Spatial distribution of the metabolically active microbiota within Italian PDO ewes' milk cheeses

PLoS ONE

Volumn 11, Issue 4, 2016, Pages

  De Pasquale, Ilaria ^a   Di Cagno, Raffaella ^a   Buchin, Solange ^b   De Angelis, Maria ^a   Gobbetti, Marco ^a  

^a UNIVERSITY OF BARI   (Italy)

^b Natl Inst of Agricultural Research   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; ALDEHYDE; AMINO ACID; ESTER; FAT; KETONE; PROTEIN; RNA 16S; SODIUM CHLORIDE; SULFUR DERIVATIVE; VOLATILE AGENT;

ARTICLE; BIOINFORMATICS; CELL DENSITY; CHEESE; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENTEROCOCCUS; ITALIAN PROTECTED DESIGNATION OF ORIGIN EWE MILK CHEESE; ITALIAN PROTECTED DESIGNATION OF ORIGIN FIORE SARDO EWE MILK CHEESE; ITALIAN PROTECTED DESIGNATION OF ORIGIN PECORINO SICILIANO EWE MILK CHEESE; ITALIAN PROTECTED DESIGNATION OF ORIGIN PECORINO TOSCANO EWE MILK CHEESE; LACTOBACILLUS; LACTOCOCCUS; MASS FRAGMENTOGRAPHY; MESOPHILIC BACTERIUM; METABOLICALLY ACTIVE MICROBIOTA; MICROFLORA; MOISTURE; NONHUMAN; OPERATIONAL TAXONOMIC UNIT; POPULATION ABUNDANCE; PROTEIN DEGRADATION; PURGE AND TRAP COUPLED WITH GAS CHROMATOGRAPHY MASS SPECTROMETRY; PYROSEQUENCING; RNA GENE; RNA INTERFERENCE; SPECIES COMPOSITION; SPECIES DISTRIBUTION; STREPTOCOCCUS; TAXONOMY; THERMOPHILIC BACTERIUM; ANIMAL; BACTERIAL COUNT; ITALY; MICROBIOLOGY; SHEEP;

ANIMALS; CHEESE; COLONY COUNT, MICROBIAL; ITALY; MICROBIOTA; SHEEP;

EID: 84963741137     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0153213     Document Type: Article

References (60)

1. Fox PF, Guinee TP, Cogan TM, McSweeney PLH. Fundamentals of cheeses sciences. 1th ed. Aspen Publishers, Gaithersburg, MD, USA. 2000.
2. Callon C, Picque D, Corrieu G, Montel MC. Ripening conditions: A tool for the control of Listeria monocytogenes in uncooked pressed type cheese. Food Control. 2011; 22: 1911-1919.
3. Callon C, Saubusse M, Didienne R, Buchin S, Montel MC. Simplification of a complex microbial antilisterial consortium to evaluate the contribution of its flora in uncooked pressed cheese. Int. J. Food Microbiol. 2011; 145: 379-389. doi: 10.1016/j.ijfoodmicro.2010.12.019 PMID: 21255857
4. Charlet M, Duboz G, Faurie F, Le Quéré J-L, Berthier F. Multiple interactions between Streptococcus thermophilus, Lactobacillus helveticus and Lactobacillus delbrueckii strongly affect their growth kinetics during the making of hard cooked cheeses. Int. J. Food Microbiol. 2009; 131: 10-19. doi: 10.1016/j. ijfoodmicro.2008.08.022 PMID: 18842314
5. Irlinger F, Mounier J. Microbial interactions in cheese: Implications for cheese quality and safety. Curr. Opin. Biotechnol. 2009; 20: 142-148. doi: 10.1016/j.copbio.2009.02.016 PMID: 19342218
6. Pelaez C, Requena T. Exploiting the potential of bacteria in the cheese ecosystem. Int. Dairy J. 2005; 15: 831-844.
7. Montel M-C, Buchin S, Mallet A, Delbes-Paus C, Vuitton DA, Desmasures N, et al. Traditional cheeses: Rich and diverse microbiota with associated benefits. Int. J. Food Microbiol. 2014; 177: 136-154. doi: 10.1016/j.ijfoodmicro.2014.02.019 PMID: 24642348
8. Sheehan A, O'Cuinn G, FitzGerald RJ, Wilkinson MG. Distribution of microbial flora, intracellular enzymes and compositional indices throughout a 12 kg Cheddar cheese block during ripening. Int. Dairy J. 2009; 19: 321-329.
9. Ercolini D, Hill PJ, Dodd CER. Bacterial Community structure and location in Stilton cheese. Appl. Environ. Microbiol. 2000; 69: 3540-3548.
10. Jeanson S, Chadoeuf J, Madec MN, Aly S, Floury J, Brocklehurst TF, et al. Spatial distribution of bacterial colonies in a model cheese. Appl. Environ. Microbiol. 2011; 77: 1493-1500. doi: 10.1128/AEM. 02233-10 PMID: 21169438
11. Monfredini L, Settanni L, Poznanski E, Cavazza A, Franciosi E. The spatial distribution of bacteria in Grana-cheese during ripening. Syst. Appl. Microbiol. 2012; 33: 54-63.
12. O'Sullivan DJ, Cotter PD, O'Sullivan O, Giblin L, McSweeeny PLH, Sheehan J.J. Temporal and spatial differences in microbial composition during the manufacture of a Continental-type cheese. Appl. Environ. Microbiol. 2015; 7: 2525-2533.
13. Gobbetti M, De Angelis M, Di Cagno R, Rizzello CG. The relative contributions of starter cultures and non-starter bacteria to the flavour of cheese,. In Weimer BC editor. Improving the flavor of cheese. Boca Raton: FL; 2007. p 121-147.
14. Gobbetti M, De Angelis M, Di Cagno R, Mancini L, Fox PF. Pros and cons for using non-starter lactic acid bacteria (NSLAB) as secondary/adjunct starters for cheese ripening. Trends Food Sci Tech. 2015; 45: 167-178.
15. Wouters JTM, Ayad EHE, Hugenholtz J, Smit G. Microbes from raw milk for fermented dairy products. Int. Dairy J. 2002: 12: 91-109.
16. 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. PMID: 11589547
17. Lessard M-H, Bélanger G, St-Gelais D, Labrie S. The composition of Camembert cheese-ripening cultures modulates both mycelial growth and appearance. Appl. Environ. Microbiol. 2012; 78: 1813-1819. doi: 10.1128/AEM.06645-11 PMID: 22247164
18. 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. doi: 10.1016/j.ijfoodmicro.2009.04.020 PMID: 19481828
19. Fleurot I, Aigle M, Fleurot R, Darrigo C, Hennekinne J-A, Gruss A, et al. Following pathogen development and gene expression in a food ecosystem: The case of Staphylococcus aureus isolate in cheese. Appl. Environ. Microbiol. 2014; 80: 5106-5115. doi: 10.1128/AEM.01042-14 PMID: 24928871
20. Gobbetti M, Burzigotti R, Smacchi E, Corsetti A, De Angelis M. Microbiology and biochemistry of gorgonzola cheese during ripening. Int. Dairy J. 1997; 7: 519-529.
21. Fitzsimons NA, Cogan TM, Condon S, Beresford T. Spatial and temporal distribution of non-starter lactic acid bacteria in Cheddar cheese. J. Appl. Microbiol. 2001; 90: 600-608. PMID: 11309072
22. Ogier J-C, Lafarge V, Girard V, Rault A, Maladen V, Gruss A, et al. Molecular Fingerprinting of dairy microbial ecosystems by use of temporal temperature and denaturing gradient gel electrophoresis. App. Environ. Micro. 2004; 70: 5628-5643.
23. Wolfe BE, Button JE, Santarelli M, Dutton RJ. Cheese rind communities provide tractable systems for in situ and in vitro studies of microbial diversity. Cell. 2014; 158: 422-433. doi: 10.1016/j.cell.2014.05. 041 PMID: 25036636
24. Gobbetti M. Extra-hard varieties. In: Fox PF, McSweeney PLH, Cogan TM, Guinee TP editors. Cheese: Chemistry, physics and microbiology. London: United Kingdom. 2004; p.51-70.
25. De Pasquale I, Calasso M, Mancini L, Ercolini D, La Storia A, De Angelis M, et al. Causal relationship between microbial ecology dynamics and proteolysis during manufacture and ripening of Canestrato Pugliese PDO cheese. Appl. Environ. Microbiol. 2014; 80: 4085?4094. doi: 10.1128/AEM.00757-14 PMID: 24771032
26. De Pasquale I, Di Cagno R, Buchin S, De Angelis M, Gobbetti M. Microbial ecology dynamics reveal a succession in the core microbiota involved in the ripening of pasta filata Caciocavallo Pugliese cheese. Appl. Environ. Microbiol. 2014; 80: 6243?6255. doi: 10.1128/AEM.02097-14 PMID: 25085486
27. Dolci P, De Filippis F, La Storia A, Ercolini D, Cocolin L. rRNA-based monitoring of the microbiota involved in Fontina PDO cheese production in relation to different stages of cow lactation. Int. J. Food Microbiol. 2014; 185: 127?135. doi: 10.1016/j.ijfoodmicro.2014.05.021 PMID: 24960294
28. 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. 2013; 9:e89680.
29. International Dairy Federation. Determination of the protein content of processed cheeses products. Standard
30. International Dairy Federation, Brussels, Belgium. 1964.
31. Institute for Industrial Research and Standards. Determination of the percentage of fat in cheese. Irish standard 69 Institute for Industrial Research and Standards, Dublin, Ireland. 1955.
32. International Dairy Federation. Cheese and processed cheese. Determination of the total solid content. IDF standard 4A. International Dairy Federation, Brussels, Belgium. 1982.
33. Fox PF. Potentiometric determination of salt in cheese. J. Dairy Sci. 1963; 46: 744?745.
34. Di Cagno R, Quinto M, Corsetti A, Minervini F, Gobbetti M. Assessing the proteolytic and lipolytic activities of single strains of mesophilic lactobacilli as adjunct cultures using a Caciotta cheese model system. Int. Dairy J. 2006; 16: 119?130.
35. Andrews AT. Proteinases in normal bovine milk and their action on caseins. J. Dairy Res. 1983; 50: 45-55. PMID: 6341422
36. Gobbetti M, Morea M, Baruzzi F, Corbo MR, Matarante A, Considine T, et al. Microbiological, compositional, biochemical and textural characterization of Caciocavallo Pugliese cheese during ripening. Int. Dairy J. 2002; 12: 511-523.
37. Di Cagno R, Buchin S, De Candia S, De Angelis M, Fox PF, Gobbetti M. Characterization of Italian cheeses ripened under nonconventional conditions. J. Dairy Sci. 2007; 90: 2689-2704. PMID: 17517708
38. 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. doi: 10.1128/AEM. 00256-13 PMID: 23475615
39. Reeder J, Knight R. Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat. Methods. 2010; 7: 668-669. doi: 10.1038/nmeth0910-668b PMID: 20805793
40. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010; 26: 2460-2461. doi: 10.1093/bioinformatics/btq461 PMID: 20709691
41. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011; 27: 2194-2200. doi: 10.1093/bioinformatics/btr381 PMID: 21700674
42. De Filippis F, La Storia A, Villani F, Ercolini D. 2013. Exploring the sources of beefsteaks contamination by culture-independent highthroughput sequencing. PLoS One. 2013; 8:e70222. doi: 10.1371/journal. pone.0070222 PMID: 23936168
43. Minervini F, Di Cagno R, Lattanzi A, De Angelis M, Antonielli L, Cardinali G, et al. Lactic acid bacterium and yeast microbiotas of 19 sourdoughs used for traditional/typical Italian breads: Interactions between ingredients and microbial species diversity. Appl. Environ. Microbiol. 2012; 78: 1251-1264. doi: 10. 1128/AEM.07721-11 PMID: 22156414
44. Ottogalli, G. Aspetti biochimici e bromatologici, In: Ottogalli G, editor. Atlante dei Formaggi. Italy: Milan; 2001. p 72-90.
45. Buccioni A, Rapaccini S, Antongiovanni M, Minieri G, Conte G, Mele M. Conjugated linoleic acid and C18:1 isomers content in milk fat of sheep and their transfer to Pecorino Toscano cheese. Int. Dairy J. 2010; 20: 190-194.
46. Albenzio M, Corbo MR, Rehman SU, Fox PF, De Angelis M, Corsetti A, et al. Microbiological and biochemical characterization of Canestrato Pugliese cheese made from raw milk, pasteurized milk or by heating the curd in hot whey. Int. J. Food Microbiol. 2001; 67: 35-48. PMID: 11482567
47. Coda R, Brechany E, De Angelis M, De Candia S, Di Cagno R, Gobbetti M. Comparison of the compositional, microbiological, biochemical, and volatile profile characteristics of nine Italian ewes' milk cheeses. J. Dairy Sci. 2006; 89: 4126-4143. PMID: 17032999
48. Savijoki K, Ingmer H, Varmanen P. Proteolytic systems of lactic acid bacteria. Appl. Microbiol. Biotechnol. 2006; 71: 394-406. PMID: 16628446
49. Smit G, Smit BA, Engels WJM. Flavour formation by lactic acid bacteria and biochemical flavour profiling of cheese products. FEMS Microbiol. Rev. 2005; 29: 591-610. PMID: 15935512
50. Crow VL. Properties of the 2,3-butanediol dehydrogenase from Lactococcus lactis sbsp. lactis in relation to citrate fermentation. Appl. Environ. Microbiol. 1990; 56: 1656-1662. PMID: 16348209
51. Hayaloglu AA. Comparisons of different single-strain starter cultures for their effects on ripening and grading of Beyaz cheese. Int. J. Food Sci. Technol. 2007; 42: 930-938.
52. McSweeney PLH, Sousa MJ. Biochemical pathways for the production of flavour compounds in cheese during ripening: A review. Lait. 2000; 80: 293-324.
53. Bockelmann W. Development of defined surface starter cultures for the ripening of smear cheeses. Int. Dairy J. 2002; 12: 123-131.
54. Fuka MM, Wallish S, Eng.el M, Welzl G, Havranek J, Schloter M. Dynamics of bacterial communities during the ripening process of different Croatian cheese types derived from raw ewe's milk cheeses. PLoS ONE. 2013; 8:e80734. doi: 10.1371/journal.pone.0080734 PMID: 24278315
55. Mangia NP, Murgia MA, Garau G, Sanna MG, Deiana P. Influence of selected lab cultures on the evolution of free amino acids, free fatty acids, and Fiore Sardo cheese microflora during the ripening. Food Microbiol. 2008; 25: 366-377. doi: 10.1016/j.fm.2007.09.009 PMID: 18206779
56. Quigley L, O'Sullivan O, Stanton C, Beresford TP, Ross RP, Fitzgerald GF, et al. The complex microbiota of raw milk. FEMS Microbiol. Rev.2013; 37: 664-698. doi: 10.1111/1574-6976.12030 PMID: 23808865
57. Fox PF, Guinee TP, Cogan TM, McSweeney PLH. Fundamentals of cheeses sciences. 1th ed. Gaithersburg: MD. 2000.
58. Bockelmann W. Surface-Ripened Cheeses. Fifth Cheese Symposium. Teagasc/University College Cork, Dublin, Irish Republic, 11-13 March 1997. p. 121-132.
59. Arfi K, Amárita F, Spinnler H-E, Bonnarme P. Catabolism of volatile sulfur compounds precursors by Brevibacterium linens and Geotrichum candidum, two microorganisms of the cheese ecosystem. J. Biotechnol. 2003; 105: 245-253. PMID: 14580796
60. Bonnarme P, Lapadatescu C, Yvon M, Spinnler H-E. L-methionine degradation potentialities of cheese ripening microorganisms. J. Dairy Res. 2001; 68: 663-674. PMID: 11928962