Skip to main content
SpringerLink
Log in

Characterization of the arsenite oxidizer Aliihoeflea sp. strain 2WW and its potential application in the removal of arsenic from groundwater in combination with Pf-ferritin

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

A heterotrophic arsenite-oxidizing bacterium, strain 2WW, was isolated from a biofilter treating arsenic-rich groundwater. Comparative analysis of 16S rRNA gene sequences showed that it was closely related (98.7 %) to the alphaproteobacterium Aliihoeflea aesturari strain N8T. However, it was physiologically different by its ability to grow at relatively low substrate concentrations, low temperatures and by its ability to oxidize arsenite. Here we describe the physiological features of strain 2WW and compare these to its most closely related relative, A. aestuari strain N8T. In addition, we tested its efficiency to remove arsenic from groundwater in combination with Pf-ferritin. Strain 2WW oxidized arsenite to arsenate between pH 5.0 and 8.0, and from 4 to 30 °C. When the strain was used in combination with a Pf-ferritin-based material for arsenic removal from natural groundwater, the removal efficiency was significantly higher (73 %) than for Pf-ferritin alone (64 %). These results showed that arsenite oxidation by strain 2WW combined with Pf-ferritin-based material has a potential in arsenic removal from contaminated groundwater.

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

  • Achour AR, Bauda P, Billard P (2007) Diversity of arsenite transporter genes from arsenic-resistant soil bacteria. Res Microbiol 158:128–137

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Aryal M, Liakopoulou-Kyriakides M (2014) Bioremoval of heavy metals by bacterial biomass. Environ Monit Assess 187:4173

    Article  PubMed  Google Scholar 

  • Bachate SP, Cavalca L, Andreoni V (2009) Arsenic-resistant bacteria isolated from agricultural soils of Bangladesh and characterization of arsenate-reducing strains. J Appl Microbiol 107:145–156

    Article  CAS  PubMed  Google Scholar 

  • Bachate SP, Khapare RM, Kodam KM (2012) Oxidation of arsenite by two β-proteobacteria isolated from soil. Appl Microbiol Biotechnol 93:2135–2145

    Article  CAS  PubMed  Google Scholar 

  • Bertin PN, Heinrich-Salmeron A, Pelletier E, Goulhen-Chollet F, Arsene-Ploetze F, Gallien S, Lauga B, Casiot C, Calteau A, Vallenet D, Bonnefoy V, Bruneel O, Chane-Woon-Ming B, Cleiss-Arnold J, Duran R, Elbaz-Poulichet F, Fonknechten N, Giloteaux L, Halter D, Koechler S, Marchal M, Mornico D, Schaeffer C, Smith AAT, Van Dorsselaer A, Weissenbach J, Medigue C, Le Paslier D (2011) Metabolic diversity among main microorganisms inside an arsenic-rich ecosystem revealed by meta- and proteo-genomics. ISME J 5:1735–1747

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cai L, Liu G, Rensing C, Wang G (2009) Genes involved in arsenic transformation and resistance associated with different levels of arsenic contaminated soils. BMC Microbiol 9:4

    Article  PubMed Central  PubMed  Google Scholar 

  • Castillo R, Saier MH Jr (2010) Functional promiscuity of homologues of the bacterial ArsA ATPases. Int J Microbiol. doi:10.1155/2010/187373

    PubMed Central  PubMed  Google Scholar 

  • Cavalca L, Corsini A, Zaccheo P, Andreoni V, Muyzer G (2013a) Microbial transformations of arsenic: perspectives for biological removal of arsenic from water. Future Microbiol 8:753–768

    Article  CAS  PubMed  Google Scholar 

  • Cavalca L, Corsini A, Andreoni V, Muyzer G (2013b) Draft genome sequence of the arsenite-oxidizing strain Aliihoeflea sp 2WW isolated from arsenic-contaminated groundwater. GenomeA 1(6):e01072-13

    Article  PubMed Central  PubMed  Google Scholar 

  • Chitpirom K, Akaracharanya A, Tanasupawat S, Leepipatpiboon N, Kim K-W (2009) Isolation and characterization of arsenic resistant bacteria from tannery wastes and agricultural soils in Thailand. Ann Microbiol 59:649–656

    Article  CAS  Google Scholar 

  • Corsini A, Zaccheo P, Muyzer G, Andreoni V, Cavalca L (2014a) Arsenic transforming abilities of groundwater bacteria and the combined use of Aliihoeflea sp. strain 2WW and goethite in metalloid removal. J Hazard Mater 269:89–97

    Article  CAS  PubMed  Google Scholar 

  • Corsini A, Cavalca L, Muyzer G, Zaccheo P (2014b) Effectiveness of various sorbents and biological oxidation in the removal of arsenic species from groundwater. Environ Chem 11:558–565

    Article  CAS  Google Scholar 

  • Drewniak L, Sklodowska A (2007) Isolation and characterization of a psychrotolerant arsenite-oxidizing bacterium from a gold mine in Zloty Stok. Poland. Adv Mater Res 20–21:575

    Article  Google Scholar 

  • Fan H, Su C, Wang Y, Yao J, Zhao K, Wang Y, Wang G (2008) Sedimentary arsenite-oxidizing and arsenate-reducing bacteria associated with high arsenic groundwater from Shanyin, Northwestern China. J Appl Microbiol 105:529–539

    Article  CAS  PubMed  Google Scholar 

  • Gosh S, Sar P (2013) Identification and characterization of metabolic properties of bacterial populations recovered from arsenic contaminated ground water of North East India (Assam). Water Res 47:6992–7005

    Article  Google Scholar 

  • Heinrich-Salmeron A, Cordi A, Brochier-Armanet C, Halter D, Pagnout C, Abbaszadeh-Fard E, Montaut D, Seby F, Bertin PN, Bauda P, Arsene-Ploetze F (2011) Unsuspected diversity of arsenite-oxidizing bacteria as revealed by widespread distribution of the aoxB gene in Prokaryotes. Appl Environ Microbiol 77:4685–4692

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Huang J-H, Elzinga EJ, Brechbuehl Y, Voegelin A, Kretzschmar R (2011) Impacts of Shewanella putrefaciens strain CN–32 cells and extracellular polymeric substances on the sorption of As(V) and As(III) on Fe(III)-(hydr)oxides. Environ Sci Technol 45:2804–2810

    Article  CAS  PubMed  Google Scholar 

  • Huo YY, Cheng H, Han XF, Jiang XW, Sun C, Zhang XQ, Zhu XF, Liu YF, Li PF, Ni PX, Wu M (2012) Complete genome sequence of Pelagibacterium halotolerans B2(T). J Bacteriol 194:197–198

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ito A, Miura JI, Ishikawa N, Teruyuki U (2012) Biological oxidation of arsenite in synthetic ground water using immobilised bacteria. Water Res 46:4825–4831

    Article  CAS  PubMed  Google Scholar 

  • Jackson CR, Jackson EF, Dugas SL, Gamble K, Williams SE (2003) Microbial transformations of As(III) and As(V) in natural environments. Recent Res Dev Microbiol 7:103–118

    CAS  Google Scholar 

  • Jacobs JF, Hasan MH, Paik KH, Hagen WR, van Loosdrecht MCM (2010) Development of a bionanotechnological phosphate removal system with thermostable ferritin. Biotechnol Bioeng 105:918

    CAS  PubMed  Google Scholar 

  • Kao A-C, Chu Y-J, Hsu F-L, Liao VH-C (2013) Removal of arsenic from groundwater by using a native isolated arsenite-oxidizing bacterium. J Contamin Hydrol 155:1–8

    Article  CAS  Google Scholar 

  • Katsoyiannis IA, Ruettimann T, Hug SJ (2008) pH dependence of Fenton reagent generation and As(III) oxidation and removal by corrosion of zero valent iron in aerated water. Environ Sci Technol 42:7424–7430

    Article  CAS  PubMed  Google Scholar 

  • Kim YT, Yoon H, Yoon C, Woo NC (2007) An assessment of sampling, preservation, and analytical procedures for arsenic speciation in potentially contaminated waters. Environ Geochem Health 29:337–346

    Article  CAS  PubMed  Google Scholar 

  • Kim HC, Lee CG, Park JA, Kim SB (2010) Arsenic removal from water using iron-impregnated granular activated carbon in the presence of bacteria. J Environ Sci Health Part A Tox Hazard Subst Environ Eng 45:177–182

    Article  CAS  Google Scholar 

  • Kruger MC, Bertin PN, Heipieper HJ, Arsène-Ploetze F (2013) Bacterial metabolism of environmental arsenic-mechanisms and biotechnological applications. Appl Microbiol Biotechnol 97:3827–3841

    Article  CAS  PubMed  Google Scholar 

  • Lai Q, Li G, Yu Z, Shao Z (2012) Genome sequence of Nitratireductor indicus type strain C115. J Bacteriol 194:6990

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liao VH, 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  PubMed  Google Scholar 

  • Lieutaud A, van Lis R, Duval S, Capowiez L, Muller D, Lebrun R, Lignon S, Fardeau M-L, Lett M-C, Nitschke W, Schoepp-Cothenet B (2010) Arsenite oxidase from Ralstonia sp. 22. J Biol Chem 285:20433–20441

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lièvremont D, N’negue MA, Behra PH, Lett M-C (2003) Biological oxidation of arsenite: batch reactor experiments in presence of kutnahorite and chabazite. Chemosphere 51:419

    Article  PubMed  Google Scholar 

  • Lugtu RT, Choi SC, Oh YS (2009) Arsenite oxidation by a facultative chemolithotrophic bacterium SDB1 isolated from mine tailing. J Microbiol 47:686–692

    Article  CAS  PubMed  Google Scholar 

  • Mondal P, Majumder CB, Mohanty B (2006) Laboratory based approaches for arsenic remediation from contaminated water: recent developments. J Hazard Mater 137:464–479

    Article  CAS  PubMed  Google Scholar 

  • Muller D, Médigue C, Koechler S, Barbe V, Barakat M, Talla E, Bonnefoy V, Krin E, Arsène-Ploetze F, Carapito C, Chandler M, Cournoyer B, Cruveiller S, Dossat C, Duval S, Heymann M, Leize E, Lieutaud A, Lièvremont D, Makita Y, Mangenot S, Nitschke W, Ortet P, Perdial N, Schoepp B, Siguier P, Simeonova DD, Rouy Z, Segurens B, Turlin E, Vaellenet D, Dorsselaer AV, Weiss S, Weissenbach J, Lett M-C, Danchin A, Bertin PN (2007) A tale of two oxidation states: bacterial colonization of arsenic-rich environments. PLoS Genet 3:0518–0530

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Osborne TH, Jamieson HE, Hudson-Edwards KA, Nordstrom DK, Walker SR, Ward S, Santini JM (2010) Microbial oxidation of arsenite in a subartic environment: diversity of arsenite oxidase genes and identification of a psichrotolerant arsenite oxidizer. BMC Microbiol 10:205–212

    Article  PubMed Central  PubMed  Google Scholar 

  • Pirt SJ (1975) Principles of microbe and cell cultivation. Blackwell Scientific, Oxford

    Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Reise K (2002) Sediment mediated species interactions in coastal waters. J Sea Res 48:127–141

    Article  Google Scholar 

  • Roh SW, Kim KH, Nam YD, Chang HW, Kim MS, Shin KS, Yoon JH, Oh HM, Bae JW (2008) Aliihoeflea aestuarii gen. nov., sp. nov. a novel bacterium isolated from tidal flat sediment. J Microbiol 46:594–598

    Article  CAS  PubMed  Google Scholar 

  • Smedley PL, Kinniburgh DG (2002) A review of the source, behaviour and distribution of arsenic in natural waters. Appl Geochem 17:517–568

    Article  CAS  Google Scholar 

  • Stolz J, Basu P, Oremland RS (2002) Microbial transformation of elements: the case of arsenic and selenium. Int Microbiol 5:201–207

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) Software Version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA for phylogenetic study. J Bacteriol 173:697–703

    CAS  PubMed Central  PubMed  Google Scholar 

  • WHO (2001) Arsenic in drinking water. Fact sheet number 210 2001. Available at http://www.who.int/inf-fs/en/fact210.html Accessed October 2013

Download references

Acknowledgments

This research was supported by CARIPLO Foundation (Project 2010-2221) and by PRIN (Project 2010JBNLJ7_004). The authors thank Dr. D.Y. Sorokin and Dr. Emily D. Melton for valuable comments.

Author information

Authors and Affiliations

  1. DeFENS - Dipartimento di Scienze per gli Alimenti, la Nutrizione e l’Ambiente, Università degli Studi di Milano, via Celoria 2, 20133, Milan, Italy

    Anna Corsini, Milena Colombo, Gerard Muyzer & Lucia Cavalca

  2. Microbial Systems Ecology, Department of Aquatic Microbiology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1090 GE, Amsterdam, The Netherlands

    Gerard Muyzer

Authors
  1. Anna Corsini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Milena Colombo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gerard Muyzer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lucia Cavalca
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lucia Cavalca.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 68 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Corsini, A., Colombo, M., Muyzer, G. et al. Characterization of the arsenite oxidizer Aliihoeflea sp. strain 2WW and its potential application in the removal of arsenic from groundwater in combination with Pf-ferritin. Antonie van Leeuwenhoek 108, 673–684 (2015). https://doi.org/10.1007/s10482-015-0523-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-015-0523-2

Keywords

Search

Navigation