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Evaluation of bioaugmentation and biostimulation on arsenic remediation in soil through biovolatilization

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Abstract

Arsenic (As) removal through microbially driven biovolatilization can be explored as a potential method for As bioremediation. However, its effectiveness needs to be improved. Biostimulation with organic matter amendment and bioaugmentation with the inoculation of genetic engineered bacteria could be potential strategies for As removal and site remediation. Here, the experiments were conducted to evaluate the impacts of rice straw and biochar amendment, inoculation of genetic engineered Pseudomonas putida KT2440 (GE P. putida) with high As volatilization activity, on microbial mediated As volatilization and removal from three different arseniferous soils. In general, the addition of rice straw (5%) significantly enhanced As methylation and volatilization in comparison with corresponding non-amended soils. Biochar amendments and inoculation of the GE P. putida increased As methylation and volatilization, respectively, but less than that of rice straw addition. The effectiveness of As volatilizations are quite different in the various paddy soils. The combined amendments of rice straw and GE P. putida exhibited the highest As removal efficiency (483.2 μg/kg/year) in Dayu soil, with 1.2% volatilization of the total As annually. The highest water-soluble As concentration (0.73 mg/kg) in this soil could be responsible for highest As volatilization besides the rice straw and bacteria in this soil.

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References

  • Akins MB, Lewis RJ (1976) Chemical distribution and gaseous evolution of arsenic-74 added to soils as DSMA-74As. Soil Sci Soc Am J 40:655–658

    Article  CAS  Google Scholar 

  • Akter KF, Owens G, Davey DE, Naidu R (2005) Arsenic speciation and toxicity in biological systems. Rev Environ Contam Toxicol 184:97–149

    CAS  Google Scholar 

  • Beesley L, Moreno-Jimenez E, Gomez-Eyles JL, Harris E, Robinson B, Sizmur T (2011) A review of biochars’ potential role in the remediation, revegetation and restoration of contaminated soils. Environ Pollut 159:3269–3282

    Article  CAS  Google Scholar 

  • Beesley L, Marmiroli M, Pagano L, Pigoni V, Fellet G, Fresno T, Vamerali T, Bandiera M, Marmiroli N (2013) Biochar addition to an arsenic contaminated soil increases arsenic concentrations in the pore water but reduces uptake to tomato plants (Solanum lycopersicum L.) Sci Total Environ 454:598–603

    Article  Google Scholar 

  • Bentley R, Chasteen TG (2002) Microbial methylation of metalloids: arsenic, antimony, and bismuth. Microbiol Mol Biol Rev 66:250–271

    Article  CAS  Google Scholar 

  • Brown S, Chaney RL, Hallfrisch JG, Xue Q (2003) Effect of biosolids processing on lead bioavailability in an urban soil. J Environ Qual 32:100–108

    Article  CAS  Google Scholar 

  • Challenger F (1945) Biological methylation. Chem Rev 36:315–361

    Article  CAS  Google Scholar 

  • Chen J, Qin J, Zhu YG, Lorenzo VD, Rosen BP (2013) Engineering the soil bacterium Pseudomonas putida for arsenic methylation. Appl Environ Microbiol 79:4493–4495

    Article  CAS  Google Scholar 

  • Chen J, Sun GX, Wang XX, Lorenzo VD, Rosen BP, Zhu YG (2014) Volatilization of arsenic from polluted soil by Pseudomonas putida engineered for expression of the arsM arsenic(III) S-adenosine methyltransferase gene. Environ Sci Technol 48:10337–10344

    Article  CAS  Google Scholar 

  • Cheng CN, Focht DD (1979) Production of arsine and methylarsines in soil and in culture. Appl Environ Microbiol 38:494–498

    CAS  Google Scholar 

  • Cheng CH, Lehmann J (2009) Ageing of black carbon along a temperature gradient. Chemosphere 75:1021–1027

    Article  CAS  Google Scholar 

  • Crawford JM, Portmann C, Zhang X, Roeffaers MBJ, Clardy J (2012) Small molecule perimeter defense in entomopathogenic bacteria. Proc Natl Acad Sci U S A 109:10821–10826

    Article  CAS  Google Scholar 

  • Cullen WR, Bentley R (2005) The toxicity of trimethylarsine: an urban myth. J Environ Monit 7:11–15

    Article  CAS  Google Scholar 

  • Cullen WR, Reimer KJ (1989) Arsenic speciation in the environment. Chem Rev 89:713–764

    Article  CAS  Google Scholar 

  • Edvantoro BB, Naidu R, Megharaj M, Merrington G, Singleton I (2004) Microbial formation of volatile arsenic in cattle dip site soils contaminated with arsenic and DDT. Appl Soil Ecol 25:207–217

    Article  Google Scholar 

  • Feldmann J, Devalla S, Raab A, Hansen HR, Hirner AV, Emons H (2004) Analytical strategies for arsenic speciation in environmental and biological samples. In: Hirner AV, Emons H (Eds) Organic metal and metalloid species in the environment: analysis, distribution, processes and toxicological evaluation. Springer, New York, pp 41–70

  • Fellet G, Marchiol L, Delle Vedove G, Peressotti A (2011) Application of biochar on mine tailings: effects and perspectives for land reclamation. Chemosphere 83:1262–1267

    Article  CAS  Google Scholar 

  • Gao S, Burau RG (1997) Environmental factors affecting rates of arsine evolution from and mineralization of arsenicals in soil. J Environ Qual 26:753–763

    Article  CAS  Google Scholar 

  • Gbaruko BC, Ana G, Nwachukwu JK (2008) Ecotoxicology of arsenic in the hydrosphere: implications for public health. Afr J Biotechnol 7:4737–4742

    CAS  Google Scholar 

  • Glaser B, Lehmann J, Zech W (2002) Ameliorating physical and chemical properties of highly weathered soils in the tropics with charcoal—a review. Biol Fertil Soils 35:219–230

    Article  CAS  Google Scholar 

  • Gong Z, Lu X, Ma M, Watt C, Le XC (2002) Arsenic speciation analysis. Talanta 58:77–96

    Article  CAS  Google Scholar 

  • Groffman PM, Tiedje JM (1991) Relationship between denitrification, CO2 production and air filled porosity in soils of different texture and drainage. Soil Biol Biochem 23:299–302

    Article  CAS  Google Scholar 

  • Hartley W, Dickinson NM, Riby P, Lepp NW (2009) Arsenic mobility in brownfield soils amended with green waste compost or biochar and planted with Miscanthus. Environ Pollut 157:2654–2662

    Article  CAS  Google Scholar 

  • Huang JH, Hu KN, Decker B (2011) Organic arsenic in the soil environment: speciation, occurrence, transformation, and adsorption behavior. Water Air Soil Pollut 219:401–415

    Article  CAS  Google Scholar 

  • Huang H, Zhu YG, Chen Z, Yin XX, Sun GX (2012a) Arsenic mobilization and speciation during iron plaque decomposition in a paddy soil. J Soils Sediments 12:402–410

    Article  CAS  Google Scholar 

  • Huang H, Jia Y, Sun GX, Zhu YG (2012b) Arsenic speciation and volatilization from flooded paddy soils amended with different organic matters. Environ Sci Technol 46:2163–2168

    Article  CAS  Google Scholar 

  • Huang K, Chen C, Zhang J, Tang Z, Shen QR, Rosen BP, Zhao FJ (2016) Efficient arsenic methylation and volatilization mediated by a novel bacterium from an arsenic-contaminated paddy soil. Environ Sci Technol 50:6389–6396

    Article  CAS  Google Scholar 

  • Jenkinson D S. 1981. The fate of plant and animal residues in soil. In: Greenland DS, Hayes MHB (Eds) The Chemistry of Soil Processes. John Wiley, New York, pp. 505–601

  • Jia Y, Huang H, Zhong M, Wang FH, Zhang LM, Zhu YG (2013a) Microbial arsenic methylation in soil and rice rhizosphere. Environ Sci Technol 47:3141–3148

    CAS  Google Scholar 

  • Jia Y, Sun GX, Huang H, Zhu YG (2013b) Biogas slurry application elevated arsenic accumulation in rice plant through increased arsenic release and methylation in paddy soil. Plant Soil 365:387–396

    Article  CAS  Google Scholar 

  • Lehmann J, Rondon M (2006) Bio-char soil management on highly weathered soils in the humid tropics biological approaches to sustainable soil systems. CRC Press, Boca Raton, pp 517–530

    Book  Google Scholar 

  • Lehmann J, Silva JPD, Steiner C, Nehls T, Zech W, Glaser B (2003) Nutrient availability and leaching in an archaeological Anthrosol and a Ferralsol of the central Amazon basin: fertilizer, manure and charcoal amendments. Plant Soil 249:343–357

    Article  CAS  Google Scholar 

  • Liao HC, Chu YJ, Su YC, Hsiao SY, Wei CC, Liu CW, Liao CM, Shen WC, Chang FJ (2011) Arsenite-oxidizing and arsenate-reducing bacteria associated with arsenic-rich groundwater in Taiwan. J Contam Hydrol 123:20–29

    Article  CAS  Google Scholar 

  • Liu WJ, Zhu YG, Hu Y, Williams PN, Gault AG, Meharg AA, Charnock JM, Smith FA (2006) Arsenic sequestration in iron plaque, its accumulation and speciation in mature rice plants (Oryza sativa L). Environ Sci Technol 40:5730–5736

    Article  CAS  Google Scholar 

  • Liu S, Zhang F, Chen J, Sun GX (2011) Arsenic removal from contaminated soil via biovolatilization by genetically engineered bacteria under laboratory conditions. J Environ Sci 23:1544–1550

    Article  CAS  Google Scholar 

  • Lomax C, Liu WJ, Wu L, Xue K, Xiong J, Zhou J, Mcgrath SP, Meharg AA, Miller AJ, Zhao FJ (2012) Methylated arsenic species in plants originate from soil microorganisms. New Phytol 193:665–672

    Article  CAS  Google Scholar 

  • Mestrot A, Uroic MK, Plantevin T, Islam MR, Krupp EM, Feldmann J, Meharg AA (2009) Quantitative and qualitative trapping of arsines deployed to assess loss of volatile arsenic from paddy soil. Environ Sci Technol 43:8270–8275

    Article  CAS  Google Scholar 

  • Mestrot A, Feldmann J, Krupp EM, Hossain MS, Romanross G, Meharg AA (2011a) Field fluxes and speciation of arsines emanating from soils. Environ Sci Technol 45:1798–1804

    Article  CAS  Google Scholar 

  • Mestrot A, Merle JK, Broglia A, Feldmann J, Krupp EM (2011b) Atmospheric stability of arsine and methylarsines. Environ Sci Technol 45:4010–4015

    Article  CAS  Google Scholar 

  • Mestrot A, Planer-Friedrich B, Feldmann J (2013) Biovolatilisation: a poorly studied pathway of the arsenic biogeochemical cycle. Environ Sci Proc Impacts 15(9):1639–1651

    Article  CAS  Google Scholar 

  • Meyer J, Schmidt A, Michalke K, Hensel R (2007) Volatilisation of metals and metalloids by the microbial population of an alluvial soil. Syst Appl Microbiol 30:229–238

    Article  CAS  Google Scholar 

  • Namgay T, Singh B, Singh BP, Krull E, Singh B, Joseph S (2010) Influence of biochar application to soil on the availability of As, Cd, Cu, Pb, and Zn to maize (Zea mays L). Aust J Soil Res 48:638–647

    Article  CAS  Google Scholar 

  • Novak JM, Busscher WJ, Watts DW, Laird DA, Ahmedna MA, Niandou MAS (2010) Short-term CO2 mineralization after additions of biochar and switchgrass to a Typic Kandiudult. Geoderma 154:281–288

    Article  CAS  Google Scholar 

  • Pakulska D, Czerczak S (2006) Hazardous effects of arsine: a short review. Int J Occup Med Environ Health 19:36–44

    Article  Google Scholar 

  • Petit C, Peterson GW, Mahle J, Bandosz TJ (2010) The effect of oxidation on the surface chemistry of sulfurcontaining carbons and their arsine adsorption capacity. Carbon 48:1779–1787

    Article  CAS  Google Scholar 

  • Qin J, Rosen BP, Zhang Y, Wang GJ, Franke S, Rensing C (2006) Arsenic detoxification and evolution of trimethylarsine gas by a microbial arsenite S-adenosylmethionine methyltransferase. Proc Natl Acad Sci U S A 103:2075–2080

    Article  CAS  Google Scholar 

  • Qin J, Lehr CR, Yuan CG, Le XC, McDermott TR, Rosen BP (2009) Biotransformation of arsenic by a Yellowstone thermoacidophilic eukaryotic alga. Proc Natl Acad Sci U S A 106:5213–5217

    Article  CAS  Google Scholar 

  • Quinn R, Dahl TA, Diamond BW, Toseland BA (2006) Removal of arsine from synthesis gas using a copper on carbon adsorbent. Ind Eng Chem Res 45(18):6272–6278

    Article  CAS  Google Scholar 

  • Redman AD, Macalady DL, Ahmann D (2002) Natural organic matter affects arsenic speciation and sorption onto hematite. Environ Sci Technol 36:2889–2896

    Article  CAS  Google Scholar 

  • Rhine ED, Garcia-Dominguez E, Phelps CD, Young LY (2005) Environmental microbes can speciate and cycle arsenic. Environ Sci Technol 39:9569–9573

    Article  CAS  Google Scholar 

  • Sanford RA, Klein DA (1988) Environmental bioremediation for organometallic compounds: microbial growth and arsenic volatillization from soil and retorted shale. Appl Organomet Chem 2:159–169

    Article  CAS  Google Scholar 

  • Shiowatana J, McLaren RG, Chanmekha N, Samphao A (2001) Fractionation of arsenic in soil by a continuous-flow sequential extraction method. J Environ Qual 30(6):1940–1949

  • Solaiman ARM, Meharg AA, Gault AG, Charnock JM (2009) Arsenic mobilization from iron oxyhydroxides is regulated by organic matter carbon to nitrogen (C:N) ratio. Environ Int 35:480–484

    Article  CAS  Google Scholar 

  • Spokas KA, Koskinen WC, Baker JM, Reicosky DC (2009) Impacts of woodchip biochar additions on greenhouse gas production and sorption/degradation of two herbicides in a Minnesota soil. Chemosphere 77:574–581

    Article  CAS  Google Scholar 

  • Sun GX, Lu XA, Williams PN, Zhu YG (2010) Distribution and translocation of selenium from soil to grain and its speciation in paddy rice (Oryza sativa L). Environ Sci Technol 44:6706–6711

    Article  CAS  Google Scholar 

  • Thomas JE, Rhue RD (1997) Volatilization of arsenic in contaminated cattle dipping vat soil. Bull Environ Contam Toxicol 59:882–887

    Article  CAS  Google Scholar 

  • Thomas B, Ruben K, Andreas K, Philippe Van C, Matthew GV, Andreas V, Kate C (2010) Biogeochemical redox processes and their impact on contaminant dynamics. Environ Sci Technol 44:15–23

    Article  Google Scholar 

  • Turpeinen R, Pantsar M (2002) Role of microbes in controlling the speciation of arsenic and production of arsines in contaminated soils. Sci Total Environ 285:133–145

    Article  CAS  Google Scholar 

  • Wang PP, Sun GX, Jia Y, Meharg AA, Zhu YG (2014a) A review on completing arsenic biogeochemical cycle: microbial volatilization of arsines in environment. J Environ Sci 26:371–381

    Article  Google Scholar 

  • Wang PP, Sun GX, Zhu YG (2014b) Identification and characterization of arsenite methyltransferase from an archaeon, Methanosarcina acetivorans C2A. Environ Sci Technol 48:12706–12713

    Article  CAS  Google Scholar 

  • Wang PP, Bao P, Sun GX (2015) Identification and catalytic residues of the arsenite methyltransferase from a sulfate-reducing bacterium, Clostridium sp BXM. FEMS Microbiol Lett 362:1–8

    Article  Google Scholar 

  • Wang HY, Wen SL, Chen P, Zhang L, Cen K, Sun GX (2016) Mitigation of cadmium and arsenic in rice grain by applying different silicon fertilizers in contaminated fields. Environ Sci Pollut Res 23:3781–3788

    Article  CAS  Google Scholar 

  • Weng LP, Van Riemsdijk WH, Hiemstra T (2009) Effects of fulvic and humic acids on arsenate adsorption to goethite: experiments and modeling. Environ Sci Technol 43:7198–7204

    Article  CAS  Google Scholar 

  • Woolson EA (1977) Generation of alkylarsines from soil. Weed Sci 25:412–416

    CAS  Google Scholar 

  • Yin XX, Chen J, Qin J, Sun GX, Rosen BP, Zhu YG (2011) Biotransformation and volatilization of arsenic by three photosynthetic cyanobacteria. Plant Physiol 156:1631–1638

    Article  CAS  Google Scholar 

  • Yuan CG, Zhang KG, Wang ZH, Jiang GB (2010) Rapid analysis of volatile arsenic species released from lake sediment by a packed cotton column coupled with atomic fluorescence spectrometry. J Anal At Spectrom 25:1605–1611

    Article  CAS  Google Scholar 

  • Zheng RL, Cai C, Liang JH, Huang Q, Chen Z, Huang YZ, Arp HPH, Sun GX (2012) The effects of biochars from rice residue on the formation of iron plaque and the accumulation of Cd, Zn, Pb, As in rice (Oryza sativa L) seedlings. Chemosphere 89:856–862

    Article  CAS  Google Scholar 

  • Zheng RL, Sun GX, Zhu YG (2013) Effects of microbial processes on the fate of arsenic in paddy soil. Chin Sci Bull 58:186–193

    Article  CAS  Google Scholar 

  • Zheng RL, Chen Z, Cai C, Tie BQ, Liu XL, Reid BJ, Huang Q, Lei M, Sun GX, Baltrėnaitė E (2015) Mitigating heavy metal accumulation into rice (Oryza sativa L) using biochar amendment—a field experiment in Hunan, China. Environ Sci Pollut Res 22:11097–11108

    Article  CAS  Google Scholar 

  • Zhu YG, Sun GX, Lei M, Teng M, Liu YX, Chen NC, Wang LH, Carey AM, Deacon C, Raab A, Meharg AA, Williams PN (2008) High percentage inorganic arsenic content of mining impacted and nonimpacted Chinese rice. Environ Sci Technol 42:5008–5013

    Article  CAS  Google Scholar 

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Acknowledgements

This project was financially supported by the Natural Science Foundation of China (Nos. 41371459, 41501336, 41501336), the State Key Program of Natural Science Foundation of China (No. 41330853), the National High Technology Research and Development Program of China (863 Program, 2013AA06A209), and Beijing Outstanding Talent Training Project (2015000020060G141).

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Authors and Affiliations

  1. State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, 100085, People’s Republic of China

    Peng Chen, Jin Li, Hong-Yan Wang & Guo-Xin Sun

  2. University of Chinese Academy of Sciences, Beijing, 100049, People’s Republic of China

    Peng Chen

  3. College of Resources and Environment, Yunnan Agricultural University, Kunming, 650201, People’s Republic of China

    Jin Li

  4. Research and Development Center for Grasses and Environment, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, People’s Republic of China

    Rui-Lun Zheng

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  1. Peng Chen
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  2. Jin Li
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  3. Hong-Yan Wang
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  4. Rui-Lun Zheng
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  5. Guo-Xin Sun
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Correspondence to Guo-Xin Sun.

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Chen, P., Li, J., Wang, HY. et al. Evaluation of bioaugmentation and biostimulation on arsenic remediation in soil through biovolatilization. Environ Sci Pollut Res 24, 21739–21749 (2017). https://doi.org/10.1007/s11356-017-9816-5

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