Temporal and spatial differences in microbial composition during the manufacture of a continental-type cheese

Applied and Environmental Microbiology

Volumn 81, Issue 7, 2015, Pages 2525-2533

  O'Sullivan, Daniel J ^a,b   Cotter, Paul D ^a,c   O'Sullivan, Orla ^a,c   Giblin, Linda ^a   McSweeney, Paul L H ^b   Sheehan, Jeremiah J ^a  

^a TEAGASC FOOD RESEARCH CENTRE   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

MICROORGANISMS; RNA;

HIGH-THROUGHPUT SEQUENCING; MICROBIAL COMMUNITIES; MICROBIAL COMMUNITY DYNAMICS; MICROBIAL COMPOSITION; MICROBIAL POPULATIONS; SPATIAL VARIATIONS; TEMPORAL AND SPATIAL; TEMPORAL AND SPATIAL DISTRIBUTION;

THROUGHPUT;

COMMUNITY STRUCTURE; MICROBIAL COMMUNITY; MILK; RNA; SPATIOTEMPORAL ANALYSIS;

BIFIDOBACTERIUM; PSEUDOALTEROMONAS; THERMUS;

BACTERIAL DNA; RIBOSOME DNA; RNA 16S;

BACTERIUM; BIOTA; CHEESE; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; FOOD HANDLING; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; SPATIOTEMPORAL ANALYSIS;

BACTERIA; BIOTA; CHEESE; DNA, BACTERIAL; DNA, RIBOSOMAL; FOOD HANDLING; MOLECULAR SEQUENCE DATA; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SPATIO-TEMPORAL ANALYSIS;

EID: 84925379678     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.04054-14     Document Type: Article

References (67)

1. Rehman S-U, McSweeney PLH, Banks JM, Brechany EY, Muir DD, Fox PF. 2000. Ripening of Cheddar cheese made from blends of raw and pasteurised milk. Int Dairy J 10:33-44. http://dx.doi.org/10.1016/S0958-6946(00)00024-8.
2. Bokulich NA, Mills DA. 2013. Facility-specific "house" microbiome drives microbial landscapes of artisan cheesemaking plants. Appl Environ Microbiol 79:5214-5223. http://dx.doi.org/10.1128/AEM.00934-13.
3. Ogier J-C, Lafarge V, Girard V, Rault A, Maladen V, Gruss A, Leveau J-Y, Delacroix-Buchet A. 2004. Molecular fingerprinting of dairy microbial ecosystems by use of temporal temperature and denaturing gradient gel electrophoresis. Appl Environ Microbiol 70:5628-5643. http://dx.doi.org/10.1128/AEM.70.9.5628-5643.2004.
4. Quigley L, McCarthy R, O'Sullivan O, Beresford TP, Fitzgerald GF, Ross RP, Stanton C, Cotter PD. 2013. The microbial content of raw and pasteurized cow milk as determined by molecular approaches. J Dairy Sci 96:4928-4937. http://dx.doi.org/10.3168/jds.2013-6688.
5. O'Sullivan DJ, Giblin L, McSweeney PL, Sheehan JJ, Cotter PD. 2013. Nucleic acid-based approaches to investigate microbial-related cheese quality defects. Front Microbiol 4:1. http://dx.doi.org/10.3389/fmicb.2013.00001.23346082.
6. Peláez C, Requena T. 2005. Exploiting the potential of bacteria in the cheese ecosystem. Int Dairy J 15:831-844. http://dx.doi.org/10.1016/j.idairyj.2004.12.001.
7. Beresford TP, Fitzsimons NA, Brennan NL, Cogan TM. 2001. Recent advances in cheese microbiology. Int Dairy J 11:259-274. http://dx.doi.org/10.1016/S0958-6946(01)00056-5.
8. Jany J-L, Barbier G. 2008. Culture-independent methods for identifying microbial communities in cheese. Food Microbiol 25:839-848. http://dx.doi.org/10.1016/j.fm.2008.06.003.
9. Cocolin L, Alessandria V, Dolci P, Gorra R, Rantsiou K. 2013. Culture independent methods to assess the diversity and dynamics of microbiota during food fermentation. Int J Food Microbiol 167:29-43. http://dx.doi.org/10.1016/j.ijfoodmicro.2013.05.008.
10. Bokulich NA, Mills DA. 2012. Next-generation approaches to the microbial ecology of food fermentations. BMB Rep 45:377-389. http://dx.doi.org/10.5483/BMBRep.2012.45.7.148.
11. Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, Arrieta JM, Herndl GJ. 2006. Microbial diversity in the deep sea and the underexplored "rare biosphere". Proc Natl Acad Sci U S A 103:12115-12120. http://dx.doi.org/10.1073/pnas.0605127103.
12. Nacke H, Thurmer A, Wollherr A, Will C, Hodac L, Herold N, Schoning I, Schrumpf M, Daniel R. 2011. Pyrosequencing-based assessment of bacterial community structure along different management types in German forest and grassland soils. PLoS One 6:e17000. http://dx.doi.org/10.1371/journal.pone.0017000.
13. Claesson MJ, O'Sullivan O, Wang Q, Nikkilä J, Marchesi JR, Smidt H, de Vos WM, Ross RP, O'Toole PW. 2009. Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine. PLoS One 4:e6669. http://dx.doi.org/10.1371/journal.pone.0006669.
14. Humblot C, Guyot J-P. 2009. Pyrosequencing of tagged 16S rRNA gene amplicons for rapid deciphering of the microbiomes of fermented foods such as pearl millet slurries. Appl Environ Microbiol 75:4354-4361. http: //dx.doi.org/10.1128/AEM.00451-09.
15. Nam Y-D, Yi S-H, Lim S-I. 2012. Bacterial diversity of cheonggukjang, a traditional Korean fermented food, analyzed by barcoded pyrosequencing. Food Control 28:135-142. http://dx.doi.org/10.1016/j.foodcont.2012.04.028.
16. Polka J, Rebecchi A, Pisacane V, Morelli L, Puglisi E. 2015. Bacterial diversity in typical Italian salami at different ripening stages as revealed by high-throughput sequencing of 16S rRNA amplicons. Food Microbiol 46:342-356. http://dx.doi.org/10.1016/j.fm.2014.08.023.
17. Marsh AJ, O'Sullivan O, Hill C, Ross RP, Cotter PD. 2013. Sequencebased analysis of the microbial composition of water kefir from multiple sources. FEMS Microbiol Lett 348:79-85. http://dx.doi.org/10.1111/1574-6968.12248.
18. Marsh AJ, O'Sullivan O, Hill C, Ross RP, Cotter PD. 2014. Sequencebased analysis of the bacterial and fungal compositions of multiple kombucha (tea fungus) samples. Food Microbiol 38:171-178. http://dx.doi.org/10.1016/j.fm.2013.09.003.
19. Jung JY, Lee SH, Kim JM, Park MS, Bae J-W, Hahn Y, Madsen EL, Jeon CO. 2011. Metagenomic analysis of kimchi, a traditional Korean fermented food. Appl Environ Microbiol 77:2264-2274. http://dx.doi.org /10.1128/AEM.02157-10.
20. Roh SW, Kim K-H, Nam Y-D, Chang H-W, Park E-J, Bae J-W. 2010. Investigation of archaeal and bacterial diversity in fermented seafood using barcoded pyrosequencing. ISME J 4:1-16. http://dx.doi.org/10.1038 /ismej.2009.83.19587773.
21. Masoud W, Vogensen FK, Lillevang S, Abu Al-Soud W, Sørensen SJ, Jakobsen M. 2012. 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. http://dx.doi.org/10.1016/j.ijfoodmicro.2011.11.014.
22. Quigley L, O'Sullivan O, Stanton C, Beresford TP, Ross RP, Fitzgerald GF, Cotter PD. 2013. The complex microbiota of raw milk. FEMS Microbiol Rev 37:664-698. http://dx.doi.org/10.1111/1574-6976.12030.
23. Aldrete-Tapia A, Escobar-Ramírez MC, Tamplin ML, Hernández-Iturriaga M. 2014. High-throughput sequencing of microbial communities in Poro cheese, an artisanal Mexican cheese. Food Microbiol 44:136-141. http://dx.doi.org/10.1016/j.fm.2014.05.022.
24. Delgado S, Rachid CTCC, Fernández E, Rychlik T, Alegría Á Peixoto RS, Mayo B. 2013. Diversity of thermophilic bacteria in raw, pasteurized and selectively-cultured milk, as assessed by culturing, PCR-DGGE and pyrosequencing. Food Microbiol 36:103-111. http://dx.doi.org/10.1016/j.fm.2013.04.015.
25. Masoud W, Takamiya M, Vogensen FK, Lillevang S, Al-Soud WA, Sørensen SJ, Jakobsen M. 2011. Characterization of bacterial populations in Danish raw milk cheeses made with different starter cultures by denaturating gradient gel electrophoresis and pyrosequencing. Int Dairy J 21: 142-148. http://dx.doi.org/10.1016/j.idairyj.2010.10.007.
26. Alegría Á 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. http://dx.doi.org/10.1128/AEM.06081-11.
27. Quigley L, O'Sullivan O, Beresford TP, Ross RP, Fitzgerald GF, Cotter PD. 2012. High-throughput sequencing for detection of subpopulations of bacteria not previously associated with artisanal cheeses. Appl Environ Microbiol 78:5717-5723. http://dx.doi.org/10.1128/AEM.00918-12.
28. Ercolini D. 2013. High-throughput sequencing and metagenomics: moving forward in the culture-independent analysis of food microbiology and ecology. Appl Environ Microbiol 79:3148-3155. http://dx.doi.org/10.1128/AEM.00256-13.
29. Fuka MM, Wallisch S, Engel M, Welzl G, Havranek J, Schloter M. 2013. Dynamics of bacterial communities during the ripening process of different Croatian cheese types derived from raw ewe's milk cheeses. PLoS One 8:e80734. http://dx.doi.org/10.1371/journal.pone.0080734.
30. Sheehan A, O'Cuinn G, FitzGerald RJ, Wilkinson MG. 2009. Distribution of microbial flora, intracellular enzymes and compositional indices throughout a 12-kg Cheddar cheese block during ripening. Int Dairy J 19:321-329. http://dx.doi.org/10.1016/j.idairyj.2008.11.008.
31. Guinee TP. 2004. Salting and the role of salt in cheese. Int J Dairy Technol 57:99-109. http://dx.doi.org/10.1111/j.1471-0307.2004.00145.x.
32. Malakar PK, Brocklehurst TF, Mackie AR, Wilson PDG, Zwietering MH, van't Riet K. 2000. Microgradients in bacterial colonies: use of fluorescence ratio imaging, a non-invasive technique. Int J Food Microbiol 56:71-80. http://dx.doi.org/10.1016/S0168-1605(00)00222-1.
33. Ercolini D, Hill PJ, Dodd CER. 2003. Development of a fluorescence in situ hybridization method for cheese using a 16S rRNA probe. J Microbiol Methods 52:267-271. http://dx.doi.org/10.1016/S0167-7012(02)00162-8.
34. Fleurot I, Aigle M, Fleurot R, Darrigo C, Hennekinne J-A, Gruss A, Borezée-Durant E, Delacroix-Buchet A. 2014. Following pathogen development and gene expression in a food ecosystem: the case of a Staphylococcus aureus isolate in cheese. Appl Environ Microbiol 80:5106-5115. http://dx.doi.org/10.1128/AEM.01042-14.
35. Monfredini L, Settanni L, Poznanski E, Cavazza A, Franciosi E. 2012. The spatial distribution of bacteria in Grana-cheese during ripening. Syst Appl Microbiol 35:54-63. http://dx.doi.org/10.1016/j.syapm.2011.07.002.
36. Fitzsimons NA, Cogan TM, Condon S, Beresford T. 2001. Spatial and temporal distribution of non-starter lactic acid bacteria in Cheddar cheese. J Appl Microbiol 90:600-608. http://dx.doi.org/10.1046/j.1365-2672.2001.01285.x.
37. Gobbetti M, Burzigotti R, Smacchi E, Corsetti A, De Angelis M. 1997. Microbiology and biochemistry of gorgonzola cheese during ripening. Int Dairy J 7:519-529. http://dx.doi.org/10.1016/S0958-6946(97)00047-2.
38. Wolfe BE, Button JE, Santarelli M, Dutton RJ. 2014. Cheese rind communities provide tractable systems for in situ and in vitro studies of microbial diversity. Cell 158:422-433. http://dx.doi.org/10.1016/j.cell.2014.05.041.
39. Daly DFM. 2014. Studies on factors relating to the development of defects in commercial cheese. Ph.D. thesis. University College Cork, County Cork, Ireland.
40. Quigley L, O'Sullivan O, Beresford TP, Paul Ross R, Fitzgerald GF, Cotter PD. 2012. A comparison of methods used to extract bacterial DNA from raw milk and raw milk cheese. J Appl Microbiol 113:96-105. http: //dx.doi.org/10.1111/j.1365-2672.2012.05294.x.
41. International Dairy Federation (IDF). 1988. Cheese and processed cheese: determination of chloride content (potentiometric titration method). International standards 4a. International Dairy Federation, Brussels, Belgium.
42. IDF. 1982. Determination of total solids content (cheese and processed cheese). International standards 4a. International Dairy Federation, Brussels, Belgium.
43. British Standards Institute. 1976. British standard methods for chemical analysis of cheese: determination of pH value. British Standards Institute, London, England.
44. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM. 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141-D145. http://dx.doi.org/10.1093/nar/gkn879.
45. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335-336. http://dx.doi.org/10.1038/nmeth.f.303.
46. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215:403-410. http://dx.doi.org/10.1016 /S0022-2836(05)80360-2.
47. Huson DH, Auch AF, Qi J, Schuster SC. 2007. MEGAN analysis of metagenomic data. Genome Res 17:377-386. http://dx.doi.org/10.1101 /gr.5969107.
48. Stearns JC, Lynch MDJ, Senadheera DB, Tenenbaum HC, Goldberg MB, Cvitkovitch DG, Croitoru K, Moreno-Hagelsieb G, Neufeld JD. 25 November 2011, posting date. Bacterial biogeography of the human digestive tract. Sci Rep http://dx.doi.org/10.1038/srep00170.
49. Montel M-C, Buchin S, Mallet A, Delbes-Paus C, Vuitton DA, Desmasures N, Berthier F. 2014. Traditional cheeses: rich and diverse microbiota with associated benefits. Int J Food Microbiol 177:136-154. http: //dx.doi.org/10.1016/j.ijfoodmicro.2014.02.019.
50. Maher MM, Murphy PM. 2000. Microbiological changes during ripening in two Irish smear-ripened, farmhouse cheeses produced from raw milk. Irish J Agric Food Res 39:107-121.
51. Spanevello MD, Patel BKC. 2004. The phylogenetic diversity of Thermus and Meiothermus from microbial mats of an Australian subsurface aquifer runoff channel. FEMS Microbiol Ecol 50:63-73. http://dx.doi.org/10.1016/j.femsec.2004.05.008.
52. Pask-Hughes R, Williams RAD. 1975. Extremely thermophilic Gramnegative bacteria from hot tap water. J Gen Microbiol 88:321-328. http: //dx.doi.org/10.1099/00221287-88-2-321.
53. Bagh LK, Albrechtsen H-J, Arvin E, Ovesen K. 2004. Distribution of bacteria in a domestic hot water system in a Danish apartment building. Water Res 38:225-235. http://dx.doi.org/10.1016/j.watres.2003.08.026.
54. Bleicher A, Neuhaus K, Scherer S. 2010. Vibrio casei sp. nov., isolated from the surfaces of two French red smear soft cheeses. Int J Syst Evol Microbiol 60:1745-1749. http://dx.doi.org/10.1099/ijs.0.016493-0.
55. Delcenserie V, Taminiau B, Delhalle L, Nezer C, Doyen P, Crevecoeur S, Roussey D, Korsak N, Daube G. 2014. Microbiota characterization of a Belgian protecteddesignation of origin cheese,Hervecheese,usingmetagenomicanalysis. J Dairy Sci 97:6046-6056. http://dx.doi.org/10.3168/jds.2014-8225.
56. Quigley L, O'Sullivan O, Beresford TP, Ross RP, Fitzgerald GF, Cotter PD. 2011. Molecular approaches to analysing the microbial composition of raw milk and raw milk cheese. Int J Food Microbiol 150:81-94. http: //dx.doi.org/10.1016/j.ijfoodmicro.2011.08.001.
57. Brennan NM, Brown R, Goodfellow M, Ward AC, Beresford TP, Simpson PJ, Fox PF, Cogan TM. 2001. Corynebacterium mooreparkense sp. nov. and Corynebacterium casei sp. nov., isolated from the surface of a smear-ripened cheese. Int J Syst Evol Microbiol 51(Pt 3):843-852. http: //dx.doi.org/10.1099/00207713-51-3-843.
58. Brennan NM, Ward AC, Beresford TP, Fox PF, Goodfellow M, Cogan TM. 2002. Biodiversity of the bacterial flora on the surface of a smear cheese. Appl Environ Microbiol 68:820-830. http://dx.doi.org/10.1128 /AEM.68.2.820-830.2002.
59. Mounier J, Rea MC, O'Connor PM, Fitzgerald GF, Cogan TM. 2007. Growth characteristics of Brevibacterium, Corynebacterium, Microbacterium, and Staphylococcus spp. isolated from surface-ripened cheese. Appl Environ Microbiol 73:7732-7739. http://dx.doi.org/10.1128/AEM.01260-07.
60. Addis E, Fleet GH, Cox JM, Kolak D, Leung T. 2001. The growth, properties and interactions of yeasts and bacteria associated with the maturation of Camembert and blue-veined cheeses. Int J Food Microbiol 69:25-36. http://dx.doi.org/10.1016/S0168-1605(01)00569-4.
61. Fuka MM, Engel M, Skelin A, Redzepović S, Schloter M. 2010. Bacterial communities associated with the production of artisanal Istrian cheese. Int J Food Microbiol 142:19-24. http://dx.doi.org/10.1016/j.ijfoodmicro.2010.05.008.
62. Irlinger F, Bimet F, Delettre J, Lefèvre M, Grimont PAD. 2005. Arthrobacter bergerei sp. nov. and Arthrobacter arilaitensis sp. nov., novel coryneform species isolated from the surfaces of cheeses. Int J Syst Evol Microbiol 55(Pt 1):457-462. http://dx.doi.org/10.1099/ijs.0.63125-0.
63. Mounier J, Gelsomino R, Goerges S, Vancanneyt M, Vandemeulebroecke K, Hoste B, Scherer S, Swings J, Fitzgerald GF, Cogan TM. 2005. Surface microflora of four smear-ripened cheeses. Appl Environ Microbiol 71:6489-6500. http://dx.doi.org/10.1128/AEM.71.11.6489-6500.2005.
64. Feurer C, Vallaeys T, Corrieu G, Irlinger F. 2004. 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 87:3189-3197. http://dx.doi.org/10.3168/jds.S0022-0302(04)73454-2.
65. Williams AG, Banks JM. 1997. Proteolytic and other hydrolytic enzyme activities in non-starter lactic acid bacteria (NSLAB) isolated from cheddar cheese manufactured in the United Kingdom. Int Dairy J 7:763-774. http://dx.doi.org/10.1016/S0958-6946(97)00092-7.
66. Porcellato D, Østlie HM, Brede ME, Martinovic A, Skeie SB. 2013. Dynamics of starter, adjunct non-starter lactic acid bacteria and propionic acid bacteria in low-fat and full-fat Dutch-type cheese. Int Dairy J 33:104-111. http://dx.doi.org/10.1016/j.idairyj.2013.01.007.
67. Litopoulou-Tzanetaki E, Tzanetakis N. 2011. Microbiological characteristics of Greek traditional cheeses. Small Rumin Res 101:17-32. http://dx.doi.org/10.1016/j.smallrumres.2011.09.022.