Microbial diversity and metabolite composition of Belgian red-brown acidic ales

International Journal of Food Microbiology

Volumn 221, Issue , 2016, Pages 1-11

  Snauwaert, Isabel ^a   Roels, Sanne P ^b   Van Nieuwerburg, Filip ^b   Van Landschoot, Anita ^b   De Vuyst, Luc ^c   Vandamme, Peter ^a  

^a GHENT UNIVERSITY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

Author keywords

454 pyrosequecing; Beer; Metabolite target analysis; Microbial diversity analysis

Indexed keywords

ACETIC ACID; ACETIC ACID ETHYL ESTER; ALCOHOL; ETHYL HEXANOATE; ETHYL OCTANOATE; HEXANOIC ACID DERIVATIVE; INTERNAL TRANSCRIBED SPACER; ISOPENTYL ACETATE; LACTIC ACID; OCTANOIC ACID DERIVATIVE; RNA 16S; UNCLASSIFIED DRUG; RIBOSOMAL SPACER DNA;

ACETOBACTER; ACETOBACTER PASTEURIANUS; AROMA; ARTICLE; BEER; BELGIAN RED BROWN ACIDIC ALES; CANDIDA; DEKKERA; DEKKERA BRUXELLENSIS; FUNGAL COMMUNITY; LACTOBACILLUS; METABOLITE; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; PEDIOCOCCUS; PEDIOCOCCUS DAMNOSUS.; PYROSEQUENCING; ANALYSIS; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; BELGIUM; BIODIVERSITY; FERMENTATION; FOOD CONTROL; GENETICS; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; YEAST;

BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BEER; BELGIUM; BIODIVERSITY; DNA, RIBOSOMAL SPACER; ETHANOL; FERMENTATION; FOOD MICROBIOLOGY; RNA, RIBOSOMAL, 16S; YEASTS;

EID: 84954565438     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2015.12.009     Document Type: Article

References (55)

1. Abbott D.A., Hynes S.H., Ingledew W.M. Growth rates of Dekkera/Brettanomyces yeasts hinder their ability to compete with Saccharomyces cerevisiae in batch corn mash fermentations. Appl. Microbiol. Biotechnol. 2005, 66:641-647.
2. Begerow D., Nilsson H., Unterseher M., Maier W. Current state and perspectives of fungal DNA barcoding and rapid identification procedures. Appl. Microbiol. Biotechnol. 2010, 87:99-108.
3. Berry D., Mahfoudh K.B., Wagner M., Loy A. Barcoded primers used in multiplex amplicon pyrosequencing bias amplification. Appl. Environ. Microbiol. 2011, 77:7846-7849.
4. Bokulich N.A., Bamforth C.W. The microbiology of malting and brewing. Microbiol. Mol. Biol. Rev. 2013, 77:157-172.
5. Bokulich N.A., Mills D.A. Next-generation approaches to the microbial ecology of food fermentations. BMB Rep. 2012, 45:377-389.
6. Bokulich N.A., Bamforth C.W., Mills D.A. Brewhouse-resident microbiota are responsible for multi-stage fermentation of American coolship ale. PLoS One 2012, 7:e35507.
7. Cleenwerck I., De Vos P., De Vuyst L. Phylogeny and differentiation of species of the genus Gluconacetobacter and related taxa based on multilocus sequence analyses of housekeeping genes and reclassification of Acetobacter xylinus subsp. sucrofermentans as Gluconacetobacter sucrofermentans (Toyosaki et al. 1996) sp. nov., comb. nov. Int. J. Syst. Evol. Microbiol. 2010, 60:2277-2283.
8. Crous P.W., Gams W., Stalpers J.A., Robert V., Stegehuis G. MycoBank: an online initiative to launch mycology into the 21st century. Stud. Mycol. 2004, 50:19-22.
9. De Bruyne K., Franz C.M.A.P., Vancanneyt M., Schillinger U., Mozzi F., de Valdez G.F., De Vuyst L., Vandamme P. Pediococcus argentinicus sp. nov. from Argentinean fermented wheat flour and identification of Pediococcus species by pheS, rpoA and atpA sequence analysis. Int. J. Syst. Evol. Microbiol. 2008, 58:2909-2916.
10. Dickie I.A. Insidious effects of sequencing errors on perceived diversity in molecular surveys. New Phytol. 2010, 188:916-918.
11. Gardes M., Bruns T.D. ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Mol. Ecol. 1993, 2:113-118.
12. Gevers D., Huys G., Swings J. Applicability of rep-PCR fingerprinting for identification of Lactobacillus species. FEMS Microbiol. Lett. 2001, 205:31-36.
13. Ghyselinck J., Van Hoorde K., Hoste B., Heylen K., De Vos P. Evaluation of MALDI-TOF MS as a tool for high-throughput dereplication. J. Microbiol. Methods 2011, 86:327-336.
14. Hartmann M., Howes C.G., Abarenkov K., Mohn W.W., Nilsson R.H. V-Xtractor: an open-source, high-throughput software tool to identify and extract hypervariable regions of small subunit (16S/18S) ribosomal RNA gene sequences. J. Microbiol. Methods 2010, 83:250-253.
15. Holzapfel W., Franz C.A.P., Ludwig W., Back W., Dicks L.T. The genera Pediococcus and Tetragenococcus. The Prokaryotes 2006, 229-266. Springer, US. M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, E. Stackebrandt (Eds.).
16. Huse S., Huber J., Morrison H., Sogin M., Welch D. Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol. 2007, 8:R143.
17. Janssens M., Myter N., De Vuyst L., Leroy F. Species diversity and metabolic impact of the microbiota are low in spontaneously acidified Belgian sausages with an added starter culture of Staphylococcus carnosus. Food Microbiol. 2012, 29:167-177.
18. Kunin V., Engelbrektson A., Ochman H., Hugenholtz P. Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ. Microbiol. 2010, 12:118-123.
19. Kurtzman C.P., Robnett C.J. Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie Van Leeuwenhoek 1998, 73:331-371.
20. Licker J., Acree T., Henick-Kling T. What is "brett" (Brettanomyces) flavor?: a preliminary investigation. ACS Symposium Series 1998, 96-115. ACS Publications.
21. Lodolo E.J., Kock J.L.F., Axcell B.C., Brooks M. The yeast Saccharomyces cerevisiae-the main character in beer brewing. FEMS Yeast Res. 2008, 8:1018-1036.
22. Lozupone C.A., Hamady M., Kelley S.T., Knight R. Quantitative and qualitative β diversity measures lead to different insights into factors that structure microbial communities. Appl. Environ. Microbiol. 2007, 73:1576-1585.
23. Lozupone C., Lladser M.E., Knights D., Stombaugh J., Knight R. UniFrac: an effective distance metric for microbial community comparison. ISME J. 2011, 5:169-172.
24. Martens H. Microbiology and Biochemistry of the Acid Ales of Roeselare 1996, K.U.Leuven. Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen, Leuven.
25. Martens H. Microbiology and Biochemistry of the Acid Ales of Roeselare 1996, 294. (Dissertationes de Agricultura (Belgium)), Katholieke Universiteit Leuven, Leuven.
26. Martens H., Iserentant D., Verachtert H. Microbiological aspects of a mixed yeast-bacterial fermentation in the production of a special Belgian acidic ale. J. Inst. Brew. 1997, 103:85-91.
27. Naser S.M., Dawyndt P., Hoste B., Gevers D., Vandemeulebroecke K., Cleenwerck I., Vancanneyt M., Swings J. Identification of lactobacilli by pheS and rpoA gene sequence analyses. Int. J. Syst. Evol. Microbiol. 2007, 57:2777-2789.
28. Naser S.M., Thompson F.L., Hoste B., Gevers D., Dawyndt P., Vancanneyt M., Swings J. Application of multilocus sequence analysis (MLSA) for rapid identification of Enterococcus species based on rpoA and pheS genes. Microbiology 2005, 151:2141-2150.
29. Nilsson R.H., Veldre V., Hartmann M., Unterseher M., Amend A., Bergsten J., Kristiansson E., Ryberg M., Jumpponen A., Abarenkov K. An open source software package for automated extraction of ITS1 and ITS2 from fungal ITS sequences for use in high-throughput community assays and molecular ecology. Fungal Ecol. 2010, 3:284-287.
30. Papalexandratou Z., Lefeber T., Bahrim B., Lee O.S., Daniel H.-M., De Vuyst L. Hanseniaspora opuntiae, Saccharomyces cerevisiae, Lactobacillus fermentum, and Acetobacter pasteurianus predominate during well-performed Malaysian cocoa bean box fermentations, underlining the importance of these microbial species for a successful cocoa bean fermentation process. Food Microbiol. 2013, 35:73-85.
31. Pires E., Teixeira J., Brányik T., Vicente A. Yeast: the soul of beer's aroma-a review of flavour-active esters and higher alcohols produced by the brewing yeast. Appl. Microbiol. Biotechnol. 2014, 98:1937-1949.
32. Quince C., Lanzen A., Davenport R.J., Turnbaugh P.J. Removing noise from pyrosequenced amplicons. BMC Bioinforma. 2011, 12:38.
33. Ravyts F., Vrancken G., D'Hondt K., Vasilopoulos C., De Vuyst L., Leroy F. Kinetics of growth and 3-methyl-1-butanol production by meat-borne, coagulase-negative staphylococci in view of sausage fermentation. Int. J. Food Microbiol. 2009, 134:89-95.
34. Sakamoto K., Konings W.N. Beer spoilage bacteria and hop resistance. Int. J. Food Microbiol. 2003, 89:105-124.
35. Schloss P.D. Evaluating different approaches that test whether microbial communities have the same structure. ISME J. 2008, 2:265-275.
36. Schloss P.D., Gevers D., Westcott S.L. Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 2011, 6:e27310.
37. Seifert K.A. Progress towards DNA barcoding of fungi. Mol. Ecol. Resour. 2009, 9:83-89.
38. Shanta Kumara H.M.C., Verachtert H. Identification of lambic superattenuating micro-organisms by the use of selective antibiotics. J. Inst. Brew. 1991, 97:181-185.
39. Smith M.T., Yamazaki M., Poot G. Dekkera, Brettanomyces and Eeniella: electrophoretic comparison of enzymes and DNA-DNA homology. Yeast 1990, 6:299-310.
40. Snauwaert I., Hoste B., De Bruyne K., Peeters K., De Vuyst L., Willems A., Vandamme P. Carnobacterium iners sp. nov., a psychrophilic, lactic acid-producing bacterium from the littoral zone of an Antarctic pond. Int. J. Syst. Evol. Microbiol. 2013, 63:1370-1375.
41. Snauwaert I., Papalexandratou Z., De Vuyst L., Vandamme P. Characterization of strains of Weissella fabalis sp. nov. and Fructobacillus tropaeoli from spontaneous cocoa bean fermentations. Int. J. Syst. Evol. Microbiol. 2013, 63:1709-1716.
42. Spaepen M., Verachtert H. Esterase activity in the genus Brettanomyces. J. Inst. Brew. 1982, 88:11-17.
43. Spaepen M., Van Oevelen D., Verachtert H. Fatty acids and esters produced during the spontaneous fermentation of lambic and gueuze. J. Inst. Brew. 1978, 84:278-282.
44. Spaepen M., Van Oevelen D., Verachtert H. Higher fatty acid (HFA) and HFA-ester content of spontaneously fermented Belgian beers and evaluation of their analytical determination. Brauwissenschaft 1979, 32:S1-S6.
45. Spitaels F., Li L., Wieme A., Balzarini T., Cleenwerck I., Van Landschoot A., De Vuyst L., Vandamme P. Acetobacter lambici sp. nov., isolated from fermenting lambic beer. Int. J. Syst. Evol. Microbiol. 2014, 64:1083-1089.
46. Spitaels F., Wieme A.D., Janssens M., Aerts M., Daniel H.-M., Van Landschoot A., De Vuyst L., Vandamme P. The microbial diversity of traditional spontaneously fermented lambic beer. PLoS One 2014, 9:e95384.
47. Spitaels F., Wieme A.D., Janssens M., Aerts M., Van Landschoot A., De Vuyst L., Vandamme P. The microbial diversity of an industrially produced lambic beer shares members of a traditionally produced one and reveals a core microbiota for lambic beer fermentation. Food Microbiol. 2015, 49:23-32.
48. Suárez R., Suárez-Lepe J., Morata A., Calderón F. The production of ethylphenols in wine by yeasts of the genera Brettanomyces and Dekkera: a review. Food Chem. 2007, 102:10-21.
49. Van Oevelen D., L'Escaille F., Verachtert H. Synthesis of aroma components during the spontaneous fermentation of lambic and gueuze. J. Inst. Brew. 1976, 82:322-326.
50. Verachtert H., Derdelinckx G. Acidic beers: enjoyable reminiscences of the past. Cerevisia 2005, 30:38-47.
51. Verachtert H., Iserentant D. Properties of Belgian acid beers and their microflora. Part I. The production of gueuze and related refreshing acid beers. Cerevisia 1995, 20:37-41.
52. Verstrepen K.J., Derdelinckx G., Dufour J.P., Winderickx J., Thevelein J.M., Pretorius I.S., Delvaux F.R. Flavor-active esters: adding fruitiness to beer. J. Biosci. Bioeng. 2003, 96:110-118.
53. Wang X., Eijkemans M.J.C., Wallinga J., Biesbroek G., Trzciński K., Sanders E.A.M., Bogaert D. Multivariate approach for studying interactions between environmental variables and microbial communities. PLoS One 2012, 7:e50267.
54. Weiss S., Samson F., Navarro D., Casaregola S. YeastIP: a database for identification and phylogeny of Saccharomycotina yeasts. FEMS Yeast Res. 2013, 13:117-125.
55. White T., Bruns T., Lee S., Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications 1990, 315-322. Academic Press. M. Innis, D. Gelfand, J. Shinsky, T. White (Eds.).