Identification of beer-spoilage bacteria using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry

International Journal of Food Microbiology

Volumn 185, Issue , 2014, Pages 41-50

  Wieme, Anneleen D ^a,b   Spitaels, Freek ^b   Aerts, Maarten ^b   De Bruyne, Katrien ^c   Van Landschoot, Anita ^a   Vandamme, Peter ^b  

^a GHENT UNIVERSITY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c Applied Maths NV   (Belgium)

Author keywords

Beer spoilage bacteria; Classifier based analysis; Identification; MALDI TOF MS; MLSA; Peak based cluster analysis

Indexed keywords

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATION; BEER; CLUSTER ANALYSIS; CONTROLLED STUDY; FOOD SPOILAGE; FUNGAL CELL CULTURE; GLUCONOBACTER; GLUCONOBACTER CERINUS; GLUCONOBACTER OXYDANS; LACTIC ACID BACTERIUM; LACTOBACILLUS BREVIS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PEDIOCOCCUS ACIDILACTICI; QUALITY CONTROL; SEQUENCE ANALYSIS; SIGNAL NOISE RATIO; SPECIES DIFFERENTIATION;

BEER-SPOILAGE BACTERIA; CLASSIFIER-BASED ANALYSIS; IDENTIFICATION; MALDI-TOF MS; MLSA; PEAK-BASED CLUSTER ANALYSIS;

BACTERIA; BEER; FOOD MICROBIOLOGY; MOLECULAR SEQUENCE DATA; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84902324408     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2014.05.003     Document Type: Article

References (92)

1. Alispahic M., Hummel K., Jandreski-Cvetkovic D., Nobauer K., Razzazi-Fazeli E., Hess M., Hess C. Species-specific identification and differentiation of Arcobacter, Helicobacter and Campylobacter by full-spectral matrix-associated laser desorption/ionization time-of-flight mass spectrometry analysis. J. Med. Microbiol. 2010, 59:295-301.
2. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
3. Andrés-Barrao C., Benagli C., Chappuis M., Ortega Perez R., Tonolla M., Barja F. Rapid identification of acetic acid bacteria using MALDI-TOF mass spectrometry fingerprinting. Syst. Appl. Microbiol. 2013, 36:75-81.
4. Applied Maths BioNumerics: instruction manual version 7.1 2013, Applied Maths N.V., Sint-Martens-Latem, Belgium.
5. Asano S., Suzuki K., Ozaki K., Kuriyama H., Yamashita H., Kitagawa Y. Application of multiplex PCR to the detection of beer-spoilage bacteria. J. Am. Soc. Brew. Chem. 2008, 66:37-42.
6. Asano S., Iijima K., Suzuki K., Motoyama Y., Ogata T., Kitagawa Y. Rapid detection and identification of beer-spoilage lactic acid bacteria by microcolony method. J. Biosci. Bioeng. 2009, 108:124-129.
7. Back W. Colour Atlas and Handbook of Beverage Biology 2005, Fachverslag Hans Carl, Nürnberg, Germany.
8. Barney M., Volgyi A., Navarro A., Ryder D. Riboprinting and 16S rRNA gene sequencing for identification of brewery Pediococcus isolates. Appl. Environ. Microbiol. 2001, 67:553-560.
9. Beimfohr C., Snaidr J. Method for the specific fast detection of bacteria which are harmful to beer 2004, 88. (US 2004/0219574 A1).
10. Benagli C., Rossi V., Dolina M., Tonolla M., Petrini O. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry for the identification of clinically relevant bacteria. PLoS One 2011, 6:e16424.
11. Bohak I., Thelen K., Beimfohr C. Description of Lactobacillus backi sp. nov., an obligate beer-spoiling bacterium. Monatschrift für, Brauwissenschaft March/April 2006, 78-80.
12. Bokulich N.A., Bamforth C.W. The microbiology of malting and brewing. Microbiol. Mol. Biol. Rev. 2013, 77:157-172.
13. 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.
14. Carbonnelle E., Mesquita C., Bille E., Day N., Dauphin B., Beretti J.L., Ferroni A., Gutmann L., Nassif X. MALDI-TOF mass spectrometry tools for bacterial identification in clinical microbiology laboratory. Clin. Biochem. 2011, 44:104-109.
15. Clark A.E., Kaleta E.J., Arora A., Wolk D.M. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry: a fundamental shift in the routine practice of clinical microbiology. Clin. Microbiol. Rev. 2013, 26:547-603.
16. 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. Appl. Microbiol. 2010, 60:2277-2283.
17. Conway G.C., Smole S.C., Sarracino D.A., Arbeit R.D., Leopold P.E. Phyloproteomics: species identification of Enterobacteriaceae using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. J. Mol. Microbiol. Biotechnol. 2001, 3:103-112.
18. De Bruyne K., Franz C.M., 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. Appl. Microbiol. 2008, 58:2909-2916.
19. Dieckmann R., Graeber I., Kaesler I., Szewzyk U., von Dohren H. Rapid screening and dereplication of bacterial isolates from marine sponges of the sula ridge by intact-cell-MALDI-TOF mass spectrometry (ICM-MS). Appl. Microbiol. Biotechnol. 2005, 67:539-548.
20. Dieckmann R., Helmuth R., Erhard M., Malorny B. Rapid classification and identification of Salmonella at the species and subspecies levels by whole-cell matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Appl. Environ. Microbiol. 2008, 74:7767-7778.
21. Dobson C.M., Deneer H., Lee S., Hemmingsen S., Glaze S., Ziola B. Phylogenetic analysis of the genus Pediococcus, including Pediococcus claussenii sp. nov., a novel lactic acid bacterium isolated from beer. Int. J. Syst. Appl. Microbiol. 2002, 52:2003-2010.
22. Dowhanick T., Sobczak J., Russell I., Stewart G.G. The rapid identification by protein fingerprinting of yeast and bacterial brewery contaminants. J. Am. Soc. Brew. Chem. 1990, 48:75-79.
23. Dušková M., Šedo O., Kšicová K., Zdráhal Z., Karpíšková R. Identification of lactobacilli isolated from food by genotypic methods and MALDI-TOF MS. Int. J. Food Microbiol. 2012, 159:107-114.
24. Evason D.J., Claydon M.A., Gordon D.B. Effects of ion mode and matrix additives in the identification of bacteria by intact cell mass spectrometry. Rapid Commun. Mass Spectrom. 2000, 14:669-672.
25. Fernandez J.L., Simpson W. Measurement and prediction of the susceptibility of lager beer to spoilage by lactic acid bacteria. J. Appl. Microbiol. 1995, 78:419-425.
26. Fischborn T. HLP medium for the detection of lactic acid bacteria (international method). J. Am. Soc. Brew. Chem. 2009, 67:247-248.
27. 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.
28. Guiraud J.P. Microbiologie Alimentaire 1998, Dunod, Paris, (in French).
29. Haakensen M., Ziola B. Identification of novel horA-harbouring bacteria capable of spoiling beer. Can. J. Microbiol. 2008, 54:321-325.
30. Haakensen M., Dobson C.M., Deneer H., Ziola B. Real-time PCR detection of bacteria belonging to the Firmicutes Phylum. Int. J. Food Microbiol. 2008, 125:236-241.
31. Haakensen M., Vickers D.M., Ziola B. Susceptibility of Pediococcus isolates to antimicrobial compounds in relation to hop-resistance and beer-spoilage. BMC Microbiol. 2009, 9. 10.1186/1471-2180-1189-1190.
32. 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.
33. Huhtamella S., Leinonen M., Nieminen T., Fahnert B., Myllykoski L., Breitenstein A., Neubauer P. RNA-based sandwich hybridisation method for detection of lactic acid bacteria in brewery samples. J. Microbiol. Methods 2007, 68:543-553.
34. Hutzler M., Koob J., Riedl R., Jacob F. Classification, identification and detection of beer spoiling microorganisms - a review. World Brewing Conference, July 28-August 1, Portland Oregon, USA 2012.
35. Hutzler M., Koob J., Riedl R., Jacob F. Beer Spoiling Microorganisms-A Current Overview 2013, 23-25. Fachverslag Hans Carl GmbH, Brauwelt International I.
36. cc. J. Appl. Microbiol. 2006, 100:1282-1288.
37. 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.
38. Iijima K., Asano S., Suzuki K., Ogata T., Kitagawa Y. Modified multiplex PCR methods for comprehensive detection of Pectinatus and beer-spoilage cocci. Biosci. Biotechnol. Biochem. 2008, 72:2764-2766.
39. Juvonen R., Koivula T., Haikara A. 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. 2008, 125:162-169.
40. Juvonen R., Partanen T., Koivula T. Evaluation of reverse-transcription PCR detection of 16S rRNA and tuf mRNA for viable/dead discrimination of beer-spoilage lactic acid bacteria. J. Am. Soc. Brew. Chem. 2010, 68:101-106.
41. Keys C.J., Dare D.J., Sutton H., Wells G., Lunt M., McKenna T., McDowall M., Shah H.N. Compilation of a MALDI-TOF mass spectral database for the rapid screening and characterisation of bacteria implicated in human infectious diseases. Infect. Genet. Evol. 2004, 4:221-242.
42. Koivula T.T., Juvonen R., Haikara A., Suihko M.L. Characterization of the brewery spoilage bacterium Obesumbacterium proteus by automated ribotyping and development of PCR methods for its biotype 1. J. Appl. Microbiol. 2006, 100:398-406.
43. Lartigue M.F., Hery-Arnaud G., Haguenoer E., Domelier A.S., Schmit P.O., van der Mee-Marquet N., Lanotte P., Mereghetti L., Kostrzewa M., Quentin R. Identification of Streptococcus agalactiae isolates from various phylogenetic lineages by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. J. Clin. Microbiol. 2009, 47:2284-2287.
44. Lisdiyanti P., Kawasaki H., Seki T., Yamada Y., Uchimura T., Komagata K. Identification of Acetobacter strains isolated from Indonesian sources, and proposals of Acetobacter syzygii sp. nov., Acetobacter cibinongensis sp. nov., and Acetobacter orientalis sp. nov. J. Gen. Appl. Microbiol. 2001, 47:119-131.
45. March C., Manclus J.J., Abad A., Navarro A., Montoya A. Rapid detection and counting of viable beer-spoilage lactic acid bacteria using a monoclonal chemiluminescence enzyme immunoassay and a CCD camera. J. Immunol. Methods 2005, 303:92-104.
46. Matoulkova D., Kosar K., Sigler K. Rapid, simple, and specific cultivation-based method for detection of Pectinatus spp. in brewery samples. J. Am. Soc. Brew. Chem. 2012, 70:29-34.
47. Matoulkova D., Kosar K., Slaby M., Sigler K. Occurrence and species distribution of strictly anaerobic bacterium Pectinatus in brewery bottling halls. J. Am. Soc. Brew. Chem. 2012, 70:262-267.
48. Menz G., Vriesekoop F., Zarei M., Zhu B., Aldred P. The growth and survival of food-borne pathogens in sweet and fermenting brewers' wort. Int. J. Food Microbiol. 2010, 140:19-25.
49. Motoyama Y., Ogata T., Sakai K. Characterization of Pectinatus cerevisiiphilus and P. frisingensis by ribotyping. J. Am. Soc. Brew. Chem. 1998, 56:19-23.
50. 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. Appl. Microbiol. 2007, 57:2777-2789.
51. Niemann S., Pühler A., Tichy H.-V., Simon R., Selbitschka W. Evaluation of the resolving power of three different DNA fingerprinting methods to discriminate among isolates of a natural Rhizobium meliloti population. J. Appl. Microbiol. 1997, 82:477-484.
52. Nonomura H., Ohara Y. Die Klassifikation de Apfelsaeure-Michsaeure-Bakterien. Mitt. Klosterneuburg 1967, 17:449-465.
53. Paradh A., Mitchell W., Hill A. Occurrence of Pectinatus and Megasphaera in the major UK breweries. J. Inst. Brew. 2011, 117:498-506.
54. Pittet V., Haakensen M., Ziola B. Rapid screening for Gram-negative and Gram-positive beer-spoilage Firmicutes using a real-time multiplex PCR. J. Am. Soc. Brew. Chem. 2010, 68:89-95.
55. Pittet V., Morrow K., Ziola B. Ethanol tolerance of lactic acid bacteria, including relevance of the exopolysaccharide gene gtf. J. Am. Soc. Brew. Chem. 2011, 69:57-61.
56. T. J. Bacteriol. 2012, 194:1271-1272.
57. Priest F.G. Microbiology and microbiological control in the brewery. Handbook of Brewing 2006, 608-625. CRC Press, Boca Raton, Florida USA. second ed. F.G. Priest, G.G. Stewart (Eds.).
58. Russell C., Walker T.K. Lactobacillus malefermentans sp. nov., isolated from beer. J. Gen. Microbiol. 1953, 8:160-162.
59. Sakamoto K., Konings W.N. Beer spoilage bacteria and hop resistance. Int. J. Food Microbiol. 2003, 89:105-124.
60. Satokari R., Mattila-Sandholm T., Suihko M.-L. Identification of pediococci by ribotyping. J. Appl. Microbiol. 2000, 88:260-265.
61. Sauer S., Kliem M. Mass spectrometry tools for the classification and identification of bacteria. Nat. Rev. Microbiol. 2010, 8:74-82.
62. Simpson W., Smith A. Factors affecting antibacterial activity of hop compounds and their derivatives. J. Appl. Microbiol. 1992, 72:327-334.
63. Sokollek S.J., Hertel C., Hammes W.P. Cultivation and preservation of vinegar bacteria. J. Biotechnol. 1998, 60:195-206.
64. 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. 2013, 64:1083-1089.
65. Steiner E., Becker T., Gastl M. Turbidity and haze formation in beer - insights and overview. J. Inst. Brew. 2010, 116:360-368.
66. Storgårds E., Tapani K., Hartwell P., Saleva R., Suihko M.L. Microbial attachment and biofilm formation in brewery bottling plants. J. Am. Soc. Brew. Chem. 2006, 64:8-15.
67. Suzuki K., Koyanagi M., Yamashita H. Genetic characterization and specific detection of beer-spoilage Lactobacillus sp. LA2 and related strains. J. Appl. Microbiol. 2004, 96:677-683.
68. Suzuki K., Ozaki K., Yamashita H. Genetic marker for differentiating beer-spoilage ability of Lactobacillus paracollinoides strains. J. Appl. Microbiol. 2004, 97:712-718.
69. Suzuki K., Iijima K., Ozaki K., Yamashita H. 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. 2005, 71:5089-5097.
70. 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.
71. Suzuki K., Asano S., Iijima K., Kuriyama H., Kitagawa Y. Development of detection medium for hard-to-culture beer-spoilage lactic acid bacteria. J. Appl. Microbiol. 2008, 104:1458-1470.
72. Takeuchi A., Iijima K., Suzuki K., Ozaki K., Yamashita H. Application of ribotyping and rDNA internal space analysis (RISA) for assessment of microflora in brewery environments. J. Am. Soc. Brew. Chem. 2005, 63:73-75.
73. Taskila S., Neubauer P., Tuomola M., Breitenstein A., Kronlöf J., Hillukkala T. Improved enrichment cultivation of beer spoiling lactic acid bacteria by continuous glucose addition to the culture. J. Inst. Brew. 2009, 115:177-182.
74. Taskila S., Tuomola M., Kronlöf J., Neubauer P. Comparison of enrichment media for routine detection of beer spoiling lactic acid bacteria and development of trouble-shooting medium for Lactobacillus backii. J. Inst. Brew. 2010, 116:151-156.
75. Timke M., Wolking D., Wang-Lieu N.Q., Altendorf K., Lipski A. Microbial composition of biofilms in a brewery investigated by fatty acid analysis, fluorescence in situ hybridisation and isolation techniques. Appl. Microbiol. Biotechnol. 2004, 66:100-107.
76. Tohno M., Kitahara M., Irisawa T., Masuda T., Uegaki R., Ohkuma M., Tajima K. Description of Lactobacillus iwatensis sp. nov., isolated from orchardgrass (Dactylis glomerata L.) silage in Iwate, Japan, and Lactobacillus backii sp. nov. Int. J. Syst. Appl. Microbiol. 2013, 63:3854-3860.
77. Tsuchiya Y., Yaizu J.P. Antibodies for the detection of beer spoilage lactic acid bacteria and kit employing the antibodies 2002, 9. Sapporo Breweries Limited, Tokyo (JP); US 6,395,500 B1, United States of America.
78. Valentine N., Wunschel S., Wunschel D., Petersen C., Wahl K. Effect of culture conditions on microorganism identification by matrix-assisted laser desorption/ionization mass spectrometry. Appl. Environ. Microbiol. 2005, 71:58-64.
79. Valera M.J., Laich F., Gonzalez S.S., Torija M.J., Mateo E., Mas A. Diversity of acetic acid bacteria present in healthy grapes from the Canary Islands. Int. J. Food Microbiol. 2011, 151:105-112.
80. van Veen S.Q., Claas E.C., Kuijper E.J. High-throughput identification of bacteria and yeast by matrix-assisted laser desorption ionization-time of flight mass spectrometry in conventional medical microbiology laboratories. J. Clin. Microbiol. 2010, 48:900-907.
81. Van Vuuren H.J.J., Priest F.G. Gram-negative brewery bacteria. Brewing Microbiology 2003, 219-246. third ed. F.G. Priest, I. Campbell (Eds.).
82. Vaughan A., O'Sullivan T., Sinderen D. Enhancing the microbiological stability of malt and beer - a review. J. Inst. Brew. 2005, 111:355-371.
83. Vriesekoop F., Krahl M., Hucker B., Menz G. 125th Anniversary review: bacteria in brewing: the good, the bad and the ugly. J. Inst. Brew. 2013, 335-345.
84. Walker J., Fox A.J., Edwards-Jones V., Gordon D.B. Intact cell mass spectrometry (ICMS) used to type methicillin-resistant Staphylococcus aureus: media effects and inter-laboratory reproducibility. J. Microbiol. Methods 2002, 48:117-126.
85. Weber D.G., Sahm K., Polen T., Wendisch V.F., Antranikian G. Oligonucleotide microarrays for the detection and identification of viable beer spoilage bacteria. J. Appl. Microbiol. 2008, 105:951-962.
86. T are strains of Pediococcus acidilactici. Int. J. Syst. Appl. Microbiol. 2012, 62:3105-3108.
87. Wieme A.D., Spitaels F., Aerts M., De Bruyne K., Van Landschoot A., Vandamme P. The effects of the growth medium on matrix-assisted laser desorption/ionization time-of-flight mass spectra: a case study of acetic acid bacteria. Appl. Environ. Microbiol. 2014, 80:1528-1538.
88. Wieme A.D., Spitaels F., Balzarini T., Cleenwerck I., Van Landschoot A., De Vuyst L., Vandamme P. Gluconobacter cerevisiae sp. nov. isolated from the brewery environment. Int. J. Syst. Appl. Microbiol. 2014, 64:1134-1141.
89. Wieser A., Schneider L., Jung J., Schubert S. MALDI-TOF MS in microbiological diagnostics-identification of microorganisms and beyond (mini review). Appl. Microbiol. Biotechnol. 2012, 93:965-974.
90. Wilhelmson A., Londesborough J., Juvonen R. Microbiological analysis of shipwreck beers, VTT Technical Research Center of Finland. 34th European Brewing Convention (EBC) congress 2013.
91. Yansanjav A., Siegumfeldt H., Jespersen L., Vancanneyt M., Swings J., Hollerova I., Leisner J.J. Detection of resistance of lactic acid bacteria to a mixture of the hop analogue compounds tetrahydroiso-alpha-acids by noninvasive measurement of intracellular pH. J. Appl. Microbiol. 2004, 96:1324-1332.
92. Ziola B., Ulmer M., Bueckert J., Giesbrecht D., Lee S. Monoclonal antibodies showing surface reactivity with Lactobacillus and Pediococcus beer spoilage bacteria. J. Am. Soc. Brew. Chem. 2000, 58:63-68.