Food and Environmental Virology

, Volume 10, Issue 2, pp 176–186 | Cite as

Virus Type-Specific Removal in a Full-Scale Membrane Bioreactor Treatment Process

  • Takayuki Miura
  • Julien Schaeffer
  • Jean-Claude Le Saux
  • Philippe Le Mehaute
  • Françoise S. Le Guyader
Original Paper
First Online:
Received:
Accepted:
  • 146 Downloads

Abstract

We investigated removal of noroviruses, sapoviruses, and rotaviruses in a full-scale membrane bioreactor (MBR) plant by monitoring virus concentrations in wastewater samples during two gastroenteritis seasons and evaluating the adsorption of viruses to mixed liquor suspended solids (MLSS). Sapoviruses and rotaviruses were detected in 25% of MBR effluent samples with log reduction values of 3- and 2-logs in geometric mean concentrations, respectively, while noroviruses were detected in only 6% of the samples. We found that norovirus and sapovirus concentrations in the solid phase of mixed liquor samples were significantly higher than in the liquid phase (P < 0.01, t test), while the concentration of rotaviruses was similar in both phases. The efficiency of adsorption of the rotavirus G1P[8] strain to MLSS was significantly less than norovirus GI.1 and GII.4 and sapovirus GI.2 strains (P < 0.01, t test). Differences in the adsorption of viruses to MLSS may cause virus type-specific removal during the MBR treatment process as shown by this study.

Keywords

Norovirus Sapovirus Rotavirus MBR Mixed liquor suspended solids Adsorption 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

We are very grateful to Jacques Le Pendu (Inserm, Nantes, France), Osamu Nakagomi, and Toyoko Nakagomi (Nagasaki University, Japan) for their helpful discussions. We also thank Cécile Le Mennec and Sylvain Parnaudeau (Ifremer) for their technical assistance. We are grateful to Catherine McLeod (Seafood Safety Assessment) for a critical review of the manuscript. This study was supported by the Japan Society for the Promotion of Science (JSPS) through Postdoctoral Fellowships for Research Abroad (H26-153), and by Ifremer through a research grant from Scientific Director.

References

  1. AFNOR (2011) U47A Méthodes d’analyse en santé animale: Association Française de Normalisation.Google Scholar
  2. Amarasiri, M., Hashiba, S., Miura, T., Nakagomi, T., Nakagomi, O., Ishii, S., et al. (2016). Bacterial histo-blood group antigens contributing to genotype-dependent removal of human noroviruses with a microfiltration membrane. Water Research, 95, 383–391.  https://doi.org/10.1016/j.watres.2016.04.018.CrossRefPubMedGoogle Scholar
  3. Armanious, A., Aeppli, M., Jacak, R., Refardt, D., Sigstam, T., Kohn, T., et al. (2016). Viruses at solid–water interfaces: A systematic assessment of interactions driving adsorption. Environmental Science and Technology, 50(2), 732–743.  https://doi.org/10.1021/acs.est.5b04644.CrossRefPubMedGoogle Scholar
  4. Atmar, R. L., Neill, F. H., Romalde, J. L., Le Guyader, F., Woodley, C. M., Metcalf, T. G., et al. (1995). Detection of Norwalk virus and Hepatitis A virus in shellfish tissues with the PCR. Applied and Environment Microbiology, 61, 3014–3018.Google Scholar
  5. Campos, C. J. A., Kershaw, S., Morgan, O. C., & Lees, D. N. (2017). Risk factors for norovirus contamination of shellfish water catchments in England and Wales. International Journal of Food Microbiology, 241, 318–324.  https://doi.org/10.1016/j.ijfoodmicro.2016.10.028.CrossRefPubMedGoogle Scholar
  6. Chaudhry, R. M., Holloway, R. W., Cath, T. Y., & Nelson, K. L. (2015a). Impact of virus surface characteristics on removal mechanisms within membrane bioreactors. Water Research, 84, 144–152.  https://doi.org/10.1016/j.watres.2015.07.020.CrossRefPubMedGoogle Scholar
  7. Chaudhry, R. M., Nelson, K. L., & Drewes, J. E. (2015b). Mechanisms of pathogenic virus removal in a full-scale membrane bioreactor. Environmental Science and Technology, 49(5), 2815–2822.  https://doi.org/10.1021/es505332n.CrossRefPubMedGoogle Scholar
  8. da Silva, A. K., Kavanagh, O. V., Estes, M. K., & Elimelech, M. (2011). Adsorption and aggregation properties of norovirus GI and GII virus-like particles demonstrate differing responses to solution chemistry. Environmental Science and Technology, 45(2), 520–526.  https://doi.org/10.1021/es102368d.CrossRefPubMedGoogle Scholar
  9. da Silva, A. K., Le Guyader, F. S., Le Saux, J.-C., Pommepuy, M., Montgomery, M. A., & Elimelech, M. (2008). Norovirus removal and particle association in a waste stabilization pond. Environmental Science and Technology, 42(24), 9151–9157.  https://doi.org/10.1021/es802787v.CrossRefPubMedGoogle Scholar
  10. da Silva, A. K., Le Saux, J. C., Parnaudeau, S., Pommepuy, M., Elimelech, M., & Le Guyader, F. S. (2007). Evaluation of removal of noroviruses during wastewater treatment, using real-time reverse transcription-PCR: Different behaviors of genogroups I and II. Applied and Environment Microbiology, 73(24), 7891–7897.  https://doi.org/10.1128/aem.01428-07.CrossRefGoogle Scholar
  11. Davenport, E. R., Mizrahi-Man, O., Michelini, K., Barreiro, L. B., Ober, C., & Gilad, Y. (2014). Seasonal variation in human gut microbiome composition. PLoS ONE, 9(3), e90731.  https://doi.org/10.1371/journal.pone.0090731.CrossRefPubMedPubMedCentralGoogle Scholar
  12. de Graaf, M., van Beek, J., & Koopmans, M. P. G. (2016). Human norovirus transmission and evolution in a changing world. Nature Reviews Microbiology, 14, 421–433.  https://doi.org/10.1038/nrmicro.2016.48.CrossRefPubMedGoogle Scholar
  13. Denisova, E., Dowling, W., LaMonica, R., Shaw, R., Scarlata, S., Ruggeri, F., et al. (1999). Rotavirus capsid protein VP5* permeabilizes membranes. Journal of Virology, 73(4), 3147–3153.PubMedPubMedCentralGoogle Scholar
  14. Estes, M. K., & Greenberg, H. B. (2013). Rotaviruses. In D. M. Knipe & P. M. Howley (Eds.), Fields virology (6th ed., Vol. 2, pp. 1347–1401). Philadelphia: Lippincott Williams & Wilkins.Google Scholar
  15. Ettayebi, K., Crawford, S. E., Murakami, K., Broughman, J. R., Karandikar, U., Tenge, V. R., et al. (2016). Replication of human noroviruses in stem cell-derived human enteroids. Science, 353, 1387–1393.  https://doi.org/10.1126/science.aaf5211.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Furtak, V., Rovalnen, M., Mirovhnichenko, O., Zagorodnyaya, T., Laassri, M., Zaldi, S. Z., et al. (2016). Environmental surveillance of viruses by tangential flow filtration and metagenomic reconstruction. Eurosurveillance Weekly, 21(15), 30193.  https://doi.org/10.2807/1560-7917.ES.2016.21.15.30193.CrossRefGoogle Scholar
  17. Geoghegan, J. L., Senior, A. M., Di Giallonardo, F., & Holmes, E. C. (2016). Virological factors that increase the transmissibility of emerging human viruses. Proceedings of the National Academy of Sciences, 113(15), 4170–4175.  https://doi.org/10.1073/pnas.1521582113.CrossRefGoogle Scholar
  18. Gerba, C. P. (1984). Applied and theoretical aspects of virus adsorption to surfaces. In I. L. Allen (Ed.), Advances in applied microbiology (Vol. 30, pp. 133–168). New York: Academic Press.Google Scholar
  19. Gerba, C. P., Goyal, S. M., Hurst, C. J., & Labelle, R. L. (1980). Type and strain dependence of enterovirus adsorption to activated sludge, soils and estuarine sediments. Water Research, 14(9), 1197–1198.  https://doi.org/10.1016/0043-1354(80)90176-1.CrossRefGoogle Scholar
  20. Havelaar, A. H., Kirk, M. D., Torgerson, P. R., Gibb, H. J., Hald, T., Lake, R. J., et al. (2015). World Health Organization global estimates and regional comparisons of the burden of foodborne disease in 2010. PLoS Medicine, 12(12), e1001923.  https://doi.org/10.1371/journal.pmed.1001923.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Jones, T. H., Brassard, J., Topp, E., Wilkes, G., & Lapen, D. R. (2017). Waterborne viruses and F-specific coliphages in mixed-use watersheds: Microbial associations, host specificities, and affinities with environmental/land use factors. Applied and Environment Microbiology, 83, e02763-16.  https://doi.org/10.1128/AEM.02763-16.CrossRefGoogle Scholar
  22. Kageyama, T., Kojima, S., Shinohara, M., Uchida, K., Fukushi, S., Hoshino, F. B., et al. (2003). Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. Journal of Clinical Microbiology, 41(4), 1548–1557.  https://doi.org/10.1128/jcm.41.4.1548-1557.2003.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Kazama, S., Miura, T., Masago, Y., Konta, Y., Tohma, K., Manaka, T., et al. (2017). Environmental surveillance of norovirus genogroups I and II for sensitive detection of epidemic variants. Applied and Environment Microbiology, 83, e03406–e03416.  https://doi.org/doi.org/10.1128/AEM.03406-16.CrossRefGoogle Scholar
  24. Kim, I. S., Trask, S. D., Babyonyshev, M., Dormitzer, P. R., & Harrison, S. C. (2010). Effect of mutations in VP5* hydrophobic loops on rotavirus cell entry. Journal of Virology, 84(12), 6200–6207.  https://doi.org/10.1128/jvi.02461-09.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kitajima, M., Iker, B. C., Pepper, I. L., & Gerba, C. P. (2014). Relative abundance and treatment reduction of viruses during wastewater treatment processes—identification of potential viral indicators. Science of the Total Environment, 488–489, 290–296.  https://doi.org/10.1016/j.scitotenv.2014.04.087.CrossRefPubMedGoogle Scholar
  26. Le Guyader, F. S., Atmar, R. L., & Le Pendu, J. (2012). Transmission of viruses through shellfish: When specific ligands come into play. Current Opinion in Virology, 2, 103–110.CrossRefPubMedGoogle Scholar
  27. Le Mennec, C., Parnaudeau, S., Rumebe, M., Le Saux, J.-C., Piquet, J.-C., & Le Guyader, F. S. (2017). Follow-up of norovirus contamination in an oyster production area linked to repeated outbreaks. Food and Environmental Virology, 9, 54–61.  https://doi.org/10.1007/s12560-016-9260-6.CrossRefPubMedGoogle Scholar
  28. Lee, J. C., & Lee, L. L. Y. (1981). Preferential solvent interactions between proteins and polyethylene glycol. Journal of Biological Chemistry, 256, 625–631.PubMedGoogle Scholar
  29. Li, D., Breiman, A., Le Pendu, J., & Uyttendaele, M. (2015). Binding to histo-blood group antigen-expressing bacteria protects human norovirus from acute heat stress. Frontiers in Microbiology, 6, 659.  https://doi.org/10.3389/fmicb.2015.00659.PubMedPubMedCentralGoogle Scholar
  30. Loisy, F., Atmar, R. L., Guillon, P., Le Cann, P., Pommepuy, M., & Le Guyader, F. S. (2005). Real-time RT-PCR for norovirus screening in shellfish. Journal of Virological Methods, 123(1), 1–7.CrossRefPubMedGoogle Scholar
  31. Ma, Z., Wen, X., Zhao, F., Xia, Y., Huang, X., Waite, D., et al. (2013). Effect of temperature variation on membrane fouling and microbial community structure in membrane bioreactor. Bioresource Technology, 133, 462–468.  https://doi.org/10.1016/j.biortech.2013.01.023.CrossRefPubMedGoogle Scholar
  32. Marti, E., Monclús, H., Jofre, J., Rodriguez-Roda, I., Comas, J., & Balcázar, J. L. (2011). Removal of microbial indicators from municipal wastewater by a membrane bioreactor (MBR). Bioresource Technology, 102(8), 5004–5009.  https://doi.org/10.1016/j.biortech.2011.01.068.CrossRefPubMedGoogle Scholar
  33. Michen, B., & Graule, T. (2010). Isoelectric points of viruses. Journal of Applied Microbiology, 109(2), 388–397.  https://doi.org/10.1111/j.1365-2672.2010.04663.x.PubMedGoogle Scholar
  34. Miura, T., Lhomme, S., Le Saux, J. C., Le Mehaute, P., Guillois, Y., Couturier, E., et al. (2016). Detection of hepatitis E virus in sewage after an outbreak on a French island. Food and Environmental Virology, 8(3), 194–199.  https://doi.org/10.1007/s12560-016-9241-9.CrossRefPubMedGoogle Scholar
  35. Miura, T., Okabe, S., Nakahara, Y., & Sano, D. (2015). Removal properties of human enteric viruses in a pilot-scale membrane bioreactor (MBR) process. Water Research, 75, 282–291.  https://doi.org/10.1016/j.watres.2015.02.046.CrossRefPubMedGoogle Scholar
  36. Miura, T., Sano, D., Suenaga, A., Yoshimura, T., Fuzawa, M., Nakagomi, T., et al. (2013). Histo-blood group antigen-like substances of human enteric bacteria as specific adsorbents for human noroviruses. Journal of Virology, 87, 9441–9451.  https://doi.org/10.1128/JVI.01060-13.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Newton, R. J., McLellan, S. L., Dila, D. K., Vineis, J. H., Morrison, H. G., Eren, A. M., et al. (2015). Sewage reflects the microbiomes of human populations. mBio.  https://doi.org/10.1128/mBio.02574-14.PubMedPubMedCentralGoogle Scholar
  38. Nguyen, T., Roddick, F., & Fan, L. (2012). Biofouling of water treatment membranes: A review of the underlying causes, monitoring techniques and control measures. Membranes, 2(4), 804.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Oka, T., Katayama, K., Hansman, G. S., Kageyama, T., Ogawa, S., Wu, F.-T., et al. (2006). Detection of human sapovirus by real-time reverse transcription-polymerase chain reaction. Journal of Medical Virology, 78(10), 1347–1353.  https://doi.org/10.1002/jmv.20699.CrossRefPubMedGoogle Scholar
  40. Ottoson, J., Hansen, A., Björlenius, B., Norder, H., & Stenström, T. A. (2006). Removal of viruses, parasitic protozoa and microbial indicators in conventional and membrane processes in a wastewater pilot plant. Water Research, 40(7), 1449–1457.CrossRefPubMedGoogle Scholar
  41. Pang, X., Cao, M., Zhang, M., & Lee, B. (2011). Increased sensitivity for various rotavirus genotypes in stool specimens by amending three mismatched nucleotides in the forward primer of a real-time RT-PCR assay. Journal of Virological Methods, 172(1–2), 85–87.  https://doi.org/10.1016/j.jviromet.2010.12.013.CrossRefPubMedGoogle Scholar
  42. Pintó, R. M., Costafreda, M. I., & Bosch, A. (2009). Risk assessment in shellfish-borne outbreaks of hepatitis A. Applied and Environment Microbiology, 75(23), 7350–7355.  https://doi.org/10.1128/aem.01177-09.CrossRefGoogle Scholar
  43. Purnell, S., Ebdon, J., Buck, A., Tupper, M., & Taylor, H. (2016). Removal of phages and viral pathogens in a full-scale MBR: Implications for wastewater reuse and potable water. Water Research, 100, 20–27.  https://doi.org/10.1016/j.watres.2016.05.013.CrossRefPubMedGoogle Scholar
  44. Qiu, Y., Lee, B. E., Neumann, N., Ashbolt, N., Craik, S., Maal-Bared, R., et al. (2015). Assessment of human virus removal during municipal wastewater treatment in Edmonton, Canada. Journal of Applied Microbiology, 119(6), 1729–1739.  https://doi.org/10.1111/jam.12971.CrossRefPubMedGoogle Scholar
  45. Samandoulgou, I., Fliss, I., & Jean, J. (2015). Zeta potential and aggregation of virus-like particle of human norovirus and feline calicivirus under different physicochemical conditions. Food and Environmental Virology, 7(3), 249–260.  https://doi.org/10.1007/s12560-015-9198-0.CrossRefPubMedGoogle Scholar
  46. Sano, D., Amarasiri, M., Hata, A., Watanabe, T., & Katayama, H. (2016). Risk management of viral infectious diseases in wastewater reclamation and reuse: Review. Environment International, 91, 220–229.  https://doi.org/10.1016/j.envint.2016.03.001.CrossRefPubMedGoogle Scholar
  47. Saxena, K., Blutt, S. E., Ettayebi, K., Zeng, X.-L., Broughman, J. R., Crawford, S. E., et al. (2016). Human intestinal enteroids: A new model to study human rotavirus infection, host restriction and pathophysiology. Journal of Virology, 90, 45–48.  https://doi.org/10.1128/JVI.01930-15.CrossRefGoogle Scholar
  48. Semenza, J. C., Lindgren, E., Balkanyi, L., Espinosa, L., Almqvist, M. S., Penttinen, P., et al. (2016). Determinants and drivers of infectious disease threat events in Europe. Emerging Infectious Diseases, 22(4), 581–589.  https://doi.org/10.3201/eid2204.151073.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Sima, L. C., Schaeffer, J., Le Saux, J. C., Parnaudeau, S., Elimelech, M., & Le Guyader, F. S. (2011). Calicivirus removal in a membrane bioreactor wastewater treatment plant. Applied and Environment Microbiology, 77(15), 5170–5177.  https://doi.org/10.1128/aem.00583-11.CrossRefGoogle Scholar
  50. Simmons, F. J., Kuo, D. H. W., & Xagoraraki, I. (2011). Removal of human enteric viruses by a full-scale membrane bioreactor during municipal wastewater processing. Water Research, 45(9), 2739–2750.  https://doi.org/10.1016/j.watres.2011.02.001.CrossRefPubMedGoogle Scholar
  51. Späth, R., Flemming, H.-C., & Wuertz, S. (1998). Sorption properties of biofilms. Water Science and Technology, 37(4–5), 207–210.Google Scholar
  52. Svraka, S., Duizer, E., Vennema, H., de Bruin, E., van der Veer, B., Dorresteijn, B., et al. (2007). Etiological role of viruses in outbreaks of acute gastroenteritis in the Netherlands from 1994 through 2005. Journal of Clinical Microbiology, 45(5), 1389–1394.  https://doi.org/10.1128/jcm.02305-06.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Thebault, A., Teunis, P. F. M., Le Pendu, J., Le Guyader, F. S., & Denis, J.-B. (2013). Infectivity of GI and GII noroviruses established from oyster related outbreaks. Epidemics, 5, 98–110.  https://doi.org/10.1016/j.epidem.2012.12.004.CrossRefPubMedGoogle Scholar
  54. U.S. EPA (2003). Environmental regulations and technology, control of pathogens and vector attraction in sewage sludge, EPA/625/R-92/013. Cincinnati: U.S. Environmental Protection Agency.Google Scholar
  55. Uyttendaele, M., Jaykus, L., Amoah, P., Chiodini, A., Cunliffe, D., Jacxsens, L., et al. (2015). Microbial hazards in irrigation water: Standards, norms, and testing to manage use of water in fresh produce primary production. Comprehensive Reviews in Food Science and Food Safety, 14(4), 336–356.  https://doi.org/10.1111/1541-4337.12133.CrossRefGoogle Scholar
  56. Wang, Q., Zhang, Z., & Saif, L. J. (2012). Stability of and attachment to lettuce by a culturable porcine sapovirus surrogate for human caliciviruses. Applied and Environment Microbiology, 78(11), 3932–3940.  https://doi.org/10.1128/aem.06600-11.CrossRefGoogle Scholar
  57. Wu, J., Li, H., & Huang, X. (2010). Indigenous somatic coliphage removal from a real municipal wastewater by a submerged membrane bioreactor. Water Research, 44(6), 1853–1862.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Laboratoire de Microbiologie, LSEM-SG2 M, IFREMERNantesFrance
  2. 2.SAUR, Direction générale OuestVannesFrance
  3. 3.Department of Environmental HealthNational Institute of Public HealthWakoJapan

Personalised recommendations