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Unique diversity and functions of the arsenic-methylating microorganisms from the tailings of Shimen Realgar Mine

Ecotoxicology volume 29, pages 86–96 (2020)Cite this article

Abstract

Microbial arsenic (As) methylation plays important roles in the As biogeochemical cycle. However, little is known about the diversity and functions of As-methylating microorganisms from the tailings of a Realgar Mine, which is characterized as containing extremely high concentrations of As. To address this issue, we collected five samples (T1–T5) from the tailings of Shimen Realgar Mine. Microcosm assays without addition of exogenous As and carbon indicated that all the five samples possess significant As-methylating activities, producing 0.8–5.7 μg/L DMAsV, and 1.1–10.7 μg/L MMAsV with an exception of T3, from which MMAsV was not detectable after 14.0 days of incubation. In comparison, addition of 20.0 mM lactate to the microcosms significantly enhanced the activities of these samples; the produced DMAsV and MMAsV are 8.0–39.7 μg/L and 5.8–38.3 μg/L, respectively. The biogenic DMAsV shows significant positive correlations with the Fe concentrations and negative correlations with the total nitrogen concentrations in the environment. A total of 63 different arsM genes were identified from the five samples, which code for new or new-type ArsM proteins, suggesting that a unique diversity of As-methylating microbes are present in the environment. The microbial community structures of the samples were significantly shaped by the environmental total organic carbon, total As contents and NO3− contents. These data help to better understand the microorganisms-catalyzed As methylation occurred in the environment with extremely high contents of As.

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References

  • Ajees AA, Marapakala K, Packianathan C, Sankaran B, Rosen BP (2012) Structure of an As(III) S-adenosylmethionine methyltransferase: insights into the mechanism of arsenic biotransformation. Biochemistry 51:5476–5485

    CAS  Google Scholar 

  • Bagade AV, Bachate SP, Dholakia BB, Giri AP, Kodam KM (2016) Characterization of Roseomonas and Nocardioides spp. for arsenic transformation. J Hazard Mater 318:742–750

    CAS  Google Scholar 

  • Bhattacharya P, Welch AH, Stollenwerk KG, McLaughlin MJ, Bundschuh J, Panaullah G (2007) Arsenic in the environment: biology and chemistry. Sci Total Environ 379(2):109–120

    CAS  Google Scholar 

  • Broderick KE, Singh V, Zhuang S, Kambo A, Chen JC, Sharma VS, Pilz RB, Boss GR (2005) Nitric oxide scavenging by the coba-613 lamin precursor cobinamide. J Biol Chem 280:8678–8685

    CAS  Google Scholar 

  • Cai L, Yu K, Yang Y, Chen BW, Li XD, Zhang T (2013) Metagenomic exploration reveals high levels of microbial arsenic metabolism genes in activated sludge and coastal sediments. Appl Microbiol Biotechnol 97:9579–9588

    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

    CAS  Google Scholar 

  • Chen X, Zeng XC, Wang J, Deng Y, Ma T, Guoji E et al. (2017) Microbial communities involved in arsenic mobilization and release from the ndeep sediments into groundwater in Jianghan plain, Central China. Sci Total Environ 579:989–999

    CAS  Google Scholar 

  • Fisher JC, Hollibaugh JT (2008) Selenate-dependent anaerobic arsenite oxidation by a bacterium from Mono Lake, California. Appl Environ Microbiol 74:2588–2594

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Huang K, Xu Y, Zhang J, Chen C, Gao F, Zhao FJ (2017) Arsenicibacter rosenii gen. nov. sp. nov. an efficient arsenic methylating and volatilizing bacterium isolated from an arsenic-contaminated paddy soil. Int J Syst Evol Microbiol 67:3186–3191

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Kim DJ, Lee DI, Keller J (2006) Effect of temperature and free ammonia on nitrification and nitrite accumulation in landfill leachate and analysis of its nitrifying bacterial community by FISH. Bioresour Technol 97:459–468

    CAS  Google Scholar 

  • Kudo K, Yamaguchi N, Makino T, Ohtsuka T, Kimura K, Dong DT et al. (2013) Release of arsenic from soil by a novel dissimilatory arsenate-reducing bacterium, Anaeromyxobacter sp. strain PSR-1. Appl Environ Microbiol 79:4635–4642

    CAS  Google Scholar 

  • Kulp TR (2014) Early earth: arsenic and primordial life. Nat Geosci 7:785–786

    CAS  Google Scholar 

  • Kuramata M, Sakakibara F, Kataoka R, Abe T, Asano M, Baba K et al. (2015) Arsenic biotransformation by Streptomyces sp. isolated from rice rhizosphere. Environ Microbiol 17:1897–1909

    CAS  Google Scholar 

  • Lear G, Song B, Gault AG, Polya DA, Lloyd JR (2007) Molecular analysis of arsenate-reducing bacteria within Cambodian sediments following amendment with acetate. Appl Environ Microbiol 73:1041–1048

    CAS  Google Scholar 

  • Li H, Zeng XC, He Z, Chen X, Guoji E, Han Y, Wang Y (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

    CAS  Google Scholar 

  • Maguffin SC, Kirk MF, Daigle AR, Hinkle SR, Jin Q (2015) Substantial contribution of biomethylation to aquifer arsenic cycling. Nat Geosci 8(4):290–293

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Nordstrom DK (2002) Public health: worldwide occurrences of arsenic in ground water. Science 296:2143–2145

    CAS  Google Scholar 

  • Ohtsuka T, Yamaguchi N, Makino T, Sakurai K, Kimura K, Kudo K et al. (2013) Arsenic dissolution from Japanese paddy soil by a dissimilatory arsenate-reducing bacterium Geobacter sp. OR-1. Environ Sci Technol 47:6263–6271

    CAS  Google Scholar 

  • Oremland RS, Stolz JF (2003) The ecology of arsenic. Science 300:939–944

    CAS  Google Scholar 

  • Osborne Kulp 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

    Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Reid MC, Maillard J, Bagnoud A, Falquet L, Le VP, Bernierlatmani R (2017) Arsenic methylation dynamics in a rice paddy soil anaerobic enrichment culture. Environ Sci Technol 51:10546–10554

    CAS  Google Scholar 

  • Rhine ED, Onesios KM, Serfes ME, Reinfelder JR, Young LY (2008) Arsenic transformation and mobilization from minerals by the arsenite oxidizing strain WAO. Environ Sci Technol 42:1423–1429

    CAS  Google Scholar 

  • Schaefer MV, Ying SC, Benner SG, Duan Y, Wang Y, Fendorf S (2016) Aquifer arsenic cycling induced by seasonal hydrologic changes within the Yangtze River basin. Environ Sci Technol 50:3521–3529

    CAS  Google Scholar 

  • Shi W, Wu W, Zeng XC, Chen X, Zhu X, Cheng S (2018) 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

    CAS  Google Scholar 

  • Singh R, Singh S, Parihar P, Singh V, Prasad S (2015) Arsenic contamination, consequences and remediation techniques: a review. Ecotoxicol Environ Saf 112:247–270

    CAS  Google Scholar 

  • Slyemi D, Bonnefoy V (2012) How prokaryotes deal with arsenic. Environ Microbiol Rep. 4:571–586

    CAS  Google Scholar 

  • Song B, Chyun E, Jaffé PR, Ward BB (2009) Molecular methods to detect and monitor dissimilatory arsenate-respiring bacteria (DARB) in sediments. FEMS Microb Ecol 68:108–117

    CAS  Google Scholar 

  • Srivastava PK, Vaish A, Dwivedi S, Chakrabarty D, Singh N, Tripathi RD (2011) Biological removal of arsenic pollution by soil fungi. Sci Total Environ 409:2430–2442

    CAS  Google Scholar 

  • Sun W, Sierraalvarez R, Field JA (2011) Long term performance of an arsenite-oxidizing-chlorate-reducing microbial consortium in an upflow anaerobic sludge bed (uasb) bioreactor. Bioresour Technol 102:5010–5016

    CAS  Google Scholar 

  • Wang J, Wu M, Gan L, Si Y (2016) Biotransformation and biomethylation of arsenic by Shewanella oneidensis MR-1. Chemosphere 145:329–335

    CAS  Google Scholar 

  • Wang J, Zeng XC, Zhu X, Chen 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 Hazard Mater 339:409–417

    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

    CAS  Google Scholar 

  • Wang PP, Sun GX, Zhu YG (2014) Identification and characterization of the arsenite methyltransferase from an archaeon, Methanosarcina acetivorans C2A. Environ Sci Technol 48(21):12706–12713

    CAS  Google Scholar 

  • Wu X, Zhang H, Chen J et al. (2016) Comparison of the fecal microbiota of dholes high-throughput Illumina sequencing of the V3–V4 region of the 16S rRNA gene. Appl Microbiol Biotechnol 100(8):3577–3586

    CAS  Google Scholar 

  • Xue XM, Ye J, Raber G et al. (2017) Arsenic methyltransferase is involved in arsenosugar biosynthesis by providing dma. Environ. Sci. Technol 51:1224–1230

    CAS  Google Scholar 

  • Yang Y, Mu Y, Zeng XC, Wu W, Yuan J, Liu Y et al. (2017) Functional genes and thermophilic microorganisms responsible for arsenite oxidation from the shallow sediment of an untraversed hot spring outlet. Ecotoxicology 26:490–501

    CAS  Google Scholar 

  • Ye J, Chang Y, Yan Y et al. (2014) Identification and characterization of the arsenite methyltransferase from a protozoan, Tetrahymena pyriformis. Aquat Toxicol 149(1):50–57

    CAS  Google Scholar 

  • Zeng XC, EG, Wang J, Wang N, Chen X, Mu Y, Li H, Yang Y, Liu 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 Microbiol 82:7019–7029

    CAS  Google Scholar 

  • Zeng XC, He Z, Chen X, Cao QAD, Li H, Wang Y (2018a) Effects of arsenic on the biofilm formations of arsenite-oxidizing bacteria. Ecotoxicol Environ Saf 165:1–10

    CAS  Google Scholar 

  • Zeng XC, Yang Y, Shi W, Peng Z, Chen X, Zhu X, Wang Y (2018b) Microbially mediated methylation of arsenic in the arsenic-rich soils and sediments of Jianghan plain. Front Microbiol 9:1389

    Google Scholar 

  • Zhai W, Wong MT, Luo F, Hashmi MZ, Liu X, Edwards EA et al. (2017) Arsenic methylation and its relationship to abundance and diversity of ARSM genes in composting manure. Sci Rep. 7:42198

    Google Scholar 

  • Zhang J, Cao T, Tang Z, Shen Q, Rosen BP, Zhao FJ (2015b) Arsenic methylation and volatilization by arsenite S-adenosylmethionine methyltransferase in Pseudomonas alcaligenes NBRC14159. Appl Environ Microbiol 81:2852–2860

    CAS  Google Scholar 

  • Zhang J, Zhou W, Liu B, He J, Shen Q, Zhao FJ (2015a) Anaerobic arsenite oxidation by an autotrophic arsenite-oxidizing bacterium from an arsenic-contaminated paddy soil. Environ Sci Technol 49:5956–5964

    CAS  Google Scholar 

  • Zhang SY, Su JQ, Sun GX, Yang Y, Zhao Y, Ding J et al. (2017) Land scale biogeography of arsenic biotransformation genes in estuarine wetland. Environ Microbiol 19:2468–2482

    CAS  Google Scholar 

  • Zhu X, Wang R, Lu X, Liu H, Li J, Ouyang B, Lu J (2015) Secondary minerals of weathered orpiment-realgar-bearing tailings in Shimen carbonate-type realgar mine, Changde, Central China. Miner Petrol 109:1–15

    Google Scholar 

  • Zhu X, Zeng XC, Chen X, Wu W, Wang Y (2019) Inhibitory effect of nitrate/nitrite on the microbial reductive dissolution of arsenic and iron from soils into pore water. Ecotoxicology 28:528–538

    CAS  Google Scholar 

  • Zhu YG, Xue XM, Kappler A, Rosen BP, Meharg AA (2017) Linking genes to microbial biogeochemical cycling: lessons from arsenic. Environ Sci Technol 51:7326–7339

    CAS  Google Scholar 

  • Zhu YG, Yoshinaga M, Zhao FJ, Rosen BP (2014) Earth abides arsenic biotransformations. Annu Rev Earth Planet Sci 42:443–467

    CAS  Google Scholar 

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Acknowledgements

This work was supported by the General Programs and the Foundations for Innovative Research Groups from the National Natural Science Foundation of China (grant nos. 41472257, 41521001), and the Fundamental Research Funds for the Central Universities, China University of Geosciences (Wuhan) (grant no. CUGCJ1702).

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  1. State Key Laboratory of Biogeology and Environmental Geology & School of Environmental Studies, China University of Geosciences, Wuhan, PR China

    Janet Victoria Ngegla, Xing Zhou, Xiaoming Chen, Xianbin Zhu, Ziwei Liu, Jilong Feng & Xian-Chun Zeng

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  1. Janet Victoria Ngegla
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Correspondence to Xian-Chun Zeng.

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Ngegla, J.V., Zhou, X., Chen, X. et al. Unique diversity and functions of the arsenic-methylating microorganisms from the tailings of Shimen Realgar Mine. Ecotoxicology 29, 86–96 (2020). https://doi.org/10.1007/s10646-019-02144-9

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Keywords

  • Arsenic methylation
  • ArsM
  • Microbially As methylation
  • Shimen Realgar Mine
  • Arsenic contaminated soils