Bacteria attenuation by iron electrocoagulation governed by interactions between bacterial phosphate groups and Fe(III) precipitates

Delaire, Caroline; van Genuchten, Case M.; Amrose, Susan E.; Gadgil, Ashok J.

doi:10.1016/j.watres.2016.07.020

Bacteria attenuation by iron electrocoagulation governed by interactions between bacterial phosphate groups and Fe(III) precipitates

Journal Article · Mon Jul 11 00:00:00 EDT 2016 · Water Research

DOI:https://doi.org/10.1016/j.watres.2016.07.020· OSTI ID:1828154

Delaire, Caroline ^[1]; van Genuchten, Case M. ^[2]; Amrose, Susan E. ^[1]; Gadgil, Ashok J. ^[3]

Univ. of California, Berkeley, CA (United States)
Univ. of Utrecht (Netherlands)
Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Iron electrocoagulation (Fe-EC) is a low-cost process in which Fe(II) generated from an Fe(0) anode reacts with dissolved O₂ to form (1) Fe(III) precipitates with an affinity for bacterial cell walls and (2) bactericidal reactive oxidants. Previous work suggests that Fe-EC is a promising treatment option for groundwater containing arsenic and bacterial contamination. However, the mechanisms of bacteria attenuation and the impact of major groundwater ions are not well understood. In this work, using the model indicator Escherichia coli (E. coli), we show that physical removal via enmeshment in EC precipitate flocs is the primary process of bacteria attenuation in the presence of HCO₃^-, which significantly inhibits inactivation, possibly due to a reduction in the lifetime of reactive oxidants. Here, we demonstrate that the adhesion of EC precipitates to cell walls, which results in bacteria encapsulation in flocs, is driven primarily by interactions between EC precipitates and phosphate functional groups on bacteria surfaces. In single solute electrolytes, both P (0.4 mM) and Ca/Mg (1-13 mM) inhibited the adhesion of EC precipitates to bacterial cell walls, whereas Si (0.4 mM) and ionic strength (2-200 mM) did not impact E. coli attenuation. Interestingly, P (0.4 mM) did not affect E. coli attenuation in electrolytes containing Ca/Mg, consistent with bivalent cation bridging between bacterial phosphate groups and inorganic P sorbed to EC precipitates. Finally, we found that EC precipitate adhesion is largely independent of cell wall composition, consistent with comparable densities of phosphate functional groups on Gram-positive and Gram-negative cells. Our results are critical to predict the performance of Fe-EC to eliminate bacterial contaminants from waters with diverse chemical compositions.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES); United States Agency for International Development (USAID)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1828154

Alternate ID(s):: OSTI ID: 1397363

Journal Information:: Water Research, Journal Name: Water Research Vol. 103; ISSN 0043-1354

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (51)

Reactions of the ferryl ion with some compounds found in cloud water Jacobsen, Frank; Holcman, Jerzy; Sehested, Knud International Journal of Chemical Kinetics, Vol. 30, Issue 3 https://doi.org/10.1002/(SICI)1097-4601(1998)30:3<215::AID-KIN7>3.0.CO;2-V	journal	January 1998
Adsorption of phenol and substituted phenols by iron oxides McBride, M. B.; Kung, King-Hsi Environmental Toxicology and Chemistry, Vol. 10, Issue 4 https://doi.org/10.1002/etc.5620100403	journal	April 1991
Effects of pH on Bacterial Inactivation in Aqueous Solutions due to Low-Temperature Atmospheric Pressure Plasma Application: Effects of pH on Bacterial Inactivation in Aqueous Solutions … Ikawa, Satoshi; Kitano, Katsuhisa; Hamaguchi, Satoshi Plasma Processes and Polymers, Vol. 7, Issue 1 https://doi.org/10.1002/ppap.200900090	journal	December 2009
Analysis of Bacterial Deposition on Metal (Hydr)oxide-Coated Sand Filter Media Truesdail, S. E.; Lukasik, J.; Farrah, S. R. Journal of Colloid and Interface Science, Vol. 203, Issue 2 https://doi.org/10.1006/jcis.1998.5541	journal	July 1998
ATR–FTIR Spectroscopic Investigation on Phosphate Adsorption Mechanisms at the Ferrihydrite–Water Interface Arai, Yuji; Sparks, D. L. Journal of Colloid and Interface Science, Vol. 241, Issue 2 https://doi.org/10.1006/jcis.2001.7773	journal	September 2001
Hydrogen peroxide for prevention of bacterial growth on polymer biomaterials Alt, Eckhard; Leipold, Francesca; Milatovic, Danica The Annals of Thoracic Surgery, Vol. 68, Issue 6 https://doi.org/10.1016/S0003-4975(99)00832-2	journal	December 1999
Adsorption of fulvic acid on goethite Filius, Jeroen D.; Lumsdon, David G.; Meeussen, Johannes C. L. Geochimica et Cosmochimica Acta, Vol. 64, Issue 1 https://doi.org/10.1016/S0016-7037(99)00176-3	journal	January 2000
Spectroscopic characterization of the structural and functional properties of natural organic matter fractions Chen, Jie; Gu, Baohua; LeBoeuf, Eugene J. Chemosphere, Vol. 48, Issue 1 https://doi.org/10.1016/S0045-6535(02)00041-3	journal	July 2002
Comparison of the acid-base behaviour and metal adsorption characteristics of a gram-negative bacterium with other strains Ngwenya, Bryne T.; Sutherland, Ian W.; Kennedy, Lynn Applied Geochemistry, Vol. 18, Issue 4 https://doi.org/10.1016/S0883-2927(02)00118-X	journal	April 2003
A combined electrochemical-irradiation treatment of highly colored and polluted industrial wastewater Barrera-Dı́az, C.; Ureña-Nuñez, F.; Campos, E. Radiation Physics and Chemistry, Vol. 67, Issue 5 https://doi.org/10.1016/S0969-806X(02)00497-8	journal	July 2003
Proton and metal adsorption onto bacterial consortia: Stability constants for metal–bacterial surface complexes Johnson, Kelly J.; Szymanowski, Jennifer E. S.; Borrok, David Chemical Geology, Vol. 239, Issue 1-2 https://doi.org/10.1016/j.chemgeo.2006.12.002	journal	April 2007
The future for electrocoagulation as a localised water treatment technology Holt, Peter K.; Barton, Geoffrey W.; Mitchell, Cynthia A. Chemosphere, Vol. 59, Issue 3 https://doi.org/10.1016/j.chemosphere.2004.10.023	journal	April 2005
ATR–FTIR spectroscopic evidence for biomolecular phosphorus and carboxyl groups facilitating bacterial adhesion to iron oxides Parikh, Sanjai J.; Mukome, Fungai N. D.; Zhang, Xiaoming Colloids and Surfaces B: Biointerfaces, Vol. 119 https://doi.org/10.1016/j.colsurfb.2014.04.022	journal	July 2014
Application of electrocoagulation in Escherichia coli culture and two surface waters Ghernaout, D.; Badis, A.; Kellil, A. Desalination, Vol. 219, Issue 1-3 https://doi.org/10.1016/j.desal.2007.05.010	journal	January 2008
Iron oxyhydroxide mineralization on microbial extracellular polysaccharides Chan, Clara S.; Fakra, Sirine C.; Edwards, David C. Geochimica et Cosmochimica Acta, Vol. 73, Issue 13 https://doi.org/10.1016/j.gca.2009.02.036	journal	July 2009
Effect of phosphate, silicate, and Ca on Fe(III)-precipitates formed in aerated Fe(II)- and As(III)-containing water studied by X-ray absorption spectroscopy Voegelin, Andreas; Kaegi, Ralf; Frommer, Jakob Geochimica et Cosmochimica Acta, Vol. 74, Issue 1 https://doi.org/10.1016/j.gca.2009.09.020	journal	January 2010
Arsenic(III, V) adsorption on a goethite-based adsorbent in the presence of major co-existing ions: Modeling competitive adsorption consistent with spectroscopic and molecular evidence Kanematsu, Masakazu; Young, Thomas M.; Fukushi, Keisuke Geochimica et Cosmochimica Acta, Vol. 106 https://doi.org/10.1016/j.gca.2012.09.055	journal	April 2013
Structure of Fe(III) precipitates generated by the electrolytic dissolution of Fe(0) in the presence of groundwater ions van Genuchten, Case M.; Peña, Jasquelin; Amrose, Susan E. Geochimica et Cosmochimica Acta, Vol. 127 https://doi.org/10.1016/j.gca.2013.11.044	journal	February 2014
Composition and structure of Fe(III)-precipitates formed by Fe(II) oxidation in water at near-neutral pH: Interdependent effects of phosphate, silicate and Ca Senn, Anna-Caterina; Kaegi, Ralf; Hug, Stephan J. Geochimica et Cosmochimica Acta, Vol. 162 https://doi.org/10.1016/j.gca.2015.04.032	journal	August 2015
Adsorption of alpha amino acids at the water/goethite interface Norén, Katarina; Loring, John S.; Persson, Per Journal of Colloid and Interface Science, Vol. 319, Issue 2 https://doi.org/10.1016/j.jcis.2007.11.046	journal	March 2008
Multi-competitive interaction of As(III) and As(V) oxyanions with Ca2+, Mg2+, PO3−4, and CO2−3 ions on goethite Stachowicz, Monika; Hiemstra, Tjisse; van Riemsdijk, Willem H. Journal of Colloid and Interface Science, Vol. 320, Issue 2 https://doi.org/10.1016/j.jcis.2008.01.007	journal	April 2008
Electro-chemical arsenic remediation: Field trials in West Bengal Amrose, Susan E.; Bandaru, Siva R. S.; Delaire, Caroline Science of The Total Environment, Vol. 488-489 https://doi.org/10.1016/j.scitotenv.2013.11.074	journal	August 2014
Arsenic removal in synthetic ground water using iron electrolysis Li, Lei; Li, Jun; Shao, Chen Separation and Purification Technology, Vol. 122 https://doi.org/10.1016/j.seppur.2013.11.012	journal	February 2014
Mechanisms of virus control during iron electrocoagulation – Microfiltration of surface water Tanneru, Charan Tej; Chellam, Shankararaman Water Research, Vol. 46, Issue 7 https://doi.org/10.1016/j.watres.2012.01.032	journal	May 2012
Virulence and Immunogenic Activities of B. Typhosus in Relation to its Antigenic Constituents Felix, A.; Pitt, R. M. Journal of Hygiene, Vol. 35, Issue 3 https://doi.org/10.1017/S0022172400032459	journal	August 1935
Escherichia coli Attenuation by Fe Electrocoagulation in Synthetic Bengal Groundwater: Effect of pH and Natural Organic Matter Delaire, Caroline; van Genuchten, Case M.; Nelson, Kara L. Environmental Science & Technology, Vol. 49, Issue 16 https://doi.org/10.1021/acs.est.5b01696	journal	July 2015
Lipopolysaccharide Density and Structure Govern the Extent and Distance of Nanoparticle Interaction with Actual and Model Bacterial Outer Membranes Jacobson, Kurt H.; Gunsolus, Ian L.; Kuech, Thomas R. Environmental Science & Technology, Vol. 49, Issue 17 https://doi.org/10.1021/acs.est.5b01841	journal	August 2015
Chemical Force Spectroscopy Evidence Supporting the Layer-by-Layer Model of Organic Matter Binding to Iron (oxy)Hydroxide Mineral Surfaces Chassé, Alexander W.; Ohno, Tsutomu; Higgins, Steven R. Environmental Science & Technology, Vol. 49, Issue 16 https://doi.org/10.1021/acs.est.5b01877	journal	August 2015
Adhesion of Shewanella oneidensis MR-1 to Goethite: A Two-Dimensional Correlation Spectroscopic Study Yan, Wei; Wang, Hongbo; Jing, Chuanyong Environmental Science & Technology, Vol. 50, Issue 8 https://doi.org/10.1021/acs.est.6b00066	journal	April 2016
Influence of Phosphate on Bacterial Adhesion onto Iron Oxyhydroxide in Drinking Water Appenzeller, Brice M. R.; Duval, Yann B.; Thomas, Fabien Environmental Science & Technology, Vol. 36, Issue 4 https://doi.org/10.1021/es010155m	journal	February 2002
Iron-Catalyzed Oxidation of Arsenic(III) by Oxygen and by Hydrogen Peroxide: pH-Dependent Formation of Oxidants in the Fenton Reaction Hug, Stephan J.; Leupin, Olivier Environmental Science & Technology, Vol. 37, Issue 12 https://doi.org/10.1021/es026208x	journal	June 2003
Arsenic Removal with Iron(II) and Iron(III) in Waters with High Silicate and Phosphate Concentrations Roberts, Linda C.; Hug, Stephan J.; Ruettimann, Thomas Environmental Science & Technology, Vol. 38, Issue 1 https://doi.org/10.1021/es0343205	journal	January 2004
Removing Arsenic from Synthetic Groundwater with Iron Electrocoagulation: An Fe and As K-Edge EXAFS Study van Genuchten, Case M.; Addy, Susan E. A.; Peña, Jasquelin Environmental Science & Technology, Vol. 46, Issue 2 https://doi.org/10.1021/es201913a	journal	December 2011
Fecal Indicator Bacteria Transport and Deposition in Saturated and Unsaturated Porous Media Chen, Gexin; Walker, Sharon L. Environmental Science & Technology, Vol. 46, Issue 16 https://doi.org/10.1021/es301378q	journal	July 2012
Modeling As(III) Oxidation and Removal with Iron Electrocoagulation in Groundwater Li, Lei; van Genuchten, Case M.; Addy, Susan E. A. Environmental Science & Technology, Vol. 46, Issue 21 https://doi.org/10.1021/es302456b	journal	October 2012
ATR-FTIR Spectroscopy Study of the Influence of pH and Contact Time on the Adhesion of Shewanella putrefaciens Bacterial Cells to the Surface of Hematite Elzinga, Evert J.; Huang, Jen-How; Chorover, Jon Environmental Science & Technology, Vol. 46, Issue 23 https://doi.org/10.1021/es303318y	journal	November 2012
Engineering Solutions to Improve the Removal of Fecal Indicator Bacteria by Bioinfiltration Systems during Intermittent Flow of Stormwater Mohanty, Sanjay K.; Torkelson, Andrew A.; Dodd, Hanna Environmental Science & Technology, Vol. 47, Issue 19 https://doi.org/10.1021/es305136b	journal	June 2013
Fe(III) Nucleation in the Presence of Bivalent Cations and Oxyanions Leads to Subnanoscale 7 Å Polymers van Genuchten, Case M.; Gadgil, Ashok J.; Peña, Jasquelin Environmental Science & Technology, Vol. 48, Issue 20 https://doi.org/10.1021/es503281a	journal	October 2014
Factors Affecting the Yield of Oxidants from the Reaction of Nanoparticulate Zero-Valent Iron and Oxygen Keenan, Christina R.; Sedlak, David L. Environmental Science & Technology, Vol. 42, Issue 4 https://doi.org/10.1021/es7025664	journal	February 2008
Adhesion of Bacterial Exopolymers to α-FeOOH: Inner-Sphere Complexation of Phosphodiester Groups Omoike, Anselm; Chorover, Jon; Kwon, Kideok D. Langmuir, Vol. 20, Issue 25 https://doi.org/10.1021/la048597+	journal	November 2004
Role of Cell Surface Lipopolysaccharides in Escherichia c oli K12 Adhesion and Transport Walker, Sharon L.; Redman, Jeremy A.; Elimelech, Menachem Langmuir, Vol. 20, Issue 18 https://doi.org/10.1021/la049511f	journal	August 2004
ATR-FTIR Spectroscopy Reveals Bond Formation During Bacterial Adhesion to Iron Oxide Parikh, Sanjai J.; Chorover, Jon Langmuir, Vol. 22, Issue 20 https://doi.org/10.1021/la061359p	journal	September 2006
Ionic Strength Effects on Silicic Acid (H ₄ SiO ₄ ) Sorption and Oligomerization on an Iron Oxide Surface: An Interesting Interplay between Electrostatic and Chemical Forces Dol Hamid, Rossuriati; Swedlund, Peter J.; Song, Yantao Langmuir, Vol. 27, Issue 21 https://doi.org/10.1021/la201775c	journal	October 2011
Rate Constants for Reactions of Inorganic Radicals in Aqueous Solution Neta, P.; Huie, Robert E.; Ross, Alberta B. Journal of Physical and Chemical Reference Data, Vol. 17, Issue 3 https://doi.org/10.1063/1.555808	journal	July 1988
The carbonate radical and related oxidants derived from bicarbonate buffer Medinas, Danilo B.; Cerchiaro, Giselle; Trindade, Daniel F. IUBMB Life, Vol. 59, Issue 4 https://doi.org/10.1080/15216540701230511	journal	January 2007
Antibiotic Resistance in the ECOR Collection: Integrons and Identification of a Novel aad Gene Mazel, Didier; Dychinco, Broderick; Webb, Vera A. Antimicrobial Agents and Chemotherapy, Vol. 44, Issue 6 https://doi.org/10.1128/AAC.44.6.1568-1574.2000	journal	June 2000
Extracellular Iron Biomineralization by Photoautotrophic Iron-Oxidizing Bacteria Miot, J.; Benzerara, K.; Obst, M. Applied and Environmental Microbiology, Vol. 75, Issue 17 https://doi.org/10.1128/AEM.00490-09	journal	July 2009
Inactivation of Escherichia coli by Nanoparticulate Zerovalent Iron and Ferrous Ion Kim, Jee Yeon; Park, Hee-Jin; Lee, Changha Applied and Environmental Microbiology, Vol. 76, Issue 22 https://doi.org/10.1128/AEM.01009-10	journal	September 2010
Binding of metals to cell envelopes of Escherichia coli K-12. Beveridge, T. J.; Koval, S. F. Applied and Environmental Microbiology, Vol. 42, Issue 2 https://doi.org/10.1128/AEM.42.2.325-335.1981	journal	January 1981
Structure of the O antigen of Escherichia coli K-12 and the sequence of its rfb gene cluster Stevenson, G.; Neal, B.; Liu, D. Journal of Bacteriology, Vol. 176, Issue 13 https://doi.org/10.1128/JB.176.13.4144-4156.1994	journal	July 1994
A universal surface complexation framework for modeling proton binding onto bacterial surfaces in geologic settings Borrok, D. American Journal of Science, Vol. 305, Issue 6-8 https://doi.org/10.2475/ajs.305.6-8.826	journal	June 2005

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59 BASIC BIOLOGICAL SCIENCES
Bacteria attenuation
Bacterial surface functional groups
Bivalent cations
Iron electrocoagulation
Oxyanions
Specific interactions

Bacteria attenuation by iron electrocoagulation governed by interactions between bacterial phosphate groups and Fe(III) precipitates

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