Abstract
The paddy soils in some areas in Jianghan Plain were severely contaminated by arsenic. However, little is known about the activity and diversity of the dissimilatory arsenate-respiring prokaryotes (DARPs) in the paddy soils, and the effects of sulfate on the microbial mobilization and release of arsenic from soils into solution. To address this issue, we collected arsenic-rich soils from the depths of 1.6 and 4.6 m in a paddy region in the Xiantao city, Hubei Province, China. Microcosm assays indicated that all of the soils have significant arsenate-respiring activities using lactate, pyruvate or acetate as the sole electron donor. Functional gene cloning and analysis suggest that there are diverse DARPs in the indigenous microbial communities of the soils. They efficiently promoted the mobilization, reduction and release of arsenic and iron from soils under anaerobic conditions. Remarkably, when sulfate was amended into the microcosms, the microorganisms-catalyzed reduction and release of arsenic and iron were significantly increased. We further found that sulfate significantly enhanced the arsenate-respiring reductase gene abundances in the soils. Taken together, a diversity of DARPs in the paddy soils significantly catalyzed the dissolution, reduction and release of arsenic and iron from insoluble phase into solution, and the presence of sulfate significantly increased the microbial reactions.
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Agusa T, Kunito T, Kubota R, Inoue S, Fujihara JU, Minh TB, Ha NN, Tu NP, Trang PT, Chamnan C, Takeshita H, Iwata H, Tuyen BC, Viet PH, Tana TS, Tanabe S (2010a) Exposure, metabolism, and health effects of arsenic in residents from arsenic-contaminated groundwater areas of Vietnam and Cambodia: a review. Rev Environ Health 25(3):193–220
Cai X, Zhang Z, Yin N, Du H, Li Z, Cui Y (2016) Comparison of arsenate reduction and release by three As(V)-reducing bacteria isolated from arsenic-contaminated soil of Inner Mongolia, China. Chemosphere 161:200–207
Chen XM, Zeng XC, Wang JN, Deng Y, Ma T, E GJ, Wang YX (2017) Microbial communities involved in arsenic mobilization and release from the deep sediments into groundwater in Jianghan plain, Central China. Sci Total Environ 579:989–999
Deng GuG, Xu B, Li L, Wu B (2018) Surface characterization of arsenopyrite during chemical and biological oxidation. Sci Total Environ 626:349
Doerfelt C, Feldmann T, Roy R, Demopoulos GP (2016) Stability of arsenate-bearing fe(III)/al(III) co-precipitates in the presence of sulfide as reducing agent under anoxic conditions. Chemosphere 151:318–323
Donahoechristiansen J, D’Imperio S, Jackson CR, Inskeep WP, Mcdermott TR (2004) Arsenite-oxidizing hydrogenobaculum strain isolated from an acid-sulfate-chloride geothermal spring in yellowstone national park. Appl Environ Microbiol 70(3):1865–1868
Duan Y, Gan Y, Wang YX, Deng Y, Guo X, Dong C (2015) Temporal variation of groundwater level and arsenic concentration at Jianghan Plain, central China. J Geochem Explor 149(12):106–119
Fodor P, Ebdon L, Pitts L, Cornelis R, Crews H, Donard OFX et al. (2001) Arsenic speciation in the environment. Chem Rev 89(4):713–764
Frankenberger WTJ, Frankenberger WTJ (2002) Environmental chemistry of arsenic. J Hazard Mater 92(2):213–215
Gan YQ, Wang YX, Duan Y, Deng Y, Guo X, Ding X (2014) Hydrogeochemistry and arsenic contamination of groundwater in the Jianghan Plain, central China. J Geochem Explor 138(3):81–93
Guo H, Liu Z, Ding S, Hao C, Xiu W, Hou W (2015) Arsenate reduction and mobilization in the presence of indigenous aerobic bacteria obtained from high arsenic aquifers of the Hetao basin, Inner Mongolia. Environ Pollut 203:50–59
Hao TW, Xiang PY, Mackey HR, Chi K, Lu H, Chui HK, Chen GH (2014) A review of biological sulfate conversions in wastewater treatment. Water Res 65:1–21
Jiang S, Lee JH, Kim D, Kanaly RA, Kim MG, Hur HG (2013) Differential arsenic mobilization from As-bearing ferrihydrite by iron-respiring shewanella strains with different arsenic-reducing activities. Env Sci Tec 47(15):8616–8623
Kirk MF, Holm TR, Park J, Jin Q, Sanford RA, Fouke BW, Bethke CM (2004) Bacterial sulfate reduction limits natural arsenic contamination in groundwater. Geology 32(11):953–956
Kudo K, Yamaguchi N, Makino T, Ohtsuka T, Kimura K, Dong DT (2013) Release of arsenic from soil by a novel dissimilatory arsenate-reducing bacterium, anaeromyxobacter sp. strain PSR-1. Appl Environ Micro 79(15):4635–42
Li H, Zeng XC, He Z (2016) Long-term performance of rapid oxidation of arsenite in simulated groundwater using a population of arsenite-oxidizing microorganisms in a bioreactor. Water Res 101:393–401
Luo XS, Wang JN, Zeng XC, Wang YX, Zhou LL (2012) Mycetocola manganoxydans sp. nov. an actinobacterium isolated from the Taklamakan desert. Int J Syst Evol Micro 62(12):2967–2970
Matlakowska R (2008) Arsenite and arsenate metabolism of Sinorhizobium sp. M14 living in the extreme environment of the Zloty Stok Gold Mine. Geomicrobiol J 25(7-8):363–370
Mccarty KM, Hanh HT, Kim KW (2011) Arsenic geochemistry and human health in South East Asia. Rev Environ Health 26(1):71–78
Mirza BS, Sorensen DL, Dupont RR, McLean JE (2017) New arsenate reductase gene (arrA) PCR primers for diversity assessment and quantification in environmental samples. Appl Environ Microb 83(4):e02725–16
Mu Y, Pan YM, Shi WX (2016a) Luteimonas arsenica sp. nov. an arsenic-tolerant bacterium isolated from arsenic-contaminated soil. Int J Syst Evol Micro 66(6):2291
Mu Y, Zhou LL, Zeng XC (2016b) Arsenicitalea aurantiaca gen. nov. sp. nov. a new member of the family Hyphomicrobiaceae, isolated from the high-arsenic sediment in Jianghan Plain. Int J Syst Evol Micro 66(12):5478–5484
Niggemyer A, Spring S, Stackebrandt E (2001) Isolation and characterization of a novel As(V)-reducing bacterium: implications for arsenic mobilization and the genus Desulfitobacterium. Appl Environ Microbiol 67(12):5568–5580
Nordstrom DK (2002) Public health: worldwide occurrences of arsenic in ground water. Science 296(5576):2143–5
Ohtsuka T, Yamaguchi N, Makino T, Sakurai K (2013) Arsenic dissolution from Japanese paddy soil by a dissimilatory arsenate-reducing bacterium Geobacter sp. OR-1. Environ Sci Technol 47:6263–6271
Oremlando RS, Stolz JF (2003) The ecology of arsenic. Science 300:939–944
Osborne TH, McArthur JM, Sikdar PK, Santini JM (2015) Isolation of an arsenate-respiring bacterium from a redox front in an arsenic-polluted aquifer in West Bengal, Bengal Basin. Environ Sci Technol 49:4193–4199
Pi K, Wang Y, Xie X, Ma T, Liu Y, Su C (2016) Remediation of arsenic-contaminated groundwater by in-situ stimulating biogenic precipitation of iron sulfides. Water Res 109:337–346
Plenge MF, Engel AS, Omelon CR, Beennett PC (2016) Thermophilic archaeal diversity and methanogenesis from El Tatio Geyser Field, Chile. Geomicrobiol J 34(3):220–230
Rahman MA, Rahman A, Mzk K, Amn R (2018) Human health risks and socio-economic perspectives of arsenic exposure in Bangladesh: a scoping review. Ecotox Environ Safe 150:335–343
Rhine ED, Onesios KM, Serfes ME, Reinfelder JR, Young LY (2008) Arsenic transformation and mobilization from minerals by the arsenite oxidizing strain WAO. Env Sci Tec 42(5):1423–9
Rodríguez-Lado L, Sun G, Berg M, Zhang Q, Xue H, Zheng Q, Johnson CA (2013) Groundwater arsenic contamination throughout China. Science 341(6148):866–868
Shao J, He Y, Zhang H, Chen A, Lei M, Chen J, Gu JD (2016) Silica fertilization and nano-mnoâ, amendment on bacterial community composition in high arsenic paddy soils. Appl Micro Biot 100(5):2429–2437
Smedley PL, Kinniburgh DG (2002) A review of the sources, behavior and distribution of arsenic in natural waters. Appl Geochem 17:517–568
Wang JN, Zeng XC, Zhu X, Zeng X, Mu Y (2017) Sulfate enhances the dissimilatory arsenate-respiring prokaryotes-mediated mobilization, reduction and release of insoluble arsenic and iron from the arsenic-rich sediments into groundwater. J Hazards Mater 339:409
Wang Y, Liu XH, Si YB, Wang RF (2016) Release and transformation of arsenic from as-bearing iron minerals by fe-reducing bacteria. Chem Eng Jl 295:29–38
Xie X, Liu Y, Pi K, Liu C, Li J, Duan M et al. (2016) In situ, fe-sulfide coating for arsenic removal under reducing conditions. J Hydrol 534:42−49
Xu LH, Zeng XC, Nie Y, Luo XS, E GJ, Zhou LL (2014) Pontibacter diazotrophicus sp. nov. a novel nitrogen-fixing bacterium of the family cytophagaceae. Plos One 9(3):e92294
Yang Y, Mu Y, Zeng XC, Wu WW et al. (2017) Functional genes and thermophilic microorganisms responsible for arsenite oxidation from the shallow sediment of an untraversed hot spring outlet. Ecotoxicology 26(4):1–12
Zeng XC, E GJ, Wang JN, Wang N, Chen XM, Mu Y, Wang Y (2016) Functions and unique diversity of genes and microorganisms involved in arsenite oxidation from the tailings of a realgar mine. Appl Environ Micro 82(24):7019–7029
Zhang L, Shi WX, Zeng XC, Ge F, Yang MK, Nie Y, Bao A, Wu SF, E GJ (2015) Unique diversity of the venom peptides from the scorpion Androctonus bicolor revealed by transcriptomic and proteomic analysis. J Proteom 128:231–250
Zhong J, Zeng XC, Zeng X, Nie Y, Zhang L, Wu SF (2016) Transcriptomic analysis of the venom glands from the scorpion hadogenes troglodytes, revealed unique and extremely high diversity of the venom peptides. J Proteom 150:40–62
Zhu W, Young LY, Yee N, Serfes M, Rhine ED, Reinfelder JR (2008) Sulfide-driven arsenic mobilization from arsenopyrite and black shale pyrite. Geochim Cosmochim Ac 72(210):5243–50
Zhu YG, Xue XM, Kappler A, Rosen BP, Meharg AA (2017) Linking genes to microbial biogeochemical cycling: lessons from arsenic. Environ Sci Techno 51(13):7326–7339
Zhu YG, Yoshinag M, Zhao FJ, Rosen BP (2014) Earth abides arsenic biotransformations. Annu Rev Earth Planet Sci 42(1):443
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This work was financially supported by the National Natural Science Foundation of China (Grant Nos. 41472219 and 41521001).
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Shi, W., Wu, W., Zeng, XC. et al. Dissimilatory arsenate-respiring prokaryotes catalyze the dissolution, reduction and release of arsenic from paddy soils into groundwater: implication for the effect of sulfate. Ecotoxicology 27, 1126–1136 (2018). https://doi.org/10.1007/s10646-018-1967-8
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DOI: https://doi.org/10.1007/s10646-018-1967-8