Abstract
To meet consumer demands for fresher and healthier foods, the pasteurization of beer has largely been replaced by membrane filtration methods. Research on beer spoilage caused by hop-resistant bacteria is thus of great interest. In this context, we have isolated a beer-spoilage strain of bacteria from turbid bottled beer treated by membrane filter sterilization, which we identified as Bacillus cereus strain 3012. Strain 3012 was able to produce acids and bioamines, resulting in a change in the flavor profile of the beer. Unlike other known strains of B. cereus, this isolate was resistant to hop compounds present in the beer and was in an evolutionarily stable state in terms of hop resistance. Our results suggest that this hop-resistant B. cereus strain 3012 is a foodborne pathogen with the potential to cause beer-spoilage incidents in the brewing industry.
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References
Back W (1992) Flash pasteurization-membrane filtration. Brauwelt Int 10:42–49
Bokulich NA, Bamforth CW (2013) The microbiology of malting and brewing. Microbiol Mol Biol R 77:157–172
Ceuppens S, Boon N, Uyttendaele M (2013) Diversity of Bacillus cereus group strains is reflected in their broad range of pathogenicity and diverse ecological lifestyles. FEMS Microbiol Ecol 84:433–450
Chen X, Wang M, Yang F, Tang W, Li X (2014) Isolation and characterization of xanthan-degrading Enterobacter sp. nov. LB37 for reducing the viscosity of xanthan in petroleum industry. World J Microbiol Biotechnol 30:1549–1557
Claus D, Berkeley RCW (1986) Genus Bacillus Cohn 1872. In: Sneath PHA, Mair NS, Sharpe ME, Holt JG (eds) Bergey’s manual of systematic bacteriology, vol 2. Williams & Wilkins, Baltimore, pp 1105–1139
Cronin UP, Wilkinson MG (2010) The potential of flow cytometry in the study of Bacillus cereus. J Appl Microbiol 108:1–16
Daifas DP, Smith JP, Blanchfield B, Cadieux B, Sanders G, Austin JW (2003) Effect of ethanol on the growth of Clostridium botulinum. J Food Prot 66:610–617
De Borba BM, Rohrer JS (2007) Determination of biogenic amines in alcoholic beverages by ion chromatography with suppressed conductivity detection and integrated pulsed amperometric detection. J Chromatogr A 115:22–30
De Jonghe V, Coorevits A, De Block J, Van Coillie E, Grijspeerdt K, Herman L, De Vos P, Heyndrickx M (2010) Toxinogenic and spoilage potential of aerobic spore-formers isolated from raw milk. Int J Food Microbiol 136:318–325
Desriac N, Broussolle V, Postollec F, Mathot AG, Sohier D, Coroller L, Leguerinel I (2013) Bacillus cereus cell response upon exposure to acid environment: toward the identification of potential biomarkers. Front Microbiol 4:284
Haakensen M, Ziola B (2008) Identification of novel horA-harbouring bacteria capable of spoiling beer. Can J Microbiol 54:321–325
Jeon SH, Kim NH, Shim MB, Jeon YW, Ahn JH, Lee SH, Hwang IG, Rhee MS (2015) Microbiological diversity and prevalence of spoilage and pathogenic bacteria in commercial fermented alcoholic beverages (beer, fruit wine, refined rice wine, and yakju). J Food Prot 78:812–818
Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36:W5–W9
Kim SA, Park HJ, Lee SH, Hwang IG, Rhee MS (2014) Fate of major foodborne pathogens and Bacillus cereus spores in sterilized and non-sterilized Korean turbid rice wine (Makgeolli). Food Control 39:139–145
Kunze W (2004) Technology brewing and malting, 3rd edn. VLB Berlin, Berlin, pp 53–487
Li H, Li H, Liu X, Chen B (2012) Analysis of volatile flavor compounds in top fermented wheat beer by headspace sampling-gas chromatography. Int J Agric Biol Eng 5(2):67–75
Logan NA (2011) Bacillus and relatives in foodborne illness. J Appl Microbiol 112:417–429
Manzano M, Iacumin L, Vendrame M, Cecchini F, Comi G, Buiatti S (2011) Craft beer microflora identification before and after a cleaning process. J I Brew 117:343–351
Matoulkova D, Kosar K, Slaby M, Sigler K (2012) Occurrence and species distribution of strictly anaerobic bacterium Pectinatus in brewery bottling halls. J Am Soc Brew Chem 70:262–267
Murray RGE, Doetsch RN, Robinow CF (1994) Determinative and cytological light microscopy. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington DC, pp 21–41
Okanlawon BM, Ogunbanwo ST, Okunlola AO (2010) Growth of Bacillus cereus isolated from some traditional condiments under different regimens. Afr J Biotechnol 8:2129–2135
Paradh A, Mitchell W, Hill A (2011) Occurrence of Pectinatus and Megasphaera in the major UK breweries. J I Brew 117:498–506
Pittet V, Morrow K, Ziola B (2011) Ethanol tolerance of lactic acid bacteria, including relevance of the exopolysaccharide gene gtf. J Am Soc Brew Chem 69:57–61
Pittet V, Phister TG, Ziola B (2013) Transcriptome sequence and plasmid copy number analysis of the brewery isolate Pediococcus claussenii ATCC BAA-344T during growth in beer. PLoS One 8(9), e73627
Richards M, Macrae RM (1964) The significance of the use of hops in regard to the biological stability of beer: II. The development of resistance to hop resins by strains of lactobacilli. J Inst Brew 70:484–488
Sakamoto K, Konings WN (2003) Beer spoilage bacteria and hop resistance. Int J Food Microbiol 89:105–124
Shui G, Leong LP (2002) Separation and determination of organic acids and phenolic compounds in fruit juices and drinks by high-performance liquid chromatography. J Chromatogr A 977:89–96
Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington DC, pp 607–654
Steiner E, Becker T, Gastl M (2010) Turbidity and haze formation in beer-insights and overview. J Inst Brew 116:360–368
Suzuki K, Sami M, Kadokura H, Nakajima H, Kitamoto K (2002) Biochemical characterization of horA-independent hop resistance mechanism in Lactobacillus brevis. Int J Food Microbiol 76:223–230
Tang T, Shi T, Qian K, Li P, Li J, Cao Y (2009) Determination of biogenic amines in beer with pre-column derivatization by high performance liquid chromatography. J Chromatogr B 877:507–512
Vanderhaegen B, Neven H, Verachtert H, Derdelinckx G (2006) The chemistry of beer aging-a critical review. Food Chem 95:357–381
Vaughan A, ÓSullivan T, van Sinderen D (2005) Enhancing the microbiological stability of malt and beer: a review. J Inst Brew 111:355–371
Wieme AD, Spitaels F, Aerts M, De Bruyne K, Van Landschoot A, Vandamme P (2014) Identification of beer-spoilage bacteria using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Int J Food Microbiol 185:41–50
Zhao X, Yu Z, Wang T, Guo X, Luan J, Sun Y, Li X (2016) The use of chitooligosaccharide in beer brewing for protection against beer-spoilage bacteria and its influence on beer performance. Biotechnol Lett 38:629–635
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This work was supported by the National Natural Science Foundation of China (31371742), the Special Fund for Agro-Scientific Research in the Public Interest (201303095) and National Spark Program (2015GA650004)
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Wang, W., Liu, Y., Sun, Z. et al. Hop resistance and beer-spoilage features of foodborne Bacillus cereus newly isolated from filtration-sterilized draft beer. Ann Microbiol 67, 17–23 (2017). https://doi.org/10.1007/s13213-016-1232-4
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DOI: https://doi.org/10.1007/s13213-016-1232-4