Application of flow cytometry to wine microorganisms

Food Microbiology

Volumn 62, Issue , 2017, Pages 221-231

  Longin, Cédric ^a   Petitgonnet, Clément ^a   Guilloux Benatier, Michèle ^a   Rousseaux, Sandrine ^a   Alexandre, Hervé ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

Author keywords

Enumeration; Flow cytometry; Identification; Physiological state; Wine bacteria; Wine yeasts

Indexed keywords

FLUORESCENT DYE;

ANALYSIS; BACTERIAL COUNT; BACTERIUM; CLASSIFICATION; FERMENTATION; FLOW CYTOMETRY; FOOD CONTROL; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PROCEDURES; SACCHAROMYCES CEREVISIAE; WINE; YEAST;

BACTERIA; COLONY COUNT, MICROBIAL; FERMENTATION; FLOW CYTOMETRY; FLUORESCENT DYES; FOOD MICROBIOLOGY; SACCHAROMYCES CEREVISIAE; WINE; YEASTS;

EID: 84992732427     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2016.10.023     Document Type: Review

References (103)

1. Adam, G., Duncan, H., Development of a sensitive and rapid method for the measurement of total microbial activity using fluorescein diacetate (FDA) in a range of soils. Soil Biol. Biochem. 33 (2001), 943–951.
2. Alexandre, H., Rousseaux, I., Charpentier, C., Relationship between ethanol tolerance, lipid composition and plasma membrane fluidity in Saccharomyces cerevisiae and Kloeckera apiculata. FEMS Microbiol. Lett. 124 (1994), 17–22.
3. Amor, K.B., Breeuwer, P., Verbaarschot, P., Rombouts, F.M., Akkermans, A.D.L., Vos, W.M.D., Abee, T., Multiparametric flow cytometry and cell sorting for the assessment of viable, injured, and dead bifidobacterium cells during bile salt stress. Appl. Environ. Microbiol. 68 (2002), 5209–5216.
4. Andorra, I., Monteiro, M., Esteve-Zarzoso, B., Albergaria, H., Mas, A., Analysis and direct enumeration of Saccharomyces cerevisiae and Hanseniaspora guilliermondii populations during alcoholic fermentation by fluorescence in situ hybridization, flow cytometry and quantitative PCR. Food Microbiol. 28 (2011), 1483–1491.
5. Bagalkot, V., Zhang, L., Levy-Nissenbaum, E., Jon, S., Kantoff, P.W., Langer, R., Farokhzad, O.C., Quantum dot−aptamer conjugates for synchronous cancer imaging, therapy, and sensing of drug delivery based on bi-fluorescence resonance energy transfer. Nano Lett. 7 (2007), 3065–3070.
6. Blasco, L., Ferrer, S., Pardo, I., Development of specific fluorescent oligonucleotide probes for in situ identification of wine lactic acid bacteria. FEMS Microbiol. Lett. 225 (2003), 115–123.
7. Bouchez, J.C., Cornu, M., Danzart, M., Leveau, J.Y., Duchiron, F., Bouix, M., Physiological significance of the cytometric distribution of fluorescent yeasts after viability staining. Biotechnol. Bioeng. 86 (2004), 520–530.
8. Bouix, M., Ghorbal, S., Rapid assessment of Oenococcus oeni activity by measuring intracellular pH and membrane potential by flow cytometry, and its application to the more effective control of malolactic fermentation. Int. J. Food Microbiol. 193 (2015), 139–146.
9. Bouix, M., Ghorbal, S., Rapid enumeration of Oenococcus oeni during malolactic fermentation by flow cytometry. J. Appl. Microbiol. 114 (2013), 1075–1081.
10. Bouix, M., Leveau, J.-Y., Rapid assessment of yeast viability and yeast vitality during alcoholic fermentation. J. Inst. Brew. 107 (2001), 217–225.
11. Branco, P., Monteiro, M., Moura, P., Albergaria, H., Survival rate of wine-related yeasts during alcoholic fermentation assessed by direct live/dead staining combined with fluorescence in situ hybridization. Int. J. Food Microbiol. 158 (2012), 49–57.
12. Bruetschy, A., Laurent, M., Jacquet, R., Use of flow cytometry in oenology to analyse yeasts. Lett. Appl. Microbiol. 18 (1994), 343–345.
13. Chaillet, L., Martin, G., Genty, V., Mise au point d'une méthode de détection des Brettanomyces par immunocytométrie. Personal communication in SFI-AFC Congress, 2014.
14. Chaney, D., Rodriguez, S., Fugelsang, K., Thornton, R., Managing high-density commercial scale wine fermentations. J. Appl. Microbiol. 100 (2006), 689–698.
15. Conterno, L., Joseph, C.M.L., Arvik, T.J., Henick-Kling, T., Bisson, L.F., Genetic and physiological characterization of Brettanomyces bruxellensis strains isolated from wines. Am. J. Enol. Vitic. 57 (2006), 139–147.
16. Dabbousi, B.O., Bawendi, M.G., Onitsuka, O., Rubner, M.F., Electroluminescence from CdSe quantum-dot/polymer composites. Appl. Phys. Lett. 66 (1995), 1316–1318.
17. Da Silveira, M.G., Romão, M.V.S., Loureiro-Dias, M.C., Rombouts, F.M., Abee, T., Flow cytometric assessment of membrane integrity of ethanol-stressed Oenococcus oeni cells. Appl. Environ. Microbiol. 68 (2002), 6087–6093.
18. Davey, H.M., Hexley, P., Red but not dead? Membranes of stressed Saccharomyces cerevisiae are permeable to propidium iodide. Environ. Microbiol. 13 (2011), 163–171.
19. Delobel, P., Pradal, M., Blondin, B., Tesniere, C., A “fragile cell” sub-population revealed during cytometric assessment of Saccharomyces cerevisiae viability in lipid-limited alcoholic fermentation. Lett. Appl. Microbiol. 55 (2012), 338–344.
20. Diaper, J.P., Edwards, C., The use of fluorogenic esters to detect viable bacteria by flow cytometry. J. Appl. Bacteriol. 77 (1994), 221–228.
21. Díaz, M., Herrero, M., García, L.A., Quirós, C., Application of flow cytometry to industrial microbial bioprocesses. Biochem. Eng. J. 48 (2010), 385–407 Invited Review Issue 2010.
22. Divol, B., Lonvaud-Funel, A., Evidence for viable but nonculturable yeasts in botrytis-affected wine. J. Appl. Microbiol. 99 (2005), 85–93.
23. Duan, N., Wu, S., Yu, Y., Ma, X., Xia, Y., Chen, X., Huang, Y., Wang, Z., A dual-color flow cytometry protocol for the simultaneous detection of Vibrio parahaemolyticus and Salmonella typhimurium using aptamer conjugated quantum dots as labels. Anal. Chim. Acta 804 (2013), 151–158.
24. Dupont, S., Beney, L., Ferreira, T., Gervais, P., Nature of sterols affects plasma membrane behavior and yeast survival during dehydration. Biochim. Biophys. Acta BBA Biomembr. 1808 (2011), 1520–1528.
25. Ellington, A.D., Szostak, J.W., In vitro selection of RNA molecules that bind specific ligands. Nature 346 (1990), 818–822.
26. Farthing, J.B., Rodriguez, S.B., Thornton, R.J., Flow cytometric analysis of Saccharomyces cerevisiae populations in high-sugar Chardonnay fermentations. J. Sci. Food Agric. 87 (2007), 527–533.
27. Fernandes, R.L., Carlquist, M., Lundin, L., Heins, A.L., Dutta, A., Sørensen, S.J., Jensen, A.D., Nopens, I., Lantz, A.E., Gernaey, K.V., Cell mass and cell cycle dynamics of an asynchronous budding yeast population: experimental observations, flow cytometry data analysis, and multi-scale modeling. Biotechnol. Bioeng. 110 (2013), 812–826.
28. Fuchs, P., Weichel, W., Dübel, S., Breitling, F., Little, M., Separation of E. coli expressing functional cell-wall bound antibody fragments by FACS. Immunotechnology 2 (1996), 97–102.
29. Fulwyler, M.J., Electronic separation of biological cells by volume. Science 150 (1965), 910–911.
30. Gant, V.A., Warnes, G., Phillips, I., Savidge, G.F., The application of flow cytometry to the study of bacterial responses to antibiotics. J. Med. Microbiol. 39 (1993), 147–154.
31. Gerbaux, V., Thomas, J., Utilisations pratiques de ma cytométrie de flux pour le suivi des levures en œnologie. Rev. Fr. Oenologie, 2009, 8–13.
32. Gibson, F.C., Hong, C., Chou, H.H., Yumoto, H., Chen, J., Lien, E., Wong, J., Genco, C.A., Innate immune recognition of invasive bacteria accelerates atherosclerosis in apolipoprotein E-deficient mice. Circulation 109 (2004), 2801–2806.
33. Greenspan, P., Mayer, E.P., Fowler, S.D., Nile red: a selective fluorescent stain for intracellular lipid droplets. J. Cell Biol. 100 (1985), 965–973.
34. Guillamón, J.M., Mas, A., Chapter 9-Acetic acid bacteria. Carrascosa, A.V., Muñoz, R., González, R., (eds.) Molecular Wine Microbiology, 2011, Academic Press, San Diego, 227–255.
35. Haines, T.H., Do sterols reduce proton and sodium leaks through lipid bilayers?. Prog. Lipid Res. 40 (2001), 299–324.
36. Han, H.S., Niemeyer, E., Huang, Y., Kamoun, W.S., Martin, J.D., Bhaumik, J., Chen, Y., Roberge, S., Cui, J., Martin, M.R., Fukumura, D., Jain, R.K., Bawendi, M.G., Duda, D.G., Quantum dot/antibody conjugates for in vivo cytometric imaging in mice. Proc. Natl. Acad. Sci. 112 (2015), 1350–1355.
37. Henderson, L.M., Chappell, J.B., Dihydrorhodamine 123: a fluorescent probe for superoxide generation?. Eur. J. Biochem. 217 (1993), 973–980.
38. Henry-Stanley, M.J., Garni, R.M., Wells, C.L., Adaptation of FUN-1 and Calcofluor white stains to assess the ability of viable and nonviable yeast to adhere to and be internalized by cultured mammalian cells. J. Microbiol. Methods 59 (2004), 289–292.
39. Henschke, P.A., Jiranek, V., Yeast: metabolism of nitrogen compounds. Fleet, G.H., (eds.) Wine Microbiology and Biotechnology, 1993, Harwood Academic, Chur, Switzerland, 77–165.
40. Herrero, M., Quirós, C., García, L.A., Díaz, M., Use of flow cytometry to follow the physiological states of microorganisms in cider fermentation processes. Appl. Environ. Microbiol. 72 (2006), 6725–6733.
41. Inácio, J., Behrens, S., Fuchs, B.M., Fonseca, Á., Spencer-Martins, I., Amann, R., In situ accessibility of Saccharomyces cerevisiae 26S rRNA to Cy3-labeled oligonucleotide probes comprising the D1 and D2 domains. Appl. Environ. Microbiol. 69 (2003), 2899–2905.
42. Jayakody, L.N., Kadowaki, M., Tsuge, K., Horie, K., Suzuki, A., Hayashi, N., Kitagaki, H., SUMO expression shortens the lag phase of Saccharomyces cerevisiae yeast growth caused by complex interactive effects of major mixed fermentation inhibitors found in hot-compressed water-treated lignocellulosic hydrolysate. Appl. Microbiol. Biotechnol. 99 (2014), 501–515.
43. Jayasena, S.D., Aptamers: an emerging class of molecules that rival antibodies in diagnostics. Clin. Chem. 45 (1999), 1628–1650.
44. Julius, M.H., Masuda, T., Herzenberg, L.A., Demonstration that antigen-binding cells are precursors of antibody-producing cells after purification with a fluorescence-activated cell sorter. Proc. Natl. Acad. Sci. U. S. A. 69 (1972), 1934–1938.
45. Kahana, J.A., Schnapp, B.J., Silver, P.A., Kinetics of spindle pole body separation in budding yeast. Proc. Natl. Acad. Sci. 92 (1995), 9707–9711.
46. Kitagaki, H., Shimoi, H., Mitochondrial dynamics of yeast during sake brewing. J. Biosci. Bioeng. 104 (2007), 227–230.
47. Kobayashi, M., Shimizu, H., Shioya, S., Physiological analysis of yeast cells by flow cytometry during serial-repitching of low-malt beer fermentation. J. Biosci. Bioeng. 103 (2007), 451–456.
48. Landolfo, S., Politi, H., Angelozzi, D., Mannazzu, I., ROS accumulation and oxidative damage to cell structures in Saccharomyces cerevisiae wine strains during fermentation of high-sugar-containing medium. Biochim. Biophys. Acta BBA Gen. Subj. 1780 (2008), 892–898.
49. Lloyd, D., Hayes, A.J., Vigour, vitality and viability of microorganisms. FEMS Microbiol. Lett. 133 (1995), 1–7.
50. Longobardi-Givan, A., Flow Cytometry: First Principles. second ed., 2001, John Wiley & Sons, New York.
51. Loubiere, P., Salou, P., Leroy, M.J., Lindley, N.D., Pareilleux, A., Electrogenic malate uptake and improved growth energetics of the malolactic bacterium Leuconostoc oenos grown on glucose-malate mixtures. J. Bacteriol. 174 (1992), 5302–5308.
52. Malacrinò, P., Zapparoli, G., Torriani, S., Dellaglio, F., Rapid detection of viable yeasts and bacteria in wine by flow cytometry. J. Microbiol. Methods 45 (2001), 127–134.
53. Mannazzu, I., Angelozzi, D., Belviso, S., Budroni, M., Farris, G.A., Goffrini, P., Lodi, T., Marzona, M., Bardi, L., Behaviour of Saccharomyces cerevisiae wine strains during adaptation to unfavourable conditions of fermentation on synthetic medium: cell lipid composition, membrane integrity, viability and fermentative activity. Int. J. Food Microbiol. 121 (2008), 84–91.
54. Marsit, S., Mena, A., Bigey, F., Sauvage, F.-X., Couloux, A., Guy, J., Legras, J.-L., Barrio, E., Dequin, S., Galeote, V., Evolutionary advantage conferred by an Eukaryote-to-Eukaryote gene transfer event in wine yeasts. Mol. Biol. Evol. 32 (2015), 1695–1707.
55. Mason, D.J., Shanmuganathan, S., Mortimer, F.C., Gant, V.A., A fluorescent gram stain for flow cytometry and epifluorescence microscopy. Appl. Environ. Microbiol. 64 (1998), 2681–2685.
56. Mattoussi, H., Mauro, J.M., Goldman, E.R., Anderson, G.P., Sundar, V.C., Mikulec, F.V., Bawendi, M.G., Self-assembly of CdSe−ZnS quantum dot bioconjugates using an engineered recombinant protein. J. Am. Chem. Soc. 122 (2000), 12142–12150.
57. Mendes-Ferreira, A., Sampaio-Marques, B., Barbosa, C., Rodrigues, F., Costa, V., Mendes-Faia, A., Ludovico, P., Leão, C., Accumulation of non-superoxide anion reactive oxygen species mediates nitrogen-limited alcoholic fermentation by Saccharomyces cerevisiae. Appl. Environ. Microbiol. 76 (2010), 7918–7924.
58. Meyer, M., Scheper, T., Walter, J.-G., Aptamers: versatile probes for flow cytometry. Appl. Microbiol. Biotechnol. 97 (2013), 7097–7109.
59. Millet, V., Lonvaud-Funel, A., The viable but non-culturable state of wine micro-organisms during storage. Lett. Appl. Microbiol. 30 (2000), 136–141.
60. Monthéard, J., Garcier, S., Lombard, E., Cameleyre, X., Guillouet, S., Molina-Jouve, C., Alfenore, S., Assessment of Candida shehatae viability by flow cytometry and fluorescent probes. J. Microbiol. Methods 91 (2012), 8–13.
61. Moon, J.-H., Kim, G., Park, S.B., Lim, J., Mo, C., The importance of FACS analysis in the development of aptamers specific to pathogens. J. Biosyst. Eng. 39 (2014), 111–114.
62. Morata, A., Gómez-Cordovés, M.C., Suberviola, J., Bartolomé, B., Colomo, B., Suárez, J.A., Adsorption of anthocyanins by yeast cell walls during the fermentation of red wines. J. Agric. Food Chem. 51 (2003), 4084–4088.
63. Müller, S., Ullrich, S., Lösche, A., Loffhagen, N., Babel, W., Flow cytometric techniques to characterise physiological states of Acinetobacter calcoaceticus. J. Microbiol. Methods 40 (2000), 67–77.
64. Müllner, H., Daum, G., Dynamics of neutral lipid storage in yeast. Acta Biochim. Pol. 51 (2004), 323–347.
65. Muñoz, R., Moreno-Arribas, M.V., Rivas, B. de las, Chapter 8-Lactic acid bacteria. Carrascosa, A.V., Muñoz, R., González, R., (eds.) Molecular Wine Microbiology, 2011, Academic Press, San Diego, 191–226.
66. Niedenthal, R.K., Riles, L., Johnston, M., Hegemann, J.H., Green fluorescent protein as a marker for gene expression and subcellular localization in budding yeast. Yeast 12 (1996), 773–786.
67. Oliver, J.D., The viable but nonculturable state in bacteria. J. Microbiol. 43 (2005), 93–100.
68. O'Neill, K., Aghaeepour, N., Špidlen, J., Brinkman, R., Flow cytometry bioinformatics. PLoS Comput. Biol., 9, 2013, e1003365.
69. Orij, R., Postmus, J., Ter Beek, A., Brul, S., Smits, G.J., In vivo measurement of cytosolic and mitochondrial pH using a pH-sensitive GFP derivative in Saccharomyces cerevisiae reveals a relation between intracellular pH and growth. Microbiology 155 (2009), 268–278.
70. Prosperi, E., Croce, A.C., Bottiroli, G., Supino, R., Flow cytometric analysis of membrane permeability properties influencing intracellular accumulation and efflux of fluorescein. Cytometry 7 (1986), 70–75.
71. Quirós, C., Herrero, M., García, L.A., Díaz, M., Quantitative approach to determining the contribution of viable-but-nonculturable subpopulations to malolactic fermentation processes. Appl. Environ. Microbiol. 75 (2009), 2977–2981.
72. Razmkhab, S., Lopez-Toledano, A., Ortega, J.M., Mayen, M., Merida, J., Medina, M., Adsorption of phenolic compounds and browning products in white wines by yeasts and their cell walls. J. Agric. Food Chem. 50 (2002), 7432–7437.
73. Röder, C., König, H., Fröhlich, J., Species-specific identification of Dekkera/Brettanomyces yeasts by fluorescently labeled DNA probes targeting the 26S rRNA. FEMS Yeast Res. 7 (2007), 1013–1026.
74. Rodriguez, S.B., Thornton, R.J., Use of flow cytometry with fluorescent antibodies in real-time monitoring of simultaneously inoculated alcoholic-malolactic fermentation of Chardonnay. Lett. Appl. Microbiol. 46 (2008), 38–42.
75. Romano, A., Perello, M.C., de Revel, G., Lonvaud-Funel, A., Growth and volatile compound production by Brettanomyces/Dekkera bruxellensis in red wine. J. Appl. Microbiol. 104 (2008), 1577–1585.
76. Rossen, L., Nørskov, P., Holmstrøm, K., Rasmussen, O.F., Inhibition of PCR by components of food samples, microbial diagnostic assays and DNA-extraction solutions. Int. J. Food Microbiol. 17 (1992), 37–45.
77. Roth, B.L., Poot, M., Yue, S.T., Millard, P.J., Bacterial viability and antibiotic susceptibility testing with SYTOX green nucleic acid stain. Appl. Environ. Microbiol. 63 (1997), 2421–2431.
78. Salema, M., Capucho, I., Poolman, B., Romão, M.V.S., Dias, M.C., In vitro reassembly of the malolactic fermentation pathway of Leuconostoc oenos (Oenococcus oeni). J. Bacteriol. 178 (1996), 5537–5539.
79. Salema, M., Poolman, B., Lolkema, J.S., Dias, M.C.L., Konings, W.N., Uniport of monoanionic L-malate in membrane vesicles from Leuconostoc Oenos. Eur. J. Biochem. 225 (1994), 289–295.
80. Salma, M., Rousseaux, S., Sequeira-Le Grand, A., Alexandre, H., Cytofluorometric detection of wine lactic acid bacteria: application of malolactic fermentation to the monitoring. J. Ind. Microbiol. Biotechnol. 40 (2012), 63–73.
81. Salma, M., Rousseaux, S., Sequeira-Le Grand, A., Divol, B., Alexandre, H., Characterization of the viable but nonculturable (VBNC) state in Saccharomyces cerevisiae. PLoS One, 8, 2013, e77600.
82. Serpaggi, V., Remize, F., Sequeira-Le Grand, A., Alexandre, H., Specific identification and enumeration of the spoilage microorganism Brettanomyces in wine by flow cytometry: a useful tool for winemakers. Cytom. A 77A (2010), 497–499.
83. Serpaggi, V., Remize, F., Recorbet, G., Gaudot-Dumas, E., Sequeira-Le Grand, A., Alexandre, H., Characterization of the “viable but nonculturable” (VBNC) state in the wine spoilage yeast Brettanomyces. Food Microbiol. 30 (2012), 438–447.
84. Shapiro, H.M., Practical Flow Cytometry. fourth ed., 2003, John Wiley & Sons. Inc., Hoboken. New Jersey.
85. Shiroma, S., Jayakody, L.N., Horie, K., Okamoto, K., Kitagaki, H., Enhancement of ethanol fermentation in Saccharomyces cerevisiae sake yeast by disrupting mitophagy function. Appl. Environ. Microbiol. 80 (2014), 1002–1012.
86. Shroff, K.E., Meslin, K., Cebra, J.J., Commensal enteric bacteria engender a self-limiting humoral mucosal immune response while permanently colonizing the gut. Infect. Immun. 63 (1995), 3904–3913.
87. Steensels, J., Meersman, E., Snoek, T., Saels, V., Verstrepen, K.J., Large-scale selection and breeding to generate industrial yeasts with superior aroma production. Appl. Environ. Microbiol. 80 (2014), 6965–6975.
88. Stender, H., Kurtzman, C., Hyldig-Nielsen, J.J., Sørensen, D., Broomer, A., Oliveira, K., Perry-O'Keefe, H., Sage, A., Young, B., Coull, J., Identification of Dekkera bruxellensis (Brettanomyces) from wine by fluorescence in situ hybridization using peptide nucleic acid probes. Appl. Environ. Microbiol. 67 (2001), 938–941.
89. Tada, Y., Grossart, H.-P., Community shifts of actively growing lake bacteria after N-acetyl-glucosamine addition: improving the BrdU-FACS method. ISME J. 8 (2014), 441–454.
90. Tesnière, C., Delobel, P., Pradal, M., Blondin, B., Impact of nutrient imbalance on wine alcoholic fermentations: nitrogen excess enhances yeast cell death in lipid-limited must. PLoS One, 8, 2013, e61645.
91. Torija, M.J., Mateo, E., Guillamón, J.M., Mas, A., Identification and enumeration of acetic acid bacteria in wine and vinegar by TaqMan–MGB probes. Food Microbiol. 27 (2010), 257–265.
92. Toulmé, J., Giegé, R., Les aptamères: des ligands et des catalyseurs oligonucléotidiques obtenus par sélection in vitro. Méd. Sci., 14, 1998, 155.
93. Tourdot-Maréchal, R., Gaboriau, D., Beney, L., Diviès, C., Membrane fluidity of stressed cells of Oenococcus oeni. Int. J. Food Microbiol. 55 (2000), 269–273.
94. Valera, M.J., Torija, M.J., Mas, A., Mateo, E., Acetobacter malorum and Acetobacter cerevisiae identification and enumeration by Real-Time PCR with TaqMan-MGB probes. Food Microbiol. 36 (2013), 30–39.
95. Wallner, G., Amann, R., Beisker, W., Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14 (1993), 136–143.
96. Walther, A., Hesselbart, A., Wendland, J., Genome sequence of Saccharomyces carlsbergensis, the world's first pure culture lager yeast. G3 Genes Genomes Genet. 4 (2014), 783–793.
97. Wang, A., Chen, L., Pu, K., Zhu, Y., Identification of stem-like cells in non-small cell lung cancer cells with specific peptides. Cancer Lett. 351 (2014), 100–107.
98. Wang, B., Wang, Q., Cai, Z., Ma, M., Simultaneous, rapid and sensitive detection of three food-borne pathogenic bacteria using multicolor quantum dot probes based on multiplex fluoroimmunoassay in food samples. LWT Food Sci. Technol. 61 (2015), 368–376.
99. Wang, C., Esteve-Zarzoso, B., Mas, A., Monitoring of Saccharomyces cerevisiae, Hanseniaspora uvarum, and Starmerella bacillaris (synonym Candida zemplinina) populations during alcoholic fermentation by fluorescence in situ hybridization. Int. J. Food Microbiol. 191 (2014), 1–9.
100. West, J.L., Halas, N.J., Applications of nanotechnology to biotechnology: commentary. Curr. Opin. Biotechnol. 11 (2000), 215–217.
101. Wilson, I.G., Inhibition and facilitation of nucleic acid amplification. Appl. Environ. Microbiol., 63, 1997, 3741.
102. Xufre, A., Albergaria, H., Inácio, J., Spencer-Martins, I., Gírio, F., Application of fluorescence in situ hybridisation (FISH) to the analysis of yeast population dynamics in winery and laboratory grape must fermentations. Int. J. Food Microbiol. 108 (2006), 376–384.
103. Yamaguchi, T., Kawakami, S., Hatamoto, M., Imachi, H., Takahashi, M., Araki, N., Yamaguchi, T., Kubota, K., In situ DNA-hybridization chain reaction (HCR): a facilitated in situ HCR system for the detection of environmental microorganisms. Environ. Microbiol. 17 (2015), 2532–2541.