The predominance, biodiversity and biotechnological properties of Kluyveromyces marxianus in the production of Pecorino di Farindola cheese

International Journal of Food Microbiology

Volumn 187, Issue , 2014, Pages 41-49

  Tofalo, Rosanna ^a   Fasoli, Giuseppe ^a   Schirone, Maria ^a   Perpetuini, Giorgia ^a   Pepe, Alessia ^a   Corsetti, Aldo ^a   Suzzi, Giovanna ^a  

^a UNIVERSITY OF TERAMO   (Italy)

Author keywords

Amino acids lactate metabolism; D1 D2 sequence analysis; Dairy yeasts; K. marxianus variants; Pecorino di Farindola; RAPD PCR

Indexed keywords

AMINO ACID; LACTIC ACID; LACTOSE;

AMINO ACID METABOLISM; ARTICLE; BIODIVERSITY; CANDIDA; CANDIDA GLAEBOSA; CANDIDA KRUSEI; CANDIDA PARAPSILOSIS; CANDIDA ZEYLANOIDES; CHEESE; CHEESE RIPENING; CHEESEMAKING; CONTROLLED STUDY; FOOD MICROBIOTECHNOLOGY; FUNGUS GROWTH; FUNGUS IDENTIFICATION; GENE SEQUENCE; GENETIC VARIABILITY; KLUYVEROMYCES MARXIANUS; NONHUMAN; POLYMERASE CHAIN REACTION; RANDOM AMPLIFIED POLYMORPHIC DNA; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SEQUENCE ALIGNMENT;

AMINO ACIDS/LACTATE METABOLISM; D1/D2 SEQUENCE ANALYSIS; DAIRY YEASTS; K. MARXIANUS VARIANTS; PECORINO DI FARINDOLA; RAPD-PCR;

ANIMALS; BIODIVERSITY; CHEESE; DNA, RIBOSOMAL SPACER; FOOD MICROBIOLOGY; KLUYVEROMYCES; POLYMERASE CHAIN REACTION; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RNA, RIBOSOMAL; YEASTS;

EID: 84904438212     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2014.06.029     Document Type: Article

References (72)

1. Addis A., Fleet G.H., Cox J.M., Kolak D., Leung T. The growth, properties and interactions of yeasts and bacteria associated with the maturation of Camembert and blue-veined cheese. Int. J. Food Microbiol. 2001, 69:25-36.
2. Altschul S.F., Madden T.L., Schaffer 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.
3. Andrighetto C., Psomas E., Tzanetakis N., Suzzi G., Lombardi A. Randomly amplified polymorphic DNA (RAPD) PCR for the identification of yeasts isolated from dairy products. Lett. Appl. Microbiol. 2000, 30:5-9.
4. Aponte M., Pepe O., Blaiotta G. Short communication: identification and technological characterization of yeast strains isolated from samples of water buffalo Mozzarella cheese. J. Dairy Sci. 2010, 93:2358-2361.
5. Bai M., Qing M., Guo Z., Zhang Y., Chen X., Bao Q., Zhang H., Sun T.S. Occurrence and dominance of yeast species in naturally fermented milk from the Tibetan Plateau of China. Can. J. Microbiol. 2010, 56:707-714.
6. Bellaver L.H., de Carvalho N.M.B., Abrahão-Neto J., Gombert A.K. Ethanol formation and enzyme activities around glucose-6-phosphate in Kluyveromyces marxianus CBS 6556 exposed to glucose or lactose excess. FEMS Yeast Res. 2004, 4:691-698.
7. Belloch C., Fernández-Espinar T., Querol A., García M.D., Barrio E. An analysis of inter- and intraspecific genetic variabilities in the Kluyveromyces marxianus group of yeast species for the reconsideration of the K. lactis taxon. Yeast 2002, 19:257-268.
8. Beresford T.P., Fitzsimons N.A., Brennan N.L., Cogan T.M. Recent advances in cheese microbiology. Int. Dairy J. 2001, 11:259-274.
9. Binetti A., Carrasco M., Reinheimer J., Suárez V. Yeasts from autochthonal cheese starters: technological and functional properties. J. Appl. Microbiol. 2013, 115:434-444.
10. Borneman A.R., Forgan A.H., Pretorius I.S., Chambers P.J. Comparative genome analysis of a Saccharomyces cerevisiae wine strain. FEMS Yeast Res. 2008, 8:1185-1195.
11. Bouzas J., Kantt C.A., Bodyfelt F., Torres J.A. Simultaneous determination of sugars and organic acids in cheddar cheese by high-performance liquid chromatography. J. Food Sci. 1991, 56:276-278.
12. Capece A., Romano P. "Pecorino di Filiano" cheese as a selective habitat for the yeast species, Debaryomyces hansenii. Int. J. Food Microbiol. 2009, 132:180-184.
13. Carreira A., Paloma L., Loureiro V. Pigment producing yeasts involved in the brown surface discoloration of ewes' cheese. Int. J. Food Microbiol. 1998, 41:223-230.
14. Casal M., Paiva S., Queirós O., Soares-Silva I. Transport of carboxylic acids in yeast. FEMS Microbiol. Rev. 2008, 32:974-994.
15. Cholet O., Hénaut A., Casaregola S., Bonnarme P. Gene expression and biochemical analysis of cheese-ripening yeasts: focus on catabolism of l-methionine, lactate, and lactose. Appl. Environ. Microbiol. 2007, 73:2561-2570.
16. Cocolin L., Aggio D., Manzano M., Cantoni C., Comi G. An application of PCR-DGGE analysis to profile the yeast populations in raw milk. Int. Dairy J. 2002, 12:407-411.
17. Corbo M.R., Lanciotti R., Albenzio M., Sinigaglia M. Occurrence and characterization of yeasts isolated from milks and dairy products of Apulia region. Int. J. Food Microbiol. 2001, 69:147-152.
18. 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.
19. Cosentino S., Fadda M.E., Deplano M., Mulargia A.F., Palmas F. Yeasts associated with Sardinian ewe's dairy products. Int. J. Food Microbiol. 2001, 69:53-58.
20. Devoyod J.J. Yeasts in cheesemaking. Yeast Technology 1990, 228-240. Springer-Verlag, Berlin. J.F.T. Spencer, D.M.S. Spencer (Eds.).
21. El-Sharoud W.M., Belloch C., Peris D., Querol A. Molecular identification of yeasts associated with traditional Egyptian dairy products. J. Food Sci. 2009, 74:341-346.
22. Esteve-Zarzoso B., Belloch C., Uruburu F., Querol A. Identification of yeasts by RFLP analysis of the 5.8 rRNA gene and the two ribosomal internal transcribed spacers. Int. J. Syst. Bacteriol. 1999, 49:329-337.
23. Fadda M.E., Cosentino S., Deplano M., Palmas F. Yeast populations in Sardinian Feta cheese. Int. J. Food Microbiol. 2001, 69:53-156.
24. Fadda M.E., Mossa V., Pisano M.B., Deplano M., Cosentino S. Occurrence and characterization of yeast isolated from artisanal Fiore Sardo cheese. Int. J. Food Microbiol. 2004, 95:51-59.
25. Fadda M.E., Viale S., Deplano M., Pisano M.B., Cosentino S. Characterization of yeast population and molecular fingerprinting of Candida zeylanoides isolated from goat's milk collected in Sardinia. Int. J. Food Microbiol. 2010, 136:376-380.
26. Fleet G.H. A review: yeasts in dairy products. J. Appl. Bacteriol. 1990, 68:199-211.
27. Fleet G.H. Yeasts in food and beverages: impact on product quality and safety. Curr. Opin. Biotechnol. 2007, 18:170-175.
28. Fleet G.H., Mian M.A. The occurrence and growth of yeasts in dairy products. Int. J. Food Microbiol. 1987, 4:145-155.
29. Folkertsma B., Fox P.F. Use of Cd-ninhydrin reagent to assess proteolysis in cheese during ripening. J. Dairy Res. 1992, 59:217-224.
30. Fonseca A., Spencer-Martins I., van Uden N. Transport of lactic acid in Kluyveromyces marxianus: evidence for a monocarboxylate uniport. Yeast 1991, 7:775-780.
31. Fonseca G.G., Heinzle E., Wittmann C., Gombert A.K. The yeast Kluyveromyces marxianus and its biotechnological potential. Appl. Microbiol. Biotechnol. 2008, 79:339-354.
32. Gardini F., Tofalo R., Belletti N., Iucci L., Suzzi G., Torriani S., Guerzoni M.E., Lanciotti R. Characterization of yeasts involved in the ripening of Pecorino Crotonese cheese. Food Microbiol. 2006, 23:641-648.
33. Giannino M.L., Buffoni J.N., Massone E., Feligini M. Internal transcribed spacer as a target to assess yeast biodiversity in Italian Taleggio PDO cheese. J. Food Sci. 2011, 76:511-514.
34. Guerzoni M.E., Gobbetti M., Lanciotti R., Vannini L., Chaves Lopez C. Yarrowia lipolytica as a potential ripening agent in milk products. Yeasts in the Dairy Industry: Positive and Negative Aspects 1998, 23-33. International Dairy Federation, Brussels, Belgium. M. Jakobsen, J. Narvhus, B.C. Viljoen (Eds.).
35. Jakobsen M., Narvhus J. Yeasts and their possible beneficial and negative effects on the quality of dairy products. Int. Dairy J. 1996, 6:755-768.
36. Kurtzman C.P., Robnett C. Identification and phylogeny of ascomycetous yeast from analysis of nuclear large subunit (26S) ribosomial DNA partial sequences. Antonie Van Leeuwenhoek 1998, 73:331-371.
37. Kurtzmann C.P., Fell J.W. The Yeasts-A Taxonomic Study 1998, 420-422. Elsevier Science B.V., Amsterdam, The Netherlands. C.P. Kurtzmann, J.W. Fell (Eds.).
38. Lachance M.A., Daniel H.M., Meyer W., Prasad G.S., Gautam S.P., Boundy-Mills K. The D1/D2 domain of the large-subunit rDNA of the yeast species Clavispora lusitaniae is unusually polymorphic. FEMS Yeast Res. 2003, 4:253-258.
39. Lane M.M., Morrissey J.P. Kluyveromyces marxianus: a yeast emerging from its sister's shadow. Fungal Biol. Rev. 2010, 24:17-26.
40. Lane M.M., Burke N., Karreman R., Wolfe K.H., O'Byrne C.P., Morrissey J.P. Physiological and metabolic diversity in the yeast Kluyveromyces marxianus. Antonie Van Leeuwenhoek 2011, 100:507-519.
41. Laurenčic M., Sulo P., Sláviková E., Piecková E., Seman M., Ebringer L. The diversity of eukaryotic microbiota in the traditional Slovak sheep cheese bryndza. Int. J. Food Microbiol. 2008, 127:176-179.
42. Lenoir J. The surface flora and its role in the ripening of cheese. Bull. IDF 1984, 171:3-20.
43. Liti G., Wardrop F.R., Cardinali G., Martini A., Walker G.M. Differential responses to antimycin A and expressions of the Crabtree effect in selected Klyuveromyces spp. Ann. Microbiol. 2001, 51:235-243.
44. Mansour S., Beckerich J.M., Bonnarme P. Lactate and amino acid catabolism in the cheese-ripening yeast Yarrowia lipolytica. Appl. Environ. Microbiol. 2008, 74:6505-6512.
45. Marcellino N.S.R., Benson D.R. Scanning electron and light microscopic study of microbial succession on Bethlehem St. Nectaire Cheese. Appl. Environ. Microbiol. 1992, 58:3448-3454.
46. Mulet J.M., Leube M.P., Kron S.J., Rios G., Fink G.R., Serrano R. A novel mechanism of ion homeostasis and salt tolerance in yeast: the Hal4 and Hal5 protein kinases modulate the Trk1-Trk2 potassium transporter. Mol. Cell. Biol. 1999, 19:3328-3337.
47. Padilla B., Manzanares P., Belloch C. Yeast species and genetic heterogeneity within Debaryomyces hansenii along the ripening process of traditional ewes' and goats' cheeses. Food Microbiol. 2014, 38:160-166.
48. Panelli S., Brambati E., Bonacina C., Feligini M. Diversity of fungal flora in raw milk from the Italian Alps in relation to pasture altitude. Springer Plus 2013, 2:1-9.
49. Pereira-Dias S., Potes M.E., Marinho A., Malfeiro-Ferreira M., Loureiro V. Characterisation of yeast flora isolated from an arti-sanal Portuguese ewe's cheese. Int. J. Food Microbiol. 2000, 60:55-63.
50. Pérez-Brito D., Tapia-Tussell R., Quijano-Ramayo A., Larqué-Saavedra A., Lappe P. Molecular characterization of Kluyveromyces marxianus strains isolated from Agave fourcroydes (Lem.) in Yucatan, Mexico. Mol. Biotechnol. 2007, 37:181-186.
51. Pirisi A., Comunian R., Urgeghe P.P., Scintu M.F. Sheep's and goat's dairy products in Italy: technological, chemical, microbiological, and sensory aspects. Small Rumin. Res. 2011, 101:102-112.
52. Piskur J., Rozpedowska E., Polakova S., Merico A., Compagno C. How did Saccharomyces evolve to become a good brewer?. Trends Genet. 2006, 22:183-186.
53. Prillinger H., Molnar O., Eliskases-Lechner F., Lopandic K. Phenotypic and genotypic identification of yeasts from cheese. Antonie Van Leeuwenhoek 1999, 75:267-283.
54. Pulvirenti A., Solieri L., Gullo M., De Vero L., Giudici P. Occurrence and dominance of yeast species in sourdough. Lett. Appl. Microbiol. 2004, 38:113-117.
55. Qian J., Qin X., Yin Q., Chu J., Wang Y. Cloning and characterization of Kluyveromyces marxianus Hog1 gene. Biotechnol. Lett. 2011, 33:571-575.
56. Querol A., Barrio E., Ramon D. A comparative study of different methods of yeast strains characterization. Syst. Appl. Microbiol. 1992, 15:439-446.
57. Romano A., Casaregola S., Torre P., Gaillardin C. Use of RAPD and mitochondrial DNA RFLP for typing of Candida zeylanoides and Debaryomyces hansenii yeast isolated from cheese. Syst. Appl. Microbiol. 1996, 19:255-264.
58. Roostita R., Fleet G.H. The occurrence and growth of yeast in Camembert and blue-veined cheeses. Int. J. Food Microbiol. 1996, 28:393-404.
59. Rossi J., Gobbetti M., Buzzinini P., Corsetti A., Smacchi E., De Angelis M. Yeasts in dairy products. Ann. Microbiol. Enzymol. 1997, 47:169-183.
60. Schirone M., Tofalo R., Mazzone G., Corsetti A., Suzzi G. Biogenic amine content and microbiological profile of Pecorino di Farindola cheese. Food Microbiol. 2011, 28:128-136.
61. Suzzi G., Lanorte M.T., Galgano F., Andrighetto C., Lombardi A., Lanciotti R., Guerzoni M.E. Proteolytic, lipolytic and molecular characterization of Yarrowia lipolytica isolated from cheese. Int. J. Food Microbiol. 2001, 69:69-77.
62. Tofalo R., Chaves-López C., Di Fabio F., Schirone M., Felis G.E., Torriani S., Paparella A., Suzzi G. Molecular identification and osmotolerant profile of wine yeasts that ferment a high sugar grape must. Int. J. Food Microbiol. 2009, 130:179-187.
63. Tofalo R., Perpetuini G., Fasoli G., Schirone M., Corsetti A., Suzzi G. Biodiversity study of wine yeasts belonging to the "terroir" of Montepulciano d'Abruzzo "Colline Teramane" revealed Saccharomyces cerevisiae strains exhibiting atypical and unique 5.8S-ITS restriction patterns. Food Microbiol. 2014, 39:7-12.
64. van den Tempel T., Jakobsen M. The technological characteristics of Debaryomyces hansenii and Yarrowia lipolytica and their potential as starter cultures for production of Danablu. Int. Dairy J. 2000, 10:263-270.
65. van Dijken J.P., Weusthuis R.A., Pronk J.T. Kinetics of growth and sugar consumption in yeasts. Antonie Van Leeuwenhoek 1993, 63:343-352.
66. Viljoen B.C. The interaction between yeasts and bacteria in dairy environments. Int. J. Food Microbiol. 2001, 69:37-44.
67. Visser W., Scheffers W.A., Batenburg-van der Vegte W.H., van Dijken J.P. Oxygen Requirements of Yeasts. Appl. Environ. Microbiol. 1990, 56:3785-3792.
68. Walker G.M. Yeast Physiology and Biotechnology 1998, John Wiley & Sons Ltd., Chichester, England.
69. Welthagen J.J., Viljoen B.C. Yeast profile in Gouda cheese during processing and ripening. Int. J. Food Microbiol. 1998, 41:185-194.
70. Welthagen J.J., Viljoen B.C. The isolation and identification of yeasts obtained during the manufacture and ripening of Cheddar cheese. Food Microbiol. 1999, 16:63-73.
71. Wyder M.T., Puhan Z. Investigation of the yeast flora in smear ripened cheeses. Milchwissenschaft 1999, 54:330-333.
72. Zeyl C. Capturing the adaptive mutation in yeast. Res. Microbiol. 2004, 155:217-223.