Virus, as nano-sized microorganisms are prevalent in aquifers, which threaten groundwater quality and human health wellbeing. Virus inactivation by attachment onto the limestone surfaces is a determining factor in the transport and retention behavior of virus in carbonaceous aquifers.
In the present study, the inactivation of MS2 -as a model virus- by attachment onto the surfaces of limestone grains was investigated in a series of batch experiments under different conditions such as limestone particle size distribution (0.25–0.50, 0.5–1 and 1–2 mm), treated wastewater and RO water, temperature (4 and 22 °C), initial MS2 concentrations (103–107 PFU/mL) and static and dynamic conditions. The experimental data of MS2 inactivation was also fitted to a non-linear kinetic model with shoulder and tailing. The characteristics of biofilm on the surfaces of limestone aquifer materials were assessed using scanning electron microscopy (SEM) and confocal laser scanning microscopy (CLSM).
The inactivation rate of virus decreased with increasing the adsorbent diameter. Furthermore, virus inactivation was greater at room temperature (22 °C) than 4 °C, in both static and dynamic conditions. The inactivation of virus via attachment onto the limestone aquifer materials in dynamic conditions was higher than under static conditions. In addition, fitting the experimental data with a kinetic model showed that virus inactivation was high at higher temperature, smaller limestone grains and dynamic conditions. Moreover, the experiments with treated wastewater showed that in authentic aqueous media, the virus inactivation was considerably higher than in RO water, due to the presence of either monovalent or divalent cations and surface roughness created by biofilms.
Finally, in terms of managed aquifer recharge systems, the presence of biofilm increases bacteria and virus retention onto the aquifer surfaces.
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Esfahani AR, Firouzi AF, Sayyad G, Kiasat A. Lead removal from aqueous solutions using polyacrylicacid-stabilized zero-Valent iron nanoparticles. Res J Environ Earth Sci. 2013;5(9):548–55.
Abuzerr S, Darwish M, Mahvi AH. Simultaneous removal of cationic methylene blue and anionic reactive red 198 dyes using magnetic activated carbon nanoparticles: equilibrium, and kinetics analysis. Water Sci Technol. 2018;2017(2):534–45.
Macler BA, Merkle JC. Current knowledge on groundwater microbial pathogens and their control. Hydrogeol J. 2000;8(1):29–40.
Hundesa A, de Motes CM, Bofill-Mas S, Albinana-Gimenez N, Girones R. Identification of human and animal adenoviruses and polyomaviruses for determination of sources of fecal contamination in the environment. Appl Environ Microbiol. 2006;72(12):7886–93.
Anders R, Chrysikopoulos C. Virus fate and transport during artificial recharge with recycled water. Water Resources Research. 2005;41(10).
Bradford SA, Tadassa YF, Jin Y. Transport of coliphage in the presence and absence of manure suspension. J Environ Qual. 2006;35(5):1692–701.
Maxwell RM, Welty C, Tompson AF. Streamline-based simulation of virus transport resulting from long term artificial recharge in a heterogeneous aquifer. Adv Water Resour. 2003;26(10):1075–96.
Lipson SM, Stotzky G. Adsorption of reovirus to clay minerals: effects of cation-exchange capacity, cation saturation, and surface area. Appl Environ Microbiol. 1983;46(3):673–82.
Lee S-H, Kim S-J. Detection of infectious enteroviruses and adenoviruses in tap water in urban areas in Korea. Water Res. 2002;36(1):248–56.
Chen KL, Elimelech M. Influence of humic acid on the aggregation kinetics of fullerene (C60) nanoparticles in monovalent and divalent electrolyte solutions. J Colloid Interface Sci. 2007;309(1):126–34.
Anders R, Chrysikopoulos CV. Evaluation of the factors controlling the time-dependent inactivation rate coefficients of bacteriophage MS2 and PRD1. Environ Sci Technol. 2006;40(10):3237–42.
Sasidharan S, Torkzaban S, Bradford SA, Kookana R, Page D, Cook PG. Transport and retention of bacteria and viruses in biochar-amended sand. Sci Total Environ. 2016;548:100–9.
Pham M, Mintz EA, Nguyen TH. Deposition kinetics of bacteriophage MS2 to natural organic matter: role of divalent cations. J Colloid Interface Sci. 2009;338(1):1–9.
Bhattacharjee S, Ryan JN, Elimelech M. Virus transport in physically and geochemically heterogeneous subsurface porous media. J Contam Hydrol. 2002;57(3–4):161–87.
Chrysikopoulos CV, Aravantinou AF. Virus attachment onto quartz sand: role of grain size and temperature. J Environ Chem Eng. 2014;2(2):796–801.
Zhang D, Zhou C-H, Lin C-X, Tong D-S, Yu W-H. Synthesis of clay minerals. Appl Clay Sci. 2010;50(1):1–11.
Zhou CH. An overview on strategies towards clay-based designer catalysts for green and sustainable catalysis. Appl Clay Sci. 2011;53(2):87–96.
Bellou MI, Syngouna VI, Tselepi MA, Kokkinos PA, Paparrodopoulos SC, Vantarakis A, et al. Interaction of human adenoviruses and coliphages with kaolinite and bentonite. Sci Total Environ. 2015;517:86–95.
Mondal PK, Sleep BE. Virus and virus-sized microsphere transport in a dolomite rock fracture. Water Resour Res. 2013;49(2):808–24.
Smirnova T, Didenko L, Azizbekyan R, Romanova YM. Structural and functional characteristics of bacterial biofilms. Microbiology. 2010;79(4):413–23.
Jian-Zhou H, Cheng-Cheng L, Deng-Jun W, Zhou D-M. Biofilms and extracellular polymeric substances mediate the transport of graphene oxide nanoparticles in saturated porous media. J Hazard Mater. 2015;300:467–74.
Thompson SS, Flury M, Yates MV, Jury WA. Role of the air-water-solid interface in bacteriophage sorption experiments. Appl Environ Microbiol. 1998;64(1):304–9.
Weng S, Dunkin N, Schwab KJ, McQuarrie J, Bell K, Jacangelo JG. Infectivity reduction efficacy of UV irradiation and peracetic acid-UV combined treatment on MS2 bacteriophage and murine norovirus in secondary wastewater effluent. J Environ Manag. 2018;221:1–9.
Hijikata N, Tezuka R, Kazama S, Otaki M, Ushijima K, Ito R, et al. Bactericidal and virucidal mechanisms in the alkaline disinfection of compost using calcium lime and ash. J Environ Manag. 2016;181:721–7.
Pang L, Farkas K, Bennett G, Varsani A, Easingwood R, Tilley R, et al. Mimicking filtration and transport of rotavirus and adenovirus in sand media using DNA-labeled, protein-coated silica nanoparticles. Water Res. 2014;62:167–79.
Chrysikopoulos CV, Syngouna VI. Attachment of bacteriophages MS2 and ΦX174 onto kaolinite and montmorillonite: extended-DLVO interactions. Colloids Surf B: Biointerfaces. 2012;92:74–83.
Schiffenbauer M, Stotzky G. Adsorption of coliphages T1 and T7 to clay minerals. Appl Environ Microbiol. 1982;43(3):590–6.
Tong M, Shen Y, Yang H, Kim H. Deposition kinetics of MS2 bacteriophages on clay mineral surfaces. Colloids Surf B: Biointerfaces. 2012;92:340–7.
Geeraerd A, Valdramidis V, Van Impe J. GInaFiT, a freeware tool to assess non-log-linear microbial survivor curves. Int J Food Microbiol. 2005;102(1):95–105.
Blake G, Hartge K. Particle Density 1. Methods of soil analysis: Part 1—Physical and mineralogical methods. 1986(methodsofsoilan1):377–82.
Noble RT, Lee IM, Schiff KC. Inactivation of indicator micro-organisms from various sources of faecal contamination in seawater and freshwater. J Appl Microbiol. 2004;96(3):464–72.
Debartolomeis J, Cabelli VJ. Evaluation of an Escherichia coli host strain for enumeration of F male-specific bacteriophages. Appl Environ Microbiol. 1991;57(5):1301–5.
Chrysikopoulos CV, Aravantinou AF. Virus inactivation in the presence of quartz sand under static and dynamic batch conditions at different temperatures. J Hazard Mater. 2012;233:148–57.
Sinton LW, Hall CH, Lynch PA, Davies-Colley RJ. Sunlight inactivation of fecal indicator bacteria and bacteriophages from waste stabilization pond effluent in fresh and saline waters. Appl Environ Microbiol. 2002;68(3):1122–31.
Hawley A, Fallowfield H. Pond walls: inclined planes to improve pathogen removal in pond systems for wastewater treatment? Water Sci Technol. 2018;78(1):31–6.
Federation WE, Association APH. Standard methods for the examination of water and wastewater. Washington, DC, USA: American Public Health Association (APHA); 2005.
Harvey RW, Ryan JN. Use of PRD1 bacteriophage in groundwater viral transport, inactivation, and attachment studies. FEMS Microbiol Ecol. 2004;49(1):3–16.
Mattle MJ, Crouzy B, Brennecke M. R. Wigginton K, Perona P, Kohn T. impact of virus aggregation on inactivation by peracetic acid and implications for other disinfectants. Environ Sci Technol. 2011;45(18):7710–7.
Ng TW, Li B, Chow A, Wong PK. Effects of bromide on inactivation efficacy and disinfection byproduct formation in photocatalytic inactivation. J Photochem Photobiol A Chem. 2016;324:145–51.
Babaei AA. Kinetic modeling of methylene blue adsorption onto acid-activated spent tea: a comparison between linear and non-linear regression analysis. J Adv Environ Health Res. 2014;2(4):129–208.
Islam MT, Hyder AG, Saenz-Arana R, Hernandez C, Guinto T, Ahsan MA, et al. Removal of methylene blue and tetracycline from water using peanut shell derived adsorbent prepared by sulfuric acid reflux. J Environ Chem Eng. 2019;7(1):102816.
Ali SN, El-Shafey E-SI, Al-Busafi S, Al-Lawati HA. Adsorption of chlorpheniramine and ibuprofen on surface functionalized activated carbons from deionized water and spiked hospital wastewater. Journal of Environmental Chemical Engineering. 2018:102860.
Dalvand A, Khoobi M, Nabizadeh R, Ganjali MR, Gholibegloo E, Mahvi AH. Reactive dye adsorption from aqueous solution on HPEI-modified Fe 3 O 4 nanoparticle as a Superadsorbent: characterization, modeling, and optimization. J Polym Environ. 2018;26(8):3470–83.
Vaidyanathan R, Tien C. Hydrosol deposition in granular beds. Chem Eng Sci. 1988;43(2):289–302.
Dika C, Ly-Chatain M, Francius G, Duval J, Gantzer C. Non-DLVO adhesion of F-specific RNA bacteriophages to abiotic surfaces: importance of surface roughness, hydrophobic and electrostatic interactions. Colloids Surf A Physicochem Eng Asp. 2013;435:178–87.
Tripathi S, Champagne D, Tufenkji N. Transport behavior of selected nanoparticles with different surface coatings in granular porous media coated with Pseudomonas aeruginosa biofilm. Environ Sci Technol. 2011;46(13):6942–9.
Hoek EM, Agarwal GK. Extended DLVO interactions between spherical particles and rough surfaces. J Colloid Interface Sci. 2006;298(1):50–8.
Joo SH, Aggarwal S. Factors impacting the interactions of engineered nanoparticles with bacterial cells and biofilms: mechanistic insights and state of knowledge. J Environ Manag. 2018;225:62–74.
Mayotte JM, Hölting L, Bishop K. Reduced removal of bacteriophage MS2 in during basin infiltration managed aquifer recharge as basin sand is exposed to infiltration water. Hydrol Process. 2017;31(9):1690–701.
Chu Y, Jin Y, Baumann T, Yates MV. Effect of soil properties on saturated and unsaturated virus transport through columns. J Environ Qual. 2003;32(6):2017–25.
Huysman F, Verstraete W. Effect of cell surface characteristics on the adhesion of bacteria to soil particles. Biol Fertil Soils. 1993;16(1):21–6.
Rahmatpour S, Shirvani M, Mosaddeghi MR, Bazarganipour M. Retention of silver nano-particles and silver ions in calcareous soils: influence of soil properties. J Environ Manag. 2017;193:136–45.
Stevenson ME, Sommer R, Lindner G, Farnleitner AH, Toze S, Kirschner AK, et al. Attachment and detachment behavior of human adenovirus and surrogates in fine granular limestone aquifer material. J Environ Qual. 2015;44(5):1392–401.
Rinck-Pfeiffer S, Ragusa S, Sztajnbok P, Vandevelde T. Interrelationships between biological, chemical, and physical processes as an analog to clogging in aquifer storage and recovery (ASR) wells. Water Res. 2000;34(7):2110–8. https://doi.org/10.1016/S0043-1354(99)00356-5.
Tong M, Ding J, Shen Y, Zhu P. Influence of biofilm on the transport of fullerene (C60) nanoparticles in porous media. Water Res. 2010;44(4):1094–103.
Bozorg A, Gates ID, Sen A. Impact of biofilm on bacterial transport and deposition in porous media. J Contam Hydrol. 2015;183:109–20.
Amirhosein Ramazanpour Esfahani was in receipt of an Australian Government Research and Training Program (RTP) at Flinders University. We like to thank Mr. Raj Indela (Flinders University) for laboratory support, Mr. Michael Ferraro Olympic Drilling, South Australia for provision of authentic aquifer substrates, Dr. Allan Pring (Flinders University) for providing guidance in the spectroscopic analyses. Dr. Jason Gascooke (Flinders University) for providing assistance in preparation of SEM images. Furthermore, the authors acknowledge Flinders Microscopy and Microanalysis and the expertise and supports provided by Dr. Jennifer Fendler for the imaging measurements on the Leica TCS SP5 Laser Scanning Confocal Microscope.
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Ramazanpour Esfahani, A., Batelaan, O., Hutson, J.L. et al. Role of biofilm on virus inactivation in limestone aquifers: implications for managed aquifer recharge. J Environ Health Sci Engineer (2020). https://doi.org/10.1007/s40201-019-00431-5
- Virus inactivation
- Batch experiment