Recent advances on multi-parameter flow cytometry to characterize antimicrobial treatments

Frontiers in Microbiology

Volumn 7, Issue AUG, 2016, Pages

  Léonard, Lucie ^a   Chibane, Lynda Bouarab ^a   Bouhedda, Balkis Ouled ^a   Degraeve, Pascal ^a   Oulahal, Nadia ^a  

^a UNIVERSITÉ LYON 1   (France)

Author keywords

Antimicrobial mechanism; Antimicrobial treatment; Culturability; Double staining; Microorganisms; Multi parameter flow cytometry; Viability

Indexed keywords

FLUORESCENT DYE; GREEN FLUORESCENT PROTEIN; PROPIDIUM MONOAZIDE; RED FLUORESCENT PROTEIN; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL THERAPY; CELL CULTURE; CELL VIABILITY; COLONY FORMING UNIT; ELECTRON TRANSPORT; ENZYME ACTIVITY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; INFRARED SPECTROSCOPY; MEMBRANE POTENTIAL; METABOLIC ACTIVITY ASSAY; MULTI PARAMETER FLOW CYTOMETRY; NONHUMAN; PLATE COUNT; POLYMERASE CHAIN REACTION; REVIEW; SCANNING ELECTRON MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY;

EID: 84988841501     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.01225     Document Type: Review

References (59)

1. Ananta, E., Heinz, V., and Knorr, D. (2004). Assessment of high pressure induced damage on Lactobacillus rhamnosus GG by flow cytometry. Food Microbiol. 21, 567-577. doi: 10.1016/j.fm.2003.11.008
2. Ananta, E., and Knorr, D. (2009). Comparison of inactivation pathways of thermal or high pressure inactivated Lactobacillus rhamnosus ATCC 53103 by flow cytometry analysis. Food Microbiol. 26, 542-546. doi: 10.1016/j.fm.2009.01.008
3. Antolinos, V., Esteban, M.-D., Ros-Chumillas, M., Huertas, J.-P., Periago, P. M., Palop, A., et al. (2014). Assessment of the of acid shock effect on viability of Bacillus cereus and Bacillus weihenstephanensis using flow cytometry. Food Res. Int. 66, 306-312. doi: 10.1016/j.foodres.2014.09.029
4. Ayari, S., Dussault, D., Hayouni, E. A., Hamdi, M., and Lacroix, M. (2013). Radiation tolerance of Bacillus cereus pre-treated with carvacrol alone or in combination with nisin after exposure to single and multiple sub-lethal radiation treatment. Food Control 32, 693-701. doi: 10.1016/j.foodcont.2013.01.019
5. Boda, S. K., Ravikumar, K., Saini, D. K., and Basu, B. (2015). Differential viability response of prokaryotes and eukaryotes to high strength pulsed magnetic stimuli. Bioelectrochemistry 106, 276-289. doi: 10.1016/j.bioelechem.2015.07.009
6. Booyens, J., and Thantsha, M. S. (2014). Fourier transform infra-red spectroscopy and flow cytometric assessment of the antibacterial mechanism of action of aqueous extract of garlic (Allium sativum) against selected probiotic Bifidobacterium strains. BMC Complement. Altern. Med. 14:289. doi: 10.1186/1472-6882-14-289
7. Bridier, A., Hammes, F., Canette, A., Bouchez, T., and Briandet, R. (2015). Fluorescence-based tools for single-cell approaches in food microbiology. Int. J. Food Microbiol. 213, 2-16. doi: 10.1016/j.ijfoodmicro.2015.07.003
8. Caldeira, E., Piskin, E., Granadeiro, L., Silva, F., and Gouveia, I. C. (2013). Biofunctionalization of cellulosic fibres with l-cysteine: assessment of antibacterial properties and mechanism of action against Staphylococcus aureus and Klebsiella pneumoniae. J. Biotechnol. 168, 426-435. doi: 10.1016/j.jbiotec.2013.10.021
9. Choi, M. J., Kim, S. A., Lee, N. Y., and Rhee, M.-S. (2013). New decontamination method based on caprylic acid in combination with citric acid or vanillin for eliminating Cronobacter sakazakii and Salmonella enterica serovar Typhimurium in reconstituted infant formula. Int. J. Food Microbiol. 166, 499-507. doi: 10.1016/j.ijfoodmicro.2013.08.016
10. Combarros, R. G., Collado, S., and Díaz, M. (2016). Toxicity of titanium dioxide nanoparticles on Pseudomonas putida. Water Res. 90, 378-386. doi: 10.1016/j.watres.2015.12.040
11. Coronel-León, J., López, A., Espuny, M. J., Beltran, M. T., Molinos-Gómez, A., Rocabayera, X., et al. (2016). Assessment of antimicrobial activity of N a-lauroyl arginate ethylester (LAE®) against Yersinia enterocolitica and Lactobacillus plantarum by flow cytometry and transmission electron microscopy. Food Control 63, 1-10. doi: 10.1016/j.foodcont.2015.10.050
12. Díaz, M., Herrero, M., García, L. A., and Quirós, C. (2010). Application of flow cytometry to industrial microbial bioprocesses. Biochem. Eng. J. 48, 385-407. doi: 10.1016/j.bej.2009.07.013
13. Duarte, A., Alves, A. C., Ferreira, S., Silva, F., and Domingues, F. C. (2015). Resveratrol inclusion complexes: antibacterial and anti-biofilm activity against Campylobacter spp. and Arcobacter butzleri. Food Res. Int. 77, 244-250. doi: 10.1016/j.foodres.2015.05.047
14. Fernandes, E., Martins, V. C., Nóbrega, C., Carvalho, C. M., Cardoso, F. A., Cardoso, S., et al. (2014). A bacteriophage detection tool for viability assessment of Salmonella cells. Biosensors Bioelectronics 52, 239-246. doi: 10.1016/j.bios.2013.08.053
15. Ferreira, S., Silva, F., Queiroz, J. A., Oleastro, M., and Domingues, F. C. (2014). Resveratrol against Arcobacter butzleri and Arcobacter cryaerophilus: activity and effect on cellular functions. Int. J. Food Microbiol. 180, 62-68. doi: 10.1016/j.ijfoodmicro.2014.04.004
16. Ferrentino, G., Tamburini, S., Bath, K., Foladori, P., Spilimbergo, S., and Jousson, O. (2015). Application of culture-independent methods for monitoring Listeria monocytogenes inactivation on food products. Process Biochemistry 50, 188-193. doi: 10.1016/j.procbio.2014.12.014
17. Freire, J. M., Gaspar, D., de la Torre, B. G., Veiga, A. S., Andreu, D., and Castanho, M. A. (2015). Monitoring antibacterial permeabilization in real time using time-resolved flow cytometry. Biochim. Biophys. Acta 1848, 554-560. doi: 10.1016/j.bbamem.2014.11.001
18. Garcia-Gonzalez, L., Geeraerd, A. H., Mast, J., Briers, Y., Elst, K., Van Ginneken, L., et al. (2010). Membrane permeabilization and cellular death of Escherichia coli, Listeria monocytogenes and Saccharomyces cerevisiae as induced by high pressure carbon dioxide treatment. Food Microbiol. 27, 541-549. doi: 10.1016/j.fm.2009.12.004
19. Grau-Campistany, A., Manresa, Á., Pujol, M., Rabanal, F., and Cajal, Y. (2016). Tryptophan-containing lipopeptide antibiotics derived from polymyxin B with activity against Gram positive and Gram negative bacteria. Biochim. Biophys. Acta 1858, 333-343. doi: 10.1016/j.bbamem.2015.11.011
20. Hammer, K. A., and Heel, K. A. (2012). Use of multiparameter flow cytometry to determine the effects of monoterpenoids and phenylpropanoids on membrane polarity and permeability in staphylococci and enterococci. Int. J. Antimicrob. Agents 40, 239-245. doi: 10.1016/j.ijantimicag.2012.05.015
21. Hayouni, E. A., Bouix, M., Abedrabba, M., Leveau, J.-Y., and Hamdi, M. (2008). Mechanism of action of Melaleuca armillaris (Sol. Ex Gaertu) Sm. essential oil on six LAB strains as assessed by multiparametric flow cytometry and automated microtiter-based assay. Food Chem. 111, 707-718. doi: 10.1016/j.foodchem.2008.04.044
22. Hoefel, D., Grooby, W. L., Monis, P. T., Andrews, S., and Saint, C. P. (2003). A comparative study of carboxyfluorescein diacetate and carboxyfluorescein diacetate succinimidyl ester as indicators of bacterial activity. J. Microbiol. Methods 52, 379-388. doi: 10.1016/S0167-7012(02)00207-5
23. Hong, J., Guan, W., Jin, G., Zhao, H., Jiang, X., and Dai, J. (2015). Mechanism of tachyplesin I injury to bacterial membranes and intracellular enzymes, determined by laser confocal scanning microscopy and flow cytometry. Microbiol. Res. 170, 69-77. doi: 10.1016/j.micres.2014.08.012
24. Huang, T., Zheng, Y., Yan, Y., Yang, L., Yao, Y., Zheng, J., et al. (2016). Probing minority population of antibiotic-resistant bacteria. Biosensors Bioelectronics 80, 323-330. doi: 10.1016/j.bios.2016.01.054
25. Kelly, B. G., Vespermann, A., and Bolton, D. J. (2009). Gene transfer events and their occurrence in selected environments. Food Chem. Toxicol. 47, 978-983. doi: 10.1016/j.fct.2008.06.012
26. Kim, H. T., Choi, H. J., and Kim, K. H. (2009). Flow cytometric analysis of Salmonella enterica serotype Typhimurium inactivated with supercritical carbon dioxide. J. Microbiol. Methods 78, 155-160. doi: 10.1016/j.mimet.2009.05.010
27. Kramer, B., and Muranyi, P. (2014). Effect of pulsed light on structural and physiological properties of Listeria innocua and Escherichia coli. J. Appl. Microbiol. 116, 596-611. doi: 10.1111/jam.12394
28. Kramer, B., and Thielmann, J. (2016). Monitoring the live to dead transition of bacteria during thermal stress by a multi-method approach. J. Microbiol. Methods 123, 24-30. doi: 10.1016/j.mimet.2016.02.009
29. Lee, H., Hwang, J.-S., Lee, J., Kim, J. I., and Lee, D. G. (2015). Scolopendin 2, a cationic antimicrobial peptide from centipede, and its membrane-active mechanism. Biochim. Biophys. Acta 1848, 634-642. doi: 10.1016/j.bbamem.2014.11.016
30. Li, H., Xu, Z., Zhao, F., Wang, Y., and Liao, X. (2015). Synergetic effects of high-pressure carbon dioxide and nisin on the inactivation of Escherichia coli and Staphylococcus aureus. Innovative Food Sci. Emerg. Technol. 33, 180-186. doi: 10.1016/j.ifset.2015.11.013
31. Li, W., O'Brien-Simpson, N. M., Tailhades, J., Pantarat, N., Dawson, R. M., Otvos, L., et al. (2015). Multimerization of a proline-rich antimicrobial peptide, Chex-Arg20, alters its mechanism of interaction with the Escherichia coli membrane. Chem. Biol. 22, 1250-1258. doi: 10.1016/j.chembiol.2015.08.011
32. Manoil, D., Filieri, A., Gameiro, C., Lange, N., Schrenzel, J., Wataha, J. C., et al. (2014). Flow cytometric assessment of Streptococcus mutans viability after exposure to blue light-activated curcumin. Photodiagnosis Photodyn. Ther. 11, 372-379. doi: 10.1016/j.pdpdt.2014.06.003
33. Martínez-Abad, A., Sánchez, G., Lagaron, J. M., and Ocio, M. J. (2012). On the different growth conditions affecting silver antimicrobial efficacy on Listeria monocytogenes and Salmonella enterica. Int. J. Food Microbiol. 158, 147-154. doi: 10.1016/j.ijfoodmicro.2012.07.010
34. Mathur, H., Rea, M. C., Fallico, V., Cotter, P. D., Hill, C., and Ross, P. (2016). Flow cytometry as a tool to study the effects of bacteriocins on prokaryotic and eukaryotic cells. J. Mol. Biomarkers Diagnosis S8:013. doi: 10.4172/2155-9929.S8-013
35. Meng, J., Gong, Y., Qian, P., Yu, J.-Y., Zhang, X.-J., and Lu, R.-R. (2016). Combined effects of ultra-high hydrostatic pressure and mild heat on the inactivation of Bacillus subtilis. LWT-Food Sci. Technol. 68, 59-66. doi: 10.1016/j.lwt.2015.12.010
36. Morishige, Y., Fujimori, K., and Amano, F. (2015). Use of flow cytometry for quantitative analysis of metabolism of VBNC (Viable But Non-Culturable) Salmonella. Biol. Pharmaceutical Bull. 38, 1255-1264. doi: 10.1248/bpb.b15-00005
37. Muñoz, M., Guevara, L., Palop, A., Tabera, J., and Fernandez, P. S. (2009). Determination of the effect of plant essential oils obtained by supercritical fluid extraction on the growth and viability of Listeria monocytogenes in broth and food systems using flow cytometry. LWT-Food Sci. Technol. 42, 220-227. doi: 10.1016/j.lwt.2008.06.007
38. Muriel-Galet, V., López-Carballo, G., Gavara, R., and Hernández-Muñoz, P. (2015). Antimicrobial effectiveness of lauroyl arginate incorporated into ethylene vinyl alcohol copolymers to extend the shelf-life of chicken stock and surimi sticks. Food Bioprocess Technol. 8, 208-217. doi: 10.1007/s11947-014-1391-x
39. Nebe-von-Caron, G., Stephens, P. J., Hewitt, C. J., Powell, J. R., and Badley, R. A. (2000). Analysis of bacterial function by multi-colour fluorescence flow cytometry and single cell sorting. J. Microbiol. Methods 42, 97-114. doi: 10.1016/S0167-7012(00)00181-0
40. Nexmann Jacobsen, C., Rasmussen, J., and Jakobsen, M. (1997). Viability staining and flow cytometric detection of Listeria monocytogenes. J. Microbiol. Methods 28, 35-43. doi: 10.1016/S0167-7012(96)00960-8
41. Novo, D. J., Perlmutter, N. G., Hunt, R. H., and Shapiro, H. M. (2000). Multiparameter flow cytometric analysis of antibiotic effects on membrane potential, membrane permeability, and bacterial counts of Staphylococcus aureus and Micrococcus luteus. Antimicrobial Agents Chemother. 44, 827-834. doi: 10.1128/AAC.44.4.827-834.2000
42. Pal, G., and Srivastava, S. (2014). Inhibitory effect of plantaricin peptides (Pln E/F and J/K) against Escherichia coli. World J. Microbiol. Biotechnol. 30, 2829-2837. doi: 10.1007/s11274-014-1708-y
43. Pianetti, A., Manti, A., Boi, P., Citterio, B., Sabatini, L., Papa, S., et al. (2008). Determination of viability of Aeromonas hydrophila in increasing concentrations of sodium chloride at different temperatures by flow cytometry and plate count technique. Int. J. Food Microbiol. 127, 252-260. doi: 10.1016/j.ijfoodmicro.2008.07.024
44. Possemiers, S., Van Camp, J., Bolca, S., and Verstraete, W. (2005). Characterization of the bactericidal effect of dietary sphingosine and its activity under intestinal conditions. Int. J. Food Microbiol. 105, 59-70. doi: 10.1016/j.ijfoodmicro.2005.05.007
45. Rossi, F., Rizzotti, L., Felis, G. E., and Torriani, S. (2014). Horizontal gene transfer among microorganisms in food: current knowledge and future perspectives. Food Microbiol. 42, 232-243. doi: 10.1016/j.fm.2014.04.004
46. Schenk, M., Raffellini, S., Guerrero, S., Blanco, G. A., and Alzamora, S. M. (2011). Inactivation of Escherichia coli, Listeria innocua and Saccharomyces cerevisiae by UV-C light: study of cell injury by flow cytometry. LWT-Food Sci. Technol. 44, 191-198. doi: 10.1016/j.lwt.2010.05.012
47. Shapiro, H. M. (2000). Microbial analysis at the single-cell level: tasks and techniques. J. Microbiol. Methods 42, 3-16. doi: 10.1016/S0167-7012(00)00167-6
48. Silva, F., Ferreira, S., Duarte, A., Mendonça, D. I., and Domingues, F. C. (2011). Antifungal activity of Coriandrum sativum essential oil, its mode of action against Candida species and potential synergism with amphotericin B. Phytomedicine 19, 42-47. doi: 10.1016/j.phymed.2011.06.033
49. Spilimbergo, S., Foladori, P., Mantoan, D., Ziglio, G., and Della Mea, G. (2010). High-pressure CO2 inactivation and induced damage on Saccharomyces cerevisiae evaluated by flow cytometry. Process Biochem. 45, 647-654. doi: 10.1016/j.procbio.2009.12.013
50. Steen, H. B. (2000). Flow cytometry of bacteria: glimpses from the past with a view to the future. J. Microbiol. Methods 42, 65-74. doi: 10.1016/S0167-7012(00)00177-9
51. Surowsky, B., Fröhling, A., Gottschalk, N., Schlüter, O., and Knorr, D. (2014). Impact of cold plasma on Citrobacter freundii in apple juice: inactivation kinetics and mechanisms. Int. J. Food Microbiol. 174, 63-71. doi: 10.1016/j.ijfoodmicro.2013.12.031
52. Tamburini, S., Anesi, A., Ferrentino, G., Spilimbergo, S., Guella, G., and Jousson, O. (2014). Supercritical CO2 induces marked changes in membrane phospholipids composition in Escherichia coli K12. J. Membr. Biol. 247, 469-477. doi: 10.1007/s00232-014-9653-0
53. Tamburini, S., Ballarini, A., Ferrentino, G., Moro, A., Foladori, P., Spilimbergo, S., et al. (2013). Comparison of quantitative PCR and flow cytometry as cellular viability methods to study bacterial membrane permeabilization following supercritical CO2 treatment. Microbiology 159, 1056-1066. doi: 10.1099/mic.0.063321-0
54. Teng, D., Wang, X., Xi, D., Mao, R., Zhang, Y., Guan, Q., et al. (2014). A dual mechanism involved in membrane and nucleic acid disruption of AvBD103b, a new avian defensin from the king penguin, against Salmonella enteritidis CVCC3377. Appl. Microbiol. Biotechnol. 98, 8313-8325. doi: 10.1007/s00253-014-5898-x
55. Thabet, S., Weiss-Gayet, M., Dappozze, F., Cotton, P., and Guillard, C. (2013). Photocatalysis on yeast cells: toward targets and mechanisms. Appl. Catalysis B Environ. 140, 169-178. doi: 10.1016/j.apcatb.2013.03.037
56. Tracy, B. P., Gaida, S. M., and Papoutsakis, E. T. (2010). Flow cytometry for bacteria: enabling metabolic engineering, synthetic biology and the elucidation of complex phenotypes. Curr. Opin. Biotechnol. 21, 85-99. doi: 10.1016/j.copbio.2010.02.006
57. Wilkinson, M. G. (2015). Flow Cytometry in Microbiology: Technology and Applications. Caister Academic Press. Department of Life sciences, University of Limerick, Ireland.
58. Wu, G., Wu, H., Fan, X., Zhao, R., Li, X., Wang, S., et al. (2010b). Selective toxicity of antimicrobial peptide S-thanatin on bacteria. Peptides 31, 1669-1673. doi: 10.1016/j.peptides.2010.06.009
59. Wu, G., Wu, H., Li, L., Fan, X., Ding, J., Li, X., et al. (2010a). Membrane aggregation and perturbation induced by antimicrobial peptide of S-thanatin. Biochem. Biophys. Res. Commun. 395, 31-35. doi: 10.1016/j.bbrc.2010.03.107