DOI QR코드

DOI QR Code

Spoilage Lactic Acid Bacteria in the Brewing Industry

  • Xu, Zhenbo (School of Food Science and Engineering, Guangdong Province Key Laboratory for Green Processing of Natural Products and Product Safety, South China University of Technology) ;
  • Luo, Yuting (School of Food Science and Engineering, Guangdong Province Key Laboratory for Green Processing of Natural Products and Product Safety, South China University of Technology) ;
  • Mao, Yuzhu (School of Food Science and Engineering, Guangdong Province Key Laboratory for Green Processing of Natural Products and Product Safety, South China University of Technology) ;
  • Peng, Ruixin (School of Food Science and Engineering, Guangdong Province Key Laboratory for Green Processing of Natural Products and Product Safety, South China University of Technology) ;
  • Chen, Jinxuan (School of Food Science and Engineering, Guangdong Province Key Laboratory for Green Processing of Natural Products and Product Safety, South China University of Technology) ;
  • Soteyome, Thanapop (Home Economics Technology, Rajamangala University of Technology Phra Nakhon) ;
  • Bai, Caiying (Guangdong Women and Children Hospital) ;
  • Chen, Ling (School of Food Science and Engineering, Guangdong Province Key Laboratory for Green Processing of Natural Products and Product Safety, South China University of Technology) ;
  • Liang, Yi (Guangdong Zhongqing Font Biochemical Science and Technology Co. Ltd.) ;
  • Su, Jianyu (School of Food Science and Engineering, Guangdong Province Key Laboratory for Green Processing of Natural Products and Product Safety, South China University of Technology) ;
  • Wang, Kan (Research Center of Translational Medicine, Second Affiliated Hospital of Shantou University Medical College) ;
  • Liu, Junyan (Department of Civil and Environmental Engineering, University of Maryland) ;
  • Kjellerup, Birthe V. (Department of Civil and Environmental Engineering, University of Maryland)
  • Received : 2019.09.06
  • Accepted : 2020.01.06
  • Published : 2020.07.28

Abstract

Lactic acid bacteria (LAB) have caused many microbiological incidents in the brewing industry, resulting in severe economic loss. Meanwhile, traditional culturing method for detecting LAB are time-consuming for brewers. The present review introduces LAB as spoilage microbes in daily life, with focus on LAB in the brewing industry, targeting at the spoilage mechanism of LAB in brewing industry including the special metabolisms, the exist of the viable but nonculturable (VBNC) state and the hop resistance. At the same time, this review compares the traditional and novel rapid detection methods for these microorganisms which may provide innovative control and detection strategies for preventing alcoholic beverage spoilage, such as improvement of microbiological quality control using advanced culture media or different isothermal amplification methods.

Keywords

References

  1. Sakamoto K, Konings WN. 2003. Beer spoilage bacteria and hop resistance. Int. J. Food Microbiol. 89: 105-24.2. https://doi.org/10.1016/S0168-1605(03)00153-3
  2. Deng Y, Liu J, Li L, Fang H, Tu J, Li B, et al. 2015. Reduction and restoration of culturability of beer-stressed and low-temperature-stressed Lactobacillus acetotolerans strain 2011-8. Int. J. Food Microbiol. 206: 96-101. https://doi.org/10.1016/j.ijfoodmicro.2015.04.046
  3. Liu JY, Deng Y, Soteyome T, Li YY, Su JY, Li L, et al. 2018. Induction and recovery of the viable but nonculturable state of hopresistance Lactobacillus brevis. Front Microbiol. 9: 6. https://doi.org/10.3389/fmicb.2018.00006
  4. Rawat S. 2015. Food Spoilage: Microorganisms and their prevention. Asian J. Plant Sci. 5: 47-56
  5. Bevilacqua A, Corbo M, Sinigaglia M. 2016. The Microbiological Quality of Food: Foodborne Spoilers, pp. 247-248. 1st Ed. Antonio Bevilacqua, Maria Rosaria Corbo and Milena Sinigaglia, Foggia, Italy.
  6. Bartowsky EJ. 2009. Bacterial spoilage of wine and approaches to minimize it. Lett. Appl. Microbiol. 48: 149-156. https://doi.org/10.1111/j.1472-765X.2008.02505.x
  7. Du Toit M, Pretorius I. S. 2000. Microbial spoilage and preservation of wine: using weapons from nature's own arsenal-a review. S. Afr. J. Enol. Vitic. 21: 74-96
  8. Holland R, Crow V, Curry B. 2011. Lactic Acid Bacteria Pediococcus spp., pp. 149-152. In Fuquay JW (ed.), Encyclopedia of Dairy Sciences (2nd Ed.), Ed. Academic Press, San Diego
  9. Back W. 1994. Secondary contamination in the filling area. Brauwelt Int. 4: 326-328.
  10. Yimin Z, Lixian Z, Wangang Z, Pengcheng D, Jiangang H, Xin L. 2018. An overview of spoilage microorganisms in fresh beef. Food Sci. 39: 289-296.
  11. Egan AF, Shay BJ, Rogers PJ. 1989. Factors affecting the production of hydrogen sulphide by Lactobacillus sake L13 growing on vacuum-packaged beef. J. Appl. Microbiol. 67: 255-262.
  12. Pothakos V, Devlieghere F, Villani F, Bjorkroth J, Ercolini D. 2015. Lactic acid bacteria and their controversial role in fresh meat spoilage. Meat Sci. 109: 66-74. https://doi.org/10.1016/j.meatsci.2015.04.014
  13. Dainty RH, Mackey BM. 1992. The relationship between the phenotypic properties of bacteria from chill-stored meat and spoilage processes. Soc. Appl. Bacteriol. Symp. Ser. 21: 103s-114s.
  14. Comi G, Iacumin L. 2012. Identification and process origin of bacteria responsible for cavities and volatile off-flavour compounds in artisan cooked ham. Int. J. Food Sci. Technol. 47: 114-121 https://doi.org/10.1111/j.1365-2621.2011.02816.x
  15. Aymerich T, Martin B, Garriga M, Hugas M. 2003. Microbial quality and direct PCR identification of lactic acid bacteria and nonpathogenic Staphylococci from artisanal low-acid sausages. Appl. Environ. Microbiol. 69: 4583-4594. https://doi.org/10.1128/AEM.69.8.4583-4594.2003
  16. Morgan ME. 1976. The chemistry of some microbially induced flavor defects in milk and dairy foods. Biotechnol. Bioeng. 18: 953-965. https://doi.org/10.1002/bit.260180708
  17. Lafarge V, Ogier JC, Girard V, Maladen V, Leveau JY, Gruss A, et al. 2004. Raw cow milk bacterial population shifts attributable to refrigeration. Appl. Environ. Microbiol. 70: 5644-5650. https://doi.org/10.1128/AEM.70.9.5644-5650.2004
  18. Somers EB, Johnson ME, Wong AC. 2001. Biofilm formation and contamination of cheese by nonstarter lactic acid bacteria in the dairy environment. J. Dairy Sci. 84: 1926-1936. https://doi.org/10.3168/jds.S0022-0302(01)74634-6
  19. Lyhs U, Korkeala H, Vandamme P, Bjorkroth J. 2001. Lactobacillus alimentarius: a specific spoilage organism in marinated herring. Int. J. Food Microbiol. 64: 355-360. https://doi.org/10.1016/S0168-1605(00)00486-4
  20. Entani E, Masai H, Suzuki KI. 1986. Lactobacillus acetotolerans, a new species from fermented vinegar broth. Int. J. Syst. Bacteriol. 36: 544-549. https://doi.org/10.1099/00207713-36-4-544
  21. Geissler AJ, Behr J, von Kamp K, Vogel RF. 2016. Metabolic strategies of beer spoilage lactic acid bacteria in beer. Int. J. Food Microbiol. 216: 60-68. https://doi.org/10.1016/j.ijfoodmicro.2015.08.016
  22. Bartowsky EJ, Henschke PA. 2004. The 'buttery' attribute of wine--diacetyl--desirability, spoilage and beyond. Int. J. Food Microbiol. 96: 235-252. https://doi.org/10.1016/j.ijfoodmicro.2004.05.013
  23. Wisselink HW, Weusthuis RA, Eggink G, Hugenholtz J, Grobben GJ. 2002. Mannitol production by lactic acid bacteria: a review. Int. Dairy J. 12: 151-161. https://doi.org/10.1016/S0958-6946(01)00153-4
  24. Bartowsky EJ. 2009. Bacterial spoilage of wine and approaches to minimize it. Lett. Appl. Microbiol. 48: 149-156. https://doi.org/10.1111/j.1472-765X.2008.02505.x
  25. Barbieri F, Montanari C, Gardini F, Tabanelli G. 2019. Biogenic amine production by lactic acid bacteria: a review. Foods 8: 17. https://doi.org/10.3390/foods8010017
  26. Xu HS, Roberts N, Singleton FL, Attwell RW, Grimes DJ, Colwell RR. 1982. Survival and viability of nonculturable Escherichia coli and Vibrio cholerae in the estuarine and marine environment. Microb. Ecol. 8: 313-323. https://doi.org/10.1007/BF02010671
  27. Nowakowska J, Oliver JD. 2013. Resistance to environmental stresses by Vibrio vulnificus in the viable but nonculturable state. FEMS Microbiol. Ecol. 84: 213-222. https://doi.org/10.1111/1574-6941.12052
  28. Dwidjosiswojo Z, Richard J, Moritz MM, Dopp E, Flemming HC, Wingender J. 2011. Influence of copper ions on the viability and cytotoxicity of Pseudomonas aeruginosa under conditions relevant to drinking water environments. Int. J. Hyg. Environ. Health 214: 485-492. https://doi.org/10.1016/j.ijheh.2011.06.004
  29. Zhang SH, Ye CS, Lin HR, Lv L, Yu X. 2015. UV disinfection induces a Vbnc state in Escherichia coli and Pseudomonas aeruginosa. Environ. Sci. Technol. 49: 1721-1728. https://doi.org/10.1021/es505211e
  30. Liu J, Li L, Li B, Peters BM, Deng Y, Xu Z, et al. 2017. Study on spoilage capability and VBNC state formation and recovery of Lactobacillus plantarum. Microb. Pathog. 110: 257-261. https://doi.org/10.1016/j.micpath.2017.06.044
  31. Suzuki K, Iijima K, Asano S, Kuriyama H, Kitagawa Y. 2006. Induction of viable but nonculturable state in beer spoilage lactic acid bacteria. J. Inst. Brew. 112: 295-301. https://doi.org/10.1002/j.2050-0416.2006.tb00734.x
  32. Deng Y, Liu J, Li L, Fang H, Tu J, Li B, et al. 2015. Reduction and restoration of culturability of beer-stressed and low-temperature-stressed Lactobacillus acetotolerans strain 2011-8. Int. J. Food Microbiol. 206: 96-101. https://doi.org/10.1016/j.ijfoodmicro.2015.04.046
  33. Liu J, Li L, Li B, Peters BM, Deng Y, Xu Z, et al. 2017. First study on the formation and resuscitation of viable but nonculturable state and beer spoilage capability of Lactobacillus lindneri. Microb. Pathog. 107: 219-224. https://doi.org/10.1016/j.micpath.2017.03.043
  34. Yang D, Jun-yan L, Hui-jing F, Jiang C, Hui-ping L, Lin L, et al. 2014. Induction and resuscitation of VBNC state beer-spoilage lactobacilli. Mod. Food Sci. Technol. 30: 154-159.
  35. Liu JY, Deng Y, Soteyome T, Li YY, Su JY, Li L, et al. 2018. Induction and recovery of the viable but nonculturable state of hop-resistance Lactobacillus brevis. Front Microbiol. 9: 6. https://doi.org/10.3389/fmicb.2018.00006
  36. Liu J, Li L, Peters BM, Li B, Chen L, Deng Y, et al. 2017. The viable but nonculturable state induction and genomic analyses of Lactobacillus casei BM-LC14617, a beer-spoilage bacterium. Microbiologyopen 6: e00506. https://doi.org/10.1002/mbo3.506
  37. Yildiz FH, Schoolnik GK. 1998. Role of rpoS in stress survival and virulence of Vibrio cholerae. J. Bacteriol. 180: 773-784. https://doi.org/10.1128/JB.180.4.773-784.1998
  38. Magnusson LU, Farewell A, Nyström T. 2005. ppGpp: a global regulator in Escherichia coli. Trends Microbiol. 13: 236-242. https://doi.org/10.1016/j.tim.2005.03.008
  39. Liu JY, Li L, Peters BM, Li B, Deng Y, Xu ZB, et al. 2016. Draft genome sequence and annotation of Lactobacillus acetotolerans BM-LA14527, a beer-spoilage bacteria. FEMS Microbiol. Lett. 363: 5.
  40. Liu J, Deng Y, Li L, Li B, Li Y, Zhou S, et al. 2018. Discovery and control of culturable and viable but non-culturable cells of a distinctive Lactobacillus harbinensis strain from spoiled beer. Sci. Rep.8: 11446. https://doi.org/10.1038/s41598-018-28949-y
  41. Liu JY, Deng Y, Peters BM, Li L, Li B, Chen LQ, et al. 2016. Transcriptomic analysis on the formation of the viable putative non-culturable state of beer-spoilage Lactobacillus acetotolerans. Sci. Rep. 6: 11. https://doi.org/10.1038/s41598-016-0013-4
  42. John. DiMichele L, Lewis MJ. 1993. Rapid, species-specific detection of lactic acid bacteria from beer using the polymerase chain reaction. J. Am. Soc. Brew. Chem. 51:63-66.
  43. Suzuki K, Asano S, Iijima K, Kitamoto K. 2008. Sake and Beer Spoilage Lactic Acid Bacteria- A Review, 114: 209-223. https://doi.org/10.1002/j.2050-0416.2008.tb00331.x
  44. Sakamoto K, Margolles A, van Veen HW, Konings WN. 2001. Hop resistance in the beer spoilage bacterium Lactobacillus brevis is mediated by the ATP-binding cassette multidrug transporter HorA. J. Bacteriol. 183: 5371-5375. https://doi.org/10.1128/JB.183.18.5371-5375.2001
  45. Suzuki K, Iijima K, Ozaki K, Yamashita H. 2005. Study on ATP production of lactic acid bacteria in beer and development of a rapid pre-screening method for beer-spoilage bacteria. J. Inst. Brew. 114: 209-223. https://doi.org/10.1002/j.2050-0416.2008.tb00331.x
  46. Jun-yan L, Lin L, Bing L, Yang D, Zhen-bo X. 2015. Application of de novo sequencing in the whole genomic study of beer-spoilage lactobacilli. Mod. Food Sci. Technol. 31: 155-162.
  47. Liu J, Li L, Peters BM, Li B, Deng Y, Xu Z, et al. 2016. Draft genome sequence and annotation of Lactobacillus acetotolerans BM-LA14527, a beer-spoilage bacteria. FEMS Microbiol. Lett. 363: fnw201.
  48. Suzuki K, Iijima K, Ozaki K, Yamashita H. 2005. Isolation of a hop-sensitive variant of Lactobacillus lindneri and identification of genetic markers for beer spoilage ability of lactic acid bacteria. Appl. Environ. Microbiol. 71: 5089-5097. https://doi.org/10.1128/AEM.71.9.5089-5097.2005
  49. Iijima K, Suzuki K, Ozaki K, Yamashita H. 2006. horC confers beer-spoilage ability on hop-sensitive Lactobacillus brevis ABBC45cc. J. Appl. Microbiol. 100: 1282-1288. https://doi.org/10.1111/j.1365-2672.2006.02869.x
  50. Suzuki K, Koyanagi M, Yamashita H. 2004. Genetic characterization of non-spoilage variant isolated from beer-spoilage Lactobacillus brevis ABBC45. J. Appl. Microbiol. 96: 946-953. https://doi.org/10.1111/j.1365-2672.2004.02244.x
  51. Suzuki K, Iijima K, Sakamoto K, Sami M, Yamashita H. 2006. A review of hop resistance in beer spoilage lactic acid bacteria. J. Inst. Brew. 112: 173-191. https://doi.org/10.1002/j.2050-0416.2006.tb00247.x
  52. Suzuki K, Ozaki K, Yamashita H. 2004. Genetic marker for differentiating beer-spoilage ability of Lactobacillus paracollinoides strains. J. Appl. Microbiol. 97: 712-718. https://doi.org/10.1111/j.1365-2672.2004.02350.x
  53. Deng Y, Liu JY, Li HP, Li L, Tu JX, Fang HJ, et al. 2014. An improved plate culture procedure for the rapid detection of beer-spoilage lactic acid bacteria. J. Inst. Brew. 120: 127-132. https://doi.org/10.1002/jib.121
  54. Fricker M, Reissbrodt R, Ehling-Schulz M. 2008. Evaluation of standard and new chromogenic selective plating media for isolation and identification of Bacilluscereus. Int. J. Food Microbiol. 121: 27-34. https://doi.org/10.1016/j.ijfoodmicro.2007.10.012
  55. Reissbrodt R. 2004. New chromogenic plating media for detection and enumeration of pathogenic Listeria spp.--An overview. Int. J. Food Microbiol. 95: 1-9. https://doi.org/10.1016/j.ijfoodmicro.2004.01.025
  56. Iversen C, Forsythe SJ. 2007. Comparison of media for the isolation of Enterobacter sakazakii. Appl. Environ. Microbiol. 73: 48-52. https://doi.org/10.1128/AEM.01562-06
  57. Xu Z, Hou Y, Peters BM, Chen D, Li B, Li L, et al. 2016. Chromogenic media for MRSA diagnostics. Mol. Biol. Rep.43: 1205-1212. https://doi.org/10.1007/s11033-016-4062-3
  58. Casey GD, Dobson AD. 2004. Potential of using real-time PCR-based detection of spoilage yeast in fruit juice--a preliminary study. Int. J. Food Microbiol. 91: 327-335. https://doi.org/10.1016/j.ijfoodmicro.2003.09.002
  59. Reynisson E, Lauzon HL, Magnusson H, Hreggvidsson GO, Marteinsson VT. 2008. Rapid quantitative monitoring method for the fish spoilage bacteria Pseudomonas. J. Environ. Monit. 10: 1357-1362. https://doi.org/10.1039/b806603e
  60. Juvonen R, Koivula T, Haikara A. 2008. Group-specific PCR-RFLP and real-time PCR methods for detection and tentative discrimination of strictly anaerobic beer-spoilage bacteria of the class Clostridia. Int. J. Food Microbiol. 125: 162-169. https://doi.org/10.1016/j.ijfoodmicro.2008.03.042
  61. Liu J, Deng Y, Li L, Li B, Li Y, Zhou S, et al. 2018. Discovery and control of culturable and viable but non-culturable cells of a distinctive Lactobacillus harbinensis strain from spoiled beer. Sci. Rep. 8: 11446. https://doi.org/10.1038/s41598-018-28949-y
  62. Notomi T, Okayama H, Masubuchi H, Yonekawa T, Watanabe K, Amino N, et al. 2000. Loop-mediated isothermal amplification of DNA. Nucleic Acids Res. 28: E63. https://doi.org/10.1093/nar/28.12.e63
  63. Fire A, Xu SQ. 1995. Rolling replication of short DNA circles. Proc. Natl. Acad. Sci. USA 92: 4641-4645. https://doi.org/10.1073/pnas.92.10.4641
  64. Walker GT, Little MC, Nadeau JG, Shank DD. 1992. Isothermal in vitro amplification of DNA by a restriction enzyme/DNA polymerase system. Proc. Natl. Acad. Sci. USA 89: 392-396. https://doi.org/10.1073/pnas.89.1.392
  65. Xu G, Hu L, Zhong H, Wang H, Yusa S, Weiss TC, et al. 2012. Cross priming amplification: mechanism and optimization for isothermal DNA amplification. Sci. Rep. 2: 246. https://doi.org/10.1038/srep00246
  66. Yun-Zhe Z, Xian-Zhou Z, Ying-Jun L, Xiao-Yan M, Wei Z. 2016. Rapid detection of Lactobacillus acidophilus in yogurt by loop-mediated isothermal amplification. J. Food Safety Qual. 7: 4581-4585.
  67. Xin L, Zhang L, Meng Z, Lin K, Zhang S, Han X, et al. 2017. Development of a novel loop-mediated isothermal amplification assay for the detection of lipolytic Pseudomonas fluorescens in raw cow milk from North China. J. Dairy Sci. 100: 7802-7811. https://doi.org/10.3168/jds.2017-12740
  68. Yin H, Dong J, Yu J, Li Y, Deng Y. 2018. A novel horA genetic mediated RCA detection of beer spoilage lactobacillus. Microb. Pathog. 114: 311-314. https://doi.org/10.1016/j.micpath.2017.11.064
  69. Wang L, Li Y, Chu J, Xu Z, Zhong Q. 2012. Development and application of a simple loop-mediated isothermal amplification method on rapid detection of Listeria monocytogenes strains. Mol. Biol. Rep. 39: 445-449. https://doi.org/10.1007/s11033-011-0757-7
  70. Xu Z, Li L, Chu J, Peters BM, Harris ML, Li B, et al. 2012. Development and application of loop-mediated isothermal amplification assays on rapid detection of various types of staphylococci strains. Food Res. Int. 47: 166-173. https://doi.org/10.1016/j.foodres.2011.04.042
  71. Qing-xin G, Bin Y, Hua Q. 2016. Application of matrix-assisted laser desorption/ionization time-of-flight mass spectrometry in the detection of MRSA $\delta$-toxin. J. Chin. Antibiotics 44: 455-459.
  72. van Baar BL. 2000. Characterisation of bacteria by matrix-assisted laser desorption/ ionisation and electrospray mass spectrometry. FEMS Microbiol. Rev. 24: 193-219. https://doi.org/10.1016/S0168-6445(99)00036-4
  73. Bohme K, Fernandez-No IC, Barros-Velazquez J, Gallardo JM, Calo-Mata P, Canas B. 2010. Species differentiation of seafood spoilage and pathogenic gram-negative bacteria by MALDI-TOF mass fingerprinting. J. Proteome Res. 9: 3169-3183. https://doi.org/10.1021/pr100047q
  74. Doan NTL, Van Hoorde K, Cnockaert M, De Brandt E, Aerts M, Thanh BL, et al. 2012. Validation of MALDI-TOF MS for rapid classification and identification of lactic acid bacteria, with a focus on isolates from traditional fermented foods in Northern Vietnam. Lett. Appl. Microbiol. 55: 265-273. https://doi.org/10.1111/j.1472-765X.2012.03287.x
  75. Tanigawa K, Kawabata H, Watanabe, K. 2010. Identification and typing of Lactococcus lactis by matrix-assisted laser desorption ionization-time of flight mass spectrometry. Appl. Environ. Microbiol. 76: 4055-4062. https://doi.org/10.1128/AEM.02698-09
  76. De Bruyne K, Slabbinck B, Waegeman W, Vauterin P, De Baets B, Vandamme P. 2011 Bacterial species identification from MALDI-TOF mass spectra through data analysis and machine learning. Syst. Appl. Microbiol. 34: 20-29. https://doi.org/10.1016/j.syapm.2010.11.003
  77. Bellanger AP, Gbaguidi-Haore H, Liapis E, Scherer E, Millon L. 2019. Rapid identification of Candida sp. by MALDI-TOF mass spectrometry subsequent to short-term incubation on a solid medium. APMIS 127: 217-222. https://doi.org/10.1111/apm.12936

Cited by

  1. Formation and Control of the Viable but Non-culturable State of Foodborne Pathogen Escherichia coli O157:H7 vol.11, 2020, https://doi.org/10.3389/fmicb.2020.01202
  2. Pathogenic and Virulence Factor Detection on Viable but Non-culturable Methicillin-Resistant Staphylococcus aureus vol.12, 2020, https://doi.org/10.3389/fmicb.2021.630053
  3. First Report on the Rapid Detection and Identification of Methicillin-Resistant Staphylococcus aureus (MRSA) in Viable but Non-culturable (VBNC) Under Food Storage Conditions vol.11, 2020, https://doi.org/10.3389/fmicb.2020.615875
  4. Probiotic and Potentially Probiotic Yeasts-Characteristics and Food Application vol.10, pp.6, 2020, https://doi.org/10.3390/foods10061306
  5. Recent Advancements in the Technologies Detecting Food Spoiling Agents vol.12, pp.4, 2020, https://doi.org/10.3390/jfb12040067
  6. A novel procedure in combination of genomic sequencing, flow cytometry and routine culturing for confirmation of beer spoilage caused by Pediococcus damnosus in viable but nonculturable state vol.154, 2020, https://doi.org/10.1016/j.lwt.2021.112623