Dynamics of bacterial communities during the ripening process of different Croatian cheese types derived from raw ewe's milk cheeses

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Fuka, Mirna Mrkonjić ^a,b   Wallisch, Stefanie ^b   Engel, Marion ^b   Welzl, Gerhard ^b   Havranek, Jasmina ^a   Schloter, Michael ^b  

^a UNIVERSITY OF ZAGREB   (Croatia)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

AEROCOCCUS; AMPLICON; ARTICLE; BACTERIUM IDENTIFICATION; BIFIDOBACTERIUM; BREVIBACTERIUM; CHEESE RIPENING; CLOSTRIDIUM; COMMUNITY DYNAMICS; COMMUNITY STRUCTURE; CORYNEBACTERIUM; CROATIA; ENTEROBACTERIACEAE; ENTEROCOCCUS; ESCHERICHIA COLI; EWE; GENE SEQUENCE; GENETIC HETEROGENEITY; HAFNIA; JANTHINOBACTERIUM; KOSMOTOGA; LACTIC ACID BACTERIUM; LACTOBACILLUS; LACTOCOCCUS; LEUCONOSTOC; MACROCOCCUS; MANNHEIMIA; MEGASPHAERA; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; NONHUMAN; PEDIOCOCCUS; PETROTOGA; PHYLOGENY; POPULATION ABUNDANCE; PSEUDOMONAS; RNA FINGERPRINTING; RNA GENE; SALMONELLA; SEQUENCE ALIGNMENT; STAPHYLOCOCCACEAE; STAPHYLOCOCCUS; STAPHYLOCOCCUS SAPROPHYTICUS; STREPTOCOCCUS; THERMOANEROBACTERIUM; VAGOCOCCUS; WEISSELLA; ANIMAL; BACTERIA; BACTERIAL GENE; CHEESE; DNA SEQUENCE; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; MICROBIOLOGY; MICROFLORA; MILK; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SHEEP;

ANIMALS; BACTERIA; BASE SEQUENCE; CHEESE; CROATIA; FEMALE; GENES, BACTERIAL; HUMANS; MICROBIOTA; MILK; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SHEEP;

EID: 84894241582     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080734     Document Type: Article

References (62)

1. Grappin R, Beuvier E (1997) Possible implications of milk pasteurization on the manufacture and sensory quality of ripened cheese. Int Dairy J 7: 751-761 (Pubitemid 28320629)
2. Leroy F, De Vuyst L (2004) Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci Technol 15: 67-78 (Pubitemid 38192839)
3. Peláez C, Requena T (2005) Exploiting the potential of bacteria in the cheese ecosystem. Int Dairy J 15: 831-844 (Pubitemid 40743081)
4. Beresford TP, Fitzsimons NA, Brennan NL, Cogan TM (2001) Recent Advances in Cheese Microbiology. Int Dairy J 11: 259-274 (Pubitemid 32752167)
5. Temmerman R, Huys G, Swings J (2004) Identification of lactic acid bacteria: culture-dependent and culture-independent methods. Trends Food Sci Technol 15: 348-359 (Pubitemid 38583550)
6. O'Sullivan DJ, Giblin L, McSweeney PLH, Sheehan JJ, Cotter PD (2013) Nucleic acid-based approaches to investigate microbial-related cheese quality defects. Front Microbiol 4: 1. doi: 10.3389/fmicb.2013.00001
7. Ndoye B, Rasolofo EA, Lapointe G, Roy D (2011) A review of the molecular approaches to investigate the diversity and activity of cheese microbiota. Dairy Sci Technol 91: 495-524
8. Giannino ML, Marzotto M, Dellaglio F, Feligini M (2009) Study of microbial diversity in raw milk and fresh curd used for Fontina cheese production by culture independent methods. Int J Food Microbiol 130: 188-195
9. Pogačić T, Kelava N, Zamberlin Š, Dolenčić-Špehar I, Samaržija D (2010) Methods for Culture-Independent Identification of Lactic Acid Bacteria in Dairy Products. Food Technol Biotech 48: 3-10
10. Caridi A, Micari P, Caparra P, Cufari A, Sarullo V (2003) Ripening and seasonal changes in microbial groups and in physico-chemical properties of the ewe's cheese Pecorino del Poro. Int Dairy J 13: 191-200 (Pubitemid 36290093)
11. Zengler K (2009) Central role of the cell in microbial ecology. Microbiol Mol Biol Rev 73: 712-729
12. Ampe F, Omar NB, Moizan C, Wacher C, Guyot JP (1999) Polyphasic study of the special distribution of microorganisms in mexican pozol, a fermented maize dough, demonstrates the need for cultivation-independent methods to investigate traditional fermentation Appl Environ Microbiol 65: 5464-5473 (Pubitemid 129520638)
13. Juste A, Thomma B, Lievens B (2008) Recent advances in molecular techniques to study microbial communities in food-associated matrices and processes. Food Microbiol 25: 745-761
14. Carraro L, Maifreni M, Bartolomeoli I, Martino ME, Novelli E, et al. (2011) Comparison of culture-dependent and -independent methods for bacterial community monitoring during Montasio cheese manufacturing. Res Microbiol 162: 231-239
15. El-Baradei G, Delacroix-Buchet AS, Ogier JC (2008) Bacterial biodiversity of traditional Zabady fermented milk. Int J Food Microbiol 121: 295-301
16. Fuka MM, Radl V, Bogovič Matijašić B, Schloter M (2012) Evaluation of a molecular fingerprinting method based on the diversity of the ribosomal 16S rRNA gene to describe the dynamic of bacterial communities in Istrian cheese. Afr J Biotechnol 101: 16650-16654
17. Masoud W, Vogensen FK, Lillevang S, AbuAl-Soud W, Sorensen SJ et al. (2011) The fate of indigenous microbiota, starter cultures, Escherichia coli, Listeria innocua and Staphylococcus aureus in Danish raw milk and cheeses determined by pyrosequencing and quantitative real time (qRT)-PCR. Int J Food Microbiol 153: 192-202
18. Cardenas E, Tiedje JM (2008) New tools for discovering and characterizing microbial diversity. Curr Opin Biotechnol 19: 544-549
19. Roh SW, Abell GCJ, Kim KH, Nam YD, Bae JW (2010) Comparing microarrays and next-generation sequencing technologies for microbial ecology research. Trends Biotechnol 28: 291-299
20. Quigley L, O'Sullivan O, Beresford TP, Ross RP, Fitzgerald GF et al (2012) High- throughput sequencing detects sub- populations of bacteria not previously associated with artisanal cheeses. Appl Environ Microbiol 78: 5717-5723
21. Alegría A, Szczesny P, Mayo B, Bardowski J, Kowalczyk M (2012) Biodiversity in Oscypek, a traditional Polish cheese, determined by culture-dependent and -independent approaches. Appl Environ Microbiol 78: 1890-1898
22. Roesch LF, Fulthorpe RR, Riva A, Casella G, Hadwin AK, et al. (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1: 283-290 (Pubitemid 47227850)
23. Fuka MM, Engel M, Skelin A, Redzepovic S, Schloter M (2010) Bacterial Communities associated with the production of artisanal Istrian cheese. Int J Food Microbiol 142: 19-24
24. Mikulec N, Kalit S, Havranek J, Antunac N, Horvat I, et al. (2008) Characteristics of traditional Croatian ewe's cheese from the island Krk. Int J Dairy Technol 61: 126-132 (Pubitemid 351506412)
25. Kitonić T, Tratnik Lj (1998) Influence of cow milk in mixture with sheep milk on the quality of cheese produced with the Paski sir cheesemaking technology. Milchwissenschaft 53: 20-22
26. Blackall LL, Seviour EM, Cunningham MA, Seviour RJ, Hugenholtz P (1994) "Microthrix parvicella" is a novel deep branching member of the actinomycetes subphylum. Syst Appl Microbiol 17: 513-518
27. Juretschko S, Timmermann G, Schmid MC, Schleifer KH, Pommerening- Röser A, et al. (1998) Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Appl Environ Microbiol 64: 3042-3051 (Pubitemid 28363182)
28. Collins RE, Rocap G (2007) REPK: an analytical web server to select restriction endonucleases for terminal restriction fragment length polymorphism analysis. Nucleic Acids Res 35 W58-W62. doi: 10.1093/nar/gkm384
29. Culman SW, Bukowski R, Gauch HG, Cadillo-Quiroz H, Buckley DH (2009) T-REX: Software for the Processing and Analysis of T-RFLP data. BMC Bioinformatics 10:171
30. Schloss PD (2009) A High-Throughput DNA Sequence Aligner for Microbial Ecology Studies. PLoS ONE 14; 4(12):e8230. doi: 10.1371/journal.pone.0008230
31. Pagani I, Liolios K, Jansson J, Chen IM, Smirnova T, et al. (2012) The Genomes OnLine Database (GOLD) v.4: status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Res. 40: 571-579
32. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261-5267 (Pubitemid 47326658)
33. Yue JC, Clayton MK (2005) A similarity measure based on species proportions. Commun Stat Theo Methods 34: 2123-2131 (Pubitemid 41605509)
34. Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Phil Trans R Soc B 345: 101-118
35. El-Baradei G, Delacroix-Buchet AS, Ogier JC (2007) Biodiversity of bacterial ecosystems in traditional Egyptian Domiati cheese. Appl Environ Microbiol 73: 1248-1255
36. Callon CF, Duthoit CD, Ferrand M, Le Frileux Y, De Cremoux R, et al. (2007) Stability of microbial communities in goat milk during a lactation year: Molecular approaches. Syst. Applied Microbiol 30: 547-560 (Pubitemid 47516566)
37. Antonsson M, Molin G, Ardö Y (2003) Lactobacillus strains isolated from Danbo cheese as adjunct cultures in a cheese model system. Int J Food Microbiol 85: 159-169 (Pubitemid 37329376)
38. Ercolini D, Frisso G, Mauriello G, Salvatore F, Coppola S (2008) Microbial diversity in natural whey cultures used for the production of Caciocavallo Silano PDO cheese. Int J Food Microbiol 124: 164-170
39. Gori K, Ryssel M, Arneborg N, Jespersen L (2013) Isolation and Identification of the Microbiota of Danish Farmhouse and Industrially Produced Surface-Ripened Cheeses. Microb Ecol 65: 602-615
40. Di Cagno R, Surico RF, Siragusa S, De Angelis M, Paradiso A, et al. (2008) Selection and use of autochthonous mixed starter for lactic acid fermentation of carrots, French beans or marrows. Int J Food Microbiol 127, 220-228
41. McSweeney PLH (2004) Biochemistry of cheese ripening. Int J Dairy Technol 57: 127-144
42. Skelin A, Mrkonjić Fuka M, Čanžek Majhenič A, Redžepović S, Samaržija D et al. (2012) Phenotypic and genotypic characterization of indigenous Lactobacillus community from traditional Istrian ewe's cheese. Food Technol Biotech 50: 362-370
43. Randazzo CL, Vaughan EE, Caggia C (2006) Artisanal and experimental Pecorino Siciliano cheese: microbial dynamics during manufacture assessed by culturing and PCR-DGGE analyses. Int J Food Microbiol 109: 1-8
44. Delves-Broughton J, Blackburn P, Evans RJ, Hugenholtz J (1996) Applications of the bacteriocin nisin. Antonie Van Leeuwenhoek 69: 193-202
45. Franz CMAP, Holzapfel WH, Stiles ME (1999) Enterococci at the crossroads of food safety. Int J Food Microbiol 47: 1-24
46. Pitkälä A, Koort J, Björkroth J (2008) Identification and antimicrobial resistance of Streptococcus uberis and Streptococcus parauberis isolated from bovine milk samples. J Dairy Sci 91: 4075-4081
47. Giannino ML, Marzotto M, Dellaglio F, Feligini M (2009) Study of microbial diversity in raw milk and fresh curd used for Fontina cheese production by culture independent methods. Int J Food Microbiol 130: 188-195
48. Marino M, Maifreni M, Rondinini G (2003) Microbiological characterization of artisanal Montasio cheese: analysis of its indigenous lactic acid bacteria. FEMS Microbiol Lett 229: 133-140 (Pubitemid 37505008)
49. Zago M, Bonvini B, Martín-Platero AM, Mucchetti G, Carminati D, et al. (2007) Characterisation of Escherichia coli isolated from raw milk cheeses, Ann Microbiol 57:49-54 (Pubitemid 46556267)
50. Kloos WE, Ballard DN, George CG, Webster A, Hubner RJ, et al. (1998) Delimiting the genus Staphylococcus through description of Macrococcus caseolyticus gen. nov., comb. nov. and Macrococcus equipercicus sp. nov., and Macrococcus bovicus sp. nov. and Macrococcus carouselicus sp. nov. Int J Syst Bacteriol 48: 859-877 (Pubitemid 28394667)
51. Irlinger F, Yung SA, Sarthou AS, Delbes-Paus C. Montel MC, et al. (2012) Ecological and aromatic impact of two Gram-negative bacteria (Psychrobacter celer and Hafnia alvei) inoculated as part of the whole microbial community of an experimental smear soft cheese. Int J Food Microbiol 153: 332-8
52. Magdić V, Kalit S, Fuka MM, Skelin A, Samaržija D, Redžepović S, et al. (2013) A survey on hygienic and physicochemical properties of Istrian cheese. Mljekarstvo 63: 55-63
53. Donnelly CW (2004) Growth and survival of microbial pathogens in cheese. In: Fox PF, McSweeney PLH, Cogan TM, Guinee TP, editors. Cheese: Chemistry, Physics and Microbiology, General Aspects. Elsevier Academic Press. pp. 541-557
54. Nero LA, de Mattos MR, de Aguiar Ferreira Barros M, Ortolani MBT, Beloti V, et al. (2008) Listeria monocytogenes and Salmonella spp. in raw milk produced in Brazil: occurrence and interference of indigenous microbiota in their isolation and development. Zoonoses Public Health 55: 299-305 (Pubitemid 352000393)
55. Moroni P, Pisoni G, Antonini M, Ruffo G, Carli S, et al. (2005) Subclinical mastitis and antimicrobial sus- ceptibility of Staphylococcus caprae and Staphylococcus epidermidis isolated from two Italian goat herds. J Dairy Sci 88:1694-1704 (Pubitemid 41431218)
56. Hovelius B, Mardh PA (1984) Staphylococcus saprophyticus as a common cause of urinary tract infections. Rev Infect Dis 6: 328-337
57. Albenzio M, Corbo MR, Rehman US, Fox PF, de Angelis M, et al. (2001) Microbiological and biochemical characteristics of Canestrato Pugliese cheese made from raw milk, pasteurized milk or by heating the curd in hot whey. Int J Food Microbiol 67: 35-48 (Pubitemid 32624370)
58. Johnson EA, Nelson JH, Johnson M (1990) Microbiological safety of cheese made from heat-treated milk. Part II. Microbiology. J Food Prot 53: 519-540
59. Glass K, Ellin Doyle M (2005) Fri briefings: Safety of Processed Cheese - A Review of the Scientific Literature, Food Research Institute, University of Wisconsin-Madison. Available at: http://fri.wisc.edu/docs/pdf/ProcCheese.pdf
60. Ishikawa M, Kodama K, Yasuda H, Okamoto-Kainuma A, Koizumi K, et al. (2007) Presence of halophilic and alkaliphilic lactic acid bacteria in various cheeses. Lett Appl Microbiol 44: 308-313
61. Yumoto I, Hirota K, Yoshimune K (2011) Environmental distribution and taxonomic diversity of alkaliphiles. In: Horikoshi K, Antranikian G, Bull AT, Robb FT, Stetter KO, editors. Extremophiles Handbook. Springer. pp. 65-67
62. Ishikawa M, Yamasato K, Kodama K, Yasuda H, Matsuyama M, et al. (2013) Alkalibacterium gilvum sp. nov., slightly halophilic and alkaliphilic lactic acid bacterium isolated from soft- and semi-hard cheeses. Int J Syst Evol Microbiol 63: 1471-1478