Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Transport of Escherichia coli phage through saturated porous media considering managed aquifer recharge

Abstract

Virus is one of the most potentially harmful microorganisms in groundwater. In this paper, the effects of hydrodynamic and hydrogeochemical conditions on the transportation of the colloidal virus considering managed aquifer recharge were systematically investigated. Escherichia coli phage, vB_EcoM-ep3, has a broad host range and was able to lyse pathogenic Escherichia coli. Bacteriophage with low risk to infect human has been found extensively in the groundwater environment, so it is considered as a representative model of groundwater viruses. Laboratory studies were carried out to analyze the transport of the Escherichia coli phage under varying conditions of pH, ionic strength, cation valence, flow rate, porous media, and phosphate buffer concentration. The results indicated that decreasing the pH will increase the adsorption of Escherichia coli phage. Increasing the ionic strength, either Na+ or Ca2+, will form negative condition for the migration of Escherichia coli phage. A comparison of different cation valence tests indicated that changes in transport and deposition were more pronounced with divalent Ca2+ than monovalent Na+. As the flow rate increases, the release of Escherichia coli phage increases and the retention of Escherichia coli phage in the aquifer medium reduces. Changes in porous media had a significant effect on Escherichia coli phage migration. With increase of phosphate buffer concentration, the suspension stability and migration ability of Escherichia coli phage are both increased. Based on laboratory-scale column experiments, a one-dimensional transport model was established to quantitatively describe the virus transport in saturated porous medium.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Abbreviations

A123:

Complex Hamaker constant for colloidal virus-water-glass beads, 7.50E-21 (kg m2/s2).

A s :

Porosity-dependent flow parameter

C :

Concentration of biocolloids in suspension, M/L3.

d c :

Average collector diameter, 0.45 mm.

d p :

Virus particle diameter, 160 nm.

D :

Hydrodynamic dispersion coefficient, L2/t.

i :

Subscript indicates colloidal virus

k B :

Boltzman’s constant, 1.38E-23(kg m2)/(s2 K).

L :

Length of the packed column, 10 cm.

M r(i) :

The mass recovery of colloidal virus.

M r(t) :

The mass recovery of tracer.

N A :

Attraction number

N G :

Gravity number

N Pe :

Peclet number

N R :

Relative size number

N vdw :

Van der Waals number

q :

Specific discharge or approach velocity

RB:

the ratio of M r(i) to M r(t)

t :

Time, t.

T :

Temperature, 283 K.

U :

Interstitial (pore water flow) velocity, L/t.

ε θ :

Equal to (1 − θ)1/3

η 0 :

Single-collector removal efficiency for favorable deposition, (−).

θ :

Porosity of porous medium volume, L3/L3.

μ w :

Water viscosity, 8.91E-04 kg/(m·s).

ρ p :

Particle density,1690 kg/m3

ρ f :

Fluid density,999.7 kg/m3

g :

Acceleration due to gravity 9.81 m/s2

References

  1. Abuashour J, Joy DM, Lee H, Whiteley HR, Zelin S (1994) Transport of microorganisms through soil. Water Air Soil Pollut 75(1):141–158. https://doi.org/10.1007/BF01100406

  2. Anders R, Chrysikopoulos CV (2005) Virus fate and transport during artificial recharge with recycled water. Water Resour Res 41(10):3251–3261

  3. Anders R, Chrysikopoulos CV (2006) Evaluation of the factors controlling the time-dependent inactivation rate coefficients of bacteriophage MS2 and PRD1. Environ Sci Technol 40(10):3237–3242. https://doi.org/10.1021/es051604b

  4. Anders R, Chrysikopoulos CV (2009) Transport of viruses through saturated and unsaturated columns packed with sand. Transp Porous Media 76(1):121–138. https://doi.org/10.1007/s11242-008-9239-3

  5. Bhattacharjee S, Ryan JN, Elimelech M (2002) Virus transport in physically and geochemically heterogeneous subsurface porous media. J Contam Hydrol 57(3–4):161–187. https://doi.org/10.1016/S0169-7722(02)00007-4

  6. Cao H, Tsai FT, Rusch KA (2010) Salinity and soluble organic matter on virus sorption in sand and soil columns. Ground Water 48(1):42–52. https://doi.org/10.1111/j.1745-6584.2009.00645.x

  7. Chrysikopoulos CV, Masciopinto C, La Mantia R, Manariotis ID (2010) Removal of biocolloids suspended in reclaimed wastewater by injection in a fractured aquifer model. Environ Sci Technol 44(3):971–977. https://doi.org/10.1021/es902754n

  8. Chu YJ, Yan J, Yates MV (2000) Virus transport through saturated sand columns as affected by different buffer solutions. J Environ Qual 29(4):1103–1110. https://doi.org/10.2134/jeq2000.00472425002900040010x

  9. Elimelech M, Nagai M, Chunhan K, Ryan JN (2000) Relative insignificance of mineral grain zeta potential to colloid transport in geochemically heterogeneous porous media. Environ Sci Technol 34(11):2143–2148. https://doi.org/10.1021/es9910309

  10. Foppen J, Okletey S, Schijven JF (2006) Effect of goethite coating and humic acid on the transport of bacteriophage PRD1 in columns of saturated sand. J Contam Hydrol 85(3–4):287–301. https://doi.org/10.1016/j.jconhyd.2006.02.004

  11. Gerba CP, Schaiberger GE (1975) Effect of particulates on virus survival in seawater. Journal - Water Pollution Control Federation 47(1):93–103

  12. Gerba CP (1984) Applied and theoretical aspects of virus adsorption to surfaces. Adv Appl Microbiol 30(4):133–168. https://doi.org/10.1016/S0065-2164(08)70054-6

  13. James SC, Chrysikopoulos CV (2011) Monodisperse and polydisperse colloid transport in water-saturated fractures with various orientations: gravity effects. Adv Water Resour 34(10):1249–1255. https://doi.org/10.1016/j.advwatres.2011.06.001

  14. Jin Y, Yates MV, Thompson SS, Jury WA (1997) Sorption of viruses during flow through saturated sand columns. Environ Sci Technol 31(2):548–555. https://doi.org/10.1021/es9604323

  15. Jin Y, Flury M (2002) Fate and transport of viruses in porous media. Adv Agron 77(02):39–102. https://doi.org/10.1016/S0065-2113(02)77013-2

  16. Katzourakis VE, Chrysikopoulos CV (2014) Mathematical modeling of colloid and virus cotransport in porous media: application to experimental data. Adv Water Resour 68(2):62–73. https://doi.org/10.1016/j.advwatres.2014.03.001

  17. MaKokkinos P, Syngouna VI, Tselepi MA, Bellou M, Chrysikopoulos CV, Vantarakis A (2015) Transport of human adenoviruses in water saturated laboratory columns. Food and Environ Virology 7(2):122–131. https://doi.org/10.1007/s12560-014-9179-8

  18. Liu D, Zhou J, Zhang W, Ying H, Yu X, Li F (2017) Column experiments to investigate transport of colloidal humic acid through porous media during managed aquifer recharge. Hydrogeol J 25:1–11

  19. Lv M, Wang S, Yan G, Sun C, Feng X, Gu J (2015) Genome sequencing and analysis of an escherichia coli phage vb_ecom-ep3 with a novel lysin, lysep3. Virus Genes 50(3):487–497. https://doi.org/10.1007/s11262-015-1195-8

  20. Masciopinto C, Mantia RL, Chrysikopoulos CV (2008) Fate and transport of pathogens in a fractured aquifer in the Salento area, Italy. Water Resour Res 44(1):186–192

  21. Penrod SL, And TMO, Grant SB (1996) Deposition kinetics of two viruses in packed beds of quartz granular media. Langmuir 12(12):5576–5587. https://doi.org/10.1021/la950884d

  22. Redman JA, Grant SB, Olson TM, Adkins JM, Jackson JL, Castillo MS (1999) Physicochemical mechanisms responsible for the filtration and mobilization of a filamentous bacteriophage in quartz sand. Water Res 33(1):43–52. https://doi.org/10.1016/S0043-1354(98)00194-8

  23. Ryan JN, Elimelech M (1996) Colloid mobilization and transport in groundwater. Colloids Surf A Physicochem Eng Aspects 107(95):1–56. https://doi.org/10.1016/0927-7757(95)03384-X

  24. Sadeghi G, Schijven JF, Behrends T, Hassanizadeh SM, Gerritse J, Kleingeld PJ (2011) Systematic study of effects of pH and ionic strength on attachment of phage PRD1. Groundwater 49(1):12–19. https://doi.org/10.1111/j.1745-6584.2010.00767.x

  25. Sadeghi G, Schijven JF, Behrends T, Hassanizadeh SM, Genuchten MTV (2013a) Bacteriophage prd1 batch experiments to study attachment, detachment and inactivation processes. J Contam Hydrol 152(8):12–17. https://doi.org/10.1016/j.jconhyd.2013.06.002

  26. Sadeghi G, Behrends T, Schijven JF, Hassanizadeh SM (2013b) Effect of dissolved calcium on the removal of bacteriophage prd1 during soil passage: the role of double-layer interactions. J Contam Hydrol 144(1):78–87. https://doi.org/10.1016/j.jconhyd.2012.10.006

  27. Syngouna VI, Chrysikopoulos CV (2010) Interaction between viruses and clays in static and dynamic batch systems. Environ Sci Technol 44(12):4539–4544. https://doi.org/10.1021/es100107a

  28. Syngouna VI, Chrysikopoulos CV (2011) Transport of biocolloids in water saturated columns packed with sand: effect of grain size and pore water velocity. J Contam Hydrol, 126(3–4):301–314, 314, https://doi.org/10.1016/j.jconhyd.2011.09.007

  29. Syngouna VI, Chrysikopoulos CV (2013) Cotransport of clay colloids and viruses in water saturated porous media. Colloids Surf A Physicochem Eng Asp 416(1):56–65. https://doi.org/10.1016/j.colsurfa.2012.10.018

  30. Torkzaban S, Bradford SA, Genuchten MTV, Walker SL (2008) Colloid transport in unsaturated porous media: the role of water content and ionic strength on particle straining. J Contam Hydrol 96(1–4):13–127

  31. Tufenkji N, Elimelech M (2004) Correlation equation for predicting single collector efficiency in physicochemical filtration in saturated porous media. Environ Sci Technol 38(2):529–536. https://doi.org/10.1021/es034049r

  32. Tufenkji N, Elimelech M (2005) Breakdown of colloid filtration theory: role of the secondary energy minimum and surface charge heterogeneities. Langmuir Acs J Surf Colloids 21(23):841–852. https://doi.org/10.1021/la048102g

  33. Tufenkji N (2007) Modeling microbial transport in porous media: traditional approaches and recent developments. Adv Water Resour 30(6–7):1455–1469. https://doi.org/10.1016/j.advwatres.2006.05.014

  34. Vanderzalm JL, Page DW, Barry KE, Dillon PJ (2010) A comparison of the geochemical response to different managed aquifer recharge operations for injection of urban stormwater in a carbonate aquifer. Appl Geochem 25(9):1350–1360. https://doi.org/10.1016/j.apgeochem.2010.06.005

  35. Wang Z, Zhang W, Li S, Zhou J, Liu D (2016) Transport of silica colloid through saturated porous media under different hydrogeochemical and hydrodynamic conditions considering managed aquifer recharge. Water 8(12):555. https://doi.org/10.3390/w8120555

  36. Walshe GE, Pang L, Flury M, Close ME, Flintoft M (2010) Effects of pH, ionic strength, dissolved organic matter, and flow rate on the co-transport of MS2 bacteriophages with kaolinite in gravel aquifer media. Water Res 44(4):1255–1269. https://doi.org/10.1016/j.watres.2009.11.034

  37. Wong K, Bouchard D, Molina M (2014) Relative transport of human adenovirus and MS2 in porous media. Colloids Surf B Biointerfaces 122:78–784

  38. Yan J, Pratt E, Yates MV (2000) Effect of mineral colloids on virus transport through saturated sand columns. J Environ Qual 29(2):532–539

  39. Zhang W, Ying H, Yu X, Dan L, Zhou J (2015) Multi-component transport and transformation in deep confined aquifer during groundwater artificial recharge. J Environ Manag 152:109–119. https://doi.org/10.1016/j.jenvman.2015.01.027

  40. Zhuang J, Jin Y (2003a) Virus retention and transport as influenced by different forms of soil organic matter. J Environ Qual 32(3):816–823. https://doi.org/10.2134/jeq2003.8160

  41. Zhuang J, Jin Y (2003b) Virus retention and transport through al-oxide coated sand columns: effects of ionic strength and composition. J Contam Hydrol 60(3–4):193–209. https://doi.org/10.1016/S0169-7722(02)00087-6

  42. Zhuang J, Jin Y (2008) Interactions between viruses and goethite during saturated flow: effects of solution pH, carbonate, and phosphate. J Contam Hydrol 98(1–2):15–21. https://doi.org/10.1016/j.jconhyd.2008.02.002

Download references

Acknowledgements

The data used in the study will be provided to the corresponding author. The authors gratefully acknowledge the financial supports by the National Natural Science Foundation of China (41472215). We would like to thank the support provided by the “985 Project” of Jilin University as well as the journal editors for valuable comments that have improved the paper considerably. The authors thank the support from College of Veterinary Medicine for great help with culture of virus and other work.

Author information

Correspondence to Wenjing Zhang.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhang, W., Li, S., Wang, S. et al. Transport of Escherichia coli phage through saturated porous media considering managed aquifer recharge. Environ Sci Pollut Res 25, 6497–6513 (2018). https://doi.org/10.1007/s11356-017-0876-3

Download citation

Keywords

  • Groundwater
  • Colloidal virus
  • Escherichia coli phage
  • Column experiment
  • Transport modal
  • Managed aquifer recharge (MAR)