The genome sequence of the highly acetic acid-tolerant zygosaccharomyces bailii-derived interspecies hybrid strain ISA1307, isolated from a sparkling wine plant

DNA Research

Volumn 21, Issue 3, 2014, Pages 299-313

  Mira, Nuno P ^a   Münsterkötter, Martin ^b   Dias Valada, Filipa ^a   Santos, Júlia ^c   Palma, Margarida ^a   Roque, Filipa C ^a   Guerreiro, Joana F ^a   Rodrigues, Fernando ^c   Sousa, Maria João ^d   Leão, Cecília ^c   Güldener, Ulrich ^b   Sá Correia, Isabel ^a  

^a UNIVERSITY OF LISBON   (Portugal)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c UNIVERSITY OF MINHO   (Portugal)

^d UNIVERSITY OF MINHO   (Portugal)

Author keywords

genome sequencing and annotation; hybrid yeast strains; weak acid food preservatives tolerance; wine yeast strains; Zygosaccharomyces bailii

Indexed keywords

ACETIC ACID; AMINO ACID; CARBOHYDRATE; FOOD PRESERVATIVE; FUNGAL DNA; FUNGAL PROTEIN; NITROGEN DERIVATIVE;

AMINO ACID METABOLISM; ARTICLE; BIOGENESIS; CARBOHYDRATE METABOLISM; CARBOHYDRATE TRANSPORT; CELL COMPONENT; CELLULAR STRESS RESPONSE; DNA BINDING; DNA CONTENT; FERMENTATION; FLOW CYTOMETRY; FUNGAL GENE; FUNGAL STRAIN; GENE DUPLICATION; GENE SEQUENCE; GENE STRUCTURE; KARYOTYPING; MATING; MEIOSIS; MITOSIS; PH; PROTEIN FOLDING; PROTEIN MODIFICATION; SPARKLING WINE; ZYGOSACCHAROMYCES BAILII; CHIMERA; CHROMOSOME MAP; FUNGAL GENOME; FUNGAL MATING TYPE GENE; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGICAL STRESS; TRANSPORT AT THE CELLULAR LEVEL; WINE; ZYGOSACCHAROMYCES;

ACETIC ACID; AMINO ACIDS; BASE SEQUENCE; BIOLOGICAL TRANSPORT; CARBOHYDRATE METABOLISM; CHIMERA; CHROMOSOME MAPPING; DNA, FUNGAL; FUNGAL PROTEINS; GENES, MATING TYPE, FUNGAL; GENOME, FUNGAL; KARYOTYPING; MEIOSIS; MOLECULAR SEQUENCE ANNOTATION; STRESS, PHYSIOLOGICAL; WINE; ZYGOSACCHAROMYCES;

EID: 84902996763     PISSN: 13402838     EISSN: 17561663     Source Type: Journal    
DOI: 10.1093/dnares/dst058     Document Type: Article

References (63)

1. Martorell, P., Stratford, M., Steels, H., Fernandez- Espinar, M.T. and Querol, A. 2007, Physiological characterization of spoilage strains of Zygosaccharomyces bailii and Zygosaccharomyces rouxii isolated from high sugar environments, Int. J. Food Microbiol., 114, 234-42. (Pubitemid 46329176)
2. Stratford, M. 2006, Food and beverage spoilage yeasts. In: Querol, A. and Fleet, G.H., eds, Yeasts in food and beverages. Springer: Heidelberg.
3. Zuehlke, J.M., Petrova, B.and Edwards,C.G.2013,Advances in the control of wine spoilage by Zygosaccharomyces and Dekkera/Brettanomyces, Annu. Rev. Food Sci. Technol., 4, 57-78.
4. Stratford, M., Steels, H., Nebe-von-Caron, G., Novodvorska, M., Hayer, K. and Archer, D.B. 2013, Extreme resistance toweak-acid preservatives in the spoilage yeast Zygosaccharomyces bailii, Int. J. Food Microbiol., 166, 126-34.
5. Pina, C., Goncalves, P., Prista, C. and Loureiro-Dias, M.C. 2004, Ffz1, a new transporter specific for fructose from Zygosaccharomyces bailii, Microbiology, 150, 2429-33. (Pubitemid 39117654)
6. Merico, A., Capitanio, D., Vigentini, I., Ranzi, B.M. and Compagno, C. 2003, Aerobic sugar metabolism in the spoilage yeast Zygosaccharomyces bailii, FEMS Yeast Res., 4, 277-83. (Pubitemid 37494726)
7. Rodrigues, F., Corte-Real,M., Leão, C., van Dijken, J.P. and Pronk, J.T. 2001, Oxygen requirements of the food spoilage yeast Zygosaccharomyces bailii in synthetic and complex media, Appl. Environ. Microbiol., 67, 2123-8.
8. Domizio, P., Romani, C., Lencioni, L., et al. 2011, Outlining a future for non-Saccharomyces yeasts: selection of putative spoilage wine strains to be used in association with Saccharomyces cerevisiae for grape juice fermentation, Int. J. Food Microbiol., 147, 170-80.
9. Romano, P., Fiore, C., Paraggio, M., Caruso, M. and Capece, A. 2003, Function of yeast species and strains in wine flavour, Int. J. Food Microbiol., 86, 169-80. (Pubitemid 36900416)
10. Dato, L., Branduardi, P., Passolunghi, S., et al. 2010, Advances in molecular tools for the use of Zygosaccharomyces bailii as host for biotechnological productions and construction of the first auxotrophic mutant, FEMS Yeast Res., 10, 894-908.
11. Branduardi, P.,Valli,M.,Brambilla, L., Sauer, M.,Alberghina, L. and Porro, D. 2004, The yeast Zygosaccharomyces bailii: a new host for heterologous protein production, secretion and for metabolic engineering applications, FEMS Yeast Res., 4, 493-504. (Pubitemid 38156213)
12. Sauer, M., Branduardi, P., Valli, M. and Porro, D. 2004, Production of L-ascorbic acid by metabolically engineered Saccharomyces cerevisiae and Zygosaccharomyces bailii, Appl. Environ. Microbiol., 70, 6086-91. (Pubitemid 39471857)
13. Mira, N.P., Teixeira, M.C. and Sá-Correia, I. 2010, Adaptive response and tolerance to weak acids in Saccharomyces cerevisiae: a genome-wide view, OMICS, 14, 525-40.
14. Genolevures, C., Souciet, J.L., Dujon, B., et al. 2009, Comparative genomics of protoploid Saccharomycetaceae, Genome Res., 19, 1696-709.
15. Galeote, V., Bigey, F., Devillers, H., Neuveglise, C. and Dequin, S. 2013, Genome sequence of the food spoilage yeast Zygosaccharomyces bailii CLIB 213T, Genome Announcements, 1, e00606-13.
16. Mollapour, M. and Piper, P.W. 2001, The ZbYME2 gene from the food spoilage yeast Zygosaccharomyces bailii confers not only YME2 functions in Saccharomyces cerevisiae, but also the capacity for catabolism of sorbate and benzoate, two major weak organic acid preservatives, Mol. Microbiol., 42, 919-30. (Pubitemid 33078376)
17. Rodrigues, F., Ludovico, P., Sousa, M.J., Steensma, H.Y., Corte-Real, M. and Leão, C. 2003, The spoilage yeast Zygosaccharomyces bailii forms mitotic spores: a screening method for haploidization, Appl. Environ. Microbiol., 69, 649-53. (Pubitemid 36077533)
18. Rodrigues, F., Sousa, M.J., Ludovico, P., Santos, H., Corte- Real, M. and Leão, C. 2012, The fate of acetic acid during glucose co-metabolism by the spoilage yeast Zygosaccharomyces bailii, PLoS ONE, 7, e52402.
19. Rodrigues, F., Zeeman, A.M., Cardoso, H., et al. 2004, Isolation of an acetyl-CoA synthetase gene (ZbACS2) from Zygosaccharomyces bailii, Yeast, 21, 325-31. (Pubitemid 38425530)
20. Dato, L., Sauer, M., Passolunghi, S., Porro, D. and Branduardi, P. 2008, Investigating the multibudded and binucleate phenotype of the yeast Zygosaccharomyces bailii growing on minimal medium, FEMS Yeast Res., 8, 906-15.
21. Guerreiro, J.F., Mira, N.P. and Sá-Correia, I. 2012, Adaptive responseto acetic acid in the highly resistant yeast species Zygosaccharomyces bailii revealed by quantitative proteomics, Proteomics, 12, 2303-18.
22. Sousa, M.J., Miranda, L., Corte-Real, M. and Leao, C. 1996, Transport of acetic acid in Zygosaccharomyces bailii: effects of ethanol and their implications on the resistance of the yeast to acidic environments, Appl. Environ. Microbiol., 62, 3152-7. (Pubitemid 26304094)
23. Ferreira, M.M., Loureiro-Dias, M.C. and Loureiro, V. 1997, Weak acid inhibition of fermentation by Zygosaccharomyces bailii and Saccharomyces cerevisiae, Int. J. Food Microbiol., 36, 145-53. (Pubitemid 27361705)
24. Suh, S.O., Gujjari, P., Beres, C., Beck, B. and Zhou, J. 2013, Proposal of Zygosaccharomyces parabailii sp. nov. and Zygosaccharomyces pseudobailii sp. nov., novel species closely related to Zygosaccharomyces bailii, Int. J. Syst. Evol. Microbiol., 63, 1922-9.
25. Sipiczki, M. 2008, Interspecies hybridization and recombination in Saccharomyces wine yeasts, FEMS Yeast Res., 8, 996-1007.
26. Bakalinsky, A.T. and Snow, R. 1990, The chromosomal constitution of wine strains of Saccharomyces cerevisiae, Yeast, 6, 367-82.
27. Nakao, Y., Kanamori, T., Itoh, T., et al. 2009, Genome sequence of the lager brewing yeast, an interspecies hybrid, DNA Res., 16, 115-29.
28. James, S.A., Bond, C.J., Stratford, M. and Roberts, I.N. 2005, Molecular evidence for the existence of natural hybrids in the genus Zygosaccharomyces, FEMS Yeast Res., 5, 747-55. (Pubitemid 40558922)
29. Gordon, J.L. and Wolfe, K.H. 2008, Recent allopolyploid origin of Zygosaccharomyces rouxii strain ATCC 42981, Yeast, 25, 449-56. (Pubitemid 351997655)
30. Solieri, L., Dakal, T.C., Croce, M.A. and Giudici, P. 2013, Unravelling genomic diversity of Zygosaccharomyces rouxii complex with a link to its life cycle, FEMS Yeast Res., 13, 245-58.
31. Ludovico, P., Sansonetty, F., Silva, M.T. and Corte-Real, M. 2003, Acetic acid induces a programmed cell death process in the food spoilage yeast Zygosaccharomyces bailii, FEMS Yeast Res., 3, 91-6. (Pubitemid 36255469)
32. Fernandes, L., Corte-Real, M., Loureiro, V., Loureiro- Dias, M.C. and Leão, C. 1997, Glucose respiration and fermentation in Zygosaccharomyces bailii and Saccharomyces cerevisiae express different sensitivity patterns to ethanol and acetic acid, Lett. Appl. Microbiol., 25, 249-53. (Pubitemid 27438344)
33. Rodrigues, F., Zeeman, A.M., Alves, C., et al. 2001, Construction of a genomic library of the food spoilage yeast Zygosaccharomyces bailii and isolation of the betaisopropylmalate dehydrogenase gene (ZbLEU2), FEMS Yeast Res., 1, 67-71. (Pubitemid 34442295)
34. Fortuna, M., Sousa, M.J., Corte-Real, M., Leao, C., Salvador, A. and Sansonetty, F. 2001, Cell cycle analysis of yeasts, Curr. Protoc. Cytom., Chapter 11, Unit 13, 11.13.1-11.13.9.
35. Ribeiro, G.F., Corte-Real, M. and Johansson, B. 2006, Characterization of DNA damage in yeast apoptosis induced by hydrogen peroxide, acetic acid, and hyperosmotic shock, Mol. Biol. Cell., 17, 4584-91.
36. Mollapour, M. and Piper, P. 2001, Targeted gene deletion in Zygosaccharomyces bailii, Yeast, 18, 173-86.
37. Morales, L. and Dujon, B. 2012, Evolutionary role of interspecies hybridization and genetic exchanges in yeasts, Microbiol. Mol. Biol. Rev., 76, 721-39.
38. Li, R., Zhu, H., Ruan, J., et al. 2010, De novo assembly of human genomes with massively parallel short read sequencing, Genome Res., 20, 265-72.
39. Louis, V.L., Despons, L., Friedrich, A., et al. 2012, Pichia sorbitophila, an interspecies yeast hybrid, reveals early steps of genome resolution after polyploidization, G3, 2, 299-311.
40. Peris, D., Lopes, C.A., Belloch, C., Querol, A. and Barrio, E. 2012, Comparative genomics among Saccharomyces cerevisiae × Saccharomyces kudriavzevii natural hybrid strains isolated from wine and beer reveals different origins, BMC Genomics, 13, 407.
41. Martin, T., Sherman, D.J. and Durrens, P. 2011, The Genolevures database, C R Biol., 334, 585-9.
42. Cherry, J.M., Hong, E.L., Amundsen, C., et al. 2012, Saccharomyces Genome Database: the genomics resource of budding yeast, Nucleic Acids Res., 40, D700-705.
43. Guldener, U., Munsterkotter, M., Kastenmuller, G., et al. 2005, CYGD: the Comprehensive Yeast Genome Database, Nucleic Acids Res., 33, D364-368. (Pubitemid 40207896)
44. Delcher, A.L., Phillippy, A., Carlton, J. and Salzberg, S.L. 2002, Fast algorithms for large-scale genome alignment and comparison, Nucleic Acids Res., 30, 2478-83. (Pubitemid 34619000)
45. Walter, M.C., Rattei, T., Arnold, R., et al. 2009, PEDANT covers all complete RefSeq genomes, Nucleic Acids Res., 37, D408-411.
46. McKay, S.J., Vergara, I.A. and Stajich, J.E. 2010, Using the Generic Synteny Browser (GBrowse-syn), Curr. Protoc. Bioinformatics, Chapter 9, 9.1-9.12.
47. Keeling, P.J. 2009, Role of horizontal gene transfer in the evolution of photosynthetic eukaryotes and their plastids, Methods Mol. Biol., 532, 501-15.
48. Ruepp, A., Zollner, A.,Maier, D., et al. 2004, The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes, Nucleic Acids Res., 32, 5539-45. (Pubitemid 39545671)
49. Veiga, A., Arrabaca, J.D. and Loureiro-Dias, M.C. 2003, Cyanide-resistant respiration, a very frequent metabolic pathway in yeasts, FEMS Yeast Res., 3, 239-45. (Pubitemid 36411977)
50. Merico, A., Sulo, P., Piskur, J. and Compagno, C. 2007, Fermentative lifestyle in yeasts belonging to the Saccharomyces complex, FEBS J., 274, 976-89. (Pubitemid 46204417)
51. Sousa-Dias, S., Gonçalves, T., Leyva, J.S., Peinado, J.M. and Loureiro-Dias, M.C. 1996, Kinetics and regulation of fructose and glucose transport systems are responsible for fructophily in Zygosaccharomyces bailii, Microbiology, 142, 1733-8. (Pubitemid 26248431)
52. Rolland, F., Winderickx, J. and Thevelein, J.M. 2002, Glucose-sensing and -signalling mechanisms in yeast, FEMS Yeast Res., 2, 183-201. (Pubitemid 34628612)
53. Ronne, H. 1995, Glucose repression in fungi, Trends Genet., 11, 12-7.
54. Belitz, H., Grosch,W. and Schieberle, P. 2009, Food chemistry. Springer: Heidelberg.
55. Novo, M., Bigey, F., Beyne, E., et al. 2009, Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118, Proc. Natl. Acad. Sci. US A, 106, 16333-38.
56. Belloch, C., Orlic, S., Barrio, E. and Querol, A. 2008, Fermentative stress adaptation of hybrids within the Saccharomyces sensu stricto complex, Int. J. Food Microbiol., 122, 188-95.
57. Garcia Sanchez, R., Solodovnikova, N. and Wendland, J. 2012, Breeding of lager yeast with Saccharomyces cerevisiae improves stress resistance and fermentation performance, Yeast, 29, 343-55.
58. Serra, A., Strehaiano, P. and Taillandier, P. 2005, Influence of temperature and pH on Saccharomyces bayanus var. uvarum growth; impact of a wine yeast interspecific hybridization on these parameters, Int. J. Food Microbiol., 104, 257-65. (Pubitemid 41443246)
59. Gasch, A.P., Spellman, P.T., Kao, C.M., et al. 2000, Genomic expression programs in the response of yeast cells to environmental changes, Mol. Biol. Cell., 11, 4241-57.
60. Hillenmeyer, M.E., Fung, E., Wildenhain, J., et al. 2008, The chemical genomic portrait of yeast: uncovering a phenotype for all genes, Science, 320, 362-5. (Pubitemid 351555656)
61. Sá-Correia, I., dos Santos, S.C., Teixeira, M.C., Cabrito, T.R. and Mira, N.P. 2009, Drug: H antiporters in chemical stress response in yeast, Trends Microbiol., 17, 22-31.
62. Paumi, C.M., Chuk, M., Snider, J., Stagljar, I. and Michaelis, S.2009,ABCtransporters in Saccharomyces cerevisiae and their interactors: new technology advances the biology of the ABCC (MRP) subfamily, Microbiol. Mol. Biol. Rev., 73, 577-93.
63. Nikolaou, E., Agrafioti, I., Stumpf, M.,Quinn, J., Stansfield, I. and Brown, A.J. 2009, Phylogenetic diversity of stress signalling pathways in fungi, BMC Evol. Biol., 9, 44.