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Research Articles

Factorial Analysis of Variance of the Inhibiting Effects of Iso-Alpha Acids, Alpha Acids, and Sulfur Dioxide on the Growth of Beer-Spoilage Bacteria in Beer

ORCID Icon, , &
Pages 424-434 | Received 28 Apr 2020, Accepted 20 Jun 2022, Published online: 02 Aug 2022

Literature cited

  • Sakamoto, K.; Konings, W. N. Beer Spoilage Bacteria and Hop Resistance. Int. J. Food Microbiol. 2003, 89, 105–124. DOI: 10.1016/s0168-1605(03)00153-3.
  • Narziss, L. Abriss der Bierbrauerei, 7th updated and expanded ed., Wiley-VCH Verlag GmbH & Co. KGaA: Weinheim, 2005.
  • Vaughan, A.; O’Sullivan, T.; van Sinderen, D. Enhancing the Microbiological Stability of Malt and Beer—A Review. J. Inst. Brew. 2005, 111, 355–371. DOI: 10.1002/j.2050-0416.2005.tb00221.x.
  • Suzuki, K.; Iijima, K.; Sakamoto, K.; Sami, M.; Yamashita, H. A Review of Hop Resistance in Beer Spoilage Lactic Acid Bacteria. J. Inst. Brew. 2006, 112, 173–191. DOI: 10.1002/j.2050-0416.2006.tb00247.x.
  • Back, W. Ausgewählte Kapitel der Brauereitechnologie; Fachverlag Hans Carl: Nürnberg, 2005.
  • Suzuki, K. 125th Anniversary Review: Microbiological Instability of Beer Caused by Spoilage Bacteria. J. Inst. Brew. 2011, 117, 131–155. DOI: 10.1002/j.2050-0416.2011.tb00454.x.
  • Vriesekoop, F.; Krahl, M.; Hucker, B.; Menz, G. 125th Anniversary Review: Bacteria in Brewing: The Good, the Bad and the Ugly. J. Inst. Brew. 2012, 118, 335–345. DOI: 10.1002/jib.49.
  • Bokulich, N. A.; Bamforth, C. W. The Microbiology of Malting and Brewing. Microbiol. Mol. Biol. Rev. 2013, 77, 157–172. DOI: 10.1128/MMBR.00060-12.
  • Hammond, J.; Brennan, M.; Price, A. The Control of Microbial Spoilage of Beer. J. Inst. Brew. 1999, 105, 113–120. DOI: 10.1002/j.2050-0416.1999.tb00014.x.
  • Suzuki, K.; Shinohara, Y.; Kurniawan, Y. N. Role of Plasmids in Beer Spoilage Lactic Acid Bacteria: A Review. J. Am. Soc. Brew. Chem. 2021, 79, 1–16.
  • Shimwell, J. L. On the Relation between the Staining Properties of Bacteria and Their Reaction towards Hop Antiseptic. Part I. J. Inst. Brew. 1937, 43, 111–118. DOI: 10.1002/j.2050-0416.1937.tb05727.x.
  • Shimwell, J. L. On the Relation between the Staining Properties of Bacteria and Their Reaction towards Hop Antiseptic. Part III. J. Inst. Brew. 1937, 43, 191–194. DOI: 10.1002/j.2050-0416.1937.tb05744.x.
  • Walker, T. K.; Blakebrough, N. Bacteriostatic Power of Humulone Boiling—Product. J. Inst. Brew. 1952, 58, 13–24. DOI: 10.1002/j.2050-0416.1952.tb02657.x.
  • Richards, M.; Macrae, R. M. 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. 1964, 70, 484–488. DOI: 10.1002/j.2050-0416.1964.tb06353.x.
  • Schmalreck, A.; Teuber, M.; Reininger, W.; Hartl, A. Structural Features Determining the Antibiotic Potencies of Natural and Synthetic Hop Bitter Resins, Their Precursors and Derivatives. Can. J. Microbiol. 1975, 21, 205–212. DOI: 10.1139/m75-029.
  • Simpson, W. J.; Smith, A. R. Factors Affecting Antibacterial Activity of Hop Compounds and Their Derivatives. J. Appl. Bacteriol. 1992, 72, 327–334. DOI: 10.1111/j.1365-2672.1992.tb01843.x.
  • Simpson, W. J.; Fernandez, J. L. Selection of Beer Spoilage Lactic Acid Bacteria and Induction of Their Ability to Grow in Beer. Lett. Appl. Microbiol. 1992, 14, 13–16. DOI: 10.1111/j.1472-765X.1992.tb00636.x.
  • Simpson, W. J. Ionophoric Action of Trans-Isohumulone on Lactobacillus brevis. J. Gen. Microbiol. 1993, 139, 1041–1045. DOI: 10.1099/00221287-139-5-1041.
  • Simpson, W. J. Cambridge Prize Lecture. Studies on the Sensitivity of Lactic Acid Bacteria to Hop Bitter Acids. J. Inst. Brew. 1993, 99, 405–411. DOI: 10.1002/j.2050-0416.1993.tb01180.x.
  • Fernandez, J. L.; Simpson, W. J. Aspects of the Resistance of Lactic Acid Bacteria to Hop Bitter Acids. J. Appl. Microbiol. 1993, 75, 315–319. DOI: 10.1111/j.1365-2672.1993.tb02782.x.
  • Simpson, W. J.; Fernandez, J. L. Mechanism of Resistance of Lactic Acid Bacteria to Trans-Isohumulone. J. Am. Soc. Brew. Chem. 1994, 52, 9–11. DOI: 10.1094/ASBCJ-52-0009.
  • Fernandez, J. L.; Simpson, W. J. Measurement and Prediction of the Susceptibility of Lager Beer to Spoilage by Lactic Acid Bacteria. J. Appl. Microbiol. 1995, 78, 419–425. DOI: 10.1111/j.1365-2672.1995.tb03428.x.
  • Yansanjav, A.; Siegumfeldt, H.; Jespersen, L.; Vancanneyt, M.; Swings, J.; Hollerová, I.; Leisner, J. J. Detection of Resistance of Lactic Acid Bacteria to a Mixture of the Hop Analogue Compounds Tetrahydroiso-α-Acids by Noninvasive Measurement of Intracellular pH. J. Appl. Microbiol. 2004, 96, 1324–1332. DOI: 10.1111/j.1365-2672.2004.02261.x.
  • Behr, J.; Gänzle, M. G.; Vogel, R. F. Characterization of a Highly Hop-Resistant Lactobacillus brevis Strain Lacking Hop Transport. Appl. Environ. Microbiol. 2006, 72, 6483–6492. DOI: 10.1128/AEM.00668-06.
  • Caballero, I.; Agut, M.; Armentia, A.; Blanco, C. A. Importance of Tetrahydroiso-α-Acids to the Microbiological Stability of Beer. J. AOAC Int. 2009, 92, 1160–1164. DOI: 10.1093/jaoac/92.4.1160.
  • Behr, J.; Vogel, R. F. Mechanisms of Hop Inhibition: Hop Ionophores. J. Agric. Food Chem. 2009, 57, 6074–6081. DOI: 10.1021/jf900847y.
  • Behr, J.; Vogel, R. F. Mechanisms of Hop Inhibition Include the Transmembrane Redox Reaction. Appl. Environ. Microbiol. 2010, 76, 142–149. DOI: 10.1128/AEM.01693-09.
  • Vogel, R. F.; Preissler, P.; Behr, J. Towards an Understanding of Hop Tolerance in Beer Spoiling Lactobacillus brevis. BrewingScience 2010, 63, 23–30.
  • Schurr, B. C.; Behr, J.; Vogel, R. F. Role of the GAD System in Hop Tolerance of Lactobacillus brevis. Eur. Food Res. Technol. 2013, 237, 199–207. DOI: 10.1007/s00217-013-1980-3.
  • Schurr, B. C.; Hahne, H.; Kuster, B.; Behr, J.; Vogel, R. F. Molecular Mechanisms behind the Antimicrobial Activity of Hop Iso-α-Acids in Lactobacillus brevis. Food Microbiol. 2015, 46, 553–563. DOI: 10.1016/j.fm.2014.09.017.
  • Schurr, B. C.; Behr, J.; Vogel, R. F. Detection of Acid and Hop Shock Induced Responses in Beer Spoiling Lactobacillus brevis by MALDI-TOF MS. Food Microbiol. 2015, 46, 501–506. DOI: 10.1016/j.fm.2014.09.018.
  • Back, W.; Biendl, M. Microbiologically Important Components in Hoppy Beers (Part 1). Brauwelt Int. 2018, 36, 2 101–103.
  • Back, W.; Biendl, M. Microbiologically Important Components in Hoppy Beers (Part 2). Brauwelt Int. 2018, 36, 3 206–208.
  • Michel, M.; Cocuzza, S.; Biendl, M.; Peifer, F.; Hans, S.; Methner, Y.; Pehl, F.; Back, W.; Jacob, F.; Hutzler, M. The Impact of Different Hop Compounds on the Growth of Selected Beer Spoilage Bacteria in Beer. J. Inst. Brew. 2020, 126, 354–361.
  • Fugelsang, K. C.; Edwards, C. G. Wine Microbiology. Practical Applications and Procedures, 2nd ed.; Springer Science + Business Media, LLC: New York, 2007.
  • Sami, M.; Yamashita, H.; Hirono, T.; Kadokura, H.; Kitamoto, K.; Yoda, K.; Yamasaki, M. Hop-Resistant Lactobacillus brevis Containing a Novel Plasmid Harboring a Multidrug Resistance-Like Gene. J. Ferm. Bioengineer. 1997, 84, 1–6. DOI: 10.1016/S0922-338X(97)82778-X.
  • Hayashi, N.; Ito, M.; Horiike, S.; Taguchi, H. Molecular Cloning of a Putative Divalent-Cation Transporter Gene as a New Genetic Marker for the Identification of Lactobacillus brevis Strains Capable of Growing in Beer. Appl. Microbiol. Biotechnol. 2001, 55, 596–603. DOI: 10.1007/s002530100600.
  • Sakamoto, K.; van Veen, H. W.; Saito, H.; Kobayashi, H.; Konings, W. N. Membrane-Bound ATPase Contributes to Hop Resistance of Lactobacillus brevis. Appl. Environ. Microbiol. 2002, 68, 5374–5378. DOI: 10.1128/AEM.68.11.5374-5378.2002.
  • Suzuki, K.; Koyanagi, M.; Yamashita, H. Genetic Characterization of Non-Spoilage Variant Isolated from Beer-Spoilage Lactobacillus brevis ABBC45C. J. Appl. Microbiol. 2004, 96, 946–953. DOI: 10.1111/j.1365-2672.2004.02244.x.
  • Fujii, T.; Nakashima, K.; Hayashi, N. Random Amplified Polymorphic DNA-PCR Based Cloning of Markers to Identify the Beer-Spoilage Strains of Lactobacillus brevis, Pediococcus damnosus, Lactobacillus collinoides and Lactobacillus coryniformis. J. Appl. Microbiol. 2005, 98, 1209–1220. DOI: 10.1111/j.1365-2672.2005.02558.x.
  • Iijima, K.; Suzuki, K.; Ozaki, K.; Yamashita, H. horC Confers Beer-Spoilage Ability on Hop-Sensitive Lactobacillus brevis ABBC45CC. J. Appl. Microbiol. 2006, 100, 1282–1288. DOI: 10.1111/j.1365-2672.2006.02869.x.
  • Behr, J.; Israel, L.; Gänzle, M. G.; Vogel, R. F. Proteomic Approach for Characterization of Hop-Inducible Proteins in Lactobacillus brevis. Appl. Environ. Microbiol. 2007, 73, 3300–3306. DOI: 10.1128/AEM.00124-07.
  • Behr, J.; Geissler, A. J.; Preissler, P.; Ehrenreich, A.; Angelov, A.; Vogel, R. F. Identification of Ecotype-Specific Marker Genes for Categorization of Beer-Spoiling Lactobacillus brevis. Food Microbiol. 2015, 51, 130–138. DOI: 10.1016/j.fm.2015.05.015.
  • Geissler, A. J.; Behr, J.; von Kamp, K.; Vogel, R. F. Metabolic Strategies of Beer Spoilage Lactic Acid Bacteria in Beer. Int. J. Food Microbiol. 2016, 216, 60–68. DOI: 10.1016/j.ijfoodmicro.2015.08.016.
  • Feyereisen, M.; Mahony, J.; O’Sullivan, T.; Boer, V.; van Sinderen, D. Beer Spoilage and Low pH Tolerance is Linked to Manganese Homeostasis in Selected Lactobacillus brevis Strains. J. Appl. Microbiol. 2020, 129, 1309–1320. DOI: 10.1111/jam.14730.
  • Feyereisen, M.; Mahony, J.; O’Sullivan, T.; Boer, V.; van Sinderen, D. A Plasmid-Encoded Putative Glycosyltransferase is Involved in Hop Tolerance and Beer Spoilage in Lactobacillus brevis. Appl. Environ. Microbiol. 2020, 86, e02268-19.
  • Lee, S. Y.; Mabee, M. S.; Jangaard, N. O. Pectinatus, a New Genus of the Family Bacteroidaceae. Int. J. Syst. Evol. Microbiol. 1978, 28, 582–594. DOI: 10.1099/00207713-28-4-582.
  • Back, W.; Weiss, N.; Seidel, H. Isolierung und systematische Zuordnung bierschädlicher gramnegativer Bakterien. II. Gramnegative anaerobe Stäbchen. Brauwissenschaft 1979, 32, 233–238.
  • Lee, S. Y.; Madee, M. S.; Jangaard, N. O.; Horiuchi, E. K. Pectinatus, a New Genus of Bacteria Capable of Growth in Hopped Beer. J. Inst. Brew. 1980, 86, 28–30. DOI: 10.1002/j.2050-0416.1980.tb03951.x.
  • Chelack, B. J.; Ingledew, W. M. Anaerobic Gram-Negative Bacteria in Brewing—A Review. J. Am. Soc. Brew. Chem. 1987, 45, 123–127. DOI: 10.1094/ASBCJ-45-0123.
  • Schleifer, K. H.; Leuteritz, M.; Weiss, N.; Ludwig, W.; Kirchhof, G.; Seidel-Rüfer, H. Taxonomic Study of Anaerobic, Gram-Negative, Rod-Shaped Bacteria from Breweries: Emended Description of Pectinatus cerevisiiphilus and Description of Pectinatus frisingensis sp. nov., Selenomonas lacticifex sp. nov., Zymophilus raffinosivorans Gen. nov., sp. nov., and Zymophilus paucivorans sp. nov. Int. J. Syst. Evol. Microbiol. 1990, 40, 19–27.
  • Membré, J. M.; Tholozan, J. L. Modeling Growth and off-Flavours Production of Spoiled Beer Bacteria, Pectinatus frisingensis. J. Appl. Bacteriol. 1994, 77, 456–460. DOI: 10.1111/j.1365-2672.1994.tb03449.x.
  • Tholozan, J. L.; Membré, J. M.; Grivet, J. P. Physiology and Development of Pectinatus cerevisiiphilus and Pectinatus frisingensis, Two Strict Anaerobic Beer Spoilage Bacteria. Int. J. Food Microbiol. 1997, 35, 29–39. DOI: 10.1016/S0168-1605(96)01206-8.
  • Ashtavinayak, P.; Elizabeth, H. A. Review: Gram Negative Bacteria in Brewing. Adv. in Microbio. 2016, 06, 195–209. DOI: 10.4236/aim.2016.63020.
  • Haikara, A.; Penttilä, L.; Enari, T. M.; Lounatmaa, K. Microbiological, Biochemical, and Electron Microscopic Characterization of a Pectinatus Strain. Appl. Environ. Microbiol. 1981, 41, 511–517. DOI: 10.1128/aem.41.2.511-517.1981.
  • Watier, D.; Leguerinel, I.; Hornez, J. P.; Chowdhury, I.; Dubourguier, H. C. Heat Resistance of Pectinatus sp., a Beer Spoilage Anaerobic Bacterium. J. Appl. Bacteriol. 1995, 78, 164–168. DOI: 10.1111/j.1365-2672.1995.tb02837.x.
  • Chowdhury, I.; Watier, D.; Hornez, J. P. Variability in Survival of Pectinatus cerevisiiphilus, Strictly Anaerobic Bacteria, under Different Oxygen Conditions. Anaerobe 1995, 1, 151–156. DOI: 10.1006/anae.1995.1012.
  • Chowdhury, I.; Watier, D.; Leguerinel, I.; Hornez, J. P. Effect of Pectinatus cerevisiiphilus on Saccharomyces cerevisiae Concerning Its Growth and Alcohol Production in Wort Medium. J. Food Microbiol. 1997, 14, 265–272. DOI: 10.1006/fmic.1996.0092.
  • Chihib, N. E.; Tholozan, J. L. Effect of Rapid Cooling and Acidic pH on Cellular Homeostasis of Pectinatus frisingensis, a Strictly Anaerobic Beer-Spoilage Bacterium. Int. J. Food Microbiol. 1999, 48, 191–202. DOI: 10.1016/S0168-1605(99)00046-X.
  • ASBC Methods of Analysis, Online. Method Beer -23. Beer Bitterness (International Method). Approved 2015. American Society of Brewing Chemists, St. Paul, MN. DOI: 10.1094/ASBCMOA-Beer-23.
  • Meguro, H.; Oorui, H.; Takahashi, C.; Kitahata, K.; Matsui, S. Microdetection of Sulfurous Acid in Food and Brew. Japan. Unexamined patent publication JPS6039560 (A), 1985.
  • Murakami, A.; Kawasaki, Y.; Ota, R.; Takahashi, Y. Methods for Producing Beer-Like Drink. Japanese patent JP5864098B, 2016.
  • Simpson, W. J. Ionization Behavior of Hop Compounds and Hop-Derived Compounds. J. Inst. Brew. 1993, 99, 317–326. DOI: 10.1002/j.2050-0416.1993.tb01169.x.
  • Iijima, K.; Suzuki, K.; Asano, S.; Kuriyama, H.; Kitagawa, Y. Isolation and Identification of Potential Beer-Spoilage Pediococcus inopinatus and Beer-Spoilage Lactobacillus backi Strains Carrying the horA and horC Gene Clusters. J. Inst. Brew. 2007, 113, 96–101. DOI: 10.1002/j.2050-0416.2007.tb00262.x.
  • Archibald, F. S.; Duong, M. N. Manganese Acquisition by Lactobacillus plantarum. J. Bacteriol. 1984, 158, 1–8. DOI: 10.1128/jb.158.1.1-8.1984.
  • Archibald, F. S.; Fridovich, I. Manganese, Superoxide Dismutase, and Oxygen Tolerance in Some Lactic Acid Bacteria. J. Bacteriol. 1981, 146, 928–936. DOI: 10.1128/jb.146.3.928-936.1981.
  • Helander, I. M.; Haikara, A.; Sadovskaya, I.; Vinogradov, E.; Salkinoja-Salonen, M. S. Lipopolysaccharides of Anaerobic Beer Spoilage Bacteria of the Genus Pectinatus-Lipopolysaccharides of a Gram-Positive Genus. FEMS Microbiol. Rev. 2004, 28, 543–552. DOI: 10.1016/j.femsre.2004.05.001.
  • Back, W. Bierschädliche Bakterien. Brauwelt 1980, 43, 1562–1569.
  • Marchandin, H.; Teyssier, C.; Campos, J.; Jean-Pierre, H.; Roger, F.; Gay, B.; Carlier, J. P.; Jumas-Bilak, E. Negativicoccus succinicivorans Gen. nov., sp. nov., Isolated from Human Clinical Samples, Emended Description of the Family Veillonellaceae and Description of Negativicutes Classis Nov., Selenomonadales Ord. nov. and Acidaminococcaceae Fam. nov. in the Bacterial Phylum Firmicutes. Int. J. Syst. Evol. Microbiol. 2010, 60, 1271–1279. DOI: 10.1099/ijs.0.013102-0.
  • Antunes, L. C.; Poppleton, D.; Klingl, A.; Criscuolo, A.; Dupuy, B.; Brochier-Armanet, C.; Beloin, C.; Gribaldo, S. Phylogenomic Analysis Supports the Ancestral Presence of LPS-Outer Membranes in the Firmicutes. eLife 2016, 5, e14589. DOI: 10.7554/eLife.14589.
  • Lewis, J. C.; Alderton, G.; Carson, J. F.; Reynolds, D. M.; Maclay, W. D. Luplon and Humulon—Antibiotic Constituents of Hops. J. Clin. Invest. 1949, 28, 916–919. DOI: 10.1172/JCI102178.
  • Rahal, J. J., Jr. Antibiotic Combinations: The Clinical Relevance of Synergy and Antagonism. Medicine (Baltimore) 1978, 57, 179–195.
  • Hough, J. S.; Briggs, D. E.; Stevens, R.; Young, T. W. Malting and Brewing Science, Volume II Hopped Wort and Beer, 2nd ed.; Chapman and Hall: London, 1982.
  • Miörner, H.; Johansson, G.; Kronvall, G. Lipoteichoic Acid Is the Major Cell Wall Component Responsible for Surface Hydrophobicity of Group a Streptococci. Infect. Immun. 1983, 39, 336–343. DOI: 10.1128/iai.39.1.336-343.1983.
  • Rismondo, J.; Percy, M. G.; Gründling, A. Discovery of Genes Required for Lipoteichoic Acid Glycosylation Predicts Two Distinct Mechanisms for Wall Teichoic Acid Glycosylation. J. Biol. Chem. 2018, 293, 3293–3306. DOI: 10.1074/jbc.RA117.001614.
  • Vos, P.; Garrity, G.; Jones, D.; Krieg, N. R.; Ludwig, W.; Rainey, F. A.; Schleifer, K. H.; Whitman, W. Bergey’s Manual of Systemic Bacteriology. Volume 3: The Firmicutes. Springer-Verlag: New York, 2009.
  • Delcour, A. H. Outer Membrane Permeability and Antibiotic Resistance Biochim. Biochim. Biophys. Acta. 2009, 1794, 808–816. [Database] DOI: 10.1016/j.bbapap.2008.11.005.
  • Ilett, D. R. Aspects of the Analysis, Role, and Fate of Sulphur Dioxide in Beer. Tech. Quart. Master Brewers Ass. Am. 1995, 32, 213–221.
  • Briggs, D. E.; Hough, J. S.; Stevens, R.; Young, T. W. Malting and Brewing Science. Volume I Malt and Sweet Wort, 2nd ed.; Chapman and Hall: London, 1981.
  • McCabe, J. T. The Practical Brewer, 3rd ed.; Master Brewers Association of the Americas: Madison, WI, 1999
  • Kunze, W. Technology Brewing and Malting, 6th revised English ed., VLB: Berlin, 2019.
  • van Haecht, J. L.; Dufour, J. P. The Production of Sulfur Compounds by Brewing Yeasts. A Review. Cerevisia. Belgian J. Brew. Biotechnol. 1995, 20, 51–64.
  • Ohno, T.; Takahashi, R. Production of Sulfite in the Brewing Process. Rept. Res. Lab. Kirin Brewery Co. Ltd 1987, 30, 15–19.
  • Hayashi, N.; Thiele, F.; Franz, O.; Back, W. Investigations into the Formation of Sulfur Dioxide by "Assimilation Yeast”. Proceedings: European Brewery Convention Congress, Prague, Poster, CD ROM, 2005.
  • Schönberger, C.; Kostelecky, T. 125th Anniversary Review: The Role of Hops in Brewing. J. Inst. Brew. 2011, 117, 259–267. DOI: 10.1002/j.2050-0416.2011.tb00471.x.
  • Parkin, E.; Shellhammer, T. Toward Understanding the Bitterness of Dry-Hopped Beer. J. Am. Soc. Brew. Chem. 2017, 75, 363–3368. DOI: 10.1094/ASBCJ-2017-4311-01.

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