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Arsenic contamination from roxarsone in livestock manure is common, and livestock manure continuously accumulates in the open environment. Evaluations of the environmental processes of As mobilization and transformation are critical for predicting the fate of As compounds after roxarsone degradation. In this study, spatiotemporal variations in As species and microbial community structure were characterized using laboratory column experiments with background soil collected from Yanggu County (northern Shandong Plain, China), a region of intense poultry production. Organic and inorganic arsenic were detected by high-performance liquid chromatography (HPLC) and HPLC with hydride generation atomic fluorescence spectrometry (HPLC-HG-AFS), respectively. High-throughput sequencing technology was used to describe microbial diversity. Results showed that roxarsone was transformed completely within 7 days, and As(Ⅲ) and As(Ⅴ) were the major degradation products. The concentration of As(Ⅲ) was much lower than that of As(Ⅴ). The As(Ⅲ) concentration increased significantly after Day 14, whereas the As(Ⅴ) concentration increased significantly after Day 84, indicating that As(Ⅲ) was initially produced. The microbial community structure changed significantly as roxarsone transformed into various As compounds. A critical and dominant bacterial strain, norank_f__Family_XVⅢ, was found to be related to the degradation of roxarsone into As(Ⅲ). This study improves our understanding of the fate of As species released from poultry litter to soil and groundwater, which is a threat to human health and environment.


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Arsenic contamination caused by roxarsone transformation with spatiotemporal variation of microbial community structure in a column experiment

Show Author's information Ya-ci Liu1,2Zhao-ji Zhang1,2Xin-yi Zhao3Meng-tuo Wen4Sheng-wei Cao1,2Ya-song Li1,2( )
Institute of Hydrogeology and Environmental Geology, Chinese Academy of Geological Sciences, Shijiazhuang 050061, China
Key Laboratory of Groundwater Remediation of Hebei Province and China Geological Survey, Shijiazhuang 050061, China
Hebei Hydrology Engineering Geological Survey Institute Co. LTD, Shijiazhuang 050061, China
China University of Geosciences, Beijing 100083, China

Abstract

Arsenic contamination from roxarsone in livestock manure is common, and livestock manure continuously accumulates in the open environment. Evaluations of the environmental processes of As mobilization and transformation are critical for predicting the fate of As compounds after roxarsone degradation. In this study, spatiotemporal variations in As species and microbial community structure were characterized using laboratory column experiments with background soil collected from Yanggu County (northern Shandong Plain, China), a region of intense poultry production. Organic and inorganic arsenic were detected by high-performance liquid chromatography (HPLC) and HPLC with hydride generation atomic fluorescence spectrometry (HPLC-HG-AFS), respectively. High-throughput sequencing technology was used to describe microbial diversity. Results showed that roxarsone was transformed completely within 7 days, and As(Ⅲ) and As(Ⅴ) were the major degradation products. The concentration of As(Ⅲ) was much lower than that of As(Ⅴ). The As(Ⅲ) concentration increased significantly after Day 14, whereas the As(Ⅴ) concentration increased significantly after Day 84, indicating that As(Ⅲ) was initially produced. The microbial community structure changed significantly as roxarsone transformed into various As compounds. A critical and dominant bacterial strain, norank_f__Family_XVⅢ, was found to be related to the degradation of roxarsone into As(Ⅲ). This study improves our understanding of the fate of As species released from poultry litter to soil and groundwater, which is a threat to human health and environment.

Keywords: Arsenic, Roxarsone, Spatiotemporal variation, Microbial community

References(45)

Abedin MJ, Cresser MS, Meharg AA, et al. 2002. Arsenic accumulation and metabolism in rice (Oryza sativa L). Environmental Science & Technology, 36(5): 962-968.

Arcega-Cabrera F, Fargher L, Quesadas-Rojas M, et al. 2018. Environmental exposure of children to toxic trace elements (Hg, Cr, As) in an urban area of Yucatan, Mexico: Water, blood, and urine levels. Bulletin of Environmental Contamination and Toxicology, 100: 620-626.

Boopathy R, Kulpa CF, Manning J. 1998. Anaerobic biodegradation of explosives and related compounds by sulfate-reducing and methanogenic bacteria: A review. Bioresource Technology, 63(1): 81-89.

Cao WG, Chen NX, Zhang YL, et al. 2014. Distribution of arsenic in sediment of Hangjinhou Bannerlinhe transect in Hetao Basin, North China. Journal of Groundwater Science and Engineering, 2(4): 87-96.

Chen C, Liu L, Li YX, et al. 2021. Efficient degradation of roxarsone and simultaneous in-situ adsorption of secondary inorganic arsenic by a combination of Co3O4-Y2O3 and peroxymonosulfate. Journal of Hazardous Materials, 407: 124559.

Chen GW, Ke ZC, Liang TF, et al. 2016. Shewanella oneidensis MR-1-induced Fe(Ⅲ) reduction facilitates roxarsone transformation. PLoS ONE, 11(4): e0154017.

Chen GW, Xu RD, Liu L, et al. 2018. Limited carbon source retards inorganic arsenic release during roxarsone degradation in Shewanella oneidensis microbial fuel cells. Applied Microbiology and Biotechnology, 102: 8093-8106.

Chen J, Rosen BP. 2016. Organoarsenical biotransformations by Shewanella putrefaciens. Environmental Science & Technology, 50(15): 7956-7963.

Chen J, Zhang J, Rosen BP. 2019. Role of arsEFG in roxarsone and nitarsone detoxification and resistance. Environmental Science & Technology, 53(11): 6182-6191.

Chen N, Wan YC, Zhan GM, et al. 2020. Simulated solar light driven roxarsone degradation and arsenic immobilization with hematite and oxalate. Chemical Engineering Journal, 384: 123254.

Chen CM, Kukkadapu RK, Lazareva O, et al. 2017. Solid-phase Fe speciation along the vertical redox gradients in floodplains using XAS and mössbauer spectroscopies. Environmental Science & Technology, 51(14): 7903-7912.

Datta R, Sarkar D, Sharma S, et al. 2006. Arsenic biogeochemistry and human health risk assessment in organo-arsenical pesticide-applied acidic and alkaline soils: An incubation study. Science of The Total Environment, 372(1): 39-48.

European Commission (EC), 1999. Council Directive 1999/29/EC of 22 April 1999 on the undesirable substances and products in animal nutrition.

Fisher E, Dawson AM, Polshyna G, et al. 2008. Transformation of inorganic and organic arsenic by Alkaliphilus oremlandii sp. nov. strain OhILAs. Annals of the New York Academy of Sciences, 1125: 230-241.

Fu QL, He JZ, Gong H, et al. 2016. Extraction and speciation analysis of roxarsone and its metabolites from soils with different physicochemical properties. Journal of Soils and Sediments, 16: 1557-1568.

Fu YR, Chen ML, Bi XY, et al. 2011. Occurrence of arsenic in brown rice and its relationship to soil properties from Hainan Island, China. Environmental Pollution, 159(7): 1757-1762.

Gorontzy T, Kuver J, Blotevogel KH, 1993. Microbial transformation of nitroaromatic compounds under anaerobic conditions. Microbiology, 139(6): 1331-1336. DOI: 10.1009/00221287-139-6-1331.

Han JC, Zhang F, Cheng L, et al. 2017. Rapid release of arsenite from roxarsone bioreduction by exoelectrogenic bacteria. Environmental Science & Technology Letters, 4: 350-355.

Hu YN, Cheng HF, Tao S, et al. 2019. China’s ban on phenylarsonic feed additives, a major step toward reducing the human and ecosystem health risk from arsenic. Environmental Science & Technology, 53: 12177-12187.

Huang K, Peng HY, Gao F, et al. 2019. Biotransformation of arsenic-containing roxarsone by an aerobic soil bacterium Enterobacter sp. CZ-1. Environmental Pollution, 247: 482-487.

Konkel L. 2016. Organoarsenic drugs over time: The pharmacokinetics of roxarsone in chicken meat. Environmental Health Perspectives, 124(8): 50.

Kowalski LM, Reid WM. 1975. Effects of roxarsone on pigmentation and coccidiosis in broilers. Poultry Science, 54(5): 1544-1549.

Li YS, Liu YC, Zhang ZJ, et al. 2020. Identification of an anaerobic bacterial consortium that degrades roxarsone. MicrobiologyOpen, 9(4): e1003.

Liang TF, Ke ZC, Chen Q, et al. 2014. Degradation of roxarsone in a silt loam soil and its toxicity assessment. Chemosphere, 112: 128-133.

Liu YC, Li YS, Zhang ZJ, et al. 2017a. Distribution of arsenic compounds in vadose zone and groundwater around the chicken farm in Lubei Plain. South-to-North Water Transfers and Water Science & Technology, 15(3): 86-93. (in Chinese)

Liu YC, Zhang ZJ, Li YS, et al. 2017b. Response of microbial communities to roxarsone under different culture conditions. Canadian Journal of Microbiology, 63: 661-670.

Liu YC, Tian X, Cao SW, et al. 2021. Pollution characteristics and health risk assessment of arsenic transformed from feed additive organoarsenicals around chicken farms on the North China Plain. Chemosphere, 278: 130438.

Masscheleyn PH, Delaune RD, Patrick WH. 1991. Effect of redox potential and pH on arsenic speciation and solubility in a contaminated soil. Environmental Science & Technology, 25(8): 1414-1419.

Ministry of Agriculture of the People’s Republic of China. 2018. Bulletin No. 2638: Regulations on the use of feed additives.

Mondal NK. 2020. Prevalence of arsenic in chicken feed and its contamination pattern in different parts of chicken flesh: a market basket study. Environmental Monitoring and Assessment, 192(9): 590.

Morrison JL. 1969. Distribution of arsenic from poultry litter in broiler chickens, soil, and crops. Journal of Agricultural and Food Chemistry, 17(6): 1288-1290.

Nachman KE, Graham JP, Price LB, et al. 2005. Arsenic: A roadblock to potential animal waste management solutions. Environmental Health Perspectives, 113(9): 1123-1124.

Rahman MA, Hogan B, Duncan E, et al. 2014. Toxicity of arsenic species to three freshwater organisms and biotransformation of inorganic arsenic by freshwater phytoplankton (Chlorellasp. CE-35). Ecotoxicology and Environmental Safety, 106(1): 126-135.

Sarkar D, Makris KC, Parra-Noonan MT, et al. 2007. Effect of soil properties on arsenic fractionation and bioaccessibility in cattle and sheep dipping vat sites. Environment International, 33(2): 164-169.

Stolz JF, Perera E, Kilonzo B, et al. 2007. Biotransformation of 3-nitro-4-hydroxybenzene arsonic acid (roxarsone) and release of inorganic arsenic by Clostridium species. Environmental Science & Technology, 41(3): 818-823.

Tang R, Yuan SJ, Wang YL, et al. 2020. Arsenic volatilization in roxarsone-loaded digester: Insight into the main factors and arsM genes. Science of The Total Environment, 711: 135123.

U. S. Food and Drug Administration. 2013. FDA’s response to the citizen petition. Food and Drug Administration:Silver Spring: MD.FDA-2009-p-0594.

Wu SS, Yang T, Mai JM, et al. 2022. Enhanced removal of organoarsenic by chlorination: Kinetics, effect of humic acid, and adsorbable chlorinated organoarsenic. Journal of Hazardous Materials, 422: 126820.

Yang T, Wu SS, Liu CP, et al. 2021. Efficient degradation of organoarsenic by UV/chlorine treatment: Kinetics, mechanism, enhanced arsenic removal, and cytotoxicity. Environmental Science & Technology, 55: 2037-2047.

Yao LX, Li GL, Dang Z, et al. 2009. Arsenic speciation in turnip as affected by application of chicken manure bearing roxarsone and its metabolites. Plant Soil, 316: 117-124.

Yao LX, Huang LX, He ZH, et al. 2016. Delivery of roxarsone via chicken diet→chicken→chicken manure→soil→rice plant. Science of The Total Environment, 566-567: 1152-1158.

Yao LX, Huang LX, Bai CH, et al. 2017. Soil calcium significantly promotes uptake of inorganic arsenic by garland chrysanthemum (ChrysanthemumL coronarium) fertilized with chicken manure bearing roxarsone and its metabolites. Environmental Science and Pollution Research, 24: 16429-16439.

Yao LX, Huang LX, Bai CH, et al. 2019a. Effect of roxarsone metabolites in chicken manure on soil biological property. Ecotoxicology and Environmental Safety, 171: 493-501.

Yao LX, Carey MP, Zhong JW, et al. 2019b. Soil attribute regulates assimilation of roxarsone metabolites by rice (Oryza sativa L). Ecotoxicology and Environmental Safety, 184: 109660.

Zhan L, Xia ZW, Xu ZM, et al. 2021. Study on the remediation of tetracycline antibiotics and roxarsone contaminated soil. Environmental Pollution, 271: 116312.

Publication history
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Publication history

Received: 09 July 2021
Accepted: 21 October 2021
Published: 29 October 2021
Issue date: December 2021

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© 2021 Journal of Groundwater Science and Engineering Editorial Office
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