Skip to main content
SpringerLink
Log in

Coliphages as Indicators for the Microbial Quality of Treated Wastewater Effluents

  • Original Paper
  • Published:
Food and Environmental Virology Aims and scope Submit manuscript

Abstract

Wastewater effluents are a reliable water source for non-potable water reuse including unrestricted crop irrigation in arid regions suffering from water scarcity. This study was performed to develop and optimize a procedure to concentrate coliphages from 100 L of treated effluent. Moreover, the reduction of coliphages by filtration and disinfection by either chlorine or UV was compared with that of fecal coliform (FC). The adsorption efficiency of MS2 and Qβ coliphages by the NanoCeram filter was similar and reached 99.8%. Elution efficiency of MS2 coliphage from the NanoCeram filters by a solution of 1% NaPP and 0.05 M glycine, pH 9.5, was 74  ±  9.5%. The highest reconcentration efficiency of MS2 and Qβ coliphages was obtained with polyethylene glycol (PEG) precipitation and reached 76  ±  28% and 90  ±  11%, respectively. In comparison, the reconcentration efficiency of organic flocculation was 0% and 1.3% for Qβ and MS2 coliphages, respectively. The overall recovery efficiency of MS2 coliphages from 100 L tertiary effluent was 57  ±  1.5%. Poor reduction was observed for coliphages compared to FC by filtration and chlorine disinfection although; the reduction of FC, as measured by cultivation, was satisfactory and within the guidelines for unrestricted irrigation. High correlation between the reduction of FC and coliphages was recorded for tertiary effluent disinfected by UV irradiation. Monitoring the microbial quality of tertiary effluent using qPCR for the enumeration of FC was found unsuitable, because DNA levels were unaffected by the treatment processes. The results of this study demonstrated that monitoring the microbial quality of tertiary effluent by FC may not reflect the health risks encountered by the application of these effluents and the addition of coliphages to the monitoring programs may allow for accurate assessment of the health risks introduced by the application of tertiary effluent.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Allwood, P. B., Malik, Y. S., Maherchandani, S., Hedberg, C. W., & Goyal, S. M. (2005). Effect of temperature on the survival of F-specific RNA coliphage, feline calicivirus, and Escherichia coli in chlorinated water. International Journal of Environmental Research Public Health, 2(3–4), 442–446.

    Article  CAS  PubMed  Google Scholar 

  • APHA, AWWA, WEF (1999). Standard methods for the examination of water 20 and wastewater. American Public Health Association, Washington, DC

  • Ashbolt, N. J., Grabow, O. K., & Snozzi, M. (2001). Indicators of microbial water quality. In L. Fewtrell & J. Bartram (Eds.), Water quality: Guidelines, standards and health (pp. 289–315). London, UK: IWA Publishing.

    Google Scholar 

  • Bennett, H. B., O’Dell, H. D., Norton, G., Shin, G., Hsu, F. C., & Meschke, J. S. (2010). Evaluation of a novel electropositive filter for the concentration of viruses from diverse water matrices. Water Science and Technology, 61(2), 317–322.

    Article  CAS  PubMed  Google Scholar 

  • Callejón, R. M., Rodríguez-Naranjo, M. I., Ubeda, C., Hornedo-Ortega, R., Garcia-Parrilla, M. C., & Troncoso, A. M. (2015). Reported foodborne outbreaks due to fresh produce in the United States and European union: Trends and causes. Foodborne Pathogens Disease, 12(1), 32–38.

    Article  PubMed  Google Scholar 

  • Cashdollar, J. L., & Wymer, L. (2013). Methods for primary concentration of viruses from water samples: A review and meta-analysis of recent studies. Journal of Applied Microbiology, 115, 1–11.

    Article  CAS  PubMed  Google Scholar 

  • Diston, D., Ebdon, J. E., & Taylor, H. D. (2012). The effect of UV-C radiation (254 nm) on candidate microbial source tracking phages infecting a human-specific strain of bacteroides fragilis (GB-124). Journal of Water and Health, 10(2), 262–270.

    Article  CAS  PubMed  Google Scholar 

  • Fout, G. S., Cashdollar, J. L., Varughese, E. A., Parshionikar, S. U., & Grimm, A. C. (2012). Method 1615: Measurement of enterovirus and norovirus occurrence in water by culture and RT-qPCR. Washington, DC: U.S. Environmental Protection Agency.

    Google Scholar 

  • Friedler, E. (2001). Water reuse - an integral part of water resources management: Israel as a case study. Water Policy, 3, 29–39.

    Article  Google Scholar 

  • Gassilloud, B., Schwartzbrod, L., & Gantzer, C. (2003). Presence of viral genomes in mineral water: A sufficient condition to assume infectious risk. Applied and Environmental Microbiology, 69(7), 3965–3969.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gerba, C. P. (1984). Applied and theoretical aspects of virus adsorption to surfaces. Advances in Applied Microbiology, 30, 133–168.

    Article  CAS  PubMed  Google Scholar 

  • Gerrity, D., Pecson, B. T., Shane, R., & Rhodes Trussell, R. (2013). Potable reuse treatment trains throughout the world. Journal of Water Supply Research and Technology - AQUA, 62(6), 321–338.

    Article  CAS  Google Scholar 

  • Gibson, K. E., Schwab, K. J., Spencer, S. K., & Borchardt, M. A. (2012). Measuring and mitigating inhibition during quantitative real-time PCR analysis of viral nucleic acid extracts from large-volume environmental water samples. Water Research, 46, 4281–4291.

    Article  CAS  PubMed  Google Scholar 

  • Gomila, M., Solis, J. J., David, Z., Ramon, C., & Lalucat, J. (2008). Comparative reductions of bacterial indicators, bacteriophage-infecting enteric bacteria and enteroviruses in wastewater tertiary treatments by lagooning and UV-radiation. Water Science and Technology, 58(11), 2223–2233.

    Article  CAS  PubMed  Google Scholar 

  • Grabow, W. O. K. (2001). Bacteriophages: Update on application as models for viruses in water. Water SA, 27, 251–268.

    Google Scholar 

  • Haramoto, E., Kitajima, M., Hata, A., Torrey, J. R., Masago, Y., Sano, D., & Katayama, H. (2018). A review on recent progress in the detection methods and prevalence of human enteric viruses in water. Water Research, 135, 168–186.

    Article  CAS  PubMed  Google Scholar 

  • Harwood, V. J., Levine, A. D., Scott, T. M., Chivukula, V., Lukasik, J., Farrah, S. R., & Rose, J. B. (2005). Validity of the indicator organism paradigm for pathogen reduction in reclaimed water and public health protection. Applied and Environment Microbiology, 71, 3163–3170.

    Article  CAS  Google Scholar 

  • Hata, A., Kitajima, M., & Katayama, H. (2012). Occurrence and reduction of human viruses, F-specific RNA coliphage geno-groups and microbial indicators at a full-scale wastewater treatment plant in Japan. Journal of Applied Microbiology, 114, 545–554.

    Article  PubMed  Google Scholar 

  • Ikner, L. A., Soto-Beltran, M., & Bright, K. R. (2011). New method using a positively charged microporous filter and ultrafiltration for concentration of viruses from tap water. Applied and Environment Microbiology, 77, 3500–3506.

    Article  CAS  Google Scholar 

  • Inbar, Y. (2007). New standards for treated wastewater reuse in Israel. In M. K. Zaidi (Ed.), Wastewater reuse-risk assessment, decision making and environmental security (pp. 291–296). Berlin, Germany: Springer.

    Chapter  Google Scholar 

  • IAWPRC. (1991). Study group on health related water microbiology, bacteriophages as model viruses in water quality control. Water Research, 25, 529–545.

    Article  Google Scholar 

  • Karim, M. R., Rhodes, E. R., Brinkman, N., Wymer, L., & Fout, G. S. (2009). New electropositive filter for concentrating enteroviruses and noroviruses from large volumes of water. Applied and Environment Microbiology, 75(8), 2393–2399.

    Article  CAS  Google Scholar 

  • Katayama, H., Shimasaki, 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 Environment Microbiology, 68(3), 1033–1039.

    Article  CAS  Google Scholar 

  • Katzenelson, E., Fattal, B., & Hostovesky, T. (1976). Organic flocculation: An efficient second-step concentration method for the detection of viruses in tap water. Applied and Environmental Microbiology, 32(4), 638–639.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kummu, M., Ward, P. J., de Moel, H., & Varis, O. (2010). Is physical water scarcity a new phenomenon? Global assessment of water shortage over the last two millennia. Environmental Research Letter, 5, 1–10.

    Article  Google Scholar 

  • Lambertini, E., Spencer, S. K., Bertz, P. D., Loge, F. J., Kieke, B. A., & Borchardt, M. A. (2008). Concentration of enteroviruses, adenoviruses, and noroviruses from drinking water by use of glass wool filters. Applied and Environment Microbiology, 74, 2990–2996.

    Article  CAS  Google Scholar 

  • Lewis, G. 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 Environment Microbiology, 54, 1983–1988.

    Article  CAS  Google Scholar 

  • Lin, J., & Ganesh, A. (2013). Water quality indicators: Bacteria, coliphages, enteric viruses. International Journal of Environmental Health Research, 23(6), 484–506.

    Article  CAS  PubMed  Google Scholar 

  • Logan, K. B., Rees, G. E., Seeley, N. D., & Primrose, S. B. (1980). Rapid concentration of bacteriophages from large volumes of freshwater: Evaluation of positively charged, microporous filters. Journal of Virological Methods, 1, 87–97.

    Article  CAS  PubMed  Google Scholar 

  • McMinn, B. R., Ashbolt, N. J., & Korajkic, A. (2017). Bacteriophages as indicators of faecal pollution and enteric virus removal. Letters in Applied Microbiology, 65, 11–26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nasser, A. M., Glozman, R., & Nitzan, Y. (2002). Contribution of microbial activity to virus reduction in saturated soil. Water Research, 36, 2589–2595.

    Article  CAS  PubMed  Google Scholar 

  • Nasser, A. M., Paulman, H., Sela, O., Ktaitzer, T., Cikurel, H., Zuckerman, O., et al. (2006). UV disinfection of wastewater effluents for unrestricted irrigation. Water Science and Technology, 54, 83–88.

    Article  CAS  PubMed  Google Scholar 

  • Nasser, A. M., Benisti, N. L., Ofer, N., Hovers, S., & Nitzan, Y. (2017). Comparative reduction of giardia cysts, F+ coliphages, sulphite reducing clostridia and fecal coliforms by wastewater treatment processes. Journal of Environmental Science Health, 52(2), 144–148.

    Article  CAS  PubMed  Google Scholar 

  • Ogorzaly, L., & Gantzer, C. (2006). Development of real-time RT-PCR methods for specific detection of F-specific RNA bacteriophage genogroups: Application to urban raw wastewater. Journal of Virological Methods, 138(1–2), 131–139.

    Article  CAS  PubMed  Google Scholar 

  • Polaczyk, A. L., Narayanan, J., Cromeans, T. L., Hahn, D., Roberts, J. M., Amburgey, J. E., & Hill, V. R. (2008). Ultrafiltration-based techniques for rapid and simultaneous concentration of multiple microbe classes from 100-L tap water samples. Journal of Microbiological Methods, 73, 92–99.

    Article  CAS  PubMed  Google Scholar 

  • Pouillot, R., van Doren, J. M., Woods, J., Plante, D., Smith, M., Goblick, G., et al. (2015). Meta-analysis of the reduction of norovirus and male-specific coliphage concentrations in wastewater treatment plants. Applied and Environmental Microbiology, 81(14), 4669–4681.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reynolds, K. A., Mena, K. D., & Gerba, C. P. (2008). Risk of waterborne illness via drinking water in the United States. Reviews of Environmental Contamination and Toxicology, 192, 117–158.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schrader, C., Schielke, A., & Johne, R. (2012). PCR inhibitors – occurrence, properties and removal. Journal of Applied Microbiology, 113, 1014–1026.

    Article  CAS  PubMed  Google Scholar 

  • Schultz, A. C., Perelle, S., Di Pasquale, S., Kovac, K., De Medici, D., Fach, P., et al. (2011). Collaborative validation of a rapid method for efficient virus concentration in bottled water. International Journal of Food Microbiology, 145, S158–S166.

    Article  PubMed  Google Scholar 

  • Sinton, L. W., Hall, C. H., Lynch, P. A., & Davies-Colley, R. J. (2002). Sunlight inactivation of fecal indicator bacteria and bacteriophages from waste stabilization pond effluent in fresh and saline waters. Applied and Environmental Microbiology, 68(3), 1122–1131.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sobsey, M. D., & Glass, J. S. (1980). Poliovirus concentration from tap water with electropositive adsorbent filters. Applied and Environment Microbiology, 40(2), 2201–2210.

    Article  Google Scholar 

  • Spellman, R. F. (2013). Handbook of water and wastewater treatment plant operations. Florida, USA: CRC Press.

    Google Scholar 

  • Tallon, P., Magajna, B., Lofranco, C., & Leung, K. (2005). Microbial indicators of fecal contamination in water: A current perspective. Water, Air, and Soil Pollution, 166, 139–166.

    Article  CAS  Google Scholar 

  • Taran-Benshoshan, M., Ofer, N., Dalit, V. O., Aharoni, A., Rebhun, M., Nitzan, Y., & Nasser, A. M. (2015). Cryptosporidium and Giardia removal by secondary and tertiary wastewater treatment. Journal of Environmental Science Health A Toxic/Hazardous Substance Environmental Engineering, 50(12), 1265–1273.

    CAS  Google Scholar 

  • Tchobanoglous, G., Abu-Orf, M., Burton, F. L., Bowden, G., Metcalf, E., Stensel, H. D., et al. (2014). Wastewater engineering: Treatment and resource recovery. New York, USA: McGraw-Hill Education.

    Google Scholar 

  • U.S. EPA (2012). Method 1615.1: Measurement of enterovirus and norovirus occurrence in water by culture and RTqPCR. Office of research and development, National exposure research laboratory, U.S. Environmental Protection Agency, EPA 600/R-10/181, Cincinnati, Ohio.

  • Wallis, C., & Melnick, J. L. (1967). Concentration of enteroviruses on membrane filters. Journal of Virology, 1, 277–472.

    Article  Google Scholar 

  • Wong, K., Fong, T. T., Bibby, K., & Molina, M. (2012). Application of enteric viruses for fecal pollution source tracking in environmental waters. Environment International, 45, 151–164.

    Article  CAS  PubMed  Google Scholar 

  • World Health Organization and International Water Association. (2009). Water safety plan manual: Step-by-step risk management for drinking-water suppliers. World Health Organization. https://apps.who.int/iris/handle/10665/75141.

  • Xander, W. H. (2002). Quantification of bacteria adherent to gastrointestinal mucosa by Real-Time PCR. Journal of Clinical Microbiology, 40, 4423–4427.

    Article  Google Scholar 

  • Zimmerman, M. C., & Gerardi, M. H. (2004). Wastewater pathogens. New Jersey, USA: John Wiley and Sons.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Water Quality Research Laboratory, National Public Health Laboratory, Ministry of Health, Tel Aviv, Israel

    Abidelfatah Nasser & Sivan sasi

  2. Faculty of Life Sciences, Bar-Ilan University, Ramat Gan, Israel

    Sivan sasi & Yeshayahu Nitzan

Authors
  1. Abidelfatah Nasser
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sivan sasi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yeshayahu Nitzan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abidelfatah Nasser.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nasser, A., sasi, S. & Nitzan, Y. Coliphages as Indicators for the Microbial Quality of Treated Wastewater Effluents. Food Environ Virol 13, 170–178 (2021). https://doi.org/10.1007/s12560-020-09459-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12560-020-09459-5

Keywords

Search

Navigation