{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T23:22:47Z","timestamp":1790378567632,"version":"4.1.0"},"reference-count":41,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2020,4,13]],"date-time":"2020-04-13T00:00:00Z","timestamp":1586736000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002941","name":"Departamento de Investigaciones Cient\u00edficas y Tecnol\u00f3gicas, Universidad de Santiago de Chile","doi-asserted-by":"publisher","award":["081871GM POSTDOC"],"award-info":[{"award-number":["081871GM POSTDOC"]}],"id":[{"id":"10.13039\/501100002941","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Brettanomyces bruxellensis is regarded as the main spoilage microorganism in the wine industry, owing to its production of off-flavours. It is difficult to eradicate owing to its high tolerance of adverse environmental conditions, such as low nutrient availability, low pH, and high levels of ethanol and SO2. In this study, the production of volatile phenols and the growth kinetics of isolates from various regions of Chile were evaluated under stressful conditions. Through randomly amplified polymorphic DNA (RAPD) analysis, 15 strains were identified. These were grown in the presence of p-coumaric acid, a natural antimicrobial and the main precursor of off-flavours, and molecular sulfur dioxide (mSO2), an antimicrobial synthetic used in the wine industry. When both compounds were used simultaneously, there were clear signs of an improvement in the fitness of most of the isolates, which showed an antagonistic interaction in which p-coumaric acid mitigates the effects of SO2. Fourteen strains were able to produce 4-vinylphenol, which showed signs of phenylacrylic acid decarboxylase activity, and most of them produced 4-ethylphenol as a result of active vinylphenol reductase. These results demonstrate for the first time the serious implications of using p-coumaric acid, not only for the production of off-flavours, but also for its protective action against the toxic effects of SO2.<\/jats:p>","DOI":"10.3390\/microorganisms8040557","type":"journal-article","created":{"date-parts":[[2020,4,14]],"date-time":"2020-04-14T03:10:01Z","timestamp":1586833801000},"page":"557","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Biodiversity among Brettanomyces bruxellensis Strains Isolated from Different Wine Regions of Chile: Key Factors Revealed about Its Tolerance to Sulphite"],"prefix":"10.3390","volume":"8","author":[{"given":"Camila","family":"G-Poblete","sequence":"first","affiliation":[{"name":"Departamento de Ciencia y Tecnolog\u00eda de los Alimentos, Facultad Tecnol\u00f3gica, Universidad de Santiago de Chile, Santiago 9170020, Chile"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Irina Charlot","family":"Pe\u00f1a-Moreno","sequence":"additional","affiliation":[{"name":"Department of Genetics, Biosciences Center, Universidade Federal de Pernambuco, Recife 50670-901, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9727-0300","authenticated-orcid":false,"suffix":"Jr.","given":"Marcos Antonio","family":"de Morais","sequence":"additional","affiliation":[{"name":"Department of Genetics, Biosciences Center, Universidade Federal de Pernambuco, Recife 50670-901, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sandra","family":"Moreira","sequence":"additional","affiliation":[{"name":"Departamento de Ciencia y Tecnolog\u00eda de los Alimentos, Facultad Tecnol\u00f3gica, Universidad de Santiago de Chile, Santiago 9170020, Chile"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mar\u00eda Ang\u00e9lica","family":"Ganga","sequence":"additional","affiliation":[{"name":"Departamento de Ciencia y Tecnolog\u00eda de los Alimentos, Facultad Tecnol\u00f3gica, Universidad de Santiago de Chile, Santiago 9170020, Chile"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,4,13]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1474","DOI":"10.1016\/j.lwt.2010.06.010","article-title":"The challenge of Brettanomyces in wine","volume":"43","author":"Wedral","year":"2010","journal-title":"LWT Food Sci. Technol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1128\/EC.00338-06","article-title":"Genome survey sequencing of the wine spoilage yeast Dekkera (Brettanomyces) bruxellensis","volume":"6","author":"Woolfit","year":"2007","journal-title":"Eukaryot. Cell"},{"key":"ref_3","unstructured":"Preedy, V. (2015). Antioxidant Properties of Hydroxycinnamic Acid Derivatives: A Focus on Biochemistry, Physicochemical Parameters, Reactive Species, and Biomolecular Interactions. Coffee in Health and Disease Prevention, Academic Press. [1st ed.]."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1088","DOI":"10.1016\/j.lwt.2014.06.006","article-title":"The effects of extracellular pH and hydroxycinnamic acids influence the intracellular pH of Brettanomyces bruxellensis DSM 7001","volume":"59","author":"Campolongo","year":"2014","journal-title":"LWT Food Sci. Technol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.foodcont.2005.08.010","article-title":"Antibacterial effect of phenolic compounds from different wines","volume":"18","author":"Vaquero","year":"2007","journal-title":"Food Control"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1016\/j.fm.2012.06.004","article-title":"Hydroxycinnamic acid decarboxylase activity of Brettanomyces bruxellensis involved in volatile phenol production: Relationship with cell viability","volume":"32","author":"Laforgue","year":"2012","journal-title":"Food Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/j.foodcont.2014.03.041","article-title":"Identification of the Dekkera bruxellensis phenolic acid decarboxylase (PAD) gene responsible for wine spoilage","volume":"45","author":"Godoy","year":"2014","journal-title":"Food Control."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1016\/j.foodchem.2007.08.008","article-title":"Formation of 4-vinyl and 4-ethyl derivatives from hydroxycinnamic acids: Occurrence of volatile phenolic flavour compounds in beer and distribution of Pad1-activity among brewing yeasts","volume":"107","author":"Vanbeneden","year":"2008","journal-title":"Food Chem."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1111\/j.1574-6968.1995.tb07374.x","article-title":"The biotransformation of simple phenolic compounds by Brettanomyces anomalus","volume":"125","author":"Edlin","year":"1995","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1016\/j.ijfoodmicro.2010.07.022","article-title":"Sulphur dioxide affects culturability and volatile phenol production by Brettanomyces\/Dekkera bruxellensis","volume":"143","author":"Agnolucci","year":"2010","journal-title":"Int. J. Food Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1450","DOI":"10.1111\/j.1365-2672.2009.04561.x","article-title":"Brettanomyces bruxellensis evolution and volatile phenols production in red wines during storage in bottles","volume":"108","author":"Coulon","year":"2010","journal-title":"J. Appl. Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"438","DOI":"10.1016\/j.fm.2011.12.020","article-title":"Characterization of the \u201cviable but nonculturable\u201d (VBNC) state in the wine spoilage yeast Brettanomyces","volume":"30","author":"Serpaggi","year":"2012","journal-title":"Food Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Rib\u00e9reau-Gayon, P., Glories, Y., Maujean, A., and Dubourdieu, D. (2006). The Chemistry of Wine-Stabilization and Treatments. Handbook of Enology, Wiley. [2nd ed.].","DOI":"10.1002\/0470010398"},{"key":"ref_14","unstructured":"Morata, A. (2018). Red Wine Technology, Academic Press. [1st ed.]."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/0027-5107(90)90016-W","article-title":"Autoxidation and mutagenicity of sodium bisulfite","volume":"228","author":"Pagano","year":"1990","journal-title":"Mutat. Res. Fundam. Mol. Mech. Mutagen."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1099\/00207713-49-1-329","article-title":"Identification of yeasts by RFLP analysis of the 5.8 S rRNA gene and the two ribosomal internal transcribed spacers","volume":"49","author":"Belloch","year":"1999","journal-title":"Int. J. Syst. E Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.ejbt.2016.07.005","article-title":"Comparative proteome analysis of Brettanomyces bruxellensis under hydroxycinnamic acid growth","volume":"23","author":"Carmona","year":"2016","journal-title":"Electron. J. Biotechnol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1260","DOI":"10.3389\/fmicb.2018.01260","article-title":"Molecular diagnosis of Brettanomyces bruxellensis sulfur dioxide sensitivity through genotype specific method","volume":"9","author":"Avramova","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1016\/j.foodchem.2008.07.064","article-title":"A comparative study on the phenolic acids identified and quantified in dry beans using HPLC as affected by different extraction and hydrolysis methods","volume":"113","author":"Ross","year":"2009","journal-title":"Food Chem."},{"key":"ref_20","first-page":"155","article-title":"Diversidad gen\u00e9tica de una colecci\u00f3n de yuca a trav\u00e9s de marcadores moleculares RAPDs","volume":"53","author":"Zambrano","year":"2003","journal-title":"Agron. Trop."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.ijfoodmicro.2005.05.014","article-title":"Molecular typing of the yeast species Dekkera bruxellensis and Pichia guilliermondii recovered from wine related sources","volume":"106","author":"Martorell","year":"2006","journal-title":"Int. J. Food Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1016\/j.ijfoodmicro.2009.01.025","article-title":"Genetic diversity and physiological traits of Brettanomyces bruxellensis strains isolated from Tuscan Sangiovese wines","volume":"130","author":"Agnolucci","year":"2009","journal-title":"Int. J. Food Microbiol."},{"key":"ref_23","first-page":"555","article-title":"Development of a molecular method for the typing of Brettanomyces bruxellensis (Dekkera bruxellensis) at the strain level","volume":"102","year":"2007","journal-title":"J. Appl. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1006\/fmic.1998.0217","article-title":"Discrimination of Brettanomyces\/Dekkera yeast isolates from wine by using various DNA finger-printing methods","volume":"16","author":"Mitrakul","year":"1999","journal-title":"Food Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"2185","DOI":"10.1111\/j.1365-2672.2007.03493.x","article-title":"High degree of correlation between molecular polymorphism and geographic origin of wine yeast strains","volume":"103","author":"Cosgaya","year":"2007","journal-title":"J. Appl. Microbiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1111\/j.1472-765X.2009.02556.x","article-title":"Study of the coumarate decarboxylase and vinylphenol reductase activities of Dekkera bruxellensis (anamorph Brettanomyces bruxellensis) isolates","volume":"48","author":"Godoy","year":"2009","journal-title":"Lett. Appl. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1007\/s10482-016-0793-3","article-title":"Identification of a second PAD1 in Brettanomyces bruxellensis LAMAP2480","volume":"110","author":"Godoy","year":"2017","journal-title":"Antonie Van Leeuwenhoek"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1016\/j.fm.2008.10.011","article-title":"Molecular identification of Brettanomyces bruxellensis strains isolated from red wines and volatile phenol production","volume":"26","author":"Oelofse","year":"2009","journal-title":"Food Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1111\/1541-4337.12422","article-title":"Alternative methods to SO2 for microbiological stabilization of wine","volume":"18","author":"Lisanti","year":"2019","journal-title":"Compr. Rev. Food Sci. Food Saf."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1016\/j.ijfoodmicro.2007.11.020","article-title":"Survival patterns of Dekkera bruxellensis in wines and inhibitory effect of sulphur dioxide","volume":"121","author":"Barata","year":"2008","journal-title":"Int. J. Food Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1016\/j.foodres.2016.09.019","article-title":"Efficiency of population-dependent sulfite against Brettanomyces bruxellensis in red wine","volume":"89","author":"Longin","year":"2016","journal-title":"Food Res. Int."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Morgan, S.C., Haggerty, J.J., Johnston, B., Jiranek, V., and Durall, D.M. (2019). Response to Sulfur Dioxide Addition by Two Commercial Saccharomyces cerevisiae Strains. Fermentation, 5.","DOI":"10.3390\/fermentation5030069"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"e02429-18","DOI":"10.1128\/AEM.02429-18","article-title":"Brettanomyces bruxellensis SSU1 haplotypes confer different levels of sulfite tolerance when expressed in a Saccharomyces cerevisiae SSU1 null mutant","volume":"85","author":"Varela","year":"2019","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.ijfoodmicro.2016.08.040","article-title":"Comparative morphological characteristics of three Brettanomyces bruxellensis wine strains in the presence\/absence of sulfur dioxide","volume":"238","author":"Louw","year":"2016","journal-title":"Int. J. Food Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"139","DOI":"10.5344\/ajev.2006.57.2.139","article-title":"Genetic and physiological characterization of Brettanomyces bruxellensis strains isolated from wines","volume":"57","author":"Conterno","year":"2006","journal-title":"Am. J. Enol. Viticult."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Curtin, C.D., Borneman, A.R., Chambers, P.J., and Pretorius, I.S. (2012). De-novo assembly and analysis of the heterozygous triploid genome of the wine spoilage yeast Dekkera bruxellensis AWRI1499. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0033840"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Avramova, M., Grbin, P., Borneman, A., Albertin, W., Masneuf-Pomar\u00e8de, I., and Varela, C. (2019). Competition experiments between Brettanomyces bruxellensis strains reveal specific adaptation to sulfur dioxide and complex interactions at intraspecies level. FEMS Yeast Res., 19.","DOI":"10.1093\/femsyr\/foz010"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Zimmer, A., Durand, C., Loira, N., Durrens, P., Sherman, D.J., and Marullo, P. (2014). QTL dissection of lag phase in wine fermentation reveals a new translocation responsible for Saccharomyces cerevisiae adaptation to sulfite. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0086298"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"581","DOI":"10.3390\/foods4040581","article-title":"Analysis of growth inhibition and metabolism of hydroxycinnamic acids by brewing and spoilage strains of Brettanomyces yeast","volume":"4","author":"Lentz","year":"2015","journal-title":"Foods"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1016\/j.ijfoodmicro.2015.04.005","article-title":"Brettanomyces yeasts\u2014From spoilage organisms to valuable contributors to industrial fermentations","volume":"206","author":"Steensels","year":"2015","journal-title":"Int. J. Food Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1016\/j.chembiol.2014.02.012","article-title":"Large-scale identification and analysis of suppressive drug interactions","volume":"21","author":"Cokol","year":"2014","journal-title":"Chem. Biol."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/8\/4\/557\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,13]],"date-time":"2025-10-13T14:08:58Z","timestamp":1760364538000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/8\/4\/557"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,4,13]]},"references-count":41,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2020,4]]}},"alternative-id":["microorganisms8040557"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms8040557","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,4,13]]}}}