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Articles

Iron Cycling Potentials of Arsenic Contaminated Groundwater in Bangladesh as Revealed by Enrichment Cultivation

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Pages 779-792 | Received 01 Jun 2015, Accepted 01 Oct 2015, Published online: 16 Jun 2016

References

  • Andreoni V, Zanchi R, Cavalca L, Corsini A, Romagnoli C, Canzi E. 2012. Arsenite oxidation in Ancylobacter dichloromethanicus As3-1b strain: detection of genes involved in arsenite oxidation and CO2 fixation. Curr Microbiol 65:212–218.
  • Benz M, Brune A, Schink B. 1998. Anaerobic and aerobic oxidation of ferrous iron at neutral pH by chemoheterotrophic nitrate-reducing bacteria. Arch Microbiol 169:159–165.
  • Blöthe M, Roden EE. 2009. Microbial iron redox cycling in a circumneutral-pH groundwater seep. Appl Environ Microbiol 75:468–473.
  • Byrne-Bailey KG, Coates JD. 2012. Complete genome sequence of the anaerobic perchlorate-reducing bacterium Azospira suillum strain PS. J Bacteriol 194:2767–2768.
  • Carlson HK, Clark IC, Blazewicz SJ, Iavarone AT, Coates JD. 2013. Fe(II) oxidation is an innate capability of nitrate-reducing bacteria that involves abiotic and biotic reactions. J Bacteriol 195:3260–3268.
  • Cavalca L, Corsini A, Zaccheo P, Andreoni V, Muyzer G. 2013. Microbial transformations of arsenic: perspectives for biological removal of arsenic from water. Future Microbiol 8:753–768.
  • Chakraborty A, Picardal F. 2013. Induction of nitrate-dependent Fe(II) oxidation by Fe(II) in Dechloromonas sp. strain UWNR4 and Acidovorax sp. strain 2AN. Appl Environ Microbiol 79:748–52.
  • Chan C, Cabaniss K, Williams K, Moore M, Michael H, Caplan J, Lin C. 2014. Fe-oxidizing microorganisms in microscopic model aquifer systems: feedbacks between flow and biomineralization. In: Proceedings of the ninth international symposium on subsurface microbiology. Pacific Grove, California USA, October 5-10, pp 22.
  • Chapelle FH. 2001. Ground-Water Microbiology and Geochemistry. New York: John Wiley & sons, pp 272–275.
  • Clarke WA, Konhauser KO, Thomas JC, Bottrell SH. 1997. Ferric hydroxide and ferric hydroxysulfate precipitation by bacteria in an acid mine drainage lagoon. FEMS Microbiol Rev 20:351–361.
  • Coates JD, Ellis DJ, Gaw CV, Lovley DR. 1999. Geothrix fermentans gen. nov., sp. nov., a novel Fe(III)-reducing bacterium from a hydrocarbon-contaminated aquifer. Int J Syst Bacteriol 49:1615–1622.
  • Coby AJ, Picardal F, Shelobolina E, Xu H, Roden EE. 2011. Repeated anaerobic microbial redox cycling of iron. Appl Environ Microbiol 77:6036–6042.
  • Edwards KJ, Rogers DR, Wirsen CO, McCollom TM. 2003. Isolation and characterization of novel psychrophilic, neutrophilic, Fe-oxidizing, chemolithoautotrophic α-and γ-Proteobacteria from the deep sea. Appl Environ Microbiol 69:2906–2913.
  • Emerson D, Weiss JV. 2004. Bacterial iron oxidation in circumneutral freshwater habitats: findings from the field and the laboratory. Geomicrobiol J 21:405–414.
  • Emerson D, Floyd MM. 2005. Enrichment and isolation of iron-oxidizing bacteria at neutral pH. Methods Enzymol 397:112–123.
  • Emerson D, De Vet W. 2015. The role of FeOB in engineered water ecosystems: A Review. J Am Water Works Assoc 107:e47–57. http://dx.doi.org/10.5942/jawwa.2015.107.0004.
  • Ghiorse W. 1984. Biology of iron-and manganese-depositing bacteria. Annu Rev Microbiol 38:515–550.
  • Gibney BP, Nüsslein K. 2007. Arsenic sequestration by nitrate respiring microbial communities in urban lake sediments. Chemosphere 70:329–336.
  • Gonzaga MIS, Santos JAG, Ma LQ. 2006. Arsenic phytoextraction and hyperaccumulation by fern species. Sci Agric 63:90–101.
  • Gülay A, Musovic S, Albrechtsen HJ, Smets BF. 2013. Neutrophilic iron-oxidizing bacteria: occurrence and relevance in biological drinking water treatment. Water Sci Technol Water Supply 13:1295–1301.
  • Hallbeck L, Ståhl F, Pedersen K. 1993. Phylogeny and phenotypic characterization of the stalk-forming and iron-oxidizing bacterium Gallionella ferruginea. J Gen Microbiol 139:1531–1535.
  • Hallberg R, Ferris FG. 2004. Biomineralization by Gallionella. Geomicrobiol J 21:325–330.
  • Hassan Z, Sultana M, van Breukelen BM, Khan SI, Röling WFM. 2015. Diverse arsenic-and iron-cycling microbial communities in arsenic-contaminated aquifers used for drinking water in Bangladesh. FEMS Microbiol Ecol doi:10.1093/femsec/fiv026.
  • Hedrich S, Schlömann M, Johnson DB. 2011. The iron-oxidizing proteobacteria. Microbiology 157:1551–1564.
  • Héry M, van Dongen BE, Gill F, Mondal D, Vaughan DJ, Pancost RD, Polya DA, Lloyd JR. 2010. Arsenic release and attenuation in low organic carbon aquifer sediments from West Bengal. Geobiology 8:155–168.
  • Héry M, Rizoulis A, Sanguin H, Cooke DA, Pancost RD, Polya DA, Lloyd JR. 2015. Microbial ecology of arsenic-mobilizing Cambodian sediments: lithological controls uncovered by stable-isotope probing. Environ Microbiol 17:1857–1869.
  • Hohmann C, Winkler E, Morin G, Kappler A. 2009. Anaerobic Fe(II)-oxidizing bacteria show As resistance and immobilize As during Fe(III) mineral precipitation. Environ Sci Technol 44:94–101.
  • Höhn R, Isenbeck-Schröter M, Kent D, Davis J, Jakobsen R, Jann S, Niedan V, Scholz C, Stadler S, Tretner A. 2006. Tracer test with As(V) under variable redox conditions controlling arsenic transport in the presence of elevated ferrous iron concentrations. J Contam Hydrol 88:36–54.
  • Huq SMI, Joardar J, Parvin S, Correll R, Naidu R. 2006. Arsenic contamination in food-chain: transfer of arsenic into food materials through groundwater irrigation. J Health Popul Nutr 24:305.
  • 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 9:934–43.
  • Ishii S, Shimoyama T, Hotta Y, Watanabe K. 2008. Characterization of a filamentous biofilm community established in a cellulose-fed microbial fuel cell. BMC Microbiol 8:6.
  • Islam FS, Gault AG, Boothman C, Polya DA, Charnock JM, Chatterjee D, Lloyd JR. 2004. Role of metal-reducing bacteria in arsenic release from Bengal delta sediments. Nature 430:68–71.
  • Kaku N, Yonezawa N, Kodama Y, Watanabe K. 2008. Plant/microbe cooperation for electricity generation in a rice paddy field. Appl Microbiol Biotechnol 79:43–49.
  • Katsoyiannis IA, Zouboulis AI. 2004. Application of biological processes for the removal of arsenic from groundwaters. Water Res 38:17–26.
  • Klueglein N, Kappler A. 2013. Abiotic oxidation of Fe(II) by reactive nitrogen species in cultures of the nitrate‐reducing Fe(II) oxidizer Acidovorax sp. BoFeN1–questioning the existence of enzymatic Fe(II) oxidation. Geobiology 11:180–190.
  • Klueglein N, Lösekann-Behrens T, Obst M, Behrens S, Appel E, Kappler A. 2013. Magnetite formation by the novel Fe(III)-reducing Geothrix fermentans strain HradG1 isolated from a hydrocarbon-contaminated sediment with increased magnetic susceptibility. Geomicrobiol J 30:863–873.
  • Kozubal M, Macur R, Korf S, Taylor W, Ackerman G, Nagy A, Inskeep W. 2008. Isolation and distribution of a novel iron-oxidizing crenarchaeon from acidic geothermal springs in Yellowstone National Park. Appl Environ Microbiol 74:942–949.
  • Kudo K, Yamaguchi N, Makino T, Ohtsuka T, Kimura K, Dong DT, Amachi S. 2014. Release of arsenic from soil by a novel dissimilatory arsenate-reducing bacterium, Anaeromyxobacter sp. Strain PSR-1. Appl Environ Microbiol 79:4635–4642.
  • 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.
  • Li B, Pan X, Zhang D, Lee DJ, Al-Misned FA, Mortuza MG. 2015. Anaerobic nitrate reduction with oxidation of Fe(II) by Citrobacter Freundii strain PXL1–a potential candidate for simultaneous removal of As and nitrate from groundwater. Ecol Eng 77:196–201.
  • Li D, Li Z, Yu J, Cao N, Liu R, Yang M. 2010. Characterization of bacterial community structure in a drinking water distribution system during an occurrence of red water. Appl Environ Microbiol 76:7171–7180.
  • Li H, Peng J, Weber KA, Zhu Y. 2011. Phylogenetic diversity of Fe(III)-reducing microorganisms in rice paddy soil: enrichment cultures with different short-chain fatty acids as electron donors. J Soils Sedim 11:1234–1242.
  • Lin B, Braster M, van Breukelen BM, van Verseveld HW, Westerhoff HV, Röling WFM. 2005. Geobacteraceae community composition is related to hydrochemistry and biodegradation in an iron-reducing aquifer polluted by a neighboring landfill. Appl Environ Microbiol 71:5983–5991.
  • Lin B, Braster M, Röling WFM, van Breukelen BM. 2007. Iron-reducing microorganisms in a landfill leachate-polluted aquifer: complementing culture-independent information with enrichments and isolations. Geomicrobiol J 24:283–294.
  • Liu C, Gorby YA, Zachara JM, Fredrickson JK, Brown CF. 2002. Reduction kinetics of Fe(III), Co (III), U (VI), Cr (VI), and Tc (VII) in cultures of dissimilatory metal‐reducing bacteria. Biotechnol Bioeng 80:637–649.
  • Liu Q, Guo H, Li Y, Xiang H. 2013. Acclimation of arsenic-resistant Fe(II)-oxidizing bacteria in aqueous environment. Inter Biodeter Biodegrad 76:86–91.
  • Lloyd JR, Oremland RS. 2006. Microbial transformations of arsenic in the environment: from soda lakes to aquifers. Elements 2:85–90.
  • Lovley DR, Roden EE, Phillips E, Woodward J. 1993. Enzymatic iron and uranium reduction by sulfate-reducing bacteria. Mar Geol 113:41–53.
  • Lovley DR, Anderson RT. 2000. Influence of dissimilatory metal reduction on fate of organic and metal contaminants in the subsurface. Hydrogeol J 8:77–88.
  • Lovley DR, Holmes DE, Nevin KP. 2004. Dissimilatory Fe(III) and Mn (IV) reduction. Adv Microb Physiol 49:219–286.
  • Lovley DR, Ueki T, Zhang T, Malvankar NS, Shrestha PM, Flanagan KA, Aklujkar M, Butler JE, Giloteaux L, Rotaru A, et al. 2011. Geobacter: the microbe Electric's physiology, ecology, and practical applications. Adv Microb Physiol 59:1–100.
  • McArthur JM, Ravenscroft P, Safiulla S, Thirlwall MF. 2001. Arsenic in groundwater: testing pollution mechanisms for sedimentary aquifers in Bangladesh. Water Resour Res 37:109–117.
  • Melton ED, Schmidt C, Kappler A. 2012. Microbial iron (II) oxidation in littoral freshwater lake sediment: the potential for competition between phototrophic vs. nitrate-reducing iron (II)-oxidizers. Front Microbiol 3:197.
  • Miot J, Benzerara K, Morin G, Kappler A, Bernard S, Obst M, Férard C, Skouri-Panet F, Guigner JM, Posth N. 2009. Iron biomineralization by anaerobic neutrophilic iron-oxidizing bacteria. Geochim Cosmochim Acta 73:696–711.
  • Mori K, Tsurumaru H, Harayama S. 2010. Iron corrosion activity of anaerobic hydrogen-consuming microorganisms isolated from oil facilities. J Biosci Bioeng 110:426–430.
  • Nickson RT, McArthur JM, Ravenscroft P, Burgess WG, Ahmed KM. 2000. Mechanism of arsenic release to groundwater, Bangladesh and West Bengal. Appl Geochem 15:403–413.
  • Ohtsuka T, Yamaguchi N, Makino T, Sakurai K, Kimura K, Kudo K, Homma E, Dong DT, Amachi S. 2013. Arsenic dissolution from Japanese paddy soil by a dissimilatory arsenate-reducing bacterium Geobacter sp. OR-1. Environ Sci Technol 47:6263–6271.
  • Omoregie EO, Couture RM, van Cappellen P, Corkhill CL, Charnock JM, Polya DA, Vaughan D, Vanbroekhoven K, Lloyd JR. 2013. Arsenic bioremediation by biogenic iron oxides and sulfides. Appl Environ Microbiol 79:4325–4335.
  • Oremland RS, Stolz JF. 2005. Arsenic, microbes and contaminated aquifers. Trends Microbiol 13:45–49.
  • 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. doi:10.1021/es504707x
  • 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.
  • Rhine ED, Phelps CD, Young LY. 2006. Anaerobic arsenite oxidation by novel denitrifying isolates. Environ Microbiol 8:899–908.
  • Rhine ED, Ni Chadhain SM, Zylstra GJ, Young LY. 2007. The arsenite oxidase genes (aroAB) in novel chemoautotrophic arsenite oxidizers. Biochem Biophys Res Commun 354:662–667.
  • Röling WFM. 2014. The Family Geobacteraceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F, (eds). The Prokaryotes. Berlin Heidelberg:Springer, 157–172.
  • Rowland HAL, Boothman C, Pancost R, Gault AG, Polya DA, Lloyd JR. 2009. The role of indigenous microorganisms in the biodegradation of naturally occurring petroleum, the reduction of iron, and the mobilization of arsenite from West Bengal aquifer sediments. J Environ Qual 38:1598–1607.
  • Salmassi TM, Walker JJ, Newman DK, Leadbetter JR, Pace NR, Hering JG. 2006. Community and cultivation analysis of arsenite oxidizing biofilms at Hot Creek. Environ Microbiol 8:50–59.
  • Santini JM, Sly LI, Wen A, Comrie D, Wulf-Durand PD, Macy JM. 2002. New Arsenite-Oxidizing Bacteria Isolated from Australian Gold Mining Environments—Phylogenetic Relationships. Geomicrobiol J 19:67–76.
  • Snoeyenbos-West OL, Nevin KP, Anderson RT, Lovley DR. 2000. Enrichment of Geobacter species in response to stimulation of Fe(III) reduction in sandy aquifer sediments. Microb Ecol 39:153–167.
  • Sun W, Sierra-Alvarez R, Milner L, Oremland RS, Field JA. 2009. Arsenite and ferrous iron oxidation linked to chemolithotrophic denitrification for the immobilization of arsenic in anoxic environments. Environ Sci Technol 43:6585–6591.
  • 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.
  • van Halem D, Olivero S, de Vet WW, Verberk JQ, Amy GL, van Dijk JC. 2010. Subsurface iron and arsenic removal for shallow tube well drinking water supply in rural Bangladesh. Water Res 44:5761–5769.
  • van Verseveld HW, Röling WFM. 2004. Cluster analysis and statistical comparison of molecular community profile data. In:Kowalchuk GA, de Bruijn FJ, Head IM, et al., editors. Molecular Microbial Ecology Manual. 2nd edn. New York, NY: Springer, pp 1373–1397.
  • vanden Hoven RN, Santini JM. 2004. Arsenite oxidation by the heterotroph Hydrogenophaga sp. str. NT-14: the arsenite oxidase and its physiological electron acceptor. Biochim Biophys Acta 1656:148–155.
  • Vishnivetskaya TA, Brandt CC, Madden AS, Drake MM, Kostka JE, Akob DM, Küsel K, Palumbo AV. 2010. Microbial community changes in response to ethanol or methanol amendments for U (VI) reduction. Appl Environ Microbiol 76:5728–5735.
  • Wang A, Liu L, Sun D, Ren N, Lee DJ. 2010. Isolation of Fe(III)-reducing fermentative bacterium Bacteroides sp. W7 in the anode suspension of a microbial electrolysis cell (MEC). Int J Hydrogen Energy. 35:3178–3182.
  • Wang J, Muyzer G, Bodelier PL, Laanbroek HJ. 2009. Diversity of iron oxidizers in wetland soils revealed by novel 16S rRNA primers targeting Gallionella-related bacteria. ISME J 3:715–725.
  • Weber KA, Achenbach LA, Coates JD. 2006a. Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol 4:752–764.
  • Weber KA, Pollock J, Cole KA, O'Connor SM, Achenbach LA, Coates JD. 2006b. Anaerobic nitrate-dependent iron (II) bio-oxidation by a novel lithoautotrophic betaproteobacterium, strain 2002. Appl Environ Microbiol 72:686–694.
  • Yu R, Gan P, MacKay AA, Zhang S, Smets BF. 2010. Presence, distribution, and diversity of iron-oxidizing bacteria at a landfill leachate-impacted groundwater surface water interface. FEMS Microbiol Ecol 71:260–271.
  • Yu WH, Harvey CM, Harvey CF. 2003. Arsenic in groundwater in Bangladesh: A geostatistical and epidemiological framework for evaluating health effects and potential remedies. Water Resour Res 39:1146–1163.
  • 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.
  • Zobrist J, Dowdle PR, Davis JA, Oremland RS. 2000. Mobilization of arsenite by dissimilatory reduction of adsorbed arsenate. Environ Sci Technol. 34:4747–4753.
  • Zouboulis AI, Katsoyiannis IA. 2005. Recent advances in the bioremediation of arsenic-contaminated groundwaters. Environ Int. 31:213–219.