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

doi:10.1007/s11783-020-1242-0

Front. Environ. Sci. Eng.

2020, Vol. 14

Issue (4) : 63 https://doi.org/10.1007/s11783-020-1242-0

RESEARCH ARTICLE

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

Wei Fan, Qi Li, Mingxin Huo, Xiaoyu Wang, Shanshan Lin(

)

School of Environment, Northeast Normal University, Changchun 130117, China

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Abstract

• 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.

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.

Keywords Artificial groundwater recharge E. coli Transport Simulated column experiments Modeling

Corresponding Author(s): Shanshan Lin

Issue Date: 09 April 2020

Cite this article:

Wei Fan,Qi Li,Mingxin Huo, et al. Transport of bacterial cell (E. coli) from different recharge water resources in porous media during simulated artificial groundwater recharge[J]. Front. Environ. Sci. Eng., 2020, 14(4): 63.

URL:

https://academic.hep.com.cn/fese/EN/10.1007/s11783-020-1242-0
https://academic.hep.com.cn/fese/EN/Y2020/V14/I4/63

Fig.1 Water quality parameters of the three types of recharge water and their 3DEEM spectra.

Fig.2 The conceptual model and experimental design used in this study.

Tab.1 Operational conditions for all column experiments

Fig.3 Variation in OD₆₀₀ and hydraulic dynamic diameter during the cultivation of E. coli in different recharge water resources, zeta potential of cells and sand particles, and SEM images of the cells pre- (LB medium) and post-cultivation for 50 h, under starvation conditions.

Fig.4 EPS compositions, contact angles and OMP profiles for E. coli cells cultivated in different media (LB, SE, river water and rainfall).

Fig.5 Breakthrough curves (a) and retention profiles (b) for E. coli cells cultivated in different media (LB, SE, river water and rainfall), with distilled-deionized water used as the background electrolyte solution (Experiments No. 1–4).

Fig.6 Breakthrough curves (a) and retention profiles (b) for E. coli cells cultivated in different media (SE, river water and rainfall), with the equivalent medium subsequently used as the background electrolyte solution in columns (Experiments No. 5–7).

Fig.7 XDLVO energy profiles for interactions between sand particles and E. coli cells cultivated in different recharge water matrices.

1	A S H A Amimi, M A Khan, R Dghaim (2014). Bacteriological quality of reclaimed wastewater used for irrigation of public parks in the United Arab Emirates. International Journal of Environmental Science and Development, 5: 309–312
2	T Asanoa, J A Cotruvo (2004). Groundwater recharge with reclaimed municipal wastewater: Health and regulatory considerations. Water Research, 38: 1941–1951 https://doi.org/101016/jwatres200401023
3	S Banzhaf, K H Hebig (2016). Use of column experiments to investigate the fate of organic micropollutants: A review. Hydrology and Earth System Sciences, 20(9): 3719–3737 https://doi.org/10.5194/hess-20-3719-2016
4	H Bouwer (2002). Artificial recharge of groundwater: Hydrogeology and engineering. Hydrogeology Journal, 10: 121–142 https://doi.org/101007/s10040–001–0182–4
5	S A Bradford, B Headd, G Arye, J Šimůnek (2015). Transport of E. coli D21g with runoff water under different solution chemistry conditions and surface slopes. Journal of Hydrology, 525: 760–768 https://doi.org/101016/jjhydrol201504038
6	S A Bradford, J Simunek, M Bettahar, M T Van Genuchten, S R Yates (2003). Modeling colloid attachment, straining, and exclusion in saturated porous media. Environmental Science & Technology, 37: 2242–2250 https://doi.org/101021/es025899u
7	P Cai, Q Huang, S L Walker (2013). Deposition and survival of Escherichia coli O157:H7 on clay minerals in a parallel plate flow system. Environmental Science & Technology, 47: 1896–1903 https://doi.org/101021/es304686a
8	T Castellanos, F Ascencio, Y Bashan (2000). Starvation-induced changes in the cell surface of Azospirillum lipoferum. FEMS Microbiology Ecology, 33: 1–9 https://doi.org/101016/S0168–6496(00)00034–9
9	F Chen, X Yuan, Z Song, S Xu, Y Yang, X Yang (2018). Gram-negative Escherichia coli promotes deposition of polymer-capped silver nanoparticle in saturated porous media. Environmental Science: Nano, 5: 1495–1505 https://doi.org/101039/C8EN00067K
10	W Chen, P Westerhoff, J A Leenheer, K Booksh (2003). Fluorescence excitation-emission matrix regional integration to quantify spectra for dissolved organic matter. Environmental Science & Technology, 37: 5701–5710 https://doi.org/101021/es034354c
11	K Chourabi, F Torrella, S Kloula, J A Rodriguez, I Trabelsi, S Campoy, A Landoulsi, A Chatti (2017). Adaptation of Shigella flexneri to starvation: morphology, outer membrane proteins and lipopolysaccharide changes. Arabian Journal of Geosciences, 10: 274–280 https://doi.org/101007/s12517–017–3064–3
12	T Chu, Y S Yang, Y Lu, X Q Du, X Y Ye (2019). Clogging process by suspended solids during groundwater artificial recharge: Evidence from lab simulations and numerical modelling. Hydrological Processes, doi: 101002/hyp13553
13	P Dillon (2005). Future management of aquifer recharge. Hydrogeology Journal, 13: 313–316 https://doi.org/101007/s10040–004–0413–6
14	D Dwivedi, B P Mohanty, B J Lesikar (2013). Estimating Escherichia coli loads in streams based on various physical, chemical, and biological factors. Water Resources Research, 49: 2896–2906 https://doi.org/101002/wrcr20265
15	E Engström, R Thunvik, R Kulabako, B Balfors (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 https://doi.org/10.1080/10643389.2013.828363
16	W Fan, X H Jiang, W Yang, Z Geng, M X Huo, Z M Liu, H Zhou (2015). Transport of graphene oxide in saturated porous media: Effect of cation composition in mixed Na-Ca electrolyte systems. Science of the Total Environment, 511: 509–515 https://doi.org/101016/jscitotenv201412099
17	J W A Foppen, J F Schijven (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, 40: 401–26 https://doi.org/101016/jwatres200511018
18	E Goldberg, M Scheringer, T D Bucheli, K Hungerbühler (2014). Critical assessment of models for transport of engineered nanoparticles in saturated porous media. Environmental Science & Technology, 48: 12732–12741 https://doi.org/101021/es502044k
19	R Hao, H Ren, J Li, Z Ma, H Wan, X Zheng, S Cheng (2012). Use of three-dimensional excitation and emission matrix fluorescence spectroscopy for predicting the disinfection by-product formation potential of reclaimed water. Water Research, 46: 5765–5776 https://doi.org/101016/jwatres201208007
20	K Hori, S Matsumoto (2010). Bacterial adhesion: From mechanism to control. Biochemical Engineering Journal, 48: 424–434 https://doi.org/101016/jbej200911014
21	K Huang, N Nitin (2017). Enhanced removal of Escherichia coli O157:H7 and Listeria innocua from fresh lettuce leaves using surfactants during simulated washing. Food Control 79: 207–217 https://doi.org/101016/jfoodcont201703032
22	K Ishii, T Iwai, H Xia (2010). Hydrodynamic measurement of Brownian particles at a liquid-solid interface by low-coherence dynamic light scattering. Optics Express, 18: 7390–7396 https://doi.org/101364/OE18007390
23	N Jalšenjak (2006). Contribution of micelles to ionic strength of surfactant solution. Journal of Colloid and Interface Science, 293(1): 230–239 https://doi.org/10.1016/j.jcis.2005.06.030
24	W P Johnson, X Li, G Yal (2007). Colloid retention in porous media: Mechanistic confirmation of wedging and retention in zone of flow stagnation. Environmental Science & Technology, 41: 1279–1287 https://doi.org/101021/es061301x
25	H Kallali, M Yoshida, J Tarhouni, N Jedidi (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, 67: 764–772 https://doi.org/102166/wst2012630
26	A A Karimi, J A Redman, R F Ruiz (1998). Ground water replenishment with reclaimed water in the city of Los Angeles. Ground Water Monitoring and Remediation, 18: 150–158 https://doi.org/101111/j1745–65921998tb00626x
27	G Kumar, A Mudhoo, P Sivagurunath, D Nagaraj, A Ghimire, C H Lay, C Y Lin, D J Lee, , J S Chang (2016). Recent insights into the cell immobilization technology applied for dark fermentative hydrogen production. Bioresource Technology, 219: 725–737 https://doi.org/101016/jbiortech201608065
28	C Levantesi, R La Mantia, C Masciopinto, U Böckelmann, M N Ayuso-Gabella, M Salgot, V Tandoi, E Van Houtte, T Wintgens, E Grohmann (2010). Quantification of pathogenic microorganisms and microbial indicators in three wastewater reclamation and managed aquifer recharge facilities in Europe. Science of the Total Environment, 408: 4923–4930 https://doi.org/101016/jscitotenv201007042
29	Q Li, J Yang, W Fan, D Zhou, X Wang, L Zhang, M Huo, J C Crittenden (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, 162: 35–42 https://doi.org/101016/jcolsurfb201711018
30	D Lin, S D Story, S L Walker, Q Huang, W Liang, P Cai (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, 228: 35–42 https://doi.org/101016/jenvpol201705025
31	Y Liu, H H P Fang (2003). Influences of extracellular polymeric substances (EPS) on flocculation, settling, and dewatering of activated sludge. Critical Reviews in Environmental Science and Technology, 33: 237–273 https://doi.org/101080/10643380390814479
32	F Lopez-Galvez, M I Gil, F Pedrero-Salcedo, J J Alarcón, A Allende (2016). Monitoring generic Escherichia coli in reclaimed and surface water used in hydroponically cultivated greenhouse peppers and the influence of fertilizer solutions. Food Control, 67: 90–95 https://doi.org/101016/jfoodcont201602037
33	X Lu, Q Liu, D Wu, H M Al-Qadiri, N I Al-Alami, D H Kang, J H Shin, J Tang, J M F Jabal, E D Aston, B A Rasco (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, 28: 537–546 https://doi.org/101016/jfm201011002
34	L Ma, R F Spalding (1997). Effects of artificial recharge on ground water quality and aquifer storage recovery. Journal of the American Water Resources Association, 33: 561–572 https://doi.org/101111/j1752–16881997tb03532x
35	G Madumathi (2017). Transport of E. coli in presence of naturally occuring colloids in saturated porous media. Water Conservation Science and Engineering, 2: 153–164 https://doi.org/101007/s41101–017–0037-z
36	M Mauter, A Fait, M Elimelech, M Herzberg (2013). Surface cell density effects on Escherichia coli gene expression during cell attachment. Environmental Science & Technology, 47: 6223–6230 https://doi.org/101021/es3047069
37	P Ollivier, H Pauwels, G Wille, N Devau, G Braibant, L Cary, G Picot-Colbeaux, J Labille (2018). Natural attenuation of TiO2 nanoparticles in a fractured hard-rock. Journal of Hazardous Materials, 359: 47–55 https://doi.org/101016/jjhazmat201807035
38	Y A Pachepsky, D R Shelton (2011). Escherichia coli and fecal coliforms in freshwater and estuarine sediments. Critical Reviews in Environmental Science and Technology, 41: 1067–1110 https://doi.org/101080/10643380903392718
39	N Perujo, A M Romaní, X Sanchez-Vilaab (2019). A bilayer coarse-fine infiltration system minimizes bioclogging: The relevance of depth-dynamics. Science of the Total Environment, 669: 559–569 https://doi.org/101016/jscitotenv201903126
40	S L Sanin, D Sanin, J D Bryers (2003). Effect of starvation on the adhesive properties of xenobiotic degrading bacteria. Process Biochemistry, 38: 909–914 https://doi.org/101016/S0032–9592(02)00173–5
41	G P Sheng, H Q Yu, X Y Li (2010). Extracellular polymeric substances (EPS) of microbial aggregates in biological wastewater treatment systems: A review. Biotechnology Advances, 28: 882–894 https://doi.org/101016/jbiotechadv201008001
42	S Sherchan, S Miles, L Ikner, H Yu, S A Snyder, I L Pepper (2018). Near real-time detection of E. coli in reclaimed water. Sensors 18, 2303–2312 https://doi.org/103390/s18072303
43	M P Tong, G Y Long, X J Jiang, H Kim (2010). Contribution of extracellular polymeric substances on representative gram negative and gram positive bacterial deposition in porous media. Environmental Science & Technology, 44: 2393–2399 https://doi.org/101021/es9027937
44	J J Walczak, L Wang, S L Bardy, L Feriancikova, J Li, S Xu (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, 90: 129–136 https://doi.org/101016/jcolsurfb201110010
45	D Wang, S A Bradford, R W Harvey, B Gao, L Cang, D Zhou (2012). Humic acid facilitates the transport of ARS-labeled hydroxyapatite nanoparticles in iron oxyhydroxide-coated sand. Environmental Science & Technology, 46: 2738–2745 https://doi.org/101021/es203784u
46	Y Wang, M Huo, Q Li, W Fan, J Yang, X Cui (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, 18: 2980–2994 https://doi.org/101007/s11368–018–1967–6
47	Z J Wang (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)
48	S P Xu, B Gao, J E Saiers (2006). Straining of colloidal particles in saturated porous media. Water Resources Research, 42: W12S16 https://doi.org/101029/2006WR004948
49	C Yan, T Chen, J Shang (2019). Effect of bovine serum albumin on stability and transport of kaolinite colloid. Water Research, 155: 204–213 https://doi.org/101016/jwatres201902022
50	J Yang, J L Bitter, B A Smith, D H Fairbrother, W P Ball (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, 47: 14034–14043 https://doi.org/101021/es402448w
51	X Y Ye, R Cui, X Du, S Ma, J Zhao, Y Lu, Y Wan (2019). Mechanism of suspended kaolinite particle clogging in porous media during managed aquifer recharge. Groundwater, 57: 764–771 https://doi.org/101111/gwat12872
52	D D Zhou, X H Jiang, Y Lu, W Fan, M X Huo, J C Crittenden (2016). Cotransport of graphene oxide and Cu (II) through saturated porous media. Science of the Total Environment, 550: 717–726 https://doi.org/101016/jscitotenv201601141
53	L Zhu, M Torres, W Q Betancourt, M Sharma, S A Micallef, C Gerba, A R Sapkota, A Sapkota, S Parveen, F Hashem, E May, K Kniel, M Pop, S Ravishankar (2019). Incidence of fecal indicator and pathogenic bacteria in reclaimed and return flow waters in Arizona, USA. Environmental Research, 170: 122–127 https://doi.org/101016/jenvres201811048
54	Y G Zhu, Y Z Zhai, Q Q Du, Y G Teng, J S Wang, G Yang (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, 33: 945–961 https://doi.org/101002/hyp13376

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