Cultivation-independent analysis of microbial communities on Austrian raw milk hard cheese rinds

International Journal of Food Microbiology

Volumn 180, Issue , 2014, Pages 88-97

  Schornsteiner, Elisa ^a   Mann, Evelyne ^a   Bereuter, Othmar ^b   Wagner, Martin ^a   Schmitz Esser, Stephan ^a  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^b Landwirtschaftskammer Vorarlberg   (Austria)

Author keywords

16S rRNA cloning; 18S rRNA cloning; Cheese rind bacteria; Cheese rind yeast; Raw milk hard cheese

Indexed keywords

GENOMIC DNA; RNA 16S; RNA 18S;

ACTINOBACTERIA; ARTICLE; AUSTRIAN ARTISANAL HARD CHEESE; CHEESE; CHEESE RIPENING; DAIRY PRODUCT; DNA EXTRACTION; FOOD QUALITY; FUNGAL COMMUNITY; GENE AMPLIFICATION; GENE LIBRARY; GENE SEQUENCE; HALOMONAS; MICROBIAL COMMUNITY; MILK; MOLECULAR CLONING; NONHUMAN; PHYLOGENETIC TREE; PROTEOBACTERIA; SCOPULARIOPSIS BREVICAULIS; TAXONOMIC IDENTIFICATION;

16S RRNA CLONING; 18S RRNA CLONING; CHEESE RIND BACTERIA; CHEESE RIND YEAST; RAW MILK HARD CHEESE;

ANIMALS; AUSTRIA; BACTERIA; BIODIVERSITY; CHEESE; FUNGI; MICROBIOTA; MILK; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, RIBOSOMAL, 16S; RNA, RIBOSOMAL, 18S;

EID: 84899849757     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2014.04.010     Document Type: Article

References (57)

1. Alegria A., Szczesny P., Mayo B., Bardowski J., Kowalczyka M. Biodiversity in Oscypek, a traditional Polish cheese, determined by culture-dependent and -independent approaches. Appl. Environ. Microbiol. 2012, 78:1890-1898.
2. Bockelmann W., Willems K.P., Neve H., Heller K.H. Cultures for the ripening of smear cheeses. Int. Dairy J. 2005, 15:719-732.
3. Brennan N.M., Ward A.C., Beresford T.P., Fox P.F., Goodfellow M., Cogan T.M. Biodiversity of the bacterial flora on the surface of a smear cheese. Appl. Environ. Microbiol. 2002, 68:820-830.
4. Camacho C., Coulouris G., Avagyan V., Ma N., Papadopoulos J., Bealer K., Madden T.L. BLAST+: architecture and applications. BMC Bioinforma. 2009, 10:421.
5. Carnio M.C., Holtzel A., Rudolf M., Henle T., Jung G., Scherer S. The macrocyclic peptide antibiotic micrococcin P(1) is secreted by the food-borne bacterium Staphylococcus equorum WS 2733 and inhibits Listeria monocytogenes on soft cheese. Appl. Environ. Microbiol. 2000, 66:2378-2384.
6. Chao A. Nonparametric-estimation of the number of classes in a population. Scand. J. Stat. 1984, 11:265-270.
7. Cole J.R., Wang Q., Fish J.A., Chai B., McGarrell D.M., Sun Y., Brown C.T., Porras-Alfaro A., Kuske C.R., Tiedje J.M. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 2014, 42:D633-D642.
8. Corsetti A., Rossi J., Gobbetti M. Interactions between yeasts and bacteria in the smear surface-ripened cheeses. Int. J. Food Microbiol. 2001, 69:1-10.
9. Coton M., Delbes-Paus C., Irlinger F., Desmasures N., Le Fleche A., Stahl V., Montel M.C., Coton E. Diversity and assessment of potential risk factors of Gram-negative isolates associated with French cheeses. Food Microbiol. 2012, 29:88-98.
10. Deetae P., Spinnler H.E., Bonnarme P., Helinck S. Growth and aroma contribution of Microbacterium foliorum, Proteus vulgaris and Psychrobacter sp. during ripening in a cheese model medium. Appl. Microbiol. Biotechnol. 2009, 82:169-177.
11. Delbes C., Ali-Mandjee L., Montel M.C. Monitoring bacterial communities in raw milk and cheese by culture-dependent and -independent 16S rRNA gene-based analyses. Appl. Environ. Microbiol. 2007, 73:1882-1891.
12. Dolci P., Barmaz A., Zenato S., Pramotton R., Alessandria V., Cocolin L., Rantsiou K., Ambrosoli R. Maturing dynamics of surface microflora in Fontina PDO cheese studied by culture-dependent and -independent methods. J. Appl. Microbiol. 2009, 106:278-287.
13. Dolci P., Zenato S., Pramotton R., Barmaz A., Alessandria V., Rantsiou K., Cocolin L. Cheese surface microbiota complexity: RT-PCR-DGGE, a tool for a detailed picture?. Int. J. Food Microbiol. 2013, 162:8-12.
14. Edgcomb V., Orsi W., Bunge J., Jeon S., Christen R., Leslin C., Holder M., Taylor G.T., Suarez P., Varela R., Epstein S. Protistan microbial observatory in the Cariaco Basin, Caribbean. I. Pyrosequencing vs Sanger insights into species richness. ISME J. 2011, 5:1344-1356.
15. Eliskases-Lechner F., Ginzinger W. The bacterial flora of surface-ripened cheeses with special regard to coryneforms. Lait 1995, 75:571-583.
16. Feurer C., Irlinger F., Spinnler H.E., Glaser P., Vallaeys T. Assessment of the rind microbial diversity in a farmhouse-produced vs a pasteurized industrially produced soft red-smear cheese using both cultivation and rDNA-based methods. J. Appl. Microbiol. 2004, 97:546-556.
17. Feurer C., Vallaeys T., Corrieu G., Irlinger F. Does smearing inoculum reflect the bacterial composition of the smear at the end of the ripening of a French soft, red-smear cheese?. J. Dairy Sci. 2004, 87:3189-3197.
18. Gavrish E.Y., Krauzova V.I., Potekhina N.V., Karasev S.G., Plotnikova E.G., Altyntseva O.V., Korosteleva L.A., Evtushenko L.I. Three new species of brevibacteria, Brevibacterium antiquum sp nov., Brevibacterium aurantiacum sp nov., and Brevibacterium permense sp nov. Microbiology 2004, 73:176-183.
19. Gibello A., Vela A.I., Martin M., Barra-Caracciolo A., Grenni P., Fernandez-Garayzabal J.F. Reclassification of the members of the genus Tetrathiobacter Ghosh et al. 2005 to the genus Advenella Coenye et al. 2005. Int. J. Syst. Evol. Microbiol. 2009, 59:1914-1918.
20. Goerges S., Mounier J., Rea M.C., Gelsomino R., Heise V., Beduhn R., Cogan T.M., Vancanneyt M., Scherer S. Commercial ripening starter microorganisms inoculated into cheese milk do not successfully establish themselves in the resident microbial ripening consortia of a South German red smear cheese. Appl. Environ. Microbiol. 2008, 74:2210-2217.
21. Gori K., Ryssel M., Arneborg N., Jespersen L. Isolation and identification of the microbiota of Danish farmhouse and industrially produced surface-ripened cheeses. Microb. Ecol. 2013, 65:602-615.
22. Hantsis-Zacharov E., Halpern M. Culturable psychrotrophic bacterial communities in raw milk and their proteolytic and lipolytic traits. Appl. Environ. Microbiol. 2007, 73:7162-7168.
23. Irlinger F., Morvan A., El Solh N., Bergere J.L. Taxonomic characterization of coagulase-negative Stapyhlococci in ripening flora from traditional French cheeses. System. Appl. Microbiol. 1997, 20:319-328.
24. Irlinger F., Mounier J. Microbial interactions in cheese: implications for cheese quality and safety. Curr. Opin. Biotechnol. 2009, 20:142-148.
25. Irlinger F., Yung S.A.Y.I., Sarthou A.S., Delbes-Paus C., Montel M.C., Coton E., Coton M., Helinck S. 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. 2012, 153:332-338.
26. Ishikawa M., Kodama K., Yasuda H., Okamoto-Kainuma A., Koizumi K., Yamasato K. Presence of halophilic and alkaliphilic lactic acid bacteria in various cheeses. Lett. Appl. Microbiol. 2007, 44:308-313.
27. Ishikawa M., Yamasato K., Kodama K., Yasuda H., Matsuyama M., Okamoto-Kainuma A., Koizumi Y. Alkalibacterium gilvum sp. nov., slightly halophilic and alkaliphilic lactic acid bacterium isolated from soft and semi-hard cheeses. Int. J. Syst. Evol. Microbiol. 2013, 63:1471-1478.
28. Jany J.L., Barbier G. Culture-independent methods for identifying microbial communities in cheese. Food Microbiol. 2008, 25:839-848.
29. Joachimiak M.P., Weisman J.L., May B. JColorGrid: software for the visualization of biological measurements. BMC Bioinforma. 2006, 7:225.
30. Juretschko S., Timmermann G., Schmid M., Schleifer K.H., Pommerening-Roser A., Koops H.P., Wagner M. Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Appl. Environ. Microbiol. 1998, 64:3042-3051.
31. Lane D.J. 16S/23S rRNA sequencing. Nucleic Acid Techniques in Bacterial Systematics 1991, 115-147. Wiley, New York.
32. Lavoie K., Touchette M., St-Gelais D., Labrie S. Characterization of the fungal microflora in raw milk and specialty cheeses of the province of Quebec. Dairy Sci. Technol. 2012, 92:455-468.
33. Lopandic K., Zelger S., Banszky L.K., Eliskases-Lechner F., Prillinger H. Identification of yeasts associated with milk products using traditional and molecular techniques. Food Microbiol. 2006, 23:341-350.
34. Ludwig W., Strunk O., Westram R., Richter L., Meier H., Yadhukumar, Buchner A., Lai T., Steppi S., Jobb G., Forster W., Brettske I., Gerber S., Ginhart A.W., Gross O., Grumann S., Hermann S., Jost R., Konig A., Liss T., Lussmann R., May M., Nonhoff B., Reichel B., Strehlow R., Stamatakis A., Stuckmann N., Vilbig A., Lenke M., Ludwig T., Bode A., Schleifer K.H. ARB: a software environment for sequence data. Nucleic Acids Res. 2004, 32:1363-1371.
35. Maoz A., Mayr R., Scherer S. Temporal stability and biodiversity of two complex antilisterial cheese-ripening microbial consortia. Appl. Environ. Microbiol. 2003, 69:4012-4018.
36. Masoud W., Takamiya M., Vogensen F.K., Lillevang S., Abu Al-Soud W., Sorensen S.J., Jakobsen M. Characterization of bacterial populations in Danish raw milk cheeses made with different starter cultures by denaturating gradient gel electrophoresis and pyrosequencing. Int. Dairy J. 2011, 21:142-148.
37. Melnyk J.P., Smith A., Scott-Dupree C., Marcone M.F., Hill A. Identification of cheese mite species inoculated on Mimolette and Milbenkase cheese through cryogenic scanning electron microscopy. J. Dairy Sci. 2010, 93:3461-3468.
38. Montel M.C., Buchin S., Mallet A., Delbes-Paus C., Vuitton D.A., Desmasures N., Berthier F. Traditional cheeses: rich and diverse microbiota with associated benefits. Int. J. Food Microbiol. 2014, 177C:136-154.
39. Mounier J., Gelsomino R., Goerges S., Vancanneyt M., Vandemeulebroecke K., Hoste B., Scherer S., Swings J., Fitzgerald G.F., Cogan T.M. Surface microflora of four smear-ripened cheeses. Appl. Environ. Microbiol. 2005, 71:6489-6500.
40. Mounier J., Monnet C., Jacques N., Antoinette A., Irlinger F. Assessment of the microbial diversity at the surface of Livarot cheese using culture-dependent and independent approaches. Int. J. Food Microbiol. 2009, 133:31-37.
41. Ndoye B., Rasolofo E.A., LaPointe G., Roy D. A review of the molecular approaches to investigate the diversity and activity of cheese microbiota. Dairy Sci. Technol. 2011, 91:495-524.
42. O'Sullivan D.J., Giblin L., McSweeney P.L., Sheehan J.J., Cotter P.D. Nucleic acid-based approaches to investigate microbial-related cheese quality defects. Front. Microbiol. 2013, 4:1.
43. Prillinger H., Molnar O., Eliskases-Lechner F., Lopandic K. Phenotypic and genotypic identification of yeasts from cheese. Antonie Van Leeuwenhoek 1999, 75:267-283.
44. Pruesse E., Quast C., Knittel K., Fuchs B.M., Ludwig W., Peplies J., Glockner F.O. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007, 35:7188-7196.
45. Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., Peplies J., Glockner F.O. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013, 41:D590-D596.
46. Quigley L., O'Sullivan O., Beresford T.P., Ross R.P., Fitzgerald G.F., Cotter P.D. Molecular approaches to analysing the microbial composition of raw milk and raw milk cheese. Int. J. Food Microbiol. 2011, 150:81-94.
47. Quigley L., O'Sullivan O., Beresford T.P., Ross R.P., Fitzgerald G.F., Cotter P.D. High-throughput sequencing for detection of subpopulations of bacteria not previously associated with artisanal cheeses. Appl. Environ. Microbiol. 2012, 78:5717-5723.
48. Quigley L., O'Sullivan O., Stanton C., Beresford T.P., Ross R.P., Fitzgerald G.F., Cotter P.D. The complex microbiota of raw milk. FEMS Microbiol. Rev. 2013, 37:664-698.
49. Rattray F.P., Fox P.F. Aspects of enzymology and biochemical properties of Brevibacterium linens relevant to cheese ripening: a review. J. Dairy Sci. 1999, 82:891-909.
50. Rea M.C., Gorges S., Gelsomino R., Brennan N.M., Mounier J., Vancanneyt M., Scherer S., Swings J., Cogan T.M. Stability of the biodiversity of the surface consortia of Gubbeen, a red-smear cheese. J. Dairy Sci. 2007, 90:2200-2210.
51. Ropars J., Cruaud C., Lacoste S., Dupont J. A taxonomic and ecological overview of cheese fungi. Int. J. Food Microbiol. 2012, 155:199-210.
52. Roth E., Miescher Schwenninger S., Hasler M., Eugster-Meier E., Lacroix C. Population dynamics of two antilisterial cheese surface consortia revealed by temporal temperature gradient gel electrophoresis. BMC Microbiol. 2010, 10:74.
53. Schloss P.D., Westcott S.L., Ryabin T., Hall J.R., Hartmann M., Hollister E.B., Lesniewski R.A., Oakley B.B., Parks D.H., Robinson C.J., Sahl J.W., Stres B., Thallinger G.G., Van Horn D.J., Weber C.F. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 2009, 75:7537-7541.
54. Schmidt V.S.J., Wenning M., Scherer S. Sphingobacterium lactis sp nov and Sphingobacterium alimentarium sp nov., isolated from raw milk and a dairy environment. Int. J. Syst. Evol. Microbiol. 2012, 62:1506-1511.
55. Shannon C.E. A mathematical theory of communication. Bell Syst. Tech. J. 1948, 27:623-656.
56. Simpson E.H. Measurement of diversity. Nature 1949, 163:688.
57. Stackebrandt E., Ebers J. Taxonomic parameters revisited: tarnished gold standards. Microbiol. Today 2006, 6-9. (November).