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Brettanomyces bruxellensis wine isolates show high geographical dispersal and long persistence in cellars


Autoři: Alice Cibrario aff001;  Marta Avramova aff001;  Maria Dimopoulou aff001;  Maura Magani aff001;  Cécile Miot-Sertier aff001;  Albert Mas aff003;  Maria C. Portillo aff003;  Patricia Ballestra aff001;  Warren Albertin aff001;  Isabelle Masneuf-Pomarede aff001;  Marguerite Dols-Lafargue aff001
Působiště autorů: Univ. Bordeaux, ISVV, Unité de recherche Œnologie EA 4577, USC 1366 INRA, Bordeaux INP, Villenave d’Ornon, France aff001;  Department of Food Science and Technology, Faculty of Agriculture, Forestry and Natural Environments, Aristotle University of Thessaloniki, Thessaloniki, Greece aff002;  Biotecnología Enológica. Dept. Bioquímica i Biotecnologia, Facultat d‘Enologia. Universitat Rovira i Virgili. C/ Marcel·lí Domingo, Tarragona, Spain aff003;  ENSCBP, Bordeaux INP, Pessac, France aff004;  Bordeaux Sciences Agro, Gradignan, France aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222749

Souhrn

Brettanomyces bruxellensis is the main wine spoiler yeast all over the world, yet the structure of the populations associated with winemaking remains elusive. In this work, we considered 1411 wine isolates from 21 countries that were genotyped using twelve microsatellite markers. We confirmed that B. bruxellensis isolates from wine environments show high genetic diversity, with 58 and 42% of putative triploid and diploid individuals respectively distributed in 5 main genetic groups. The distribution in the genetic groups varied greatly depending on the country and/or the wine-producing region. However, the two possible triploid wine groups showing sulfite resistance/tolerance were identified in almost all regions/countries. Genetically identical isolates were also identified. The analysis of these clone groups revealed that a given genotype could be isolated repeatedly in the same winery over decades, demonstrating unsuspected persistence ability. Besides cellar residency, a great geographic dispersal was also evidenced, with some genotypes isolated in wines from different continents. Finally, the study of old isolates and/or isolates from old vintages revealed that only the diploid groups were identified prior 1990 vintages. The putative triploid groups were identified in subsequent vintages, and their proportion has increased steadily these last decades, suggesting adaptation to winemaking practices such as sulfite use. A possible evolutionary scenario explaining these results is discussed.

Klíčová slova:

Phylogenetic analysis – Phylogeography – Population genetics – Triploidy – Wine – Yeast – Sulfites


Zdroje

1. Gerbaux V, Jeudy S, Monamy C. Étude des phénols volatils dans les vins de Pinot noir en Bourgogne. Bulletin de l'OIV. 2000:581–99.

2. Conterno L, Joseph CML, Arvik TJ, Henick-Kling T, Bisson LF. Genetic and Physiological Characterization of Brettanomyces bruxellensis Strains Isolated from Wines. AJEV. 2006;57(2):139–47.

3. Chatonnet P, Dubourdieu D, Boidron J-n, Pons M. The origin of ethylphenols in wines. JSFA. 1992;60(2):165–78. doi: 10.1002/jsfa.2740600205

4. Romano A, Perello MC, Lonvaud-Funel A, Sicard G, de Revel G. Sensory and analytical re-evaluation of "Brett character". Food Chemistry. 2009;114(1):15–9. doi: 10.1016/j.foodchem.2008.09.006 ISI:000263216000003.

5. Tempere S, Schaaper MH, Cuzange E, de Lescar R, de Revel G, Sicard G. The olfactory masking effect of ethylphenols: Characterization and elucidation of its origin. Food Quality and Preference. 2016;50:135–44. doi: 10.1016/j.foodqual.2016.02.004

6. Lattey KA, Bramley BR, Francis IL. Consumer acceptability, sensory properties and expert quality judgements of Australian Cabernet Sauvignon and Shiraz wines. Australian Journal of Grape and Wine Research. 2010;16(1):189–202. doi: 10.1111/j.1755-0238.2009.00069.x

7. Agnolucci M, Rea F, Sbrana C, Cristani C, Fracassetti D, Tirelli A, et al. Sulphur dioxide affects culturability and volatile phenol production by Brettanomyces/Dekkera bruxellensis. International Journal of Food Microbiology. 2010;143(1):76–80. doi: 10.1016/j.ijfoodmicro.2010.07.022 20705352

8. Campolongo S, Rantsiou K, Giordano M, Gerbi V, Cocolin L. Prevalence and Biodiversity of Brettanomyces bruxellensis in Wine from Northwestern Italy. Am J Enol Vitic. 2010;61(4):486–91. doi: 10.5344/ajev.2010.10034

9. Dias L, Pereira-da-Silva S, Tavares M, Malfeito-Ferreira M, Loureiro V. Factors affecting the production of 4-ethylphenol by the yeast Dekkera bruxellensis in enological conditions. Food Microbiology. 2003;20(4):377–84. doi: 10.1016/S0740-0020(03)00023-6 ISI:000182882900001.

10. Romano A, Perello MC, Revel Gd, Lonvaud-Funel A. Growth and volatile compound production by Brettanomyces/Dekkera bruxellensis in red wine. Journal of Applied Microbiology. 2008;104(6):1577–85. doi: 10.1111/j.1365-2672.2007.03693.x 18194246

11. Barata A, Caldeira J, Botelheiro R, Pagliara D, Malfeito-Ferreira M, Loureiro V. Survival patterns of Dekkera bruxellensis in wines and inhibitory effect of sulphur dioxide. Int J Food Microbiol. 2008;121(2):201–7. doi: 10.1016/j.ijfoodmicro.2007.11.020 18077036.

12. Berbegal C, Garofalo C, Russo P, Pati S, Capozzi V, Spano G. Use of Autochthonous Yeasts and Bacteria in Order to Control Brettanomyces bruxellensis in Wine. Fermentation. 2017;3(4):65. doi: 10.3390/fermentation3040065

13. de Barros Pita W, Tiukova I, Leite FCB, Passoth V, Simões DA, de Morais MA. The influence of nitrate on the physiology of the yeast Dekkera bruxellensis grown under oxygen limitation. Yeast. 2013;30(3):111–7. doi: 10.1002/yea.2945 23440690

14. Moktaduzzaman M, Galafassi S, Capusoni C, Vigentini I, Ling Z, Piskur J, et al. Galactose utilization sheds new light on sugar metabolism in the sequenced strain Dekkera bruxellensis CBS 2499. FEMS Yeast Res. 2015;15(2). doi: 10.1093/femsyr/fou009 25673757.

15. Renouf V, Falcou M, Miot-Sertier C, Perello MC, De Revel G, Lonvaud-Funel A. Interactions between Brettanomyces bruxellensis and other yeast species during the initial stages of winemaking. J Appl Microbiol. 2006;100(6):1208–19. doi: 10.1111/j.1365-2672.2006.02959.x 16696668

16. Capozzi V, Di Toro MR, Grieco F, Michelotti V, Salma M, Lamontanara A, et al. Viable But Not Culturable (VBNC) state of Brettanomyces bruxellensis in wine: New insights on molecular basis of VBNC behaviour using a transcriptomic approach. Food Microbiol. 2016;59:196–204. doi: 10.1016/j.fm.2016.06.007 27375260.

17. Serpaggi V, Remize F, Recorbet G, Gaudot-Dumas E, Sequeira-Le Grand A, Alexandre H. Characterization of the "viable but nonculturable" (VBNC) state in the wine spoilage yeast Brettanomyces. Food Microbiol. 2012;30(2):438–47. doi: 10.1016/j.fm.2011.12.020 22365358.

18. Galafassi S, Capusoni C, Moktaduzzaman M, Compagno C. Utilization of nitrate abolishes the "Custers effect" in Dekkera bruxellensis and determines a different pattern of fermentation products. J Ind Microbiol Biotechnol. 2013;40(3–4):297–303. doi: 10.1007/s10295-012-1229-3 23354425.

19. Tubia I, Prasad K, Perez-Lorenzo E, Abadin C, Zumarraga M, Oyanguren I, et al. Beverage spoilage yeast detection methods and control technologies: A review of Brettanomyces. Int J Food Microbiol. 2018;283:65–76. doi: 10.1016/j.ijfoodmicro.2018.06.020 30099997.

20. Mitrakul CM, Henick-Kling T, Egli CM. Discrimination ofBrettanomyces/Dekkerayeast isolates from wine by using various DNA finger-printing methods. Food Microbiology. 1999;16(1):3–14. doi: 10.1006/fmic.1998.0217

21. Curtin CD, Bellon JR, Henschke PA, Godden PW, De Barros Lopes MA. Genetic diversity of Dekkera bruxellensis yeasts isolated from Australian wineries. FEMS Yeast Research. 2007;7(3):471–81. doi: 10.1111/j.1567-1364.2006.00183.x 17233769

22. Miot-Sertier C, Lonvaud-Funel A. Development of a molecular method for the typing of Brettanomyces bruxellensis (Dekkera bruxellensis) at the strain level. Journal of Applied Microbiology. 2007;102(2):555–62. doi: 10.1111/j.1365-2672.2006.03069.x 17241362

23. Di Toro MR, Capozzi V, Beneduce L, Alexandre H, Tristezza M, Durante M, et al. Intraspecific biodiversity and ‘spoilage potential’ of Brettanomyces bruxellensis in Apulian wines. LWT—Food Science and Technology. 2015;60(1):102–8. doi: 10.1016/j.lwt.2014.06.059

24. Oelofse A, Lonvaud-Funel A, du Toit M. Molecular identification of Brettanomyces bruxellensis strains isolated from red wines and volatile phenol production. Food Microbiol. 2009;26(4):377–85. doi: 10.1016/j.fm.2008.10.011 19376458.

25. Vigentini I, De Lorenzis G, Picozzi C, Imazio S, Merico A, Galafassi S, et al. Intraspecific variations of Dekkera/Brettanomyces bruxellensis genome studied by capillary electrophoresis separation of the intron splice site profiles. International Journal of Food Microbiology. 2012;157(1):6–15. doi: 10.1016/j.ijfoodmicro.2012.02.017 22607811

26. Guzzon R, Larcher R, Guarcello R, Francesca N, Settanni L, Moschetti G. Spoilage potential of brettanomyces bruxellensis strains isolated from Italian wines. Food Research International. 2018;105:668–77. doi: 10.1016/j.foodres.2017.11.078 29433261

27. Agnolucci M, Vigentini I, Capurso G, Merico A, Tirelli A, Compagno C, et al. Genetic diversity and physiological traits of Brettanomyces bruxellensis strains isolated from Tuscan Sangiovese wines. International Journal of Food Microbiology. 2009;130(3):238–44. doi: 10.1016/j.ijfoodmicro.2009.01.025 19237217

28. Oro L, Canonico L, Marinelli V, Ciani M, Comitini F. Occurrence of Brettanomyces bruxellensis on Grape Berries and in Related Winemaking Cellar. Front Microbiol. 2019;10:415. doi: 10.3389/fmicb.2019.00415 30899251; PubMed Central PMCID: PMC6416197.

29. Renouf V, Lonvaud-Funel A. Development of an enrichment medium to detect Dekkera/Brettanomyces bruxellensis, a spoilage wine yeast, on the surface of grape berries. Microb Research. 2007;162(2):154–67. doi: 10.1016/j.micres.2006.02.006 16595174

30. Piškur J, Ling Z, Marcet-Houben M, Ishchuk OP, Aerts A, LaButti K, et al. The genome of wine yeast Dekkera bruxellensis provides a tool to explore its food-related properties. Int J Food Microbiol. 2012;157(2):202–9. doi: 10.1016/j.ijfoodmicro.2012.05.008 22663979

31. Curtin CD, Borneman AR, Chambers PJ, Pretorius IS. De-Novo Assembly and Analysis of the Heterozygous Triploid Genome of the Wine Spoilage Yeast Dekkera bruxellensis AWRI1499. PLoS One. 2012;7(3). doi: 10.1371/journal.pone.0033840 ISI:000304489000038. 22470482

32. Fournier T, Gounot JS, Freel K, Cruaud C, Lemainque A, Aury JM, et al. High-Quality de Novo Genome Assembly of the Dekkera bruxellensis Yeast Using Nanopore MinION Sequencing. G3 (Bethesda). 2017;7(10):3243–50. doi: 10.1534/g3.117.300128 28983066; PubMed Central PMCID: PMC5633375.

33. Valdes J, Tapia P, Cepeda V, Varela J, Godoy L, Cubillos FA, et al. Draft genome sequence and transcriptome analysis of the wine spoilage yeast Dekkera bruxellensis LAMAP2480 provides insights into genetic diversity, metabolism and survival. FEMS Microbiol Lett. 2014;361(2):104–6. doi: 10.1111/1574-6968.12630 25328076.

34. Olsen RA, Bunikis I, Tiukova I, Holmberg K, Lotstedt B, Pettersson OV, et al. De novo assembly of Dekkera bruxellensis: a multi technology approach using short and long-read sequencing and optical mapping. GigaScience. 2015;4:56. doi: 10.1186/s13742-015-0094-1 26617983; PubMed Central PMCID: PMC4661999.

35. Borneman AR, Zeppel R, Chambers PJ, Curtin CD. Insights into the Dekkera bruxellensis Genomic Landscape: Comparative Genomics Reveals Variations in Ploidy and Nutrient Utilisation Potential amongst Wine Isolates. PLoS Genet. 2014;10(2):e1004161. doi: 10.1371/journal.pgen.1004161 24550744

36. Crauwels S, Zhu B, Steensels J, Busschaert P, De Samblanx G, Marchal K, et al. Assessing Genetic Diversity among Brettanomyces Yeasts by DNA Fingerprinting and Whole-Genome Sequencing. Applied and Environmental Microbiology. 2014;80(14):4398–413. doi: 10.1128/AEM.00601-14 PMC4068659. 24814796

37. Albertin W, Marullo P, Aigle M, Bourgais A, Bely M, Dillmann C, et al. Evidence for autotetraploidy associated with reproductive isolation in Saccharomyces cerevisiae: towards a new domesticated species. J Evol Biol. 2009;22(11):2157–70. Epub 2009/09/22. doi: 10.1111/j.1420-9101.2009.01828.x 19765175. 19765175

38. Feng B, Yi SV, Zhang M, Zhou X. Development of novel EST-SSR markers for ploidy identification based on de novo transcriptome assembly for Misgurnus anguillicaudatus. PloS one. 2018;13(4):e0195829–e. doi: 10.1371/journal.pone.0195829 29649332.

39. Dalton NJ, Horsburgh GJ, Dawson DA. The characterisation of microsatellite markers reveals tetraploidy in the Greater Water Parsnip, Sium latifolium (Apiaceae). BMC Res Notes. 2017;10(1):204–. doi: 10.1186/s13104-017-2528-6 28606172.

40. Albertin W, Panfili A, Miot-Sertier C, Goulielmakis A, Delcamp A, Salin F, et al. Development of microsatellite markers for the rapid and reliable genotyping of Brettanomyces bruxellensis at strain level. Food Microbiol. 2014;42:188–95. doi: 10.1016/j.fm.2014.03.012 24929736

41. Avramova M, Cibrario A, Peltier E, Coton M, Coton E, Schacherer J, et al. Brettanomyces bruxellensis population survey reveals a diploid-triploid complex structured according to substrate of isolation and geographical distribution. Scientific reports. 2018;8(4136). doi: 10.1038/s41598-018-22580-7 29515178

42. Dimopoulou M, Hatzikamari M, Masneuf-Pomarede I, Albertin W. Sulfur dioxide response of Brettanomyces bruxellensis strains isolated from Greek wine. Food Microbiol. 2019;78:155:63. doi: 10.1016/j.fm.2018.10.013 30497597

43. Avramova M, Vallet-Courbin A, Maupeu J, Masneuf-Pomarède I, Albertin W. Molecular Diagnosis of Brettanomyces bruxellensis’ Sulfur Dioxide Sensitivity Through Genotype Specific Method. Frontiers in Microbiology. 2018;9(1260). doi: 10.3389/fmicb.2018.01260 29942296

44. Avramova M, Varela C, Grbin P, Borneman A, Albertin W, Masneuf-Pomarede I. Competition experiments between Brettanomyces bruxellensis strains reveal specific adaptation to SO2. FEMS Yeast Res. 2019;19(3). doi: 10.1093/femsyr/foz010 30721945

45. Dimopoulou M, Renault M, Dols-Lafargue M, Albertin W, Herry JM, Bellon-Fontaine MN, et al. Microbiological, biochemical, physicochemical surface properties and biofilm forming ability of Brettanomyces bruxellensis. Ann Microbiol. 2019;In press. doi: 10.1101/579144v1

46. Dray S, Dufour A. The ade4 Package: Implementing the Duality Diagram for Ecologists. Journal of Statistical Software. 2007;22(4):1–20. doi: 10.18637/jss.v022.i04

47. Jombart T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics. 2008;24(11):1403–5. doi: 10.1093/bioinformatics/btn129 18397895.

48. Jombart T, Ahmed I. adegenet 1.3–1: new tools for the analysis of genome-wide SNP data. Bioinformatics. 2011;27(21):3070–1. doi: 10.1093/bioinformatics/btr521 21926124; PubMed Central PMCID: PMC3198581.

49. Kamvar ZN, Brooks JC, Grunwald NJ. Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Frontiers in genetics. 2015;6:208. doi: 10.3389/fgene.2015.00208 26113860; PubMed Central PMCID: PMC4462096.

50. Kamvar ZN, Tabima JF, Grunwald NJ. Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ. 2014;2:e281. doi: 10.7717/peerj.281 24688859; PubMed Central PMCID: PMC3961149.

51. Bivand RS, Pebesma E, Gomez-Rubio V. Applied spatial data analysis with R. New York: Springer-Verlag; 2013.

52. Lustrato G, Vigentini I, De Leonardis A, Alfano G, Tirelli A, Foschino R, et al. Inactivation of wine spoilage yeasts Dekkera bruxellensis using low electric current treatment (LEC). Journal of Applied Microbiology. 2010;109(2):594–604. doi: 10.1111/j.1365-2672.2010.04686.x 20148995

53. Buzrul S. High hydrostatic pressure treatment of beer and wine: A review. Innovative Food Science & Emerging Technologies. 2012;13:1–12. doi: 10.1016/j.ifset.2011.10.001

54. Fabrizio V, Vigentini I, Parisi N, Picozzi C, Compagno C, Foschino R. Heat inactivation of wine spoilage yeast Dekkera bruxellensis by hot water treatment. Letters in Applied Microbiology. 2015;61(2):186–91. doi: 10.1111/lam.12444 25989358

55. Borlin M, Venet P, Claisse O, Salin F, Legras JL, Masneuf-Pomarede I. Cellar-associated Saccharomyces cerevisiae population structure revealed high diversity and perennial persistence in Sauternes wine estates. Appl Environ Microbiol. 2016. Epub 2016/03/13. doi: 10.1128/AEM.03627-15 26969698.

56. Joseph CML, Kumar G, Su E, Bisson LF. Adhesion and Biofilm Production by Wine Isolates of Brettanomyces bruxellensis. AJEV. 2007;58(3):373–8.

57. Goddard MR, Anfang N, Tang R, Gardner RC, Jun C. A distinct population of Saccharomyces cerevisiae in New Zealand: evidence for local dispersal by insects and human-aided global dispersal in oak barrels. Environmental Microbiology. 2010;12(1):63–73. doi: 10.1111/j.1462-2920.2009.02035.x 19691498

58. Francesca N, Canale DE, Settanni L, Moschetti G. Dissemination of wine-related yeasts by migratory birds. Environmental microbiology reports. 2012;4(1):105–12. doi: 10.1111/j.1758-2229.2011.00310.x 23757236.

59. Stefanini I, Dapporto L, Legras JL, Calabretta A, Di Paola M, De Filippo C, et al. Role of social wasps in Saccharomyces cerevisiae ecology and evolution. Proc Natl Acad Sci U S A. 2012;109(33):13398–403. Epub 2012/08/01. doi: 10.1073/pnas.1208362109 22847440; PubMed Central PMCID: PMC3421210.

60. Licker JL, Acree TE, Henick-Kling T. What Is "Brett" (Brettanomyces) Flavor?: A Preliminary Investigation. Chemistry of Wine Flavor. ACS Symposium Series. 714: American Chemical Society; 1998. p. 96–115.

61. Bock A, Sparks TH, Estrella N, Menzel A. Climate-Induced Changes in Grapevine Yield and Must Sugar Content in Franconia (Germany) between 1805 and 2010. PLOS ONE. 2013;8(7):e69015. doi: 10.1371/journal.pone.0069015 23894395

62. Gaidos S. Grape expectations: Climate change is already transforming the wine industry. Science News. 2014;185(3):20–4. doi: 10.1002/scin.5591850316

63. Cibrario A, Miot-Sertier C, Paulin M, Bullier B, Riquier L, Perello MC, et al. Brettanomyces bruxellensis phenotypic diversity, tolerance to wine stress and spoilage ability. Submitted to Food Microbiology.

64. Chatonnet P, Boidron JN, Dubourdieu D. Influence des conditions d'élevage et de sulfitage des vins rouges en barriques sur leur teneur en acide acétique et en ethyl-phenols1993. 277–98 p.

65. Curtin C, Borneman A, Zeppel R, Cordente T, Kievit R, Chambers P, et al. AWRI: Staying a step ahead of 'Brett' Wine & Viticulture Journal. 2014;29(5):34–7.

66. Curtin C, Kennedy E, Henschke PA. Genotype-dependent sulphite tolerance of Australian Dekkera (Brettanomyces) bruxellensis wine isolates. Lett Appl Microbiol. 2012;55(1):56–61. doi: 10.1111/j.1472-765X.2012.03257.x 22537453


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