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Response of soil microbial communities to elevated antimony and arsenic contamination indicates the relationship between the innate microbiota and contaminant fractions Weimin Sun, Enzong Xiao, Tangfu Xiao, Valdis Krumins, Qi Wang, Max M. Haggblom, Yiran Dong, Song Tang, Min Hu, Baoqin Li, Bingqing Xia, and Wei Liu Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b00294 • Publication Date (Web): 12 Jul 2017 Downloaded from http://pubs.acs.org on July 12, 2017
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Response of soil microbial communities to elevated antimony and arsenic
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contamination indicates the relationship between the innate microbiota and
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contaminant fractions
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Weimin Sun1 , Enzong Xiao2,3,4 , Tangfu Xiao 2,3*, Valdis Krumins5, Qi Wang1, Max
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Häggblom6, Yiran Dong7, Song Tang8, Min Hu1, Baoqin Li1, Bingqing Xia1,Wei Liu9
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1. Guangdong Key Laboratory of Agricultural Environment Pollution Integrated
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†
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Control, Guangdong Institute of Eco-Environmental Science & Technology,
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Guangzhou 510650, China
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2. Key Laboratory of Water Quality and Conservation in the Pearl River Delta,
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Ministry of Education, School of Environmental Science and Engineering,
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Guangzhou University, Guangzhou 510006, China
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3. State Key Laboratory of Environmental Geochemistry, Chinese Academy of Sciences, Guiyang 550081, China
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4. University of Chinese Academy of Sciences, Beijing 100049, China.
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5. Department of Environmental Sciences, Rutgers University, New Brunswick NJ
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08901, USA 6. Department of Biochemistry and Microbiology, Rutgers University, New Brunswick NJ 08901, USA 7. Institute for Genomic Biology, University of Illinois, Urbana-Champaign, Urbana IL 61801, USA
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8. National Institute of Environmental Health, Chinese Center for Disease Control
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and Prevention, Beijing 100021, China Water Resources Protection Bureau of
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Pearl River Water Resources Commission, Guangzhou 510611, China
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*Corresponding author.
Mailing address: 99 Lincheng Road West, Guiyang 550081,
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Guizhou Province, P. R. China. Phone: +86-851-85895318. Fax: +86-851-85891334. Email:
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[email protected] 27
†These authors contributed equally to this work.
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Abstract
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Mining of sulfide ore deposits containing metalloids, such as antimony and arsenic,
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has introduced serious soil contamination around the world, posing severe threats to
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food safety and human health. Hence, it is important to understand the behavior and
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composition of the microbial communities that control the mobilization or
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sequestration of these metal(loid)s. Here, we selected two sites in Southwest China
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with different levels of Sb and As contamination to study interactions among various
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Sb and As fractions and the soil microbiota, with a focus on the microbial response to
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metalloid contamination. Comprehensive geochemical analyses and 16S rRNA gene
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amplicon sequencing demonstrated distinct soil taxonomic inventories depending on
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Sb and As contamination levels. Stochastic gradient boosting indicated that citric acid
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extractable Sb(V) and As(V) contributed 5% and 15%, respectively, to influencing the
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community diversity. Random forest predicted that low concentrations of Sb(V) and
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As(V) could enhance the community diversity but generally, the Sb and As
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contamination impairs microbial diversity. Co-occurrence network analysis indicated
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a strong correlation between the indigenous microbial communities and various Sb
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and As fractions. A number of taxa were identified as core genera due to their
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elevated abundances and positive correlation with contaminant fractions (total Sb and
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As concentrations, bioavailable Sb and As extractable fractions, and Sb and As redox
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species). Shotgun metagenomics indicated that Sb and As biogeochemical redox
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reactions may exist in contaminated soils. All these observations suggest the potential
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for bioremediation of Sb- and As-contaminated soils. 3 ACS Paragon Plus Environment
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Keywords: Sb and As contaminated soil; Metagenomics; Stochastic gradient boosting;
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Random forest; Co-occurrence network
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Introduction
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Antimony (Sb) and arsenic (As) are two toxic metalloids belonging to group 15 of the
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Periodic Table. Both are suspected carcinogens and US EPA priority pollutants 1, 2. Sb
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is widely distributed in the lithosphere and frequently associated with As in
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sulfide-rich ores 3. Thus, co-contamination of Sb and As is commonly observed in
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mining areas 4. The environmental toxicities of Sb and As are strongly dependent on
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their redox species 5. For both, their reduced forms, i.e., Sb(III) and As(III), are more
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toxic than their oxidized counterparts, (Sb(V) and As(V)) 6-8. In general, background
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concentrations of Sb in soil are low (
