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Reduced Iron-Containing Clay Minerals as Antibacterial Agents Xi Wang, Hailiang Dong, Qiang Zeng, Qingyin Xia, Limin Zhang, and Ziqi Zhou Environ. Sci. Technol., Just Accepted Manuscript • Publication Date (Web): 01 Jun 2017 Downloaded from http://pubs.acs.org on June 1, 2017
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Environmental Science & Technology
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Reduced Iron-Containing Clay Minerals as Antibacterial Agents
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Xi Wang,1Hailiang Dong,*,1,2Qiang Zeng,1Qingyin Xia,1 Limin Zhang,1 Ziqi Zhou1
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1. Geomicrobiology Laboratory, State Key Laboratory of Biogeology and
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Environmental Geology, China University of Geosciences, Beijing 100083, China
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2. Department of Geology and Environmental Earth Science, Miami University, OH
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45056, USA.
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* Corresponding author at: Hailiang Dong
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Geomicrobiology Laboratory, State Key Laboratory of Biogeology and
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Environmental Geology, China University of Geosciences, Beijing 100083, China
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Tel.: 86-010-82320969; Email:
[email protected] 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27
Further revised for Environmental Science and Technology May 27, 2017
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TOC Art
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ABSTRACT Previous work documented the general antibacterial mechanism of
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iron containing clays that involved hydroxyl radical (•OH) production from soluble
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Fe2+, and attack of cell membrane and intracellular proteins. Here we explore the role
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of clay structural Fe(II) in •OH production at near neutral pH and identify a lipid
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involved in the antibacterial process. Structural Fe(III) in nontronite NAu-2 was
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reduced (rNAu-2) and E. coli, a model bacterium, was exposed to rNAu-2 in oxic
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suspension. The antibacterial activity of rNAu-2 was dependent on pH and Fe(II)
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concentration, where E.coli were completely killed at pH 6, but survived at pH 7 and
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8. In the presence of a •OH scavenger or in anaerobic atmosphere, E. coli survived
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better, suggesting that cell death may be caused by •OH generated from oxidation of
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structural Fe(II) in rNAu-2. In-situ imaging revealed damage of a membrane lipid,
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cardiolipin, in the polar region of E. coli cells, where reactive oxygen species and
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redox-active labile Fe were enriched. Our results advance the previous antibacterial
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model by demonstrating that the structural Fe(II) is the primary source of •OH,
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which damages cardiolipin, triggers the influx of soluble Fe2+ into the cell, and
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ultimately leads to cell death.
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INTRODUCTION
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Previous studies1,
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have documented various natural clays that kill
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antibiotic-resistant human pathogens and as a result, these clays have been proposed
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as antibiotic alternatives.2 Reduced iron-containing clays (RIC), illite-smectite
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minerals in particular, are important components of natural antibacterial clays.3, 4 One
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specific role that RIC play in the antibacterial activity is its capacity to buffer pH and
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promote Fe2+ solubility.5, 6 Soluble Fe2+ diffuses into cell and is oxidized to Fe3+ with
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generation of lethal hydroxyl radicals (•OH) and other reactive oxygen species (ROS),
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which result in cell death.5 However, the role of structurally-bound Fe(II) in the
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bactericidal process of RIC has not been elucidated.
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Another important component of natural antibacterial clay is pyrite,5, 6 which can
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produce • OH upon oxidation in aqueous suspension. The generated • OH could
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trigger membrane lipid peroxidation, which ultimately may lead to cell death.7
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However, for natural antibacterial clay this process is effective at non-neutral pH (e.g.,
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either
