Fluorescent probes to evaluate the physiological state and activity of microbial biocatalysts: A guide for prokaryotic and eukaryotic investigation

Biotechnology Journal

Volumn 3, Issue 7, 2008, Pages 890-903

  Cao Hoang, Lan ^a,b   Marechal, Pierre André ^a   Lê Thanh, Mai ^b   Gervais, Patrick ^a   Waché, Yves ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b HANOI UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Viet Nam)

Author keywords

Activity; Cell physiology; Fluorescent probes; Membrane state; Viability

Indexed keywords

ACTIVITY; BACTERIAL CELLS; CELL PHYSIOLOGY; EUKARYOTIC MICROORGANISMS; FLUORESCENT PROBES; FLUORESCENT PROBING; INTRACELLULAR PH; MEMBRANE POTENTIALS; MEMBRANE STATE; MICROBIAL BIOCATALYSTS; MICROBIAL CELLS; NEW DEVELOPMENTS; PHYSIOLOGICAL STATES; VIABILITY; YEAST CELLS;

ACIDS; BACTERIOLOGY; BIOTECHNOLOGY; CELL MEMBRANES; CELLS; CHLORINE COMPOUNDS; FLUORESCENCE; LIGHT EMISSION; LUMINESCENCE; NUCLEIC ACIDS; RELIABILITY; TECHNOLOGY;

CYTOLOGY;

FLUORESCENT DYE; NUCLEIC ACID;

ACCURACY; BACTERIAL CELL; BIOCATALYST; BIOTECHNOLOGY; CELL ACTIVITY; CELL COMPARTMENTALIZATION; CELL INTERACTION; CELL MEMBRANE PERMEABILITY; CELL MEMBRANE POTENTIAL; CELL PH; CELL VIABILITY; EUKARYOTE; FLUORESCENCE ANALYSIS; GRAM NEGATIVE BACTERIUM; MEMBRANE FLUIDITY; MICROBIAL ACTIVITY; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROKARYOTE; REVIEW; YEAST CELL;

CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; FLUORESCENT DYES; GRAM-NEGATIVE BACTERIA; HYDROGEN-ION CONCENTRATION; INDUSTRIAL MICROBIOLOGY; MEMBRANE FLUIDITY; MEMBRANE POTENTIALS; MICROSCOPY, FLUORESCENCE; SPECTROMETRY, FLUORESCENCE; YEASTS;

BACTERIA (MICROORGANISMS); EUKARYOTA; NEGIBACTERIA; PROKARYOTA;

EID: 48749109058     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.200700206     Document Type: Review

References (81)

1. Trevors, J. T., Fluorescent probes for bacterial cytoplasmic membrane research. J. Biochem. Biophys. Methods 2003, 57, 87-103.
2. Greenspan, P., Fowler, S. D., Spectrofluorometric studies of the lipid probe, nile red. J. Lipid Res. 1985, 26, 781-789.
3. Demeule, B., Gurny R., Arvinte, T., Detection and characterization of protein aggregates by fluorescence microscopy Int. J. Pharm. 2007, 329, 37-45.
4. Albani, J. R., Plancke, Y. D., Interaction between calcofluor white and carbohydrates of alpha 1-acid glycoprotein. Carbohydr. Res. 1998, 314, 169-175.
5. Delic, J., Coppey J., Magdelenat, H., Coppey-Moisan, M., Impossibility of acridine orange intercalation in nuclear DNA of the living cell. Exp. Cell Res. 1991, 194, 147-153.
6. Arbildua, J. J., Brunet, J. E., Jameson, D. M., Lopez, M. et al., Fluorescence resonance energy transfer and molecular modeling studies on 4′,6-diamidino-2-phenylindole (DAPI) complexes with tubulin. Protein Sci. 2006, 15, 410-419.
7. Tsien, R. Y., The green fluorescent protein. Annu. Rev. Biochem. 1998, 67, 509-544.
8. Bastiaens, P. I. H., Squire, A., Fluorescence lifetime imaging microscopy: Spatial resolution of biochemical processes in the cell. Trends Cell Biol. 1999, 9, 48-52.
9. North, A. J., Seeing is believing? A beginners'guide to practical pitfalls in image acquisition. J. Cell Biol. 2006, 172, 9-18.
10. Lakowicz, J. R., Principles of Fluorescence Spectroscopy, Plenum Press, New York 1983.
11. Repakova, J., Holopainen, J. M., Morrow, M. R., McDonald, M. C. et al., Influence of DPH on the structure and dynamics of a DPPC bilayer. Biophys. J. 2005, 88, 3398-3410.
12. Somerharju, P., Pyrene-labeled lipids as tools in membrane biophysics and cell biology. Chem. Phys. Lipids 2002, 116, 57-74.
13. Santos, N. C., Prieto, M., Castanho, M. A., Quantifying molecular partition into model systems of biomembranes: An emphasis on optical spectroscopic methods. Biochim. Biophys. Acta 2003, 1612, 123-135.
14. Hazel, J. R., Thermal adaptation in biological membranes: Is homeoviscous adaptation the explanation? Annu. Rev. Physiol. 1995, 57, 19-42.
15. Novo, D. J., Perlmutter, N. G., Hunt, R. H., Shapiro, H. M., Multiparameter flow cytometric analysis of antibiotic effects on membrane potential, membrane permeability and bacterial counts of Staphylococcus aureus and Micrococcus luteus. Antimicrob. Agents Chemother. 2000, 44, 827-834.
16. Vives-Rego, J., Lebaron, P., Nebe-von Caron, G., Current and future applications of flow cylometry in aquatic microbiology. FEMS Microbiol. Rev. 2000, 24, 429-448.
17. Lloyd, D., Hayes, A. J., Vigour, vitality and viability of microorganisms. FEMS Microbiol. Lett. 1995, 133, 1-7.
18. Nebe-von-Caron, G., Stephens, P.J., Hewitt, C.J., Powell, J. R., Badley R. A., Analysis of bacterial function by multi-colour fluorescence flow cytometry and single cell sorting. J. Microbiol. Methods 2000, 42, 97-114.
19. Ly, M. H., Vo, N. H., Le, T. M., Belin, J. M., Waché, Y., Diversity of the surface properties of Lactococci and consequences on adhesion to food components. Colloids Surf. 2006, 52, 149-153.
20. 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. 1997, 63, 2421-2431.
21. Kell, D. B., Kaprelyants, A. S., Weichart, D. H., Harwood, C. R., Barer, M. R., Viability and activity in readily culturable bacteria: A review and discussion of the practical issues. Antonie Van Leeuwenhoek 1998, 73, 169-187.
22. Singer, S. J., The structure and function of membranes - Personal memoir. J. Membr. Biol. 1992, 129, 3-12.
23. Joux, F., Lebaron, P., Troussellier, M., Succession of cellular states in a Salmonella typhimurium population during starvation in artificial seawater microcosms. FEMS Microbiol. Ecol. 1997, 22, 65-76.
24. Beney L., Gervais, P., Influence of the fluidity of the membrane on the response of microorganisms to environmental stresses. Appl. Microbiol. Biotechnol. 2001, 57, 34-42.
25. Shechter, E., Fluidité membranaire, in: Shechter, E. (Ed.), Biochimie et Biophysique des Membranes. Aspects Structuraux et Fonctionnels, Masson, Paris 1997, pp. 95-110.
26. Kaiser, R. D., London, E., Location of diphenylhexatriene (DPH) and its derivatives within membranes: Comparison of different fluorescence quenching analyses of membrane depth. Biochemistry 1998, 37, 8180-8190.
27. Fiorini, R., Littarru, G. P., Coppa, G. V., Kantar, A., Plasma membrane polarity of polymorphonuclear leucocytes from children with primary ciliary dyskinesia. Eur. J. Clin. Invest. 2000, 30, 519-525.
28. Parasassi, T., Krasnowska, E. K., Bagatolli, L., Gratton, E., Laurdan and prodan as polarity-sensitive fluorescent membrane probes. J. Fluoresc. 1998, 8, 365-373.
29. Chattopadhyay A., Chemistry and biology of N-(7-nitrobenz-2-oxa-1,3-diazol-4-yl)-labeled lipids: Fluorescent probes of biological and model membranes. Chem. Phys. Lipids 1990, 53, 1-15.
30. Kitagawa, S., Matsubayashi, M., Kotani, K., Usui, K., Kametani, F., Asymmetry of membrane fluidity in the lipid bilayer of blood platelets: Fluorescence study with diphenylhexatriene and analogs. J. Membr. Biol. 1991, 119, 221-227.
31. Williams, E. E., Hazel, J. R., Membrane fluidity and hemilayer temperature sensitivity in trout hepatocytes during brief in vitro cold exposure. Am. J. Physiol. 1994, 266, 773-780.
32. Shinitzky, M., Barenholz, Y., Fluidity parameters of lipid regions determined by fluorescence polarization. Biochim. Biophys. Acta 1978, 515, 367-394.
33. Cao-Hoang, L., Dumont, F., Marechal, P., Le-Thanh, M., Gervais, P., Rates of chilling to 0°C: Implications for the survival of microorganisms and relationship with membrane fluidity modifications. Appl. Microbiol. Biotechnol. 2008, 77, 1379-1387.
34. Fishov, I., Woldringh, C. L., Visualization of membrane domains in Escherichia coli. Mol. Microbiol. 1999, 32, 1166-1172.
35. Vincent, M., England, L. S., Trevors, J. T., Cytoplasmic membrane polarization in Gram-positive and Gram-negative bacteria grown in the absence and presence of tetracycline. Biochim. Biophys. Acta 2004, 1672, 131-134.
36. Billard, C., Phan Dinh Tuy, F., Rosenfeld, C., Tapiero, H., Membrane dynamics in human leukemia and lymphoma cells: pH dependency of diphenylhexatriene fluorescence polarization. FEBS Lett. 1983, 158, 229-233.
37. Ambrosini, A., Zolese, G., Balercia, G., Bertoli, E. et al., Laurdan fluorescence: A simple method to evaluate sperm plasma membrane alterations. Fertil. Steril. 2001, 76, 501-505.
38. Harris, F. M., Best, K. B., Bell, J. D., Use of laurdan fluorescence intensity and polarization to distinguish between changes in membrane fluidity and phospholipid order. Biochim. Biophys. Acta 2002, 1565, 123-128.
39. Proszynski, T. J., Klemm, R., Bagnat, M., Gaus, K., Simons, K., Plasma membrane polarization during mating in yeast cells. J. Cell Biol. 2006, 173, 861-866.
40. Vest, R., Wallis, R., Jensen, L. B., Haws, A. C. et al., Use of steady-state laurdan fluorescence to detect changes in liquid ordered phases in human erythrocyte membranes. J. Membr. Biol. 2006, 211, 15-25.
41. Harold, F. M., Gleanings of a chemiosmotic eye. BioEssays 2001, 23, 848-855.
42. Bonnet, M., Rafi, M. M., Chikindas, M. L., Montville, T. J., Bioenergetic mechanism for nisin resistance, induced by the acid tolerance response of Listeria monocytogenes. Appl. Environ. Microbiol. 2006, 72, 2556-2563.
43. Lolkema, J. S., Abbing, A., Hellingwerf, K. J., Konings, W. N., The transmembrane electrical potential in Rhodopseudomonas sphaeroides determined from the distribution of tetraphenylphosphonium after correction for its binding to cell components. Eur. J. Biochem. 1983, 130, 287-292.
44. Riondet, C., Cachon, R., Waché, Y., Alcaraz, G., Divies, C., Changes in the proton-motive force in Escherichia coli in response to external oxidoreduction potential. Eur. J. Biochem. 1999, 262, 595-599.
45. Gaskova, D., Brodska, B., Herman, P., Vecer, J. et al., Fluorescent probing of membrane potential in walled cells: diS-C3(3) assay in Saccharomyces cerevisiae. Yeast 1998, 14, 1189-1197.
46. Gaskova, D., Cadek, R., Chaloupka, R., Plasek, J., Sigler, K., Factors underlying membrane potential-dependent and -independent fluorescence responses of potentiometric dyes in stressed cells: diS-C(3)(3) in yeast. Biochim. Biophys. Acta 2001, 1511, 74-79.
47. Gaskova, D., Cadek, R., Chaloupka, R., Vacata, V. et al., Monitoring the kinetics and performance of yeast membrane ABC transporters by diS-C3(3) fluorescence. Int. J. Biochem. Cell Biol. 2002, 34, 931-937.
48. Hartig, S., Fries, S., Balcarcel, R. R., Reduced mitochondrial membrane potential and metabolism correspond to acute chloroform toxicity of in vitro hepatocytes. J. Appl. Toxicol. 2005, 25, 310-317.
49. Riondet, C., Cachon, R., Waché, Y., Alcaraz, G., Diviès, C., Measurement of the intracellular pH in Escherichia coli with the internally conjugated fluorescent probe 5- (and 6-)carboxyfluorescein succinimidyl ester. Biotechnol. Tech. 1997, 11, 735-738.
50. Pena, A., Ramirez, J., Rosas, G., Calahorra, M., Proton pumping and the internal pH of yeast cells, measured with pyranine introduced by electroporation. J. Bacteriol. 1995, 177, 1017-1022.
51. Aguedo, M., Waché, Y., Belin, J. M., Intracellular pH-dependent efflux of the fluorescent probe pyranine in the yeast Yarrowia lipolytica. FEMS Microbiol. Lett. 2001, 200, 185-189.
52. Dansen, T. B., Wirtz, K. W., Wanders, R. J., Pap, E. H., Peroxisomes in human fibroblasts have a basic pH. Nat. Cell Biol. 2000, 2, 51-53.
53. Jankowski, A., Kim, J. H., Collins, R. F., Daneman, R. et al., In situ measurements of the pH of mammalian peroxisomes using the fluorescent protein pHluorin. J. Biol. Chem. 2001, 276, 48748-48753.
54. Lasorsa, F. M., Scarcia, P., Erdmann, R., Palmieri, F. et al., The yeast peroxisomal adenine nucleotide transporter: Characterization of two transport modes and involvement in DeltapH formation across peroxisomal membranes. Biochem. J. 2004, 381, 581-585.
55. Nicolay, K., Veenhuis, M., Douma, A. C., Harder, W., A 31P NMR study of the internal pH of yeast peroxisomes. Arch. Microbiol. 1987, 147, 37-41.
56. Millard, P. J., Roth, B. L., Thi, H. P., Yue, S. T., Haugland, R. P., Development of the FUN-1 family of fluorescent probes for vacuole labeling and viability testing of yeasts. Appl. Environ. Microbiol. 1997, 63, 2897-2905.
57. Brul, S., Nussbaum, J., Dielbandhoesing, S. K., Fluorescent probes for wall porosity and membrane integrity in filamentous fungi. J. Microbiol. Methods 1997, 28, 169-178.
58. Aguedo, M., Waché, Y., Mazoyer, V., Sequeira-Le Grand, A., Belin, J. M., Increased electron donor and electron acceptor characters enhance the adhesion between oil droplets and cells of Yarrowia lipolytica as evaluated by a new cytometric assay. J. Agric. Food Chem. 2003, 51, 3007-3011.
59. Prudencio, C., Sansonetty, F., Corte-Real, M., Flow cytometric assessment of cell structural and functional changes induced by acetic acid in the yeasts Zygosaccharomyces bailii and Soccharornyces cerevisiae. Cytometry 1998, 31, 307-313.
60. Iturriaga, R., Zhang, S., Sonek, G. J., Stibbs, H., Detection of respiratory enzyme activity in Giardia cysts and Cryptosporidium oocysts using redox dyes and immunofluorescence techniques. J. Microbiol. Methods 2001, 46, 19-28.
61. Hatzinger, P. B., Palmer, P., Smith, R. L., Penarrieta, C. T., Yoshinari, T., Applicability of tetrazolium salts for the measurement of respiratory activity and viability of groundwater bacteria. J. Microbiol. Methods 2003, 52, 47-58.
62. Ullrich, S., Karrasch, B., Hoppe, H., Jeskulke, K., Mehrens, M., Toxic effects on bacterial metabolism of the redox dye 5-cyano-2,3-ditolyl tetrazolium chloride. Appl. Environ. Microbiol. 1996, 62, 4587-4593.
63. Aronsson, K., Ronner, U., Borch, E., Inactivation of Escherichia coli, Listeria innocua and Saccharomyces cerevisiae in relation to membrane permeabilization and subsequent leakage of intracellular compounds due to pulsed electric field processing. Int. J. Food Microbiol. 2005, 99, 19-32.
64. Delius, M., Adams, G., Shock wave permeabilization with ribosome inactivating proteins: A new approach to tumor therapy. Cancer Res. 1999, 59, 5227-5232.
65. Escande-Geraud, M. L., Rols, M. P., Dupont, M. A., Gas, N., Teissie, J., Reversible plasma membrane ultrastructural changes correlated with electropermeabilization in Chinese hamster ovary cells. Biochim. Biophys. Acta 1988, 939, 247-259.
66. El-Kosasy A. M., Potentiometric assessment of Gram-negative bacterial permeabilization of tobramycin. J. Pharm. Biomed. Anal. 2006, 42, 389-394.
67. Helander, I. M., Mattila-Sandholm, T., Fluorometric assessment of gram-negative bacterial permeabilization. J. Appl. Microbiol. 2000, 88, 213-219.
68. Leive, L., Release of lipopolysaccharide by EDTA treatment of E. coli. Biochem. Biophys. Res. Commun. 1965, 21, 290-296.
69. Virto, R., Manas, P., Alvarez, I., Condon, S., Raso, J., Membrane damage and microbial inactivation by chlorine in the absence and presence of a chlorine-demanding substrate. Appl. Environ. Microbiol. 2005, 71, 5022-5028.
70. Peterson, R. V., Pitt, W. G., The effect of frequency and power density on the ultrasonically-enhanced killing of biofilm-sequestered Escherichia coli. Colloids Surf. 2000, 17, 219-227.
71. Alakomi, H. L., Skytta, E., Saarela, M., Mattila-Sandholm, T. et al., Lactic acid permeabilizes gram-negative bacteria by disrupting the outer membrane. Appl. Environ. Microbiol. 2000, 66, 2001-2005.
72. Hancock, R. E., Farmer, S. W., Li, Z. S., Poole, K., Interaction of aminoglycosides with the outer membranes and purified lipopolysaccharide and OmpF porin of Escherichia coli. Antimicrob. Agents Chemother. 1991, 35, 1309-1314.
73. Loh, B., Grant, C., Hancock, R. E., Use of the fluorescent probe 1-N-phenylnaphthylamine to study the interactions of aminoglycoside antibiotics with the outer membrane of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 1984, 26, 546-551.
74. Tsuchido, T., Aoki, I., Takano, M., Interaction of the fluorescent dye 1-N-phenylnaphthylamine with Escherichia coli cells during heat stress and recovery from heat stress. J. Gen. Microbiol. 1989, 135, 1941-1947.
75. Vaara, M., Agents that increase the permeability of the outer membrane. Microbiol. Rev. 1992, 56, 395-411.
76. Cao-Hoang, L., Le-Thanh, M., Marechal, P. A., Gervais, P., Synergistic action of rapid chilling and nisin on the inactivation of Escherichia coli. Appl. Microbiol. Biotechnol. 2008, 79, 105-109.
77. Breusegem, S. Y., Levi, M., Barry N. P., Fluorescence correlation spectroscopy and fluorescence lifetime imaging microscopy. Nephron Exp. Nephrol. 2006, 103, e41-49.
78. Mullineaux, C. W., Kirchhoff, H., Using fluorescence recovery after photobleaching to measure lipid diffusion in membranes. Methods Mol. Biol. 2007, 400, 267-275.
79. Suhling, K., French, P. M., Phillips, D., Time-resolved fluorescence microscopy. Photochem. Photobiol. Sci. 2005, 4, 13-22.
80. Cash, T. P., Pan, Y., Simon, M. C., Reactive oxygen species and cellular oxygen sensing. Free Radic. Biol. Med. 2007, 43, 1219-1225.
81. Margolin, W., Green fluorescent protein as a reporter for macromolecular localization in bacterial cells. Methods 2000, 20, 62-72.