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Environmental Monitoring and Assessment

, Volume 185, Issue 3, pp 2565–2576 | Cite as

Evaluation of concentration efficiency of the Pseudomonas aeruginosa phage PP7 in various water matrixes by different methods

  • Hugo Ramiro Poma
  • Verónica Beatriz Rajal
  • María Dolores Blanco Fernández
  • Patricia Angélica Barril
  • Miguel Oscar Giordano
  • Gisela Masachessi
  • Laura Cecilia Martínez
  • María Beatriz Isa
  • María Cecilia Freire
  • Gabriela López Riviello
  • Daniel Cisterna
  • Silvia Viviana Nates
  • Viviana Andrea Mbayed
Article

Abstract

Enteric viruses monitoring in surface waters requires the concentration of viruses before detection assays. The aim of this study was to evaluate different methods in terms of recovery efficiencies of bacteriophage PP7 of Pseudomonas aeruginosa, measured by real-time PCR, using it as a viral control process in water analysis. Different nucleic acid extraction methods (silica–guanidinium thiocyanate, a commercial kit (Qiagen Viral RNA Kit) and phenol–chloroform with alcohol precipitation) exhibited very low recovery efficiencies (0.08–4.18 %), being the most efficient the commercial kit used for subsequent experiments. To evaluate the efficiency of three concentration methods, PBS (as model for clean water) and water samples from rivers were seeded to reach high (HC, 106 pfu ml−1) and low concentrations (LC, 104 pfu ml−1) of PP7. Tangential ultrafiltration proved to be more efficient (50.36 ± 12.91, 17.21 ± 9.22 and 12.58 ± 2.35 % for HC in PBS and two river samples, respectively) than adsorption–elution with negatively charged membranes (1.00 ± 1.34, 2.79 ± 2.62 and 0.05 ± 0.08 % for HC in PBS and two river samples, respectively) and polyethylene glycol precipitation (15.95 ± 7.43, 4.01 ± 1.12 and 3.91 ± 0.54 %, for HC in PBS and two river samples, respectively), being 3.2–50.4 times more efficient than the others for PBS and 2.7–252 times for river samples. Efficiencies also depended on the initial virus concentration and aqueous matrixes composition. In consequence, the incorporation of an internal standard like PP7 along the process is useful as a control of the water concentration procedure, the nucleic acid extraction, the presence of inhibitors and the variability of the recovery among replicas, and for the calculation of the sample limit of detection. Thus, the use of a process control, as presented here, is crucial for the accurate quantification of viral contamination.

Keywords

Virus concentration Surface water PP7 Absorption/elution Polyethylene glycol Ultrafiltration qRT-PCR 

Notes

Acknowledgments

This research was part of the project PICT-Red 276/06 funded by the Agencia Nacional de Promoción de Ciencia y Técnica in Argentina (ANPCyT). This project was partially supported by NIH Grant D43 TW005718 funded by the Fogarty International Center and the National Institute of Environmental Health Sciences, USA. Hugo Ramiro Poma, Patricia Angélica Barril and Gisela Masachessi received fellowships from CONICET and María Dolores Blanco Fernández from ANPCyT.

References

  1. Albinana-Gimenez, N., Clemente-Casares, P., Calgua, B., Huguet, J. M., Courtois, S., & Girones, R. (2009). Comparison of methods for concentrating human adenoviruses, polyomavirus JC, and noroviruses in source waters and drinking water using quantitative PCR. Journal of Virological Methods, 158, 104–109.CrossRefGoogle Scholar
  2. Aranha-Creado, H., & Brandwein, H. (1999). Application of bacteriophages as surrogates for mammalian viruses: a case for use in filter validation based on precedents and current practices in medical and environmental virology. Journal of Pharmaceutical Science and Technology, 53(2), 75–82.Google Scholar
  3. Atha, D. H., & Ingham, K. C. (1981). Mechanism of precipitation of proteins by polyethylene glycols: analysis in terms of excluded volumes. The Journal of Biological Chemistry, 256, 12108–12117.Google Scholar
  4. Bae, J., & Schwab, K. J. (2008). Evaluation of murine norovirus, feline calicivirus, poliovirus, and MS2 as surrogates for human norovirus in a model of viral persistence in surface water and groundwater. Applied and Environmental Microbiology, 74(2), 477–484.CrossRefGoogle Scholar
  5. Blatchley, E. R., Gong, W. L., Alleman, J. E., Rose, J. B., Huffman, D. E., Otaki, M., & Lisle, J. T. (2007). Effects of wastewater disinfection on waterborne bacteria and viruses. Water Environmental Research, 79(1), 81–92.CrossRefGoogle Scholar
  6. Boom, R., Sol, C. J., Salimans, M. M., Jansen, C. L., Wertheim-van Dillen, P. M., & van der Noordaa, J. (1990). Rapid and simple method for purification of nucleic acids. Journal of Clinical Microbiology, 28(3), 495–503.Google Scholar
  7. Costafreda, M. I., Bosch, A., & Pinto, R. M. (2006). Development, evaluation, and standardization of a real-time TaqMan reverse transcription-PCR assay for quantification of hepatitis A virus in clinical and shellfish samples. Applied and Environmental Microbiology, 72(6), 3846–3855.CrossRefGoogle Scholar
  8. D’Souza, D. H., & Su, X. (2010). Efficacy of chemical treatments against murine norovirus, feline calicivirus, and MS2 bacteriophage. Foodborne Pathogens and Disease, 7(3), 319–326.CrossRefGoogle Scholar
  9. Espinosa, A. C., Mazari-Hiriart, M., Espinosa, R., Maruri-Avidal, L., Méndez, E., & Arias, C. F. (2008). Infectivity and genome persistence of rotavirus and astrovirus in groundwater and surface water. Water Research, 42(10–11), 2618–2628.CrossRefGoogle Scholar
  10. Farrah, S. R. (1982). Chemical factors influencing adsorption of bacteriophage MS2 to membrane filters. Applied and Environmental Microbiology, 43(3), 659–663.Google Scholar
  11. Ferguson, C. M., Coote, B. G., Ashbolt, N. J., & Stevenson, I. M. (1996). Relationships between indicators, pathogens and water quality in an estuarine system. Water Research, 30, 2045–2054.CrossRefGoogle Scholar
  12. Greening, G. E., Hewitt, J., & Lewis, G. D. (2002). Evaluation of integrated cell 3 culture-PCR (C-PCR) for virological analysis of environmental samples. Journal of Applied Microbiology, 93, 745–750.CrossRefGoogle Scholar
  13. Horm, K. M., & D’Souza, D. H. (2011). Survival of human norovirus surrogates in milk, orange, and pomegranate juice, and juice blends at refrigeration (4 °C). Food Microbiology, 28, 1054–1061.CrossRefGoogle Scholar
  14. Huang, Q. S., Greening, G., Baker, M. G., Grimwood, K., Hewitt, J., Hulston, D., van Duin, L., Fitzsimons, A., Garrett, N., Graham, D., Lennon, D., Shimizu, H., Miyamura, T., & Pallansch, M. A. (2005). Persistence of oral polio vaccine virus after its removal from the immunization schedule in New Zealand. Lancet, 366, 394–396.CrossRefGoogle Scholar
  15. Katayama, H., Shimazaki, A., & Ohgaki, S. (2002). Development of a virus concentration method and its application to detection of enterovirus and norwalk virus from coastal seawater. Applied and Environmental Microbiology, 68(3), 1033–1039.CrossRefGoogle Scholar
  16. Lee, J. C., & Lee, L. L. Y. (1981). Preferential solvent interactions between proteins and polyethylene glycols. The Journal of Biological Chemistry, 256(2), 625–631.Google Scholar
  17. Lee, C., Kim, J., & Yoon, J. (2011). Inactivation of MS2 bacteriophage by streamer corona discharge in water. Chemosphere, 82, 1135–1140.CrossRefGoogle Scholar
  18. Lewis, D., & Metcalf, T. G. (1988). Polyethylene glycol precipitation for recovery of pathogenic viruses, including hepatitis A virus and human rotavirus, from oyster, water, and sediment samples. Applied and Environmental Microbiology, 54(8), 1983–1988.Google Scholar
  19. Lukasik, J., Scott, T. M., Andryshak, D., & Farrah, S. R. (2000). Influence of salts on virus adsorption to microporous filters. Applied and Environmental Microbiology, 66(7), 2914–2920.CrossRefGoogle Scholar
  20. Lute, S., Aranha, H., Tremblay, D., Liang, D., Ackermann, H.-W., Chu, B., Moineau, S., & Brorson, K. (2004). Characterization of coliphage PR772 and evaluation of its use for virus filter performance testing. Applied and Environmental Microbiology, 70(8), 4864–4871.CrossRefGoogle Scholar
  21. Mattison, K., Brassard, J., Gagné, M. J., Ward, P., Houde, A., Lessard, L., Simard, C., Shukla, A., Pagotto, F., Jones, T. H., & Trottier, Y. L. (2009). The feline calicivirus as a sample process control for the detection of food and waterborne RNA viruses. International Journal of Food Microbiology, 132, 73–77.CrossRefGoogle Scholar
  22. Méndez, J., Audicana, A., Isern, A., Llaneza, J., Moreno, B., Tarancón, M. L., Cofre, J., & Lucena, F. (2004). Standardised evaluation of the performance of a simple membrane filtration–elution method to concentrate bacteriophages from drinking water. Journal of Virology Methods, 117, 19–25.CrossRefGoogle Scholar
  23. Mesquita, M. M. F., Stimson, J., Chae, G.-T., Tufenkji, N., Ptacek, C. J., Blowes, D. W., & Emelko, M. B. (2010). Optimal preparation and purification of PRD1-like bacteriophages for use in environmental fate and transport studies. Water Research, 44, 1114–1125.CrossRefGoogle Scholar
  24. Morales-Morales, H. A., Vidal, G., Olszewski, J., Rock, C. M., Dasgupta, D., Oshima, K. H., & Smith, G. B. (2003). Optimization of a reusable hollow-fiber ultrafilter for simultaneous concentration of enteric bacteria, protozoa, and viruses from water. Applied and Environmental Microbiology, 69, 4098–4102.CrossRefGoogle Scholar
  25. Muller, J. E., Bessaud, M., Huang, Q. S., Martinez, L. C., Barril, P. A., Morel, V., Balanant, J., Bocacao, J., Hewitt, J., Gessner, B. D., Delpeyroux, F., & Nates, S. V. (2009). Environmental poliovirus surveillance during oral poliovirus vaccine and inactivated poliovirus vaccine use in Córdoba Province, Argentina. Applied and Environmental Microbiology, 75(5), 1395–1401.CrossRefGoogle Scholar
  26. Oshima, K. H. (2001). Efficient and predictable recovery of viruses and Cryptosporidium parvum oocysts from water by ultrafiltration systems. Technical Completion Report, New Mexico Water Research Resources Institute, New Mexico State University.Google Scholar
  27. Park, G. W., Linden, K. G., & Sobsey, M. D. (2011). Inactivation of murine norovirus, feline calicivirus and echovirus 12 as surrogates for human norovirus (NoV) and coliphage (F+) MS2 by ultraviolet light (254 nm) and the effect of cell association on UV inactivation. Letters in Applied Microbiology, 52, 162–167.CrossRefGoogle Scholar
  28. Paul, J. H., Jiang, S. C., & Rose, J. B. (1991). Concentration of viruses and dissolved DNA from aquatic environments by vortex flow filtration. Applied and Environmental Microbiology, 57, 2197–2204.Google Scholar
  29. Perry, R., La Torre, J., Kelley, D., & Greemberg, J. (1972). On the lability of poly(A) sequences during extraction of messenger RNA from polyribosomes. Biochimica et Biophysica Acta, 262, 220–226.CrossRefGoogle Scholar
  30. Petrinca, A. R., Donia, D., Pierangeli, A., Gabrieli, R., Degener, A. M., Bonanni, E., Diaco, L., Cecchini, G., Anastasi, P., & Divizia, M. (2009). Presence and environmental circulation of enteric viruses in three different wastewater treatment plants. Journal of Applied Microbiology, 106(5), 1608–1617.CrossRefGoogle Scholar
  31. Polson, A., Potgieter, G. M., Largier, J. F., Mears, G. E. F., & Joubert, F. J. (1964). The fractionation of protein mixtures by linear polymers of high molecular weight. Biochimca et Biophysica Acta, 82, 463–475.CrossRefGoogle Scholar
  32. Prüss-Üstün, A., & Corvalán, C. (2006). Preventing disease through healthy environments. Towards an estimate of the environmental burden of disease. France: World Health Organization.Google Scholar
  33. Pusch, D., Oh, D. Y., Wolf, S., Dumke, R., Schröter-Bobsin, U., Höhne, M., Röske, I., & Schreier, E. (2005). Detection of enteric viruses and bacterial indicators in German environmental waters. Archives of Virology, 150(5), 929–947.CrossRefGoogle Scholar
  34. Rajal, V. B., McSwain, B. S., Thompson, D. E., Leutenegger, C. M., Kildare, B. J., & Wuertz, S. (2007). Validation of hollow fiber ultrafiltration and real-time PCR using bacteriophage PP7 as surrogate for the quantification of viruses from water samples. Water Research, 41, 1411–1422.CrossRefGoogle Scholar
  35. Rhodes, E. R., Hamilton, D. W., See, M. J., & Wymer, L. (2011). Evaluation of hollow-fiber ultrafiltration primary concentration of pathogens and secondary concentration of viruses from water. Journal of Virological Methods, 176, 38–45.CrossRefGoogle Scholar
  36. Schroeder, E. D., Stallard, W. M., Thompson, D. E., Loge, F. J., Deshusses, M. A., & Cox, H. H. (2002). Management of pathogens associated with storm drain discharge. Davis, Division of Environmental Analysis, California Department of Transportation. California, US.Google Scholar
  37. Sheih, Y. S., Baric, R. S., & Sobsey, M. D. (1997). Detection of low levels of enteric viruses in metropolitan and airplane sewage. Applied and Environmental Microbiology, 63(11), 4401–4407.Google Scholar
  38. Skraber, S., Gassilloud, B., & Gantzer, C. (2004). Comparison of coliforms and coliphages as tools for assessment of viral contamination in river water. Applied and Environmental Microbiology, 70(6), 3644–3649.CrossRefGoogle Scholar
  39. Sobsey, M. D., & Glass, J. S. (1984). Influence of water quality on enteric virus concentration by microporous filter methods. Applied and Environmental Microbiology, 47(5), 956–960.Google Scholar
  40. Sobsey, M. D., & Hickey, A. R. (1985). Effects of humic and fulvic acids on poliovirus concentration from water by microporous filtration. Applied and Environmetal Microbiology, 49(2), 259–264.Google Scholar
  41. Straub, T. M., & Chandler, D. P. (2003). Towards a unified system for detecting waterborne pathogens. Journal of Microbiological Methods, 53, 185–197.CrossRefGoogle Scholar
  42. Subramanian, S., Altaras, G. M., Chen, J., Hughes, B. S., Zhou, W., & Altaras, N. E. (2005). Pilot-scale adenovirus seed production through concurrent virus release and concentration by hollow fiber filtration. Biotechnology Progress, 21, 851–859.CrossRefGoogle Scholar
  43. Syngouna, V. I., & Chrysikopoulos, C. V. (2010). Interaction between viruses and clays in static and dynamic batch systems. Environmental Science and Technology, 44, 4539–4544.CrossRefGoogle Scholar
  44. Victoria, M., Guimarães, F., Fumian, T., Ferreira, F., Vieira, C., Leite, J. P., & Miagostovich, M. (2009). Evaluation of an adsorption–elution method for detection of astrovirus and norovirus in environmental waters. Journal of Virological Methods, 156, 73–76.CrossRefGoogle Scholar
  45. Weiss, S. A. (1980). Concentration of baboon endogenous virus in large-scale production by use of hollow-fiber ultrafiltration technology. Biotechnology and Bioengineering, 22, 19–31.CrossRefGoogle Scholar
  46. Winona, L. J., Ommani, A. W., Olszewski, J., Nuzzo, J. B., & Oshima, K. H. (2001). Efficient and predictable recovery of viruses from water by small scale ultrafiltration systems. Canadian Journal of Microbiolgy, 47, 1033–1041.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Hugo Ramiro Poma
    • 1
  • Verónica Beatriz Rajal
    • 1
    • 2
  • María Dolores Blanco Fernández
    • 3
  • Patricia Angélica Barril
    • 4
  • Miguel Oscar Giordano
    • 4
  • Gisela Masachessi
    • 4
  • Laura Cecilia Martínez
    • 4
  • María Beatriz Isa
    • 4
  • María Cecilia Freire
    • 6
  • Gabriela López Riviello
    • 5
  • Daniel Cisterna
    • 6
  • Silvia Viviana Nates
    • 4
  • Viviana Andrea Mbayed
    • 3
  1. 1.INIQUI-CONICETUniversidad Nacional de SaltaSaltaArgentina
  2. 2.Fogarty International CenterUniversity of California at DavisDavisUSA
  3. 3.Cátedra de Virología, Facultad de Farmacia y BioquímicaUniversidad de Buenos AiresCiudad Autónoma de Buenos AiresArgentina
  4. 4.Instituto de Virología Dr. J. M. VanellaUniversidad Nacional de CórdobaCórdobaArgentina
  5. 5.Departamento Científico PericialPrefectura Naval ArgentinaCiudad Autónoma de Buenos AiresArgentina
  6. 6.Instituto Nacional de Enfermedades Infecciosas INEI-ANLIS Dr. Carlos G. MalbránCiudad Autónoma de Buenos AiresArgentina

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