RRNA-based monitoring of the microbiota involved in Fontina PDO cheese production in relation to different stages of cow lactation

International Journal of Food Microbiology

Volumn 185, Issue , 2014, Pages 127-135

  Dolci, Paola ^a   De Filippis, Francesca ^b   La Storia, Antonietta ^b   Ercolini, Danilo ^b   Cocolin, Luca ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Fontina PDO cheese; Lactation; Microbiota; Pyrosequencing; RNA; RT PCR DGGE

Indexed keywords

RIBOSOME RNA; UREA;

ACIDIFICATION; ARTICLE; BACTERIAL FLORA; CHEESE; CHEESE RIPENING; COW; DENATURING GRADIENT GEL ELECTROPHORESIS; ESCHERICHIA; FERMENTATION; FONTINA PROTECTED DENOMINATION OF ORIGIN CHEESE; FOOD INDUSTRY; FOOD QUALITY; HIGH THROUGHPUT SEQUENCING; LACTATION; MARINOBACTER; MICROBIAL ACTIVITY; NONHUMAN; NUTRITIONAL STATUS; PH; PROPIONIBACTERIUM ACNES; PSYCHROBACTER; PYROSEQUENCING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; SEASONAL VARIATION; SENSORY ANALYSIS; STAPHYLOCOCCUS AUREUS; STARTER CULTURE;

FONTINA PDO CHEESE; LACTATION; MICROBIOTA; PYROSEQUENCING; RNA; RT-PCR-DGGE;

ANIMALS; BACTERIA; BIODIVERSITY; CATTLE; CHEESE; CLUSTER ANALYSIS; FEMALE; FOOD MICROBIOLOGY; ITALY; LACTATION; MICROBIOTA; MILK; RNA, RIBOSOMAL;

EID: 84904597574     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2014.05.021     Document Type: Article

References (46)

1. Afzal M.I., Ariceaga C.C.G., Lhomme E., Ali N.K., Payot S., Burgain J., Gaiani C., Borges F., Revol-Junelles A.M., Delaunay S., Cailliez-Grimal C. Characterization of Carnobacterium maltaromaticum LMA 28 for its positive technological role in soft cheese making. Food Microbiol. 2013, 36:223-230.
2. 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.
3. Alessandria V., Dolci P., Rantsiou K., Pattono D., Dalmasso A., Civera T., Cocolin L. Microbiota of the Planalto de Bolona: an artisanal cheese produced in uncommon environmental conditions in the Cape Verde Islands. World J. Microbiol. Biotechnol. 2010, 26:2211-2221.
4. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
5. Ampe F., Ben Omar N., Moizan C., Wacher C., Guyot J.P. Polyphasic study of the spatial distribution of microorganisms in Mexican pozol, a fermented maize dough, demonstrates the need for cultivation-independent methods to investigate traditional fermentations. Appl. Environ. Microbiol. 1999, 65:5464-5473.
6. Bérodier F., Lavanchy P., Zannoni M., Casals J., Herrero L., Adamo C. Guide d'Évaluation Olfacto-Gustative des Fromages à Pâte Dure et Semi-dure. LWT Food Sci. Technol. 1997, 30:653-664.
7. Caporaso J.G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F.D., et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 2010, 7:335-336.
8. Chao A., Bunge J. Estimating the number of species in a stochastic abundance model. Biometrics 2002, 58:531-539.
9. Cocolin L., Manzano M., Cantoni C., Comi G. Denaturing gradient gel electrophoresis analysis of the 16S rRNA gene V1 region to monitor dynamic changes in the bacterial population during fermentation of Italian sausages. Appl. Environ. Microbiol. 2001, 67:5113-5121.
10. De Filippis F., La Storia A., Villani F., Ercolini D. Exploring the sources of bacterial spoilers in beefsteaks by culture-independent high-throughput sequencing. PLoS ONE 2013, 8:e70222.
11. De Filippis F., La Storia A., Stellato G., Gatti M., Ercolini D. A selected core microbiome drives the early stages of three popular Italian cheese manufactures. PLoS ONE 2014, 9:e89680.
12. Dolci P., Alessandria V., Rantsiou K., Rolle L., Zeppa G., Cocolin L. Microbial dynamics of Castelmagno PDO, a traditional Italian cheese, with a focus on lactic acid bacteria ecology. Int. J. Food Microbiol. 2008, 122:302-311.
13. Dolci P., Alessandria V., Rantsiou K., Bertolino M., Cocolin L. Microbial diversity, dynamics and activity throughout manufacturing and ripening of Castelmagno PDO cheese. Int. J. Food Microbiol. 2010, 143:71-75.
14. 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.
15. Edgar R.C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010, 26:2460-2461.
16. Ercolini D. High-throughput sequencing and metagenomics: moving forward in the culture-independent analysis of food microbial ecology. Appl. Environ. Microbiol. 2013, 79:3148-3155.
17. Ercolini D., Russo F., Torrieri E., Masi P., Villani F. Changes in the spoilage-related microbiota of beef during refrigerated storage under different packaging conditions. Appl. Environ. Microbiol. 2006, 72:4663-4671.
18. Ercolini D., De Filippis F., La Storia A., Iacono M. "Remake" by high-throughput sequencing of the microbiota involved in the production of water buffalo mozzarella cheese. Appl. Environ. Microbiol. 2012, 78:8142-8145.
19. Franciosi E., De Sabbata G., Gardini F., Cavazza A., Poznanski E. Changes in psychrotrophic microbial populations during milk creaming to produce Grana Trentino cheese. Food Microbiol. 2011, 28:43-51.
20. Giannino M.L., Marzotto M., Dellaglio F., Feligini M. Study of microbial diversity in raw milk and fresh curd used for Fontina cheese production by culture-independent methods. Int. J. Food Microbiol. 2009, 130:188-195.
21. Hayes W., White C.H., Drake M.A. Sensory aroma characteristics of milk spoilage by Pseudomonas species. J. Food Sci. 2002, 67:448-454.
22. Krooneman J., Faber F., Alderkamp A.C., Elferink S.J.H.W.O., Driehuis F., Cleenwerck I., Swings J., Gottschal J.C., Vancanneyt M. Lactobacillus diolivorans sp. nov., a 1,2-propanediol-degrading bacterium isolated from aerobically stable maize silage. Int. J. Syst. Evol. Microbiol. 2002, 52:639-646.
23. Lozupone C., Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 2005, 71:8228-8235.
24. Mallet A., Guéguen M., Kauffmann F., Chesneau C., Sesboué A., Desmasures N. Quantitative and qualitative microbial analysis of raw milk reveals substantial diversity influenced by herd management practices. Int. Dairy J. 2012, 27:13-21.
25. Mariani P., Bonatti P., Sandri S. Contenuto di urea, pH, acidità totale e caratteristiche di coagulazione del latte di singoli allevamenti. Ind. Latte 1992, 28:3-17.
26. 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.
27. Masoud W., Vogensen F.K., Lillevang S., Abu Al-Soud W., Sorensen S.J., Jakobsen M. 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. 2012, 153:192-202.
28. McDonald D., Price M.N., Goodrich J., Nawrocki E.P., De Santis T.Z., et al. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 2012, 6:610-618.
29. Meile L., Le Blay G., Thierry A. Safety assessment of dairy microorganisms: Propionibacterium and Bifidobacterium. Int. J. Food Microbiol. 2008, 126:316-320.
30. Mills D.A., Johannsen E.A., Cocolin L. Yeast diversity and persistence in botrytis-affected wine fermentations. Appl. Environ. Microbiol. 2002, 68:4884-4893.
31. Pisano M.B., Patrignani F., Cosentino S., Guerzoni M.E., Franz C.M.A.P., Holzapfel W.H. Diversity and functional properties of Lactobacillus plantarum-group strains isolated from Italian cheese products. Dairy Sci. Technol. 2011, 91:65-76.
32. Podhorsky M., Cvak Z. The influence of nonprotein nitrogen on hygiene and processing properties of milk. Prumysl Potravin. 1989, 40:83-84.
33. 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.
34. 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.
35. Randazzo C.L., Torriani S., Akkermans A.D.L., de Vos W.M., Vaughan E.E. Diversity, dynamics, and activity of bacterial communities during production of an artisanal sicilian cheese as evaluated by 16S rRNA analysis. Appl. Environ. Microbiol. 2002, 68:1882-1892.
36. Rantsiou K., Urso R., Dolci P., Comi G., Cocolin L. Microflora of Feta cheese from four Greek manufacturers. Int. J. Food Microbiol. 2008, 126:36-42.
37. Reeder J., Knight R. Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat. Methods 2010, 7:668-669.
38. Senini L., Cappa F., Cocconcelli P.S. Use of rRNA-targeted oligonucleotide probes for the characterization of the microflora from fermentation of Fontina cheese. Food Microbiol. 1997, 14:469-476.
39. Shannon C.E., Weaver W. The Mathematical Theory of Communication 1949, University of Illinois Press, Urbana, (125 pp.).
40. Shannon P., Markiel A., Ozier O., Baliga N.S., Wang J.T., et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13:2498-2504.
41. Sheehan J.J., Fenelon M.A., Wilkinson M.G., McSweeney P.L.H. Effect of cook temperature on starter and non-starter lactic acid bacteria viability, cheese composition and ripening indices of a semi-hard cheese manufactured using thermophilic cultures. Int. Dairy J. 2007, 17:704-716.
42. Taïbi A., Dabour N., Lamoureux M., Roy D., LaPointe G. Comparative transcriptome analysis of Lactococcus lactis subsp. cremoris strains under conditions simulating Cheddar cheese manufacture. Int. J. Food Microbiol. 2011, 146:263-275.
43. van Beek S., Priest F.G. Evolution of the lactic acid bacterial community during malt whisky fermentation: a polyphasic study. Appl. Environ. Microbiol. 2002, 68:297-305.
44. Vega-Pérez J.M., Periñán I., Argandoña M., Vega-Holm M., Palo-Nieto C., Burgos-Morón E., López-Lázaro M., Vargas C., Nieto J.J., Iglesias-Guerra F. Isoprenyl-thiourea and urea derivatives as new farnesyl diphosphate analogues: synthesis and in vitro antimicrobial and cytotoxic activities. Eur. J. Med. Chem. 2012, 58:591-612.
45. Wang Q., Garrity G.M., Tiedje J.M., Cole J.R. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 2007, 73:5261-5267.
46. Yu J., Sun Z.H., Liu W.J., Bao Q.H., Zhang J.C., Zhang H.P. Phylogenetic study of Lactobacillus acidophilus group, L. casei group and L. plantarum group based on partial hsp60, pheS and tuf gene sequences. Eur. Food Res. Technol. 2012, 234:927-934.