Fate of Staphylococcus aureus in traditional Greek Graviera cheese manufactured with or without Lactococcus lactis M104, a nisin-producing raw milk isolate. Abstr. EFFoST 2009 Conf. New Chall. Food Preserv., Budapest, Hungary, abstr P-329, p P298.
39. Kakouri A, Lianou A, Samelis J. 2012. Antilisterial activity of wild, novel nisin-producing Lactococcus lactis subsp. cremoris strains in synthetic culture media and different dairy foods. Abstr. 23rd Intl. ICFMH Symp. (FoodMicro 2012), Istanbul, Turkey, abstr P-573, p 761.
40. Ayad EHE, Verheul A, Wouters JTM, Smit G. 2002. Antimicrobialproducing wild lactococci isolated from artisanal and non-dairy origins. Int. Dairy J. 12:145-150.
41. Bravo D, Rodriguez E, Medina M. 2009. Nisin and lacticin 481 coproduction by Lactococcus lactis strains isolated from raw ewes' milk. J. Dairy Sci. 92:4805- 4811.
42. Alegría A, Delgado S, Roces C, Lopez B, Mayo B. 2010. Bacteriocins produced by wild Lactococcus lactis strains isolated from traditional, starter-free cheeses made of raw milk. Int. J. Food Microbiol. 143:61- 66.
43. Perin LM, Moraes PM, Vicosa GN, Junior AS, Nero LA. 2012. Identification of bacteriocinogenic Lactococcus isolates from raw milk and cheese capable of producing nisin A and nisin Z. Int. Dairy J. 25:46 -51.
44. Dal Bello B, Rantsiou K, Bellio A, Zeppa G, Ambrosoli R, Civera T, Cocolin L. 2010. Microbial ecology of artisanal products from North West of Italy and antimicrobial activity of the autochthonous populations. LWT-Food Sci. Technol. 43:1151-1159.
45. Dal Bello B, Cocolin L, Zeppa G, Field D, Cotter PD, Hill C. 2012. Technological characterization of bacteriocin producing Lactococcus lactis strains employed to control Listeria monocytogenes in cottage cheese. Int. J. Food Microbiol. 153:58-65.
46. Versalovic J, Koeuth T, Lupski JR. 1991. Distribution of repetitive DNAsequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res. 19:6823- 6831.
47. Rossetti L, Giraffa G. 2005. Rapid identification of dairy lactic acid bacteria by M13-generated, RAPD-PCR fingerprint databases. J. Microbiol. Methods 63:135-144.
48. Samelis J, Roller S, Metaxopoulos J. 1994. Sakacin B, a bacteriocin produced by Lactobacillus sake isolated from Greek dry fermented sausages. J. Appl. Bacteriol. 76:475- 486.
49. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248 -254.
50. Parapouli M, Fragkos-Livanios L, Samiotaki M, Koukkou AI, Perisynakis A, Hatziloukas E, Panagiotou G, Drainas C. 2010. Comparative proteomic analysis of alcoholic fermentation employing a new environmental strain of Saccharomyces cerevisiae. Proc. Biochem. 45:1094 -1102.
51. Hanahan D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
52. Sambrook J, Russell D. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
53. Altschul SF, Madden TL, Schäver AA, Zhang J, Zhang Z, Miller W, Lipman D. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389 -3402.
54. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596 -1599.
55. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673- 4680.
56. Fallico V, McAuliffe O, Fitzgerald GF, Ross RP. 2011. Plasmids of raw milk cheese isolate Lactococcus lactis subsp. lactis biovar diacetylactis DPC3901 suggest a plant-based origin for the strain. Appl. Environ. Microbiol. 77:6451- 6462.
57. Prodelalová J, Spanová A, Rittich B. 2005. Application of PCR, rep-PCR and RAPD techniques for typing of Lactococcus lactis strains. Folia Microbiol. (Praha) 50:150 -154.