Viable But Not Culturable (VBNC) state of Brettanomyces bruxellensis in wine: New insights on molecular basis of VBNC behaviour using a transcriptomic approach

Food Microbiology

Volumn 59, Issue , 2016, Pages 196-204

  Capozzi, Vittorio ^a   Di Toro, Maria Rosaria ^a   Grieco, Francesco ^b   Michelotti, Vania ^c   Salma, Mohammad ^d   Lamontanara, Antonella ^c   Russo, Pasquale ^a   Orrù, Luigi ^c   Alexandre, Hervé ^d   Spano, Giuseppe ^a  

^a UNIVERSITY OF FOGGIA   (Italy)

^b INSTITUTE OF SCIENCES OF FOOD PRODUCTION   (Italy)

^c ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

^d UNIVERSITÉ DE BOURGOGNE   (France)

Author keywords

Brettanomyces; Spoilage; Sulphite; Transcriptomics; Viable But Not Culturable (VBNC); Wine

Indexed keywords

CULTURE MEDIUM; HEAT SHOCK PROTEIN; PHENOL DERIVATIVE; SULFITE; SULFUR DIOXIDE;

ANALYSIS; BACTERIAL COUNT; BRETTANOMYCES; CARBOHYDRATE METABOLISM; CULTURE MEDIUM; DRUG EFFECTS; FOOD CONTROL; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOMEOSTASIS; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PHYSIOLOGY; PROCEDURES; WINE;

BRETTANOMYCES; CARBOHYDRATE METABOLISM; COLONY COUNT, MICROBIAL; CULTURE MEDIA; FOOD MICROBIOLOGY; GENE EXPRESSION PROFILING; HEAT-SHOCK PROTEINS; HOMEOSTASIS; MICROBIAL VIABILITY; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHENOLS; SULFITES; SULFUR DIOXIDE; WINE;

EID: 84975505064     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2016.06.007     Document Type: Article

References (47)

1. Agnolucci M., Rea F., Sbrana C., Cristani C., Fracassetti D., Tirelli A., Nuti M. Sulphur dioxide affects culturability and volatile phenol production by Brettanomyces/Dekkera bruxellensis. Int. J. Food Microbiol. 2010, 143:76-80. 10.1016/j.ijfoodmicro.2010.07.022.
2. Agnolucci M., Cristani C., Maggini S., Rea F., Cossu A., Tirelli A., Nuti M. Impact of sulphur dioxide on the viability, culturability, and volatile phenol production of Dekkera bruxellensis in wine. Ann. Microbiol. 2013, 64:653-659. 10.1007/s13213-013-0698-6.
3. Albertin W., Panfili A., Miot-Sertier C., Goulielmakis A., Delcamp A., Salin F., Lonvaud-Funel A., Curtin C., Masneuf-Pomarede I. Development of microsatellite markers for the rapid and reliable genotyping of Brettanomyces bruxellensis at strain level. Food Microbiol. 2014, 42:188-195. 10.1016/j.fm.2014.03.012.
4. Anders S., Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010, 11:R106. 10.1186/gb-2010-11-10-r106.
5. Atack J.M., Kelly D.J. Oxidative stress in Campylobacter jejuni: responses, resistance and regulation. Future Microbiol. 2009, 4:677-690. 10.2217/fmb.09.44.
6. Ayrapetyan M., Williams T.C., Oliver J.D. Bridging the gap between viable but non-culturable and antibiotic persistent bacteria. Trends Microbiol. 2015, 23:7-13. 10.1016/j.tim.2014.09.004.
7. Capozzi V., Weidmann S., Fiocco D., Rieu A., Hols P., Guzzo J., Spano G. Inactivation of a small heat shock protein affects cell morphology and membrane fluidity in Lactobacillus plantarum WCFS1. Res. Microbiol. 2011, 162:419-425. 10.1016/j.resmic.2011.02.010.
8. Carvalhais V., França A., Cerca F., Vitorino R., Pier G.B., Vilanova M., Cerca N. Dormancy within Staphylococcus epidermidis biofilms: a transcriptomic analysis by RNA-seq. Appl. Microbiol. Biotechnol. 2014, 98:2585-2596. 10.1007/s00253-014-5548-3.
9. Childs B.C., Bohlscheid J.C., Edwards C.G. Impact of available nitrogen and sugar concentration in musts on alcoholic fermentation and subsequent wine spoilage by Brettanomyces bruxellensis. Food Microbiol. 2015, 46:604-609. 10.1016/j.fm.2014.10.006.
10. Conesa A., Götz S., García-Gómez J.M., Terol J., Talón M., Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21:3674-3676. 10.1093/bioinformatics/bti610.
11. Cuny C., Dukan L., Fraysse L., Ballesteros M., Dukan S. Investigation of the first events leading to loss of culturability during Escherichia coli starvation: future nonculturable bacteria form a subpopulation. J. Bacteriol. 2005, 187:2244-2248. 10.1128/JB.187.7.2244-2248.2005.
12. Curtin C.D., Pretorius I.S. Genomic insights into the evolution of industrial yeast species Brettanomyces bruxellensis. FEMS Yeast Res. 2014, 14:997-1005. 10.1111/1567-1364.12198.
13. Curtin C., Kennedy E., Henschke P.A. Genotype-dependent sulphite tolerance of Australian Dekkera (Brettanomyces) bruxellensis wine isolates. Lett. Appl. Microbiol. 2012, 55:56-61. 10.1111/j.1472-765X.2012.03257.x.
14. Desnues B., Cuny C., Grégori G., Dukan S., Aguilaniu H., Nyström T. Differential oxidative damage and expression of stress defence regulons in culturable and non-culturable Escherichia coli cells. EMBO Rep. 2003, 4:400-404. 10.1038/sj.embor.embor799.
15. Di Toro M.R., Capozzi V., Beneduce L., Alexandre H., Tristezza M., Durante M., Tufariello M., Grieco F., Spano G. Intraspecific biodiversity and "spoilage potential" of Brettanomyces bruxellensis in Apulian wines. LWT - Food Sci. Technol. 2015, 60:102-108. 10.1016/j.lwt.2014.06.059.
16. Divol B., Lonvaud-Funel A. Evidence for viable but nonculturable yeasts in botrytis-affected wine. J. Appl. Microbiol. 2005, 99:85-93. 10.1111/j.1365-2672.2005.02578.x.
17. Du Toit W.J., Pretorius I.S., Lonvaud-Funel A. The effect of sulphur dioxide and oxygen on the viability and culturability of a strain of Acetobacter pasteurianus and a strain of Brettanomyces bruxellensis isolated from wine. J. Appl. Microbiol. 2005, 98:862-871. 10.1111/j.1365-2672.2004.02549.x.
18. Fiocco D., Capozzi V., Gallone A., Hols P., Guzzo J., Weidmann S., Rieu A., Msadek T., Spano G. Characterization of the CtsR stress response regulon in Lactobacillus plantarum. J. Bacteriol. 2010, 196:896-900.
19. Garde-Cerdán T., Lorenzo C., Carot J.M., Jabaloyes J.M., Esteve M.D., Salinas M.R. Statistical differentiation of wines of different geographic origin and aged in barrel according to some volatile components and ethylphenols. Food Chem. 2008, 111:1025-1031. 10.1016/j.foodchem.2008.05.006.
20. González-Arenzana L., Sevenich R., Rauh C., López R., Knorr D., López-Alfaro I. Inactivation of Brettanomyces bruxellensis by high hydrostatic pressure technology. Food Control 2016, 59:188-195. 10.1016/j.foodcont.2015.04.038.
21. Hartl F.U., Bracher A., Hayer-Hartl M. Molecular chaperones in protein folding and proteostasis. Nature 2011, 475:324-332. 10.1038/nature10317.
22. Haslbeck M., Braun N., Stromer T., Richter B., Model N., Weinkauf S., Buchner J. Hsp42 is the general small heat shock protein in the cytosol of Saccharomyces cerevisiae. EMBO J. 2004, 23:638-649. 10.1038/sj.emboj.7600080.
23. Jungwirth H., Kuchler K. Yeast ABC transporters - a tale of sex, stress, drugs and aging. FEBS Lett. 2006, 580:1131-1138. 10.1016/j.febslet.2005.12.050.
24. Laforgue R., Lonvaud-Funel A. Hydroxycinnamic acid decarboxylase activity of Brettanomyces bruxellensis involved in volatile phenol production: relationship with cell viability. Food Microbiol. 2012, 32:230-234. 10.1016/j.fm.2012.06.004.
25. Lamb H.K., Leslie K., Dodds A.L., Nutley M., Cooper A., Johnson C., Thompson P., Stammers D.K., Hawkins A.R. The negative transcriptional regulator NmrA discriminates between oxidized and reduced dinucleotides. J. Biol. Chem. 2003, 278:32107-32114. 10.1074/jbc.M304104200.
26. Li L., Mendis N., Trigui H., Oliver J.D., Faucher S.P. The importance of the viable but non-culturable state in human bacterial pathogens. Front. Microbiol. 2014, 5:258. 10.3389/fmicb.2014.00258.
27. Meng L., Alter T., Aho T., Huehn S. Gene expression profiles of Vibrio parahaemolyticus in viable but non-culturable state. FEMS Microbiol. Ecol. 2015, 91. 10.1093/femsec/fiv035.
28. Millet V., Lonvaud-Funel A. The viable but non-culturable state of wine micro-organisms during storage. Lett. Appl. Microbiol. 2000, 30:136-141.
29. Nardi T., Corich V., Giacomini A., Blondin B. A sulphite-inducible form of the sulphite efflux gene SSU1 in a Saccharomyces cerevisiae wine yeast. Microbiol. Read. Engl. 2010, 156:1686-1696. 10.1099/mic.0.036723-0.
30. Nowakowska J., Oliver J.D. Resistance to environmental stresses by Vibrio vulnificus in the viable but nonculturable state. FEMS Microbiol. Ecol. 2013, 84:213-222. 10.1111/1574-6941.12052.
31. Nyström T. Nonculturable bacteria: programmed survival forms or cells at death's door?. Bioessays 2003, 25:204-211. 10.1002/bies.10233.
32. 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, 26:377-385. 10.1016/j.fm.2008.10.011.
33. Oliver J.D. Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol. Rev. 2010, 34:415-425. 10.1111/j.1574-6976.2009.00200.x.
34. Park H., Hwang Y.-S. Genome-wide transcriptional responses to sulfite in Saccharomyces cerevisiae. J. Microbiol. 2008, 46:542-548. 10.1007/s12275-008-0053-y.
35. Postnikova O.A., Shao J., Mock N.M., Baker C.J., Nemchinov L.G. Gene expression profiling in viable but nonculturable (VBNC) cells of Pseudomonas syringae pv. syringae. Front. Microbiol. 2015, 6:1419. 10.3389/fmicb.2015.01419.
36. Ramamurthy T., Ghosh A., Pazhani G.P., Shinoda S. Current perspectives on viable but non-culturable (VBNC) pathogenic bacteria. Front. Public Health 2014, 2:103. 10.3389/fpubh.2014.00103.
37. Reuter M., Mallett A., Pearson B.M., van Vliet A.H.M. Biofilm formation by Campylobacter jejuni is increased under aerobic conditions. Appl. Environ. Microbiol. 2010, 76:2122-2128. 10.1128/AEM.01878-09.
38. Rodrigues N., Gonçalves G., Pereira-da-Silva S., Malfeito-Ferreira M., Loureiro V. Development and use of a new medium to detect yeasts of the genera Dekkera/Brettanomyces. J. Appl. Microbiol. 2001, 90:588-599.
39. Salma M., Rousseaux S., Sequeira-Le Grand A., Divol B., Alexandre H. Characterization of the viable but nonculturable (VBNC) state in Saccharomyces cerevisiae. PLoS ONE 2013, 8:e77600. 10.1371/journal.pone.0077600.
40. Schmieder R., Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics 2011, btr026. 10.1093/bioinformatics/btr026.
41. 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, 30:438-447. 10.1016/j.fm.2011.12.020.
42. Swiegers J.H., Pretorius I.S. Modulation of volatile sulfur compounds by wine yeast. Appl. Microbiol. Biotechnol. 2007, 74:954-960. 10.1007/s00253-006-0828-1.
43. Usseglio-Tomasset L. Chimie Oenologique. Technique et documentation 1995, Lavoisier, Paris.
44. Vigentini I., Joseph C.M.L., Picozzi C., Foschino R., Bisson L.F. Assessment of the Brettanomyces bruxellensis metabolome during sulphur dioxide exposure. FEMS Yeast Res. 2013, 13:597-608. 10.1111/1567-1364.12060.
45. Wang H.-W., Chung C.-H., Ma T.-Y., Wong H. Roles of alkyl hydroperoxide reductase subunit C (AhpC) in viable but nonculturable Vibrio parahaemolyticus. Appl. Environ. Microbiol. 2013, 79:3734-3743. 10.1128/AEM.00560-13.
46. Young M.D., Wakefield M.J., Smyth G.K., Oshlack A. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. 2010, 11:R14. 10.1186/gb-2010-11-2-r14.
47. Zuehlke J.M., Edwards C.G. Impact of sulfur dioxide and temperature on culturability and viability of Brettanomyces bruxellensis in Wine. J. Food Prot. 2013, 76:2024-2030. 10.4315/0362-028X.JFP-13-243R.