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Microbial arsenite oxidation with oxygen, nitrate, or an electrode as the sole electron acceptor

  • Environmental Microbiology - Original Paper
  • Published:
Journal of Industrial Microbiology & Biotechnology

Abstract

The purpose of this study was to identify bacteria that can perform As(III) oxidation for environmental bioremediation. Two bacterial strains, named JHS3 and JHW3, which can autotrophically oxidize As(III)–As(V) with oxygen as an electron acceptor, were isolated from soil and water samples collected in the vicinity of an arsenic-contaminated site. According to 16S ribosomal RNA sequence analysis, both strains belong to the ɤ-Proteobacteria class and share 99% sequence identity with previously described strains. JHS3 appears to be a new strain of the Acinetobacter genus, whereas JHW3 is likely to be a novel strain of the Klebsiella genus. Both strains possess the aioA gene encoding an arsenite oxidase and are capable of chemolithoautotrophic growth in the presence of As(III) up to 10 mM as a primary electron donor. Cell growth and As(III) oxidation rate of both strains were significantly enhanced during cultivation under heterotrophic conditions. Under anaerobic conditions, only strain JHW3 oxidized As(III) using nitrate or a solid-state electrode of a bioelectrochemical system as a terminal electron acceptor. Kinetic studies of As(III) oxidation under aerobic condition demonstrated a higher V max and K m from strain JHW3 than strain JHS3. This study indicated the potential application of strain JHW3 for remediation of subsurface environments contaminated with arsenic.

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References

  1. Ai LN, Sato A, Inoue D, Sei K, Soda S, Ike M (2012) Enrichment of arsenite oxidizing bacteria under autotrophic conditions and the isolation and characterization of facultative chemolithoautotrophic arsenite oxidizing bacteria for removal of arsenic from groundwater. Water Sci Technol Water Supply 12:707–714. doi:10.2166/ws.2012.045

    Article  CAS  Google Scholar 

  2. Bahar MM, Megharaj M, Naidu R (2012) Arsenic bioremediation potential of a new arsenite-oxidizing bacterium Stenotrophomonas sp. MM-7 isolated from soil. Biodegradation 23:803–812. doi:10.1007/s10532-012-9567-4

    Article  CAS  PubMed  Google Scholar 

  3. Bahar MM, Megharaj M, Naidu R (2013) Bioremediation of arsenic-contaminated water: recent advances and future prospects. Water Air Soil Pollut 224:1722. doi:10.1007/s11270-013-1722-y

    Article  Google Scholar 

  4. Bahar MM, Megharaj M, Naidu R (2013) Kinetics of arsenite oxidation by Variovorax sp. MM-1 isolated from a soil and identification of arsenite oxidase gene. J Hazard Mater 262:997–1003. doi:10.1016/j.jhazmat.2012.11.064

    Article  CAS  PubMed  Google Scholar 

  5. Balch WE, Fox GE, Magrum LJ, Woese CR, Wolfe RS (1979) Methanogens: reevaluation of a unique biological group. Microbiol Rev 43:260–296

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Battaglia-Brunet F, Dictor M-C, Garrido F, Crouzet C, Morin D, Dekeyser K, Clarens M, Baranger P (2002) An arsenic(III)-oxidizing bacterial population: selection, characterization, and performance in reactors. J Appl Microbiol 93:656–667. doi:10.1046/j.1365-2672.2002.01726.x

    Article  CAS  PubMed  Google Scholar 

  7. Berg M, Stengel C, Pham TKT, Pham HV, Sampson ML, Leng M, Samreth S, Fredericks D (2007) Magnitude of arsenic pollution in the Mekong and Red River Deltas—Cambodia and Vietnam. Sci Total Environ 372:413–425. doi:10.1016/j.scitotenv.2006.09.010

    Article  CAS  PubMed  Google Scholar 

  8. Bernhardt PV, Santini JM (2006) Protein film voltammetry of arsenite oxidase from the chemolithoautotrophic arsenite-oxidizing bacterium NT-26. Biochemistry 45:2804–2809. doi:10.1021/bi0522448

    Article  CAS  PubMed  Google Scholar 

  9. Butt AS, Rehman A (2011) Isolation of arsenite-oxidizing bacteria from industrial effluents and their potential use in wastewater treatment. World J Microbiol Biotechnol 27:2435–2441. doi:10.1007/s11274-011-0716-4

    Article  CAS  Google Scholar 

  10. Chang J-S, Yoon I-H, Lee J-H, Kim K-R, An J, Kim K-W (2010) Arsenic detoxification potential of aox genes in arsenite-oxidizing bacteria isolated from natural and constructed wetlands in the Republic of Korea. Environ Geochem Health 32:95–105. doi:10.1007/s10653-009-9268-z

    Article  CAS  PubMed  Google Scholar 

  11. Chen W, Parette R, Zou J, Cannon FS, Dempsey BA (2007) Arsenic removal by iron-modified activated carbon. Water Res 41:1851–1858. doi:10.1016/j.watres.2007.01.052

    Article  CAS  PubMed  Google Scholar 

  12. Chitpirom K, Akaracharanya A, Tanasupawat S, Leepipatpiboon N, Kim KW (2009) Isolation and characterization of arsenic resistant bacteria from tannery wastes and agricultural soils in Thailand. Ann Microbiol 59:649–656. doi:10.1007/BF03179204

    Article  CAS  Google Scholar 

  13. Choong TSY, Chuah TG, Robiah Y, Gregory Koay FL, Azni I (2007) Arsenic toxicity, health hazards and removal techniques from water: an overview. Desalination 217:139–166. doi:10.1016/j.desal.2007.01.015

    Article  CAS  Google Scholar 

  14. Daware V, Kesavan S, Patil R, Natu A, Kumar A, Kulkarni M, Gade W (2012) Effects of arsenite stress on growth and proteome of Klebsiella pneumoniae. J Biotechnol 158:8–16. doi:10.1016/j.jbiotec.2011.12.013

    Article  CAS  PubMed  Google Scholar 

  15. Dong D, Ohtsuka T, Dong DT, Amachi S (2014) Arsenite oxidation by a facultative chemolithoautotrophic Sinorhizobium sp. KGO-5 isolated from arsenic-contaminated soil. Biosci Biotechnol Biochem 78:1963–1970. doi:10.1080/09168451.2014.940276

    Article  CAS  PubMed  Google Scholar 

  16. Drewniak L, Sklodowska A (2013) Arsenic-transforming microbes and their role in biomining processes. Environ Sci Pollut Res 20:7728–7739. doi:10.1007/s11356-012-1449-0

    Article  CAS  Google Scholar 

  17. Ehrlich HL, Newman DK (2009) Geomicrobiology, 5th edn. CRC Press, New York

    Google Scholar 

  18. Garcia-Dominguez E, Mumford A, Rhine ED, Paschal A, Young LY (2008) Novel autotrophic arsenite-oxidizing bacteria isolated from soil and sediments. FEMS Microbiol Ecol 66:401–410. doi:10.1111/j.1574-6941.2008.00569.x

    Article  CAS  PubMed  Google Scholar 

  19. Garelick H, Dybowska A, Valsami-Jones E, Priest N (2005) Remediation technologies for arsenic contaminated drinking waters. J Soils Sediments 5:182–190. doi:10.1065/jss2005.06.140

    Article  CAS  Google Scholar 

  20. Gossett JM (2010) Sustained aerobic oxidation of vinyl chloride at low oxygen concentrations. Environ Sci Technol 44:1405–1411. doi:10.1021/es9033974

    Article  CAS  PubMed  Google Scholar 

  21. Inskeep WP, Macur RE, Hamamura N, Warelow TP, Ward SA, Santini JM (2007) Detection, diversity and expression of aerobic bacterial arsenite oxidase genes. Environ Microbiol 9:934–943. doi:10.1111/j.1462-2920.2006.01215.x

    Article  CAS  PubMed  Google Scholar 

  22. Ito A, Miura J-I, Ishikawa N, Umita T (2012) Biological oxidation of arsenite in synthetic groundwater using immobilised bacteria. Water Res 46:4825–4831. doi:10.1016/j.watres.2012.06.013

    Article  CAS  PubMed  Google Scholar 

  23. Jain C, Ali I (2000) Arsenic: occurrence, toxicity and speciation techniques. Water Res 34:4304–4312. doi:10.1016/S0043-1354(00)00182-2

    Article  CAS  Google Scholar 

  24. Jukes TH, Cantor CR (1969) Evolution of protein molecule. In: Munro HN (ed) Mamm. protein Metab. Academic Press, New York, pp 21–132

    Chapter  Google Scholar 

  25. Liu L, Li FB, Feng CH, Li XZ (2009) Microbial fuel cell with an azo-dye-feeding cathode. Appl Microbiol Biotechnol 85:175–183. doi:10.1007/s00253-009-2147-9

    Article  CAS  PubMed  Google Scholar 

  26. Mandal BK, Suzuki KT (2002) Arsenic round the world: a review. Talanta 58:201–235. doi:10.1016/S0039-9140(02)00268-0

    Article  CAS  PubMed  Google Scholar 

  27. Masscheleyn PH, Delaune RD, Patrick WH (1991) Effect of redox potential and pH on arsenic speciation and solubility in a contaminated soil. Environ Sci Technol 25:1414–1419. doi:10.1021/es00020a008

    Article  CAS  Google Scholar 

  28. Mattes A, Gould D, Taupp M, Glasauer S (2013) A novel autotrophic bacterium isolated from an engineered wetland system links nitrate-coupled iron oxidation to the removal of As, Zn and S. Water Air Soil Pollut 224:1490. doi:10.1007/s11270-013-1490-8

    Article  Google Scholar 

  29. Neff JM (1997) Ecotoxicology of arsenic in the marine environment. Environ Toxicol Chem 16:917–927. doi:10.1002/etc.5620160511

    CAS  Google Scholar 

  30. Nguyen VK, Hong S, Park Y, Jo K, Lee T (2015) Autotrophic denitrification performance and bacterial community at biocathodes of bioelectrochemical systems with either abiotic or biotic anodes. J Biosci Bioeng 119:180–187. doi:10.1016/j.jbiosc.2014.06.016

    Article  CAS  PubMed  Google Scholar 

  31. Nguyen VK, Lee J-U (2014) Isolation and characterization of antimony-reducing bacteria from sediments collected in the vicinity of an antimony factory. Geomicrobiol J 31:855–861. doi:10.1080/01490451.2014.901440

    Article  CAS  Google Scholar 

  32. Nguyen VK, Lee J-U (2015) Antimony-oxidizing bacteria isolated from antimony-contaminated sediment–a phylogenetic study. Geomicrobiol J 32:50–58. doi:10.1080/01490451.2014.925009

    Article  CAS  Google Scholar 

  33. Paulo A (2014) Anaerobic degradation of anionic surfactants by denitrifying bacteria. Wageningen University, Wageningen

    Google Scholar 

  34. Pous N, Casentini B, Rossetti S, Fazi S, Puig S, Aulenta F (2015) Anaerobic arsenite oxidation with an electrode serving as the sole electron acceptor: A novel approach to the bioremediation of arsenic-polluted groundwater. J Hazard Mater 283:617–622. doi:10.1016/j.jhazmat.2014.10.014

    Article  CAS  PubMed  Google Scholar 

  35. Quéméneur M, Heinrich-Salmeron A, Muller D, Lièvremont D, Jauzein M, Bertin PN, Garrido F, Joulian C (2008) Diversity surveys and evolutionary relationships of aoxB genes in aerobic arsenite-oxidizing bacteria. Appl Environ Microbiol 74:4567–4573. doi:10.1128/AEM.02851-07

    Article  PubMed  PubMed Central  Google Scholar 

  36. Rabaey K, Angenent L, Schroder U, Keller J (2010) Bioelectrochemical systems: from extracellular electron transfer to biotechnological application. IWA Publishing, London

    Google Scholar 

  37. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  38. Sánchez JA, Rivas BL, Pooley SA, Basaez L, Pereira E, Pignot-Paintrand I, Bucher C, Royal G, Saint-Aman E, Moutet J-C (2010) Electrocatalytic oxidation of As(III) to As(V) using noble metal–polymer nanocomposites. Electrochim Acta 55:4876–4882. doi:10.1016/j.electacta.2010.03.080

    Article  Google Scholar 

  39. Santini JM, Sly LI, Schnagl RD, Macy JM (2000) A new chemolithoautotrophic arsenite-oxidizing bacterium isolated from a gold mine: phylogenetic, physiological, and preliminary biochemical studies. Appl Environ Microbiol 66:92–97. doi:10.1128/AEM.66.1.92-97.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Smith AH, Hopenhayn-Rich C, Bates MN, Goeden HM, Hertz-Picciotto I, Duggan HM, Wood R, Kosnett MJ, Smith MT (1992) Cancer risks from arsenic in drinking water. Environ Health Perspect 97:259–267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Vadahanambi S, Lee S-H, Kim W-J, Oh I-K (2013) Arsenic removal from contaminated water using three-dimensional graphene-carbon nanotube-iron oxide nanostructures. Environ Sci Technol 47:10510–10517. doi:10.1021/es401389g

    CAS  PubMed  Google Scholar 

  43. WHO (2011) Arsenic in drinking water. WHO Press, Geneva

    Google Scholar 

  44. Winkel LHE, Pham TKT, Vi ML, Stengel C, Amini M, Nguyen TH, Pham HV, Berg M (2011) Arsenic pollution of groundwater in Vietnam exacerbated by deep aquifer exploitation for more than a century. Proc Natl Acad Sci U S A 108:1246–1251. doi:10.1073/pnas.1011915108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Zhang J, Zhou W, Liu B, He J, Shen Q, Zhao F-J (2015) Anaerobic arsenite oxidation by an autotrophic arsenite-oxidizing bacterium from an arsenic-contaminated paddy soil. Environ Sci Technol 49:5956–5964. doi:10.1021/es506097c

    Article  CAS  PubMed  Google Scholar 

  46. Zhang L, Zhou S, Zhuang L, Li W, Zhang J, Lu N, Deng L (2008) Microbial fuel cell based on Klebsiella pneumoniae biofilm. Electrochem Commun 10:1641–1643. doi:10.1016/j.elecom.2008.08.030

    Article  CAS  Google Scholar 

  47. Zuckerlandl E, Pauling L (1965) Evolving genes and proteins. Evol Genes Proteins. doi:10.1016/B978-1-4832-2734-4.50017-6

    Google Scholar 

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Acknowledgements

This work was supported by the Financial Supporting Project of Long-term Overseas Dispatch of PNU’s Tenure-track Faculty, 2013.

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Authors and Affiliations

  1. Department of Environmental Engineering, Dong-a University, Busan, 49315, Republic of Korea

    Van Khanh Nguyen

  2. Department of Molecular Biology, Pusan National University, Busan, 46241, Republic of Korea

    Huong T. Tran

  3. Department of Civil and Environmental Engineering, Pusan National University, No. 2 Busandaehak-ro 63beon-gil, Geumjeong-gu, Busan, 46241, Republic of Korea

    Younghyun Park, Jaecheul Yu & Taeho Lee

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  1. Van Khanh Nguyen
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Correspondence to Taeho Lee.

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Nguyen, V.K., Tran, H.T., Park, Y. et al. Microbial arsenite oxidation with oxygen, nitrate, or an electrode as the sole electron acceptor. J Ind Microbiol Biotechnol 44, 857–868 (2017). https://doi.org/10.1007/s10295-017-1910-7

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