Skip to main content
SpringerLink
Log in

Arsenic contamination in areas surrounding mines and selection of potential As-resistant purple nonsulfur bacteria for use in bioremediation based on their detoxification mechanisms

  • Original Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

The objectives of this study were to investigate arsenic (As) contamination in areas surrounding mines in Thailand and to isolate As-resistant purple nonsulfur bacteria (PNSB) for their potential application in microbial As bioremediation. Total As in water and soil samples collected from two As-contaminated sites in Thailand exceeded the standard guidelines. Four strains of As-resistant PNSB were selected from 348 isolates based on their As detoxification mechanisms, including biofilm formation, As redox transformations, glutathione (GSH) production, and production of methylcobalamin (vitamin B12) and S-adenosylmethionine (SAM) for As biomethylation. GSH production in these strains followed the order AB3 > L28 > C1. Strains AB3, C31, and L28 accumulated higher levels of intracellular vitamin B12 than strain C1. However, only strain C1 produced SAM and showed As biovolatilization activity. When strain C1 was incubated under microaerobic light conditions, it produced arsenobetaine [(AsB(V)] in medium with As(III) and monomethylarsonic acid [MMA(V)] in medium with As(V), which were found in the culture supernatants. Volatile methylated As compounds, such as dimethylarsenic acid [DMA(V)] and MMA(V)], were also detected in strain C1 during 30 days of incubation with As(III) and As(V). Strains AB3, C1, and L28 were identified as Rhodopseudomonas palustris and strain C31 as Rubrivivax benzoatilyticus. The resistance of these strains to As [As(III) and As(V)] based on minimum inhibition concentration values under aerobic dark and microaerobic light conditions, respectively, was in the order of C1 > AB3 > C31 > L28. The overall results demonstrate that all four selected strains of PNSB have a great potential for future application in the remediation of As-contaminated areas although R. palustris C1 was the most effective candidate.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

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

    CAS  PubMed  Google Scholar 

  • Bahar M, Megharaj M, Naidu R (2013) Bioremediation of arsenic-contaminated water: recent advances and future prospects. Water Air Soil Pollut 224:1722

    Article  Google Scholar 

  • Bahar MM, Megharaj M, Naidu R (2016) Influence of phosphate on toxicity and bioaccumulation of arsenic in a soil isolate of microalga Chlorella sp. Environ Sci Pollut Res 23:2663–2668

    Article  CAS  Google Scholar 

  • Barnett V (2005) Environmental statistics: methods and spplications. John Wiley & Sons, Chichester. doi: 10.1002/0470024747

  • Basturea GN, Harris TK, Deutscher MP (2012) Growth of bacterium that apparently uses arsenic instead of phosphorus is a consequence of massive ribosome breakdown. J Biol Chem 287:28816–28819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blecker PM, Hakvoort W, Bliek M, Souer E, Schart H (2006) Enhanced arsenate reduction by a CDC25-like tyrosine phosphatase explains increased phytochelation accumulation in arsenate-tolerant Holcuslanatus. Plant J45:917–929

    Article  Google Scholar 

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

  • Harrington C, Brima EI, Jenkins RO (2008) Biotransformation of arsenobetaine by microorganisms from the human gastrointestinal tract. Chem Spec Bioavailab 20(3):173–180

    Article  CAS  Google Scholar 

  • Hudson-Edwards KA, Santini JM (2013) Arsenic-microbe-mineral interaction in mining-affected environments. Minerals 3:337–351

    Article  Google Scholar 

  • Hugenschmidt S, Schwenninger SM, Gnehm N, Lacroix C (2010) Screening of a natural biodiversity of lactic acid and propionic acid bacteria for folate and vitamin B12 production in supplemented whey permeate. Int Dairy J 20:852–857

    Article  CAS  Google Scholar 

  • Imhoff JF, Trüper HG (2005) Bergey’s manual of determinative bacteriology, vol. 2, 2nd edn. Michigan State University, East Lansing

    Google Scholar 

  • Jackson CR, Harrison KG, Dugas SL (2005) Enumeration and characterization of culturable arsenate resistant bacteria in large estuary. Syst Appl Microbiol 28:727–734

    Article  CAS  PubMed  Google Scholar 

  • James GS (2010) Universal Bacterial Identification by PCR and DNA Sequencing of 16S rRNA Gene. In: Schuller M, Sloots TP, James SG, Halliday CL, Carter Ian WJ (eds) PCR for clinical microbiology. Springer, New York, pp 209–214

    Chapter  Google Scholar 

  • Jeong Y, Maohong F, Leeuwen JV, Belczyk JF (2007) Effect of competing solute on arsenic (V) adsorption using iron and aluminum oxides. J Environ Sci 19:910–919

    Article  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kantachote D, Torpee S, Umsakul K (2005) The potential use of anoxygenic phototrophic bacteria for treating latex rubber sheet wastewater. Electron J Biotechnol 8:314–323

    Article  CAS  Google Scholar 

  • Kantachote D, Nunkaew T, Kantha T, Chaiprapat S (2016) Biofertilizers from Rhodopseudomonas palustris strains to enhance rice yields and reduce methane emissions. Appl Soil Ecol 100:154–161

    Article  Google Scholar 

  • Kantha T, Kantachote D, Klongdee N (2015) Potential of biofertilizers from selected Rhodopseudomonas palustris strains to assist rice (Oryza sativa L. subsp. indica) growth under salt stress and to reduce greenhouse gas emissions. Ann Microbiol 65:2109–2118

    Article  Google Scholar 

  • Katrusiak AE, Paterson PG, Kamencic H, ShokerA LAL (2001) Pre-Column derivatization high-performance liquid chromatographic method for determination of cysteine, cysteinyl-glycine, homocysteine and glutathione in plasma and cell extract. J Chromatogr B 758:207–212

    Article  CAS  Google Scholar 

  • Khan H, Khan M, Khan BA, Wahab A, Jan SU, Mukhtair M, Ullah N, Haque N, Fair A (2012) Oxidation of glutathione (GSH) in blood plasma due to oxidative stressors: A case study of silver. J Pharm Pharmacol 6:1502–1507

    CAS  Google Scholar 

  • Krömer JO, Heinzle E, Wittman C (2006) Quantification of S-adenosylmethione in microbial cell extracts. Biotechnol Lett 28:69–71

  • Leist M, Casey RJ, Caridi D (2000) The management of arsenic wastes: problem and prospects. J Hazard Mater 76:125–138

    Article  CAS  PubMed  Google Scholar 

  • Mandal BK, Suzuki KT (2002) Arsenic round the world: a review. Talanta 58:201–235

    Article  CAS  PubMed  Google Scholar 

  • Merrite JH, Kadouri DE, O’Tool GA (2011) Growing and analyzing static biofilms. Curr Protoc Microbiol 22:1B.1.1–1B.1.18

    Article  Google Scholar 

  • Michel C, Jean M, Coulon S (2007) Biofilms of As (III) oxidizing bacteria: formation and activity studies for bioremediation process development. Appl Microbiol Biotechnol 77:457–467

    Article  CAS  PubMed  Google Scholar 

  • Murray LA, Raab A, Marr IL, Feldmann J (2003) Biotransformation of arsenate to arsenosugars by Chlorella vulgaris. Appl Organomet Chem 17:669–674

    Article  CAS  Google Scholar 

  • Naidu R, Bhattacharya P (2009) Arsenic in the environment—risks and management strategies. Environ Geochem Health 31:1–8

    Article  CAS  PubMed  Google Scholar 

  • Ngu TT, Easton A, Stillman MJ (2008) Kinetic analysis of Arsenic-metalation of human metallothionein: significance of two domain structure. J Am Chem Soc 130:17016–17028

    Article  CAS  PubMed  Google Scholar 

  • Nunkaew T, Kantachote D, Nitoda T, Kanzaki H (2015a) Selection of salt tolerant purple nonsulfur bacteria producing 5-aminolevulinic acid (ALA) and reducing methane emissions from microbial rice straw degradation. Appl Soil Ecol 86:113–120

    Article  Google Scholar 

  • Nunkaew T, Kantachote D, Nitoda T, Kanzaki H, Ritchie RJ (2015b) Characterization of exopolymeric substances from selected Rhodopseudomonas palustris strains and their ability to adsorb sodium ions. Carbohydr Polym 115:334–341

    Article  CAS  PubMed  Google Scholar 

  • Panwichian S, Kantachote D, Wittayaweerasak B, Mallavarapu M (2011) Removal of heavy metals by exopolymeric substances produced by resistant purple nonsulfur bacteria isolated from contaminated shrimp ponds. Electron J Biotechnol 14(4). doi:10.2225/vol14-issue4-fulltext-2

  • Pawlik-Skowrońska B, Pirszel J, Kalinowska R, Skowroński T (2004) Arsenic availability toxicity and direct role of GSH and phytochelatins in As detoxification in green alga Stichococcus bacillaris. Aquat Toxicol 70:201–212

    Article  PubMed  Google Scholar 

  • Pollution Control Department (2004) Soil quality standard. Thailand Minister of Environmental and Natural Resources. National Environment Committee 25:170–181 Available at: http://www.pcd.go.th/info_serv/en_reg_std_soil01.html

  • 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-adenosylmethionemethyltansferase. Proc Natl Acad Sci USA 103:2075–2080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rahman I, Kode A, Biswas SK (2007) Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc 1:3159–3165

    Article  Google Scholar 

  • Rahman MM, Owens G, Naidu R (2009a) Arsenic levels in rice grain and assessment of daily dietary intake of arsenic from rice in arsenic-contaminated regions of Bangladesh—implications to groundwater irrigation. Environ Geochem Health 31:179–187

    Article  CAS  PubMed  Google Scholar 

  • Rahman MM, Ng J, Naidu R (2009b) Chronic exposure of arsenic via drinking water and its adverse health impacts on humans. Environ Geochem Health 31:189–200

    Article  CAS  PubMed  Google Scholar 

  • Rouhier N, Lemaire SD, Jacquot JP (2008) Photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annu Rev Plant Physiol 59:143–166

    CAS  Google Scholar 

  • Simeonova DD, Lievremont D, Lagarde F, Muller DA, Groudeva VI, Lett MC (2004) Microplate screening assay for the detection of arsenite-oxidazing and arsenate-reducing bacteria. FEMS Microbiol Lett 237:249–253

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  PubMed  Google Scholar 

  • Tsai SL, Singh S, Chen W (2009) Arsenic metabolism by microbes in nature and the impact on arsenic remediation. Biotechnol J 20:659–667

    CAS  Google Scholar 

  • Vahidnia A, Van der Voct GB, de Wolf FA (2007) Arsenic neurotoxicity—a review. Hum Exp Toxicol 26:823–832

    Article  CAS  PubMed  Google Scholar 

  • Webb S, Bartos J, Boles R, Hasty E, Thuotte E, Thiex NJ (2014) Simultaneous determination of arsenic, cadmium, calcium, chromium, cobalt, copper, iron, lead, magnesium, manganese, molybdenum, nickel, selenium, and zinc in fertilizers by microwave acid digestion and inductively coupled plasma-optical emission spectrometry detection: single-laboratory validation of a modification and extension of AOAC 2006.03. J AOAC Int 97:700–711

    Article  CAS  PubMed  Google Scholar 

  • Yamamura S, Ike M, Fujita M (2003) Dissimilatory arsenate reduction by a facultative anaerobe, Bacillus sp. strain SF-1. J Biosci Bioeng 96:454–460

    Article  CAS  PubMed  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 

Download references

Acknowledgments

This study was supported by Thailand Research Fund, Royal Golden Jubilee Ph.D. Program, Grant No. : PHD/0056/2553) and partly supported by Graduate School, Prince of Songkla University. We thank Dr. Brian Hodgson for assistance with the English.

Author information

Authors and Affiliations

  1. Department of Microbiology, Faculty of Science, Prince of Songkla University, Hat Yai, 90112, Thailand

    Phitthaya Nookongbut & Duangporn Kantachote

  2. Center of Excellence on Hazardous Substance Management (HSM), Bangkok, 10330, Thailand

    Duangporn Kantachote

  3. Global Centre for Environmental Remediation, Faculty of Science and Information Technology, The University of Newcastle, Callaghan, NSW, 2308, Australia

    Mallavarapu Megharaj

  4. Cooperative Research Centre for Contamination Assessment and Remediation of the Environment (CRC-CARE), The University of Newcastle, Callaghan, NSW, 2308, Australia

    Mallavarapu Megharaj

Authors
  1. Phitthaya Nookongbut
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Duangporn Kantachote
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mallavarapu Megharaj
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Duangporn Kantachote.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nookongbut, P., Kantachote, D. & Megharaj, M. Arsenic contamination in areas surrounding mines and selection of potential As-resistant purple nonsulfur bacteria for use in bioremediation based on their detoxification mechanisms. Ann Microbiol 66, 1419–1429 (2016). https://doi.org/10.1007/s13213-016-1229-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-016-1229-z

Keywords

Search

Navigation