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Transport of bacterial cell (E. coli) from different recharge water resources in porous media during simulated artificial groundwater recharge

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Abstract

Commonly used recharge water resources for artificial groundwater recharge (AGR) such as secondary effluent (SE), river water and rainfall, are all oligotrophic, with low ionic strengths and different cationic compositions. The dwelling process in recharge pond imposed physiologic stress on Escherichia coli (E. coli) cells, in all three types of investigated recharge water resources and the cultivation of E. coli under varying recharge water conditions, induced changes in cell properties. During adaptation to the recharge water environment, the zeta potential of cells became more negative, the hydrodynamic diameters, extracellular polymeric substances content and surface hydrophobicity decreased, while the cellular outer membrane protein profiles became more diverse. The mobility of cells altered in accordance with changes in these cell properties. The E. coli cells in rainfall recharge water displayed the highest mobility (least retention), followed by cells in river water and finally SE cells, which had the lowest mobility. Simulated column experiments and quantitative modeling confirmed that the cellular properties, driven by the physiologic state of cells in different recharge water matrices and the solution chemistry, exerted synergistic effects on cell transport behavior. The findings of this study contribute to an improved understanding of E. coli transport in actual AGR scenarios and prediction of spreading risk in different recharge water sources.

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References

  • Amimi A S H A, Khan M A, Dghaim R (2014). Bacteriological quality of reclaimed wastewater used for irrigation of public parks in the United Arab Emirates. International Journal of Environmental Science and Development, 1: 309–312

    Article  Google Scholar 

  • Asanoa T, Cotruvo J A (2004). Groundwater recharge with reclaimed municipal wastewater: Health and regulatory considerations. Water Research, 1: 1941–1951

    Article  CAS  Google Scholar 

  • Banzhaf S, Hebig K H (2016). Use of column experiments to investigate the fate of organic micropollutants: A review. Hydrology and Earth System Sciences, 20(9): 3719–3737

    Article  CAS  Google Scholar 

  • Bouwer H (2002). Artificial recharge of groundwater: Hydrogeology and engineering. Hydrogeology Journal, 1: 121–142

    Article  CAS  Google Scholar 

  • Bradford S A, Headd B, Arye G, Šimůnek J (2015). Transport of E. coli D21g with runoff water under different solution chemistry conditions and surface slopes. Journal of Hydrology, 1: 760–768

    Article  CAS  Google Scholar 

  • Bradford S A, Simunek J, Bettahar M, Van Genuchten M T, Yates S R (2003). Modeling colloid attachment, straining, and exclusion in saturated porous media. Environmental Science & Technology, 1: 2242–2250

    Article  CAS  Google Scholar 

  • Cai P, Huang Q, Walker S L (2013). Deposition and survival of Escherichia coli O157:H7 on clay minerals in a parallel plate flow system. Environmental Science & Technology, 1: 1896–1903

    Article  CAS  Google Scholar 

  • Castellanos T, Ascencio F, Bashan Y (2000). Starvation-induced changes in the cell surface of Azospirillum lipoferum. FEMS Microbiology Ecology, 1: 1–9

    Article  Google Scholar 

  • Chen F, Yuan X, Song Z, Xu S, Yang Y, Yang X (2018). Gram-negative Escherichia coli promotes deposition of polymer-capped silver nanoparticle in saturated porous media. Environmental Science: Nano, 1: 1495–1505

    Google Scholar 

  • Chen W, Westerhoff P, Leenheer J A, Booksh K (2003). Fluorescence excitation-emission matrix regional integration to quantify spectra for dissolved organic matter. Environmental Science & Technology, 1: 5701–5710

    Article  CAS  Google Scholar 

  • Chourabi K, Torrella F, Kloula S, Rodriguez J A, Trabelsi I, Campoy S, Landoulsi A, Chatti A (2017). Adaptation of Shigella flexneri to starvation: morphology, outer membrane proteins and lipopolysaccharide changes. Arabian Journal of Geosciences, 1: 274–280

    Article  Google Scholar 

  • Chu T, Yang Y S, Lu Y, Du X Q, Ye X Y (2019). Clogging process by suspended solids during groundwater artificial recharge: Evidence from lab simulations and numerical modelling. Hydrological Processes, doi: https://doi.org/101002/hyp13553

  • Dillon P (2005). Future management of aquifer recharge. Hydrogeology Journal, 1: 313–316

    Article  Google Scholar 

  • Dwivedi D, Mohanty B P, Lesikar B J (2013). Estimating Escherichia coli loads in streams based on various physical, chemical, and biological factors. Water Resources Research, 1: 2896–2906

    Article  Google Scholar 

  • Engström E, Thunvik R, Kulabako R, Balfors B (2014). Water transport, retention, and survival of Escherichia coli in unsaturated porous media: A comprehensive review of processes, models, and factors. Critical Reviews in Environmental Science and Technology, 45(1): 1–100

    Article  CAS  Google Scholar 

  • Fan W, Jiang X H, Yang W, Geng Z, Huo M X, Liu Z M, Zhou H (2015). Transport of graphene oxide in saturated porous media: Effect of cation composition in mixed Na-Ca electrolyte systems. Science of the Total Environment, 1: 509–515

    Article  CAS  Google Scholar 

  • Foppen J W A, Schijven J F (2006). Evaluation of data from the literature on the transport and survival of Escherichia coli and thermotolerant coliforms in aquifers under saturated conditions. Water Research, 1: 401–26

    Article  CAS  Google Scholar 

  • Goldberg E, Scheringer M, Bucheli T D, Hungerbühler K (2014). Critical assessment of models for transport of engineered nanoparticles in saturated porous media. Environmental Science & Technology, 1: 12732–12741

    Article  CAS  Google Scholar 

  • Hao R, Ren H, Li J, Ma Z, Wan H, Zheng X, Cheng S (2012). Use of three-dimensional excitation and emission matrix fluorescence spectroscopy for predicting the disinfection by-product formation potential of reclaimed water. Water Research, 1: 5765–5776

    Article  CAS  Google Scholar 

  • Hori K, Matsumoto S (2010). Bacterial adhesion: From mechanism to control. Biochemical Engineering Journal, 1: 424–434

    Article  CAS  Google Scholar 

  • Huang K, Nitin N (2017). Enhanced removal of Escherichia coli O157: H7 and Listeria innocua from fresh lettuce leaves using surfactants during simulated washing. Food Control 1: 207–217

    Article  CAS  Google Scholar 

  • Ishii K, Iwai T, Xia H (2010). Hydrodynamic measurement of Brownian particles at a liquid-solid interface by low-coherence dynamic light scattering. Optics Express, 1: 7390–7396

    Article  CAS  Google Scholar 

  • Jalšenjak N (2006). Contribution of micelles to ionic strength of surfactant solution. Journal of Colloid and Interface Science, 293(1): 230–239

    Article  CAS  Google Scholar 

  • Johnson W P, Li X, Yal G (2007). Colloid retention in porous media: Mechanistic confirmation of wedging and retention in zone of flow stagnation. Environmental Science & Technology, 1: 1279–1287

    Article  CAS  Google Scholar 

  • Kallali H, Yoshida M, Tarhouni J, Jedidi N (2013). Generalization and formalization of the US EPA procedure for design of treated wastewater aquifer recharge basins: II Retrofit of Souhil Wadi (Nabeul, Tunisia) pilot plant. Water Science & Technology, 1: 764–772

    Article  CAS  Google Scholar 

  • Karimi A A, Redman J A, Ruiz R F (1998). Ground water replenishment with reclaimed water in the city of Los Angeles. Ground Water Monitoring and Remediation, 1: 150–158

    Article  Google Scholar 

  • Kumar G, Mudhoo A, Sivagurunath P, Nagaraj D, Ghimire A, Lay C H, Lin C Y, Lee, D J, Chang J S (2016). Recent insights into the cell immobilization technology applied for dark fermentative hydrogen production. Bioresource Technology, 1: 725–737

    Article  CAS  Google Scholar 

  • Levantesi C, La Mantia R, Masciopinto C, Böckelmann U, Ayuso-Gabella M N, Salgot M, Tandoi V, Van Houtte E, Wintgens T, Grohmann E (2010). Quantification of pathogenic microorganisms and microbial indicators in three wastewater reclamation and managed aquifer recharge facilities in Europe. Science of the Total Environment, 1: 4923–4930

    Article  CAS  Google Scholar 

  • Li Q, Yang J, Fan W, Zhou D, Wang X, Zhang L, Huo M, Crittenden J C (2018). Different transport behaviors of Bacillus subtilis cells and spores in saturated porous media: Implications for contamination risks associated with bacterial sporulation in aquifer. Colloids and surfaces B: Biointerfaces, 1: 35–42

    Article  CAS  Google Scholar 

  • Lin D, Story S D, Walker S L, Huang Q, Liang W, Cai P (2017). Role of pH and ionic strength in the aggregation of TiO2 nanoparticles in the presence of extracellular polymeric substances from Bacillus subtilis. Environmental Pollution, 1: 35–42

    Article  CAS  Google Scholar 

  • Liu Y, Fang H H P (2003). Influences of extracellular polymeric substances (EPS) on flocculation, settling, and dewatering of activated sludge. Critical Reviews in Environmental Science and Technology, 1: 237–273

    Article  Google Scholar 

  • Lopez-Galvez F, Gil M I, Pedrero-Salcedo F, Alarcón J J, Allende A (2016). Monitoring generic Escherichia coli in reclaimed and surface water used in hydroponically cultivated greenhouse peppers and the influence of fertilizer solutions. Food Control, 1: 90–95

    Article  CAS  Google Scholar 

  • Lu X, Liu Q, Wu D, Al-Qadiri H M, Al-Alami N I, Kang D H, Shin J H, Tang J, Jabal J MF, Aston E D, Rasco B A (2011). Using of infrared spectroscopy to study the survival and injury of Escherichia coli O157:H7, Campylobacter jejuni and Pseudomonas aeruginosa under cold stress in low nutrient media. Food Microbiology, 1: 537–546

    Article  CAS  Google Scholar 

  • Ma L, Spalding R F (1997). Effects of artificial recharge on groundwater quality and aquifer storage recovery. Journal of the American Water Resources Association, 1: 561–572

    Article  Google Scholar 

  • Madumathi G (2017). Transport of E. coli in presence of naturally occuring colloids in saturated porous media. Water Conservation Science and Engineering, 1: 153–164

    Article  Google Scholar 

  • Mauter M, Fait A, Elimelech M, Herzberg M (2013). Surface cell density effects on Escherichia coli gene expression during cell attachment. Environmental Science & Technology, 1: 6223–6230

    Article  CAS  Google Scholar 

  • Ollivier P, Pauwels H, Wille G, Devau N, Braibant G, Cary L, Picot-Colbeaux G, Labille J (2018). Natural attenuation of TiO2 nanoparticles in a fractured hard-rock. Journal of Hazardous Materials, 1: 47–55

    Article  CAS  Google Scholar 

  • Pachepsky Y A, Shelton D R (2011). Escherichia coli and fecal coliforms in freshwater and estuarine sediments. Critical Reviews in Environmental Science and Technology, 1: 1067–1110

    Article  CAS  Google Scholar 

  • Perujo N, Romaní A M, Sanchez-Vilaab X (2019). A bilayer coarse-fine infiltration system minimizes bioclogging: The relevance of depth-dynamics. Science of the Total Environment, 1: 559–569

    Article  CAS  Google Scholar 

  • Sanin S L, Sanin D, Bryers J D (2003). Effect of starvation on the adhesive properties of xenobiotic degrading bacteria. Process Biochemistry, 1: 909–914

    Article  Google Scholar 

  • Sheng G P, Yu H Q, Li X Y (2010). Extracellular polymeric substances (EPS) of microbial aggregates in biological wastewater treatment systems: A review. Biotechnology Advances, 1: 882–894

    Article  CAS  Google Scholar 

  • Sherchan S, Miles S, Ikner L, Yu H, Snyder S A, Pepper I L (2018). Near real-time detection of E. coli in reclaimed water. Sensors 18, 2303–2312

    Article  CAS  Google Scholar 

  • Tong M P, Long G Y, Jiang X J, Kim H (2010). Contribution of extracellular polymeric substances on representative gram negative and gram positive bacterial deposition in porous media. Environmental Science & Technology, 1: 2393–2399

    Article  CAS  Google Scholar 

  • Walczak J J, Wang L, Bardy S L, Feriancikova L, Li J, Xu S (2012). The effects of starvation on the transport of Escherichia coli in saturated porous media are dependent on pH and ionic strength. Colloids and surfaces B: Biointerfaces, 1: 129–136

    Article  CAS  Google Scholar 

  • Wang D, Bradford S A, Harvey R W, Gao B, Cang L, Zhou D (2012). Humic acid facilitates the transport of ARS-labeled hydroxyapatite nanoparticles in iron oxyhydroxide-coated sand. Environmental Science & Technology, 1: 2738–2745

    Article  CAS  Google Scholar 

  • Wang Y, Huo M, Li Q, Fan W, Yang J, Cui X (2018). Comparison of clogging induced by organic and inorganic suspended particles in a porous medium: Implications for choosing physical clogging indicators. Journal of Soils and Sediments, 1: 2980–2994

    Article  CAS  Google Scholar 

  • Wang Z J (2012). Laboratory research on the law of suspended solids clogging during urban stormwater groundwater recharge. Dissertation for the Doctoral Degree. Changchun: Jilin University, 11–21 (in Chinese)

    Google Scholar 

  • Xu S P, Gao B, Saiers J E (2006). Straining of colloidal particles in saturated porous media. Water Resources Research, 42: W12S16

    Article  Google Scholar 

  • Yan C, Chen T, Shang J (2019). Effect of bovine serum albumin on stability and transport of kaolinite colloid. Water Research, 1: 204–213

    Article  CAS  Google Scholar 

  • Yang J, Bitter J L, Smith B A, Fairbrother D H, Ball W P (2013). Transport of oxidized multi-walled carbon nanotubes through silica based porous media: Influences of aquatic chemistry, surface chemistry, and natural organic matter. Environmental Science & Technology, 1: 14034–14043

    Article  CAS  Google Scholar 

  • Ye X Y, Cui R, Du X, Ma S, Zhao J, Lu Y, Wan Y (2019). Mechanism of suspended kaolinite particle clogging in porous media during managed aquifer recharge. Groundwater, 1: 764–771

    Article  CAS  Google Scholar 

  • Zhou D D, Jiang X H, Lu Y, Fan W, Huo M X, Crittenden J C (2016). Cotransport of graphene oxide and Cu (II) through saturated porous media. Science of the Total Environment, 1: 717–726

    Article  CAS  Google Scholar 

  • Zhu L, Torres M, Betancourt W Q, Sharma M, Micallef S A, Gerba C, Sapkota A R, Sapkota A, Parveen S, Hashem F, May E, Kniel K, Pop M, Ravishankar S (2019). Incidence of fecal indicator and pathogenic bacteria in reclaimed and return flow waters in Arizona, USA. Environmental Research, 1: 122–127

    Article  CAS  Google Scholar 

  • Zhu Y G, Zhai Y Z, Du Q Q, Teng Y G, Wang J S, Yang G (2019). The impact of well drawdowns on the mixing process of river water and groundwater and water quality in a riverside well field, Northeast China. Hydrological Processes, 1: 945–961

    Article  CAS  Google Scholar 

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Acknowledgements

This work was funded by the National Natural Science Foundation of China (Grant Nos. 51678121, 51978135, and 41772236). It was als o supported by “the Fundamental Research Funds for the Central Universities, China” (No. 2412019ZD004).

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Correspondence to Shanshan Lin.

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Highlights

• The recharge pond dwelling process induced changes in cell properties.

• Cell properties and solution chemistry exerted confounding effect on cell transport.

E. coli cells within different recharge water displayed different spreading risks.

Electronic Supplementary Material

11783_2020_1242_MOESM1_ESM.pdf

Transport of bacterial cell (E. coli) from different recharge water resources in porous media during simulated artificial groundwater recharge

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Fan, W., Li, Q., Huo, M. et al. Transport of bacterial cell (E. coli) from different recharge water resources in porous media during simulated artificial groundwater recharge. Front. Environ. Sci. Eng. 14, 63 (2020). https://doi.org/10.1007/s11783-020-1242-0

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  • DOI: https://doi.org/10.1007/s11783-020-1242-0

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