Effects of ionic strength on bacteriophage MS2 behavior and their implications for the assessment of virus retention by ultrafiltration membranes

Applied and Environmental Microbiology

Volumn 77, Issue 1, 2011, Pages 229-236

  Furiga, Aurelie ^a   Pierre, Gwenaelle ^a   Glories, Marie ^a   Aimar, Pierre ^a   Roques, Christine ^a   Causserand, Christel ^a   Berge, Mathieu ^a  

^a UNIVERSITÉ PAUL SABATIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPHAGE MS2; BATCH EXPERIMENTS; BIOLOGICAL ACTIVITIES; FILTRATION PROCESS; INFECTIOUS VIRUS; MEMBRANE FILTRATIONS; MEMBRANE ULTRAFILTRATION; MOLECULAR METHODS; PATHOGENIC VIRUS; PFU METHOD; Q-RT-PCR; RETENTATE; RETENTION EFFICIENCIES; REVERSE TRANSCRIPTASES; RNA EXTRACTION; STATIC CONDITIONS; ULTRA-FILTRATION MEMBRANES; VIRAL GENOME; WATER TECHNOLOGIES;

BACTERIOPHAGES; BIOFILTRATION; EXPERIMENTS; GENES; MEMBRANES; MICROFILTRATION; NUCLEIC ACIDS; POLYMERASE CHAIN REACTION; RNA; ULTRAFILTRATION; WATER FILTRATION; WATER TREATMENT;

IONIC STRENGTH;

VIRUS RNA;

ASSESSMENT METHOD; BACTERIOPHAGE; BIOACTIVITY; DEVELOPMENTAL BIOLOGY; ESTIMATION METHOD; EXPERIMENTAL STUDY; GENETIC ANALYSIS; GENOME; INFECTIOUS DISEASE; ION; MEMBRANE; MOLECULAR ANALYSIS; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; ULTRAFILTRATION; VIRAL DISEASE; WATER TREATMENT;

ARTICLE; COLIPHAGE; DRUG EFFECT; GENETICS; ISOLATION AND PURIFICATION; MEMBRANE; METHODOLOGY; MICROBIAL VIABILITY; MICROBIOLOGY; OSMOLARITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ULTRAFILTRATION; VIRUS CULTURE;

LEVIVIRUS; MEMBRANES; MICROBIAL VIABILITY; OSMOLAR CONCENTRATION; PLAQUE ASSAY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, VIRAL; ULTRAFILTRATION; WATER MICROBIOLOGY;

MIRIDAE;

EID: 79251648119     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01075-10     Document Type: Article

References (42)

1. Anders, R., and C. V. Chrysikopoulos. 2006. Evaluation of the factors controlling the time-dependent inactivation rate coefficients of bacteriophage MS2 and PRD1. Environ. Sci. Technol. 40:3237-3242.
2. Anderson, T. F., C. Rappaport, and N. A. Muscatine. 1953. On the structure and osmotic properties of phage particles. Ann. Inst. Pasteur (Paris) 84:5-14.
3. AWPRC Study Group on Health Related Water Microbiology. 1991. Bacteriophages as model viruses in water quality control. Water Res. 25:529-545.
4. Borrego, J. J., and P. Romero. 1985. Coliphage survival in seawater. Water Res. 19:557-562.
5. Cordova, A., M. Deserno, W. M. Gelbart, and A. Ben-Shaul. 2003. Osmotic shock and the strength of viral capsids. Biophys. J. 85:70-74.
6. Dong, Y., J. Kim, and G. D. Lewis. 2010. Evaluation of methodology for detection of human adenoviruses in wastewater, drinking water, stream water and recreational waters. J. Appl. Microbiol. 108:800-809.
7. Dryden, S. K., B. Ramaswami, Z. Yuan, D. E. Giammar, and L. T. Angenent. 2006. A rapid reverse transcription-PCR assay for F+ RNA coliphages to trace fecal pollution in Table Rock Lake on the Arkansas-Missouri border. Water Res. 40:3719-3724.
8. Espinosa, A. C., M. Mazari-Hiriart, R. Espinosa, L. Maruri-Avidal, E. Méndez, and C. F. Arias. 2008. Infectivity and genome persistence of rotavirus and astrovirus in groundwater and surface water. Water Res. 42:2618-2628.
9. Feng, Y. Y., S. L. Ong, J. Y. Hu, X. L. Tan, and W. J. Ng. 2003. Effects of pH and temperature on the survival of coliphages MS2 and Q.β. J. Ind. Microbiol. Biotechnol. 30:549-552.
10. Fields, B. N., D. M. Knipe, P. M. Howley, and D. E. Griffin. 2001. Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
11. Floyd, R., and D. G. Sharp. 1979. Viral aggregation: buffer effects in the aggregation of poliovirus and reovirus at low and high pH. Appl. Environ. Microbiol. 38:395-401.
12. Fong, T. T., and E. K. Lipp. 2005. Enteric viruses of humans and animals in aquatic environments: health risks, detection, and potential water quality assessment tools. Microbiol. Mol. Biol. Rev. 69:357-371.
13. Gassilloud, B., and C. Gantzer. 2005. Adhesion-aggregation and inactivation of poliovirus 1 in groundwater stored in a hydrophobic container. Appl. Environ. Microbiol. 71:912-920.
14. Grabow, W. O. K. 2001. Bacteriophages: update on application as models for viruses in water. Water S. A. 27:251-268.
15. Guan, D., R. D. Joerger, K. E. Kniel, K. R. Calci, D. T. Hicks, L. F. Pivarnik, and D. G. Hoover. 2007. Effect of high hydrostatic pressure on four genotypes of F-specific RNA bacteriophages. J. Appl. Microbiol. 102:51-56.
16. Havelaar, A. H., M. van Olphen, and Y. C. Drost. 1993. F-specific RNA bacteriophages are adequate model organisms for enteric viruses in fresh water. Appl. Environ. Microbiol. 59:2956-2962.
17. Hill, V. R., A. M. Kahler, N. Jothikumar, T. B. Johnson, D. Hahn, and T. L. Cromeans. 2007. Multistate evaluation of an ultrafiltration-based procedure for simultaneous recovery of enteric microbes in 100-liter tap water samples. Appl. Environ. Microbiol. 73:4218-4225.
18. Hu, J. Y., S. L. Ong, L. F. Song, Y. Y. Feng, W. T. Liu, T. W. Tan, L. Y. Lee, and W. J. Ng. 2003. Removal of MS2 bacteriophage using membrane technologies. Water Sci. Technol. 47(12):163-168.
19. International Organization of Standardization. 1995. Water quality-detection and enumeration of bacteriophages-part 1: enumeration of F-specific RNA bacteriophages. EN ISO 10705-1. International Organization of Standardization, Geneva, Switzerland.
20. Jacangelo, J. G., R. R. Trussell, and M. Watson. 1997. Role of membrane technology in drinking water treatment in the United States. Desalination 113:119-127.
21. Johnson, H. R., J. M. Hooker, M. B. Francis, and D. S. Clark. 2007. Solubilization and stabilization of bacteriophage MS2 in organic solvents. Biotechnol. Bioeng. 97:224-234.
22. Kirs, M., and D. C. Smith. 2007. Multiplex quantitative real-time reversetranscriptase PCR for F+-specific RNA coliphages: a method for use in microbial source tracking. Appl. Environ. Microbiol. 73:808-814.
23. Kubista, M., J. M. Andrade, M. Bengtsson, A. Forootan, J. Jonak, K. Lind, R. Sindelka, R. Sjoback, B. Sjogreen, L. Strombom, A. Stahlberg, and N. Zoric. 2006. The real-time polymerase chain reaction. Mol. Aspects Med. 27:95-125.
24. Langlet, J., F. Gaboriaud, and C. Gantzer. 2007. Effects of pH on plaque forming unit counts and aggregation of MS2 bacteriophage. J. Appl. Microbiol. 103:1632-1638.
25. LeChevallier, M. W., and K. K. Au. 2004. Water treatment and pathogen control: process efficiency in achieving safe drinking water. IWA Publishing, London, United Kingdom.
26. Moriñigo, M. A., D. Wheeler, C. Berry, C. Jones, M. A. Muñoz, R. Cornax, and J. J. Borrego. 1992. Evaluation of different bacteriophage groups as faecal indicators in contaminated natural waters in southern England. Water Res. 26:267-271.
27. O'Connell, K. P., J. R. Bucher, P. E. Anderson, C. J. Cao, A. S. Khan, M. V. Gostomski, and J. J. Valdes. 2006. Real-time fluorogenic reverse transcription- PCR assays for detection of bacteriophage MS2. Appl. Environ. Microbiol. 72:478-483.
28. Ogorzaly, L., and C. Gantzer. 2006. Development of real-time RT-PCR methods for specific detection of F-specific RNA bacteriophage genogroups: application to urban raw wastewater. J. Virol. Methods 138:131-139.
29. Otaki, M., K. Yano, and S. Ohgaki. 1998. Virus removal in a membrane separation process. Water Sci. Technol. 37:107-116.
30. Pierre, G., C. Causserand, C. Roques, and P. Aimar. 2010. Adsorption of MS2 bacteriophage on ultrafiltration membrane laboratory equipments. Desalination 250:762-766.
31. Polaczyk, A. L., J. Narayanan, T. L. Cromeans, D. Hahn, J. M. Roberts, J. E. Amburgey, and V. R. Hill. 2008. Ultrafiltration-based techniques for rapid and simultaneous concentration of multiple microbe classes from 100-L tap water samples. J. Microbiol. Methods 73:92-99.
32. Rajal, V. B., B. S. McSwain, D. E. Thompson, C. M. Leutenegger, B. J. Kildare, and S. Wuertz. 2007. Validation of hollow fiber ultrafiltration and real-time PCR using bacteriophage PP7 as surrogate for the quantification of viruses from water samples. Water Res. 41:1411-1422.
33. Rose, J. B., X. Zhou, D. W. Griffin, and J. H. Paul. 1997. Comparison of PCR and plaque assay for detection and enumeration of coliphage in polluted marine waters. Appl. Environ. Microbiol. 63:4564-4566.
34. Savichtcheva, O., and S. Okabe. 2006. Alternative indicators of fecal pollution: relations with pathogens and conventional indicators, current methodologies for direct pathogen monitoring and future application perspectives. Water Res. 40:2463-2476.
35. Strauss, J. H., Jr., and R. L. Sinsheimer. 1963. Purification and properties of bacteriophage MS2 and of its ribonucleic acid. J. Mol. Biol. 7:43-54.
36. Thompson, S. S., M. Flury, M. V. Yates, and W. A. Jury. 1998. Role of the air-water-solid interface in bacteriophage sorption experiments. Appl. Environ. Microbiol. 64:304-309.
37. Thompson, S. S., and M. V. Yates. 1999. Bacteriophage inactivation at the air-water-solid interface in dynamic batch systems. Appl. Environ. Microbiol. 65:1186-1190.
38. Trouwborst, T., S. Kuyper, J. C. de Jong, and A. D. Plantinga. 1974. Inactivation of some bacterial and animal viruses by exposure to liquid-air interfaces. J. Gen. Virol. 24:155-165.
39. Urase, T., K. Yamamoto, and S. Ohgaki. 1993. Evaluation of virus removal in membrane separation processes using coliphage Q.-beta. Water Sci. Technol. 28:9-15.
40. Vinje, J., S. J. Oudejans, J. R. Stewart, M. D. Sobsey, and S. C. Long. 2004. Molecular detection and genotyping of male-specific coliphages by reverse transcription-PCR and reverse line blot hybridization. Appl. Environ. Microbiol. 70:5996-6004.
41. Williams, D. F., and J. C. Berg. 1992. The aggregation of colloidal particles at the air-water interface. J. Colloid Interface Sci. 152:218-229.
42. Wolf, S., J. Hewitt, M. Rivera-Aban, and G. E. Greening. 2008. Detection and characterization of F+ RNA bacteriophages in water and shellfish: application of a multiplex real-time reverse transcription PCR. J. Virol. Methods 149:123-128.