Flow cytometric bacterial cell counts challenge conventional heterotrophic plate counts for routine microbiological drinking water monitoring

Water Research

Volumn 113, Issue , 2017, Pages 191-206

  Van Nevel, S ^a   Koetzsch, S ^b   Proctor, C R ^b,c   Besmer, M D ^b   Prest, E I ^d   Vrouwenvelder, J S ^d,e,f   Knezev, A ^g   Boon, N ^a   Hammes, F ^b  

^a GHENT UNIVERSITY   (Belgium)

^b SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

^c ETH ZURICH   (Switzerland)

^d DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^e Wetsus European Centre of Excellence for Sustainable Water Technology   (Netherlands)

^f KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^g Het Waterlaboratorium   (Netherlands)

Author keywords

Cultivation; Flow cytometry (FCM); Heterotrophic plate counts (HPC); Microbiological drinking water quality; Routine water monitoring

Indexed keywords

BACTERIA; CELLS; CYTOLOGY; MONITORING; POTABLE WATER; WATER QUALITY; WATER TREATMENT;

BACTERIAL CELLS; CELL CONCENTRATIONS; DRINKING-WATER QUALITIES; FLOW CYTOMETRY; HETEROTROPHIC PLATE COUNT; HETEROTROPHIC PLATE COUNTS; MICROBIOLOGICAL DRINKING WATER QUALITY; ROUTINE WATER MONITORING; WATER MONITORING; WATER QUALITY MONITORING;

FLOW CYTOMETRY;

DRINKING WATER; WATER;

BACTERIUM; CELLS AND CELL COMPONENTS; DRINKING WATER; FLOW CYTOMETRY; HETEROTROPHY; LABORATORY METHOD; MICROBIAL COMMUNITY; WATER QUALITY; WATER TREATMENT;

AUTOMATION; BACTERIAL CELL; BACTERIAL COUNT; COST BENEFIT ANALYSIS; DISINFECTION; FLOW CYTOMETRY; HETEROTROPHY; MICROBIAL COMMUNITY; NONHUMAN; ONLINE ANALYSIS; PLATE COUNT; PRIORITY JOURNAL; REVIEW; VELOCITY; WATER CONTAMINATION; WATER QUALITY; BACTERIUM; CELL COUNT; MICROBIOLOGY; WATER SUPPLY;

BACTERIA (MICROORGANISMS);

BACTERIA; CELL COUNT; COLONY COUNT, MICROBIAL; DRINKING WATER; FLOW CYTOMETRY; WATER MICROBIOLOGY; WATER QUALITY; WATER SUPPLY;

EID: 85013170645     PISSN: 00431354     EISSN: 18792448     Source Type: Journal    
DOI: 10.1016/j.watres.2017.01.065     Document Type: Review

References (152)

1. Achtman, M., Wagner, M., Microbial diversity and the genetic nature of microbial species. Nat. Rev. Micro 6:6 (2008), 431–440.
2. Aghaeepour, N., Finak, G., Hoos, H., Mosmann, T.R., Brinkman, R., Gottardo, R., Scheuermann, R.H., Critical assessment of automated flow cytometry data analysis techniques. Nat. Methods 10:3 (2013), 228–238.
3. Allen, M.J., Edberg, S.C., Reasoner, D.J., Heterotrophic plate count bacteria—what is their significance in drinking water?. Int. J. Food Microbiol. 92:3 (2004), 265–274.
4. Amann, J., Die direkte Zählung der Wasserbakterien mittels des Ultramikroskops. Zentralbl. Bakteriol. Parasitenkd. Infekt. Hyg. 29 (1911), 381–384.
5. Anonymous, The Microbiology of Drinking Water (2012) – Part 7 – Methods for the Enumeration of Heterotrophic Bacteria. Methods for the Examination of Waters and Associated Materials. 2012, Environment Agency, Nottingham.
6. Appenzeller, B.M., Duval, Y.B., Thomas, F., Block, J.C., Influence of phosphate on bacterial adhesion onto iron oxyhydroxide in drinking water. Environ. Sci. Technol. 36:4 (2002), 646–652.
7. Bailey, J.E., Fazel-Makjlessi, J., McQuitty, D.N., Lee, Y.N., Allred, J.C., Oro, J.A., Characterization of bacterial growth by means of flow microfluorometry. Science 198:4322 (1977), 1175–1176.
8. Bautista-de los Santos, Q.M., Schroeder, J.L., Sevillano-Rivera, M.C., Sungthong, R., Ijaz, U.Z., Sloan, W.T., et al. Emerging investigators series: microbial communities in full-scale drinking water distribution systems - a meta-analysis. Environ. Sci. Res. Technol. 2 (2016), 631–644.
9. Berney, M., Vital, M., Huelshoff, I., Weilenmann, H.-U., Egli, T., Hammes, F., Rapid, cultivation-independent assessment of microbial viability in drinking water. Water Res. 42:14 (2008), 4010–4018.
10. Berry, D., Xi, C., Raskin, L., Microbial ecology of drinking water distribution systems. Curr. Opin. Biotechnol. 17 (2006), 297–302.
11. Besmer, M.D., Weissbrodt, D.G., Kratochvil, B.E., Sigrist, J.A., Weyland, M.S., Hammes, F., The feasibility of automated online flow cytometry for in-situ monitoring of microbial dynamics in aquatic ecosystems. Front. Microbiol., 5, 2014, 265.
12. Besmer, M.D., Epting, J., Page, R.M., Sigrist, J.A., Huggenberger, P., Hammes, F., et al. Online flow cytometry reveals microbial dynamics influenced by concurrent natural and operational events in groundwater used for drinking water treatment. Sci. Rep., 6, 2016, 38462.
13. Besmer, M.D., Sigrist, J.A., Hammes, F., Auckenthaler, A., Online-Durchflusszytometrie in der Praxis. Fenster in die Welt mikrobiologischer Dynamiken in Wasser - von der Quelle bis zum Wasserhahn. Aqua Gas 7 (2016), 73–77.
14. Besmer, M.D., Hammes, F., Short-term microbial dynamics in a drinking water plant treating groundwater with occasional high microbial loads. Water Res. 107 (2016), 11–18.
15. Bogosian, G., Bourneuf, E.V., A matter of bacterial life and death. EMBO Rep. 2:9 (2001), 770–774.
16. Brognaux, A., Han, S., Sorensen, S.J., Lebeau, F., Thonart, P., Delvigne, F., A low-cost, multiplexable, automated flow cytometry procedure for the characterization of microbial stress dynamics in bioreactors. Microb. Cell Fact., 12, 2013, 100.
17. Buesing, N., Gessner, M.O., Comparison of detachment procedures for direct counts of bacteria associated with sediment particles, plant litter and epiphytic biofilms. Aquat. Microb. Ecol. 27:1 (2002), 29–36.
18. Bundesministerium der Justiz und für Verbraucherschutz, Verordnung über die Qualität von Wasser für den menschlichen Gebrauch (Trinkwasserverordnung - TrinkwV 2001) (Update 2013). 2013.
19. Burtscher, M., Zibuschka, F., Mach, R., Lindner, G., Farnleitner, A., Heterotrophic plate count vs. in situ bacterial 16S rRNA gene amplicon profiles from drinking water reveal completely different communities with distinct spatial and temporal allocations in a distribution net. Water SA 35 (2009), 495–504.
20. Camper, A.K., LeChevallier, M.W., Broadaway, S.C., McFeters, G.A., Bacteria associated with granular activated carbon particles in drinking water. Appl. Environ. Microbiol. 52 (1986), 434–438.
21. Chowdhury, S., Heterotrophic bacteria in drinking water distribution system: a review. Environ. Monit. Assess. 184 (2012), 6087–6137.
22. D'Onofrio, A., Crawford, J.M., Stewart, E.J., Witt, K., Gavrish, E., Epstein, S., Clardy, J., Lewis, K., Siderophores from neighboring organisms promote the growth of uncultured bacteria. Chem. Biol. 17:3 (2010), 254–264.
23. De Roy, K., Clement, L., Thas, O., Wang, Y., Boon, N., Flow cytometry for fast microbial community fingerprinting. Water Res. 46:3 (2012), 907–919.
24. Douterelo, I., Boxall, J.B., Deines, P., Sekar, R., Fish, K.E., Biggs, C.A., Methodological approaches for studying the microbial ecology of drinking water distribution systems. Water Res. 65c (2014), 134–156.
25. EDI, Hygieneverordnung des EDI (HyV) vom 23. November 2005 (Stand am 1. Januar 2014). 2014, Eidgenössische Departement des Innern.
26. Epstein, S.S., The phenomenon of microbial uncultivability. Curr. Opin. Microbiol. 16:5 (2013), 636–642.
27. Exner, M., Vacanta, V., Gebel, J., Public health aspects of the role of HPC - an introduction. Bartram, J., Cotruvo, J.A., Exner, M., Fricker, C.R., Glasmacher, A., (eds.) Heterotrophic Plate Counts and Drinking-water Safety - the Significance of HPCs for Water Quality and Human Health, 2003, IWA Publishing on behalf of the World Health Organisation, London.
28. Farnleitner, A.H., Zibuschka, F., Burtscher, M.M., Lindner, G., Reischer, G., Mach, R.L., Eubacterial 16S-rDNA amplicon profiling: a rapid technique for comparison and differentiation of heterotrophic plate count communities from drinking water. Int. J. Food Microbiol. 92 (2004), 333–345.
29. Foladori, P., Bruni, L., Tamburini, S., Ziglio, G., Direct quantification of bacterial biomass in influent, effluent and activated sludge of wastewater treatment plants by using flow cytometry. Water Res. 44:13 (2010), 3807–3818.
30. Francisque, A., Rodriguez, M.J., Miranda-Moreno, L.F., Sadiq, R., Proulx, F., Modeling of heterotrophic bacteria counts in a water distribution system. Water Res. 43:4 (2009), 1075–1087.
31. Frankland, P., Frankland, G.C.T., Micro-organisms in Water: Their Significance, Identification and Removal. 1894, Longmans, Green, London.
32. Gensberger, E.T., Gössl, E.-M., Antonielli, L., Sessitsch, A., Kostic, T., Effect of different heterotrophic plate count methods on the estimation of the composition of the culturable microbial community. Peer J., 3, 2015, e862.
33. Gillespie, S., Lipphaus, P., Green, J., Parsons, S., Weir, P., Juskowiak, K., Jefferson, B., Jarvis, P., Nocker, A., Assessing microbiological water quality in drinking water distribution systems with disinfectant residual using flow cytometry. Water Res. 65 (2014), 224–234.
34. Green, B.D., Keller, M., Capturing the uncultivated majority. Curr. Opin. Biotechnol. 17:3 (2006), 236–240.
35. Hammes, F., Berney, M., Egli, T., Cultivation-independent assessment of bacterial viability. High. Resolut. Microb. Single Cell Anal. 124 (2011), 123–150.
36. Hammes, F., Berney, M., Wang, Y., Vital, M., Koester, O., Egli, T., Flow-cytometric total bacterial cell counts as a descriptive microbiological parameter for drinking water treatment processes. Water Res. 42:1–2 (2008), 269–277.
37. Hammes, F., Broger, T., Weilenmann, H.-U., Vital, M., Helbing, J., Bosshart, U., Huber, P., Odermatt, R.P., Sonnleitner, B., Development and laboratory-scale testing of a fully automated online flow cytometer for drinking water analysis. Cytom. Part A 81A:6 (2012), 508–516.
38. Hammes, F., Egli, T., Cytometric methods for measuring bacteria in water: advantages, pitfalls and applications. Anal. Bioanal. Chem. 397:3 (2010), 1083–1095.
39. Hammes, F., Goldschmidt, F., Vital, M., Wang, Y., Egli, T., Measurement and interpretation of microbial adenosine tri-phosphate (ATP) in aquatic environments. Water Res. 44:13 (2010), 3915–3923.
40. Hammes, F., Berger, C., Egli, O., Köster T., Biological stability of drinking water without disinfectant residuals: a case-study of the Zürich water supply system. J. Water Supply Res. T 59:1 (2010), 31–40.
41. Hammes, F.A., Egli, T., New method for assimilable organic carbon determination using flow-cytometric enumeration and a natural microbial consortium as inoculum. Environ. Sci. Technol. 39:9 (2005), 3289–3294.
42. Health Canada, Guidelines for Canadian Drinking Water Quality-summary Table. Water, Air and Climate Change Bureau and Healthy Environments and Consumers Safety Branch. 2012, Health Canada, Ottawa, Ontario.
43. Helmi, K., Barthod, F., Méheut, G., Henry, A., Poty, F., Laurent, F., Charni-Ben-Tabassi, N., Methods for microbiological quality assessment in drinking water: a comparative study. J. Water Health, 13, 2014, 34.
44. Helmi, K., Watt, A., Jacob, P., Ben-Hadj-Salah, I., Henry, A., Méheut, G., Charni-Ben-Tabassi, N., Monitoring of three drinking water treatment plants using flow cytometry. Wa Sci. Technol. 14:5 (2014), 850–856.
45. Hijnen, W.A.M., Beerendonk, E.F., Medema, G.J., Inactivation credit of UV radiation for viruses, bacteria and protozoan (oo)cysts in water: a review. Water Res. 40:1 (2006), 3–22.
46. Ho, L., Braun, K., Fabris, R., Hoefel, D., Morran, J., Monis, P., Drikas, M., Comparison of drinking water treatment process streams for optimal bacteriological water quality. Water Res. 46:12 (2012), 3934–3942.
47. Hoefel, D., Grooby, W.L., Monis, P.T., Andrews, S., Saint, C.P., Enumeration of water-borne bacteria using viability assays and flow cytometry: a comparison to culture-based techniques. J. Microbiol. Meth 55:3 (2003), 585–597.
48. Hoefel, D., Monis, P.T., Grooby, W.L., Andrews, S., Saint, C.P., Culture-independent techniques for rapid detection of bacteria associated with loss of chloramine residual in a drinking water system. Appl. Environ. Microbiol. 71:11 (2005), 6479–6488.
49. Hoefel, D., Monis, P.T., Grooby, W.L., Andrews, S., Saint, C.P., Profiling bacterial survival through a water treatment process and subsequent distribution system. J. Appl. Microbiol. 99 (2005), 175–186.
50. Holm-Hansen, O., Booth, C.R., Measurement of adenosine triphospate in the ocean and its ecological significance. Limnol. Oceanogr. 11 (1966), 510–519.
51. Hug, L.A., Baker, B.J., Anantharaman, K., Brown, C.T., Probst, A.J., Castelle, C.J., Butterfield, C.N., Hernsdorf, A.W., Amano, Y., Ise, K., Suzuki, Y., Dudek, N., Relman, D.A., Finstad, K.M., Amundson, R., Thomas, B.C., Banfield, J.F., A new view of the tree of life. Nat. Microbiol. 1 (2016), 1–6.
52. Hwang, C., Ling, F., Andersen, G.L., LeChevallier, M.W., Liu, W.-T., Evaluation of methods for the extraction of DNA from drinking water distribution system biofilms. Microbes Environ. 27 (2012), 9–18.
53. Infrastructuur en Milieu, Besluit van 23 mei 2011, houdende bepalingen inzake de productie en distributie van drinkwater en de organisatie van de openbare drinkwatervoorziening (Drinkwaterbesluit). 2011.
54. Kaeberlein, T., Lewis, K., Epstein, S.S., Isolating “uncultivable” microorganisms in pure culture in a simulated natural environment. Science 296:5570 (2002), 1127–1129.
55. Kahlisch, L., Henne, K., Grobe, L., Brettar, I., Hofle, M.G., Assessing the viability of bacterial species in drinking water by combined cellular and molecular analyses. Microb. Ecol. 63:2 (2012), 383–397.
56. Kahlisch, L., Henne, K., Groebe, L., Draheim, J., Hofle, M.G., Brettar, I., Molecular analysis of the bacterial drinking water community with respect to live/dead status. Water Sci. Technol. 61:1 (2010), 9–14.
57. Karl, D.M., Cellular nucleotide measurements and applications in microbial ecology. Microbiol. Rev. 44:4 (1980), 739–796.
58. 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. Ant. Van Leeuwenhoek 73:2 (1998), 169–187.
59. Keserue, H.A., Baumgartner, A., Felleisen, R., Egli, T., Rapid detection of total and viable Legionella pneumophila in tap water by immunomagnetic separation, double fluorescent staining and flow cytometry. Microb. Biotechnol. 5:6 (2012), 753–763.
60. Koch, C., Harnisch, F., Schröder, U., Müller, S., Cytometric fingerprints: evaluation of new tools for analyzing microbial community dynamics. Front. Microbiol., 5, 2014.
61. Koch, R., Zur Untersuchung von pathogenen Organismen. Mittl. Des. Kais. Gesundheitsamtes 1 (1881), 1–48.
62. Koch, R., Wasserfiltration und Cholera. Gesammelte Werke, Bd 2 Teil 1. 1893, Georg Thieme, Leipzig 1912, 183–206.
63. Koetzsch, S., Alisch, S., Egli, T., Hammes, F., Weilenmann, H.U., Pfister, L., Karmann, S., Durchflusszytometrische Analyse von Wasserproben. Sweizerisches Buch für Lebensmittel. 2012, Bundesamtes für Gesundheit.
64. Koetzsch, S., Sinreich, M., Zellzaheln zum grundwasser. Bestimmung mittels Durchflusszytometrie. Aqua Gas 3 (2014), 14–21.
65. Lautenschlager, K., Boon, N., Wang, Y.Y., Egli, T., Hammes, F., Overnight stagnation of drinking water in household taps induces microbial growth and changes in community composition. Water Res. 44:17 (2010), 4868–4877.
66. Lautenschlager, K., Hwang, C., Liu, W.T., Boon, N., Koster, O., Vrouwenvelder, H., Egli, T., Hammes, F., A microbiology-based multi-parametric approach towards assessing biological stability in drinking water distribution networks. Water Res. 47:9 (2013), 3015–3025.
67. Lautenschlager, K., Hwang, C., Ling, F., Liu, W.T., Boon, N., Koster, O., et al. Abundance and composition of indigenous bacterial communities in a multi-step biofiltration-based drinking water treatment plant. Water Res. 62 (2014), 40–52.
68. Lebaron, P., Parthuisot, N., Catala, P., Comparison of blue nucleic acid dyes for flow cytometric enumeration of bacteria in aquatic systems. Appl. Environ. Microb. 64:5 (1998), 1725–1730.
69. LeChevallier, M.W., Hassenauer, T.S., Camper, A.L., McFeters, G.A., Disinfection of bacteria attached to granular activated carbon. Appl. Environ. Microbiol. 48 (1984), 918–923.
70. LeChevallier, M.W., Seidler, R.J., Evans, T.M., Enumeration and characterization of standard plate count bacteria in chlorinated and raw water supplies. Appl. Environ. Microbiol. 40 (1980), 922–930.
71. Leclerc, H., Relationships between common water bacteria and pathogens in drinking water. Bartram, J., Cotruvo, J.A., Exner, M., Fricker, C.R., Glasmacher, A., (eds.) Heterotrophic Plate Counts and Drinking-water Safety, 2003, IWA Publishing on behalf of the World Health Organisation, London.
72. Legendre, L., Yentsch, C.M., Overview of flow cytometry and image analysis in biological oceanography and limnology. Cytometry 10 (1989), 501–510.
73. Lewis, K., Epstein, S., D'Onofrio, A., Ling, L.L., Uncultured microorganisms as a source of secondary metabolites. J. Antibiot. (Tokyo) 63:8 (2010), 468–476.
74. Liikanen, R., Miettinen, I., Laukkanen, R., Selection of NF membrane to improve quality of chemically treated surface water. Water Res. 37 (2003), 864–872.
75. Lipphaus, P., Hammes, F., Kotzsch, S., Green, J., Gillespie, S., Nocker, A., Microbiological tap water profile of a medium-sized building and effect of water stagnation. Environ. Technol. 35:5–8 (2014), 620–628.
76. Lisle, J.T., Pyle, B.H., McFeters, G.A., The use of multiple indices of physiological activity to access viability in chlorine disinfected Escherichia coli O157:H7. Lett. Appl. Microbiol. 29:1 (1999), 42–47.
77. Liu, G., Van der Mark, E.J., Verberk, J.Q., Van Dijk, J.C., Flow cytometry total cell counts: a field study assessing microbiological water quality and growth in unchlorinated drinking water distribution systems. Biomed. Res. Int., 2013, 595872.
78. Liu, G., Ling, F.Q., Magic-Knezev, A., Liu, W.T., Verberk, J.Q.J.C., Van Dijk, J.C., Quantification and identification of particle-associated bacteria in unchlorinated drinking water from three treatment plants by cultivation-independent methods. Water Res. 47 (2013), 3523–3533.
79. Lopez-Roldan, R., Tusell, P., Courtois, S., Cortina, J.L., On-line bacteriological detection in water. Trends Anal. Chem. 44 (2013), 46–56.
80. Ma, L., Mao, G., Liu, J., Yu, H., Gao, G., Wang, Y., Rapid quantification of bacteria and viruses in influent, settled water, activated sludge and effluent from a wastewater treatment plant using flow cytometry. Water Sci. Technol. 68:8 (2013), 1763–1769.
81. Magic-Knezev, A., van der Kooij, D., Optimisation and significance of ATP analysis for measuring active biomass in granular activated carbon filters used in water treatment. Water Res. 38:18 (2004), 3971–3979.
82. Mimoso, J., Pronk, W., Morgenroth, E., Hammes, F., Bacterial growth in batch-operated membrane filtration systems for drinking water treatment. Sep. Purif. Technol. 156 (2015), 165–174.
83. Ministère de la santé et des solidarités, Arrêté du 11 janvier 2007 relatif aux limites et références de qualité des eaux brutes et des eaux destinées à la consommation humaine mentionnées aux articles R. 1321–2, R. 1321-2, R. 1321-7 et R. 1321-38 du code de la santé publique. Paris. 2007.
84. Monfort, P., Baleux, B., "Comparison of flow cytometry and epifluorescence microscopy for counting bacteria in aquatic ecosystems. Cytometry 13:2 (1992), 188–192.
85. Nadkarni, M.A., Martin, F.E., Jacques, N.A., Hunter, N., Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148:Pt 1 (2002), 257–266.
86. Nescerecka, A., Rubulis, J., Vital, M., Juhna, T., Hammes, F., Biological instability in a chlorinated drinking water distribution network. PLoS One, 9(5), 2014, e96354.
87. Nescerecka, A., Hammes, F., Juhna, T., A pipeline for developing and testing staining protocols for flow cytometry, demonstrated with SYBR Green I and propidium iodide viability staining. J. Microbiol. Methods 131 (2016), 172–180.
88. Nescerecka, A., Juhna, T., Hammes, F., Behavior and stability of adenosine triphosphate (ATP) during chlorine disinfection. Water Res. 101 (2016), 490–497.
89. NHMRC and NRMMC, Australian Drinking Water Guidelines Paper 6 National Water Quality Management Strategy. 2011, National Health and Medical Research Council and National Resource Management Ministrial Council. Commonwealth of Australia, Canberra.
90. Nocker, A., Sossa, K.E., Camper, A.K., Molecular monitoring of disinfection efficacy using propidium monoazide in combination with quantitative PCR. J. Microbiol. Methods 70:2 (2007), 252–260.
91. Oliver, J.D., The viable but nonculturable state in bacteria. J. Microbiol., 43, 2005 Spec No: 93–100.
92. Oliver, J.D., Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol. Rev. 34:4 (2010), 415–425.
93. Paau, A.S., Cowles, J.R., Oro, J., Flow-microfluorometric analysis of Escherichia coli, Rhizobium meliloti, and Rhizobium japonicum at different stages of the growth cycle. Can. J. Microbiol. 23:9 (1977), 1165–1169.
94. Payment, P., Sartory, D.P., Reasoner, D.J., The history and use of HPC in drinking-water quality management. Bartram, J., Cotruvo, J.A., Exner, M., Fricker, C.R., Glasmacher, A., (eds.) Heterotrophic Plate Counts and Drinking-water Safety, 2003, IWA Publishing, World Health Organisation, London.
95. Pepper, I.L., Rusin, P., Quintanar, D.R., Haney, C., Josephson, K.L., Gerba, C.P., Tracking the concentration of heterotrophic plate count bacteria from the source to the consumer's tap. Int. J. Food Microbiol. 92 (2004), 289–295.
96. Phe, M.H., Dossot, M., Guilloteau, H., Block, J.C., Nucleic acid fluorochromes and flow cytometry prove useful in assessing the effect of chlorination on drinking water bacteria. Water Res. 39:15 (2005), 3618–3628.
97. Pianetti, A., Falcioni, T., Bruscolini, F., Sabatini, L., Sisti, E., Papa, S., Determination of the viability of Aeromonas hydrophila in different types of water by flow cytometry, and comparison with classical methods. Appl. Environ. Microbiol. 71:12 (2005), 7948–7954.
98. Pinto, A.J., Schroeder, J., Lunn, M., Sloan, W., Raskin, L., Spatial-temporal survey and occupancy-abundance modeling to predict bacterial community dynamics in the drinking water microbiome. MBio, 5(3), 2014 e01135–01114.
99. Pinto, A.J., Xi, C., Raskin, L., Bacterial community structure in the drinking water microbiome is governed by filtration processes. Environ. Sci. Technol. 46 (2012), 8851–8859.
100. Prest, E.I., El-Chakhtoura, J., Hammes, F., Saikaly, P.E., van Loosdrecht, M.C., Vrouwenvelder, J.S., Combining flow cytometry and 16S rRNA gene pyrosequencing: a promising approach for drinking water monitoring and characterization. Water Res. 63 (2014), 179–189.
101. Prest, E.I., Hammes, F., Kotzsch, S., van Loosdrecht, M.C., Vrouwenvelder, J.S., Monitoring microbiological changes in drinking water systems using a fast and reproducible flow cytometric method. Water Res. 47:19 (2013), 7131–7142.
102. Prest, E.I., Weissbrodt, D.G., Hammes, F., van Loosdrecht, M.C.M., Vrouwenvelder, J.S., Long-term bacterial dynamics in a full-scale drinking water distribution system. PLoS One, 11(10), 2016, e0164445.
103. Prest, E.I., Hammes, F., van Loosdrecht, M.C.M., Vrouwenvelder, J.S., Biological stability of drinking water: controlling factors, methods and challenges. Front. Microbiol., 7, 2016, 45.
104. Proctor, C.R., Hammes, F., Drinking water microbiology—from measurement to management. Curr. Opin. Biotechnol. 33 (2015), 87–94.
105. Props, R., Kerckhof, F.-M., Rubbens, P., De Vrieze, J., Hernandez Sanabria, E., Waegeman, W., et al. Absolute quantification of microbial taxon abundances. ISME J. 11:2 (2016), 584–587.
106. Radcliff, R., International Drinking Water Regulations - the Developed World Sets the Standards. 2003 Retrieved Sept 18, 2014, from: http://www.nesc.wvu.edu/ndwc/articles/ot/sp03/inter_dwregs.html.
107. Ramseier, M.K., von Gunten, U., Freihofer, P., Hammes, F., Kinetics of membrane damage to high (HNA) and low (LNA) nucleic acid bacterial clusters in drinking water by ozone, chlorine, chlorine dioxide, monochloramine, ferrate(VI), and permanganate. Water Res. 45:3 (2011), 1490–1500.
108. Rappe, M.S., Connon, S.A., Vergin, K.L., Giovannoni, S.J., Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418:6898 (2002), 630–633.
109. Reasoner, D.J., Monitoring heterotrophic bacteria in potable water. McFeters, Gordon A., (eds.) Drinking Water Microbiology, 1990, Springer-Verlag, New York.
110. Reasoner, D.J., Heterotrophic plate count methodology in the United States. Int. J. Food Microbiol. 92:3 (2004), 307–315.
111. Reasoner, D.J., Geldreich, E.E., A new medium for the enumeration and subculture of bacteria from potable water. Appl. Environ. Microbiol. 49:1 (1985), 1–7.
112. Rice, E.W., Baird, R.B., Eaton, A.D., Clesceri, L.S., Standard Methods for the Examination of Water and Wastewater. twenty-second ed., 2012, American Public Health Association, American Water Works Association and Water Environment Federation, New York.
113. Richardson, H.Y., Nichols, G., Lane, C., Lake, I.R., Hunter, P.R., Microbiological surveillance of private water supplies in England: the impact of environmental and climate factors on water quality. Water Res. 43:8 (2009), 2159–2168.
114. Salter, S.J., Cox, M.J., Turek, E.M., Calus, S.T., Cookson, W.O., Moffatt, M.F., Turner, P., Parkhill, J., Loman, N.J., Walker, A.W., Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol., 12, 2014, 87.
115. Sangwan, P., Kovac, S., Davis, K.E., Sait, M., Janssen, P.H., Detection and cultivation of soil verrucomicrobia. Appl. Environ. Microbiol. 71:12 (2005), 8402–8410.
116. Sartory, D.P., Heterotrophic plate count monitoring of treated drinking water in the UK: a useful operational tool. Int. J. Food Microbiol. 92 (2004), 297–306.
117. Sedlak, D.L., Water 4.0-The Past, Present and Future of the World's Most Vital Resource. 2014, Yale University Press/New Haven & London.
118. Shapiro, H.M., Practical Flow Cytometry. fourth ed., 2003, Wiley-Liss, New York.
119. Siebel, E., Wang, Y., Egli, T., Hammes, F., Correlations between total cell concentration, total adenosine tri-phosphate concentration and heterotrophic plate counts during microbial monitoring of drinking water. Drink Water Eng. Sci. 1 (2008), 1–6.
120. Sinreich, M., Pronk, M., Kozel, R., Microbiological monitoring and classification of karst springs. Environ. Earth Sci. 71:2 (2014), 563–572.
121. SLMB, Determining the Total Cell Count and Ratios of High and Low Nucleic Acid Content Cells in Freshwater Using Flow Cytometry. Analysis Method 333.1, Swiss Food Book. 2012, Federal Office of Public Health, Swiss Confederation.
122. Staley, J.T., Konopka, A., Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu. Rev. Microbiol. 39 (1985), 321–346.
123. Trousellier, M., Courties, C., Vaquer, S., Recent applications of flow cytometry in aquatic microbial ecology. Biol. Cell. 78 (1993), 111–121.
124. Uhl, W., Schaule, G., Establishment of HPC(R2A) for regrowth control in non-chlorinated distribution systems. Int. J. Food Microbiol. 92 (2004), 317–325.
125. USEPA, National Primary Drinking Water Regulations. 2009, United States Environmental Protection Agency.
126. van der Kooij, D., Veenendaal, H.R., Egrowth problems and biological stability assessment in The Netherlands. Van der Kooij, D., Van der Wielen, P.W., (eds.) Microbial Growth in Drinking-water Supplies, 2014, IWA Publishing, London.
127. van der Kooij, D., van der Wielen, P.W., General introduction. Van der Kooij, D., Van der Wielen, P.W., (eds.) Microbial Growth in Drinking-water Supplies, 2014, IWA Publishing, London.
128. van der Kooij, D., van der Wielen, P.W., Research needs. Van der Kooij, D., Van der Wielen, P.W., (eds.) Microbial Growth in Drinking-water Supplies, 2014, IWA Publishing, London.
129. van der Kooij, D., Vrouwenvelder, J.S., Veenendaal, H.R., Elucidation and control of biofilm formation processes in water treatment and distribution using the Unified Biofilm Approach. Water Sci. Technol. 47:5 (2003), 83–90.
130. van der Wielen, P.W.J.J., van der Kooij, D., Effect of water composition, distance and season on the adenosine triphosphate concentration in unchlorinated drinking water in The Netherlands. Water Res. 44:17 (2010), 4860–4867.
131. Van Nevel, S., Buysschaert, B., De Gusseme, B., Boon, N., Flow cytometric examination of bacterial growth in a local drinking water network. J. Water Environ. 30:1–2 (2016), 167–176.
132. Van Nevel, S., De Roy, K., Boon, N., Bacterial invasion potential in water is determined by nutrient availability and the indigenous community. Fems Microbiol. Ecol. 85:3 (2013), 593–603.
133. Van Nevel, S., Hennebel, T., De Beuf, K., Du Laing, G., Verstraete, W., Boon, N., Transparent exopolymer particle removal in different drinking water production centers. Water Res. 46:11 (2012), 3603–3611.
134. Van Nevel, S., Koetzsch, S., Weilenmann, H.U., Boon, N., Hammes, F., Routine bacterial analysis with automated flow cytometry. J. Microbiol. Methods 94:2 (2013), 73–76.
135. Velten, S., Boller, M., Köster, O., Helbing, J., Weilenmann, H.-U., Hammes, F., Development of biomass in a drinking water granular active carbon (GAC) filter. Water Res. 45 (2011), 6347–6354.
136. Vesey, G., Slade, J.S., Fricker, C.R., Taking the eye strain out of environmental cryptosporidium analysis. Lett. Appl. Microbiol. 13:2 (1991), 62–65.
137. Villarino, A., Rager, M.N., Grimont, P.A., Bouvet, O.M., Are UV-induced nonculturable Escherichia coli K-12 cells alive or dead?. Eur. J. Biochem. 270:12 (2003), 2689–2695.
138. Vital, M., Dignum, M., Magic-Knezev, A., Ross, P., Rietveld, L., Hammes, F., Flow cytometry and adenosine tri-phosphate analysis: alternative possibilities to evaluate major bacteriological changes in drinking water treatment and distribution systems. Water Res. 46:15 (2012), 4665–4676.
139. Vital, M., Fuechslin, H.P., Hammes, F., Egli, T., Growth of Vibro cholerae O1 Ogawa Eltor in freshwater. Microbiol. SGM 153 (2007), 1993–2001.
140. Vital, M., Stucki, D., Egli, T., Hammes, F., Evaluating the growth potential of pathogenic bacteria in water. Appl. Environ. Microb. 76:19 (2010), 6477–6484.
141. VMM, Algemeen Waterverkoopreglement. 2014, Vlaamse Milieumaatschappij.
142. Vrouwenvelder, J.S., Manolarakis, S.A., van der Hoek, J.P., van Paassen, J.A., van der Meer, W.G., van Agtmaal, J.M., Prummel, H.D., Kruithof, J.C., van Loosdrecht, M.C., Quantitative biofouling diagnosis in full scale nanofiltration and reverse osmosis installations. Water Res. 42:19 (2008), 4856–4868.
143. Wang, Y., Hammes, F., Egli, T., The impact of industrial-scale cartridge filtration on the native microbial communities from groundwater. Water Res. 42:16 (2008), 4319–4326.
144. Wang, Y., Hammes, F., Boon, N., Chami, M., Egli, T., Isolation and characterization of low nucleic acid (LNA)-content bacteria. Isme J. 3:8 (2009), 889–902.
145. Wang, Y., Hammes, F., De Roy, K., Verstraete, W., Boon, N., Past, present and future applications of flow cytometry in aquatic microbiology. Trends Biotechnol. 28:8 (2010), 416–424.
146. Wen, G., Ma, J., Huang, T.L., Egli, T., Using coagulation to restrict microbial re-growth in tap water by phosphate limitation in water treatment. J. Hazard Mater 280c (2014), 348–355.
147. Wert, E.C., Dong, M.M., Rosario-Ortiz, F.L., Using digital flow cytometry to assess the degradation of three cyanobacteria species after oxidation processes. Water Res. 47:11 (2013), 3752–3761.
148. WHO, Expert consensus. Bartram, J., Cotruvo, J.A., Exner, M., Fricker, C.R., Glasmacher, A., (eds.) Heterotrophic Plate Counts and Drinking-water Safety - the Significance of HPCs for Water Quality and Human Health, 2003, IWA Publishing on behalf of the World Health Organisation, London.
149. WHO, Heterotrophic Plate Counts and Drinking-water Safety - the Significance of HPCs for Water Quality and Human Health. 2003, IWA Publishing on behalf of the World Health Organisation, London.
150. Winterberg, H., Zur Methodik der Bakterienzählung. Z. Hyg. Infekt. 29:1 (1898), 75–93.
151. Yang, L., Wu, L., Zhu, S., Long, Y., Hang, W., Yan, X., Rapid, absolute, and simultaneous quantification of specific pathogenic strain and total bacterial cells using an ultrasensitive dual-color flow cytometer. Anal. Chem. 82:3 (2010), 1109–1116.
152. Zeder, M., Pernthaler, J., Multispot live-image autofocusing for high-throughput microscopy of fluorescently stained bacteria. Cytom. A 75:9 (2009), 781–788.