Abstract
Microbially reduced iron minerals can reductively transform a variety of contaminants including heavy metals, radionuclides, chlorinated aliphatics, and nitroaromatics. A number of Cellulomonas spp. strains, including strain ES6, isolated from aquifer samples obtained at the U.S. Department of Energy’s Hanford site in Washington, have been shown to be capable of reducing Cr(VI), TNT, natural organic matter, and soluble ferric iron [Fe(III)]. This research investigated the ability of Cellulomonas sp. strain ES6 to reduce solid phase and dissolved Fe(III) utilizing different carbon sources and various electron shuttling compounds. Results suggest that Fe(III) reduction by and growth of strain ES6 was dependent upon the type of electron donor, the form of iron present, and the presence of synthetic or natural organic matter, such as anthraquinone-2,6-disulfonate (AQDS) or humic substances. This research suggests that Cellulomonas sp. strain ES6 could play a significant role in metal reduction in the Hanford subsurface and that the choice of carbon source and organic matter addition can allow for independent control of growth and iron reduction activity.
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Amonette J, Workman D, Kennedy D, Fruchter J, Gorby Y (2000) Dechlorination of carbon tetrachloride by Fe(II) associated with goethite. Environ Sci Technol 34:4606–4613
Bauer I, Kappler A (2009) Rates and extent of reduction of Fe(III) and O2 by humic substances. Environ Sci Technol 43:4902–4908
Benz M, Schink B, Brune A (1998) Humic acid reduction by Propionibacterium freudenreichii and other fermenting bacteria. Appl Environ Microbiol 64:4507–4512
Borch T, Inskeep W, Harwood J, Gerlach R (2005) Impact of ferrihydrite and anthraquinone-2,6-disulfonate on the reductive transformation of 2,4,6-trinitrotoluene by a gram-positive fermenting bacterium. Environ Sci Technol 39:7126–7133
Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein using the principle of protein-dye release. Anal Biochem 72:248–254
Cervantes F, Velde S, Lettinga G, Field J (2000) Competition between methanogenesis and quinone respiration for ecologically important substrates in anaerobic consortia. FEMS Microbiol Ecol 34:161–171
Cervantes F, de Bok F, Duong-Dac T, Stams A, Lettinga G, Field J (2002) Reduction of humic substances by halorespiring, sulphate-reducing and methanogenic microorganisms. Environ Microbiol 4:51–57
Chilakapati A, Williams M, Yabusaki S, Cole C, Szecsody J (2000) Optimal design of an in situ Fe(II) barrier: transport limited reoxidation. Environ Sci Technol 34:5215–5221
Cooper D, Picardal F, Rivera J, Talbot C (2000) Zinc immobilization and magnetite formation via ferric oxide reduction by Shewanella putrefaciens 200. Environ Sci Technol 34:100–106
Dong H, Fredrickson J, Kennedy D, Zachara J, Kukkadapu R, Onstott T (2000) Mineral transformations associated with the microbial reduction of magnetite. Chem Geol 169:299–318
Dong H, Kukkadapu RK, Fredrickson JK, Zachara JM, Kennedy DW, Kostandarithes HM (2003) Microbial Reduction of Structural Fe(III) in Illite and Goethite. Environ Sci Technol 37:1268–1276
Eary L, Rai D (1988) Chromate removal from aqueous wastes by reduction with ferrous ion. Environ Sci Technol 22:972–977
Emde R, Schink B (1990) Oxidation of glycerol, lactate, and propionate by Propionibacterium freudenreichii in a poised-potential amperometric culture system. Arch Microbiol 153:506–512
Erbs M, Hansen H, Olsen C (1999) Reductive dechlorination of carbon tetrachloride using iron (II) iron (III) hydroxide sulfate (green rust). Environ Sci Technol 33:307–311
Fredrickson J, Zachara J, Kennedy D, Dong H, Onstott T, Hinman N, Li S (1998) Biogenic iron mineralization accompanying the dissimilatory reduction of hydrous ferric oxide by a groundwater bacterium. Geochim Cosmochim Acta 62:3239–3257
Fredrickson J, Kostandarithes H, Li S, Plymale A, Daly M (2000a) Reduction of Fe(III), Cr(VI), U(VI), and Tc(VII) by Deinococcus radiodurans R1. Appl Environ Microbiol 66:2006–2011
Fredrickson J, Zachara J, Kennedy D, Duff M, Gorby Y, Li S, Krupka K (2000b) Reduction of U(VI) in goethite (a-FeOOH) suspensions by a dissimilatory metal-reducing bacterium. Geochim Cosmochim Acta 64:3085–3098
Heijman C, Grieder E, Holliger C, Schwarzenbach R (1995) Reduction of nitroaromatic compounds coupled to microbial iron reduction in laboratory aquifer columns. Environ Sci Technol 29:775–783
Hernandez M, Kappler A, Newman D (2004) Phenazines and other redox-active antibiotics promote microbial mineral reduction. Appl Environ Microbiol 70:921–928
Hofstetter T, Schwarzenbach R, Haderlein S (2003) Reactivity of Fe(II) species associated with clay minerals. Environ Sci Technol 37:519–528
Istok J, Amonette J, Cole C, Fruchter J, Humphrey M, Szecsody J, Teel S, Vermeul V, Williams M, Yabusaki S (1999) In situ redox manipulation by dithionite injection: intermediate-scale laboratory experiments. Ground Water 37:884–889
Jiang J, Kappler A (2008) Kinetics of microbial and chemical reduction of humic substances: implications for electron shuttling. Environ Sci Technol 42:3563–3569
Kappler A, Benz M, Schink B, Brune A (2004) Electron shuttling via humic acids in microbial iron(III) reduction in a freshwater sediment. FEMS Microbiol Ecol 47:85–92
Kostka J, Nealson K (1995) Dissolution and reduction of magnetite by bacteria. Environ Sci Technol 29:2535–2540
Lee W, Batchelor B (2002a) Abiotic reductive dechlorination of chlorinated ethylenes by iron-bearing soil minerals. 1. Pyrite and magnetite. Environ Sci Technol 36:5147–5154
Lee W, Batchelor B (2002b) Abiotic reductive dechlorination of chlorinated ethylenes by iron-bearing soil minerals. 2. Green rust. Environ Sci Technol 36:5348–5354
Liu C, Gorby Y, Zachara J, Fredrickson J, Brown C (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
Lovley D (1987) Organic matter mineralization with the reduction of ferric iron: a review. Geomicrobiol J 5:375–399
Lovley D (1997) Microbial Fe(III) reduction in subsurface environments. FEMS Microbiol Rev 20:305–313
Lovley D, Blunt-Harris E (1999) Role of humic-bound iron as an electron transfer agent in dissimilatory Fe(III) reduction. Appl Environ Microbiol 65:4252–4254
Lovley D, Phillips E (1986a) Availability of ferric iron for microbial reduction in bottom sediments of the freshwater tidal Potomac River. Appl Environ Microbiol 52:751–757
Lovley D, Phillips E (1986b) Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Appl Environ Microbiol 51:683–689
Lovley D, Phillips E, Lonergan D (1991) Enzymatic versus nonenzymatic mechanisms for Fe(III) reduction in aquatic sediments. Environ Sci Technol 25:1062–1067
Lovley D, Coates J, Blunt-Harris E, Phillips E, Woodward J (1996) Humic substances as electron acceptors for microbial respiration. Nature 382:445–448
Lovley D, Fraga J, Blunt-Harris E, Hayes L, Phillips E, Coates J (1998) Humic substances as a mediator for microbially catalyzed metal reduction. Acta Hydrochim Hydrobiol 26:152–157
Luijten M, Weelink S, Godschalk B, Langenhoff A, Eekert M, Schraa G, Stams A (2004) Anaerobic reduction and oxidation of quinone moieties and the reduction of oxidized metals by halorespiring and related organisms. FEMS Microbiol Ecol 49:145–150
Nealson K, Saffarini D (1994) Iron and manganese in anaerobic respiration: environmental significance, physiology, and regulation. Ann Rev Microbiol 48:311–343
Nevin K, Lovley D (2000) Potential for nonenzymatic reduction of Fe(III) via electron shuttling in subsurface sediments. Environ Sci Technol 34:2472–2478
Newman D (2001) How bacteria respire minerals. Science 292:1312–1313
Petersen J, Skeen R, Amos K, Hooker B (1994) Biological destruction of CCl4: I. Experimental design and data. Biotechnol Bioeng 43:521–528
Prescott S, Dunn C (1983) Prescott and Dunn’s industrial microbiology. AVI Publishing Company, Inc, Westport
Roberts P, Hopkins G, Semprini L, McCarty P, MacKay D (1991) Pulsing of electron donor and electron acceptor for enhanced biotransformation of chemicals. U.S. Patent 5,006,250
Roden E, Zachara J (1996) Microbial reduction of crystalline iron (III) oxides: influence of oxide surface area and potential for cell growth. Environ Sci Technol 30:1618–1628
Royer R, Burgos W, Fisher A, Jeon B, Unz R, Dempsey B (2002a) Enhancement of hematite bioreduction by natural organic matter. Environ Sci Technol 36:2897–2904
Royer R, Burgos W, Fisher A, Unz R, Dempsey B (2002b) Enhancement of biological reduction of hematite by electron shuttling and Fe(II) complexation. Environ Sci Technol 36:1939–1946
Saffarini D, Blumerman S, Mansoorabadi K (2002) Role of menaquinones in Fe(III) reduction by membrane fractions of Shewanella putrefaciens. J Bacteriol 184:846–848
Sani R, Peyton B, Smith W, Apel W, Petersen J (2002) Dissimilatory reduction of Cr(VI), Fe(III), and U(VI) by Cellulomonas isolates. Appl Microbiol Biotechnol 60:192–199
Semprini L, Hopkins G, Janssen D, Lang M, Roberts P, McCarty P (1991) In situ biotransformation of carbon tetrachloride under anoxic conditions. EPA Report No. EPA 2–90/060. US EPA, Ada
Shouche M, Petersen J, Skeen R (1993) Use of a mathematical model for prediction of optimum feeding strategies for in situ bioremediation. Appl Biochem Biotechnol 39:763–779
Shyu J, Lies D, Newman D (2002) Protective role of tolC in efflux of the electron shuttle anthraquinone-2,6-disulfonate. J Bacteriol 184:1806–1810
Smith W, Apel W, Petersen J, Peyton B (2002) Effect of carbon and energy source on bacterial chromate reduction. Biorem J 6:205–215
Stackebrandt E, Schumann P, Prauser H (2006) The family Cellulomonadaceae. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K, Stackebrandt E (eds) The prokaryotes, vol 3, 3rd edn. Springer Science & Business Media, LLC, New York, pp 983–1001
Turick C, Tisa L, Caccavo F Jr (2002) Melanin production and use as a soluble electron shuttle for Fe(III) oxide reduction and as a terminal electron acceptor by Shewanella algae BrY. Appl Environ Microbiol 68:2436–2444
Viamajala S, Smith W, Sani R, Apel W, Petersen J, Neal A, Roberto F, Newby D, Peyton B (2007) Isolation and characterization of Cr(VI) reducing Cellulomonas spp. from subsurface soils: implications for long-term chromate reduction. Bioresour Technol 98:612–622
Viamajala S, Gerlach R, Sivaswamy V, Peyton BM, Apel WA, Cunningham AB, Petersen JN (2008) Permeable reactive biobarriers for in situ Cr(VI) reduction: bench scale tests using Cellulomonas sp. strain ES6. Biotechnol Bioeng 101(6):1150–1162
Wolf M, Kappler A, Jiang J, Meckenstock RU (2009) Effects of humic substances and quinones at low concentrations on ferrihydrite reduction by Geobacter metallireducens. Environ Sci Technol 43:5679–5685
Yin Y, Allen H (1999) Technology evaluation report: in situ chemical treatment. Ground Water Remediation Technologies Analysis Center TE-99-01 1, pp 1–74
Zachara J, Fredrickson J, Li S, Kennedy D, Smith S, Gassman P (1998) Bacterial reduction of crystalline Fe3+ oxides in single phase suspensions and subsurface materials. Am Miner 83:1426–1443
Acknowledgments
The authors thank Kristy Weaver and Laura Jennings for their assistance in the laboratory. This research was supported by the U.S. Department of Energy, Office of Science, Environmental Management Science Program, under Grant No. DE-FG02-03ER63582 and DOE-NE Idaho Operations Office Contract DE-AC07-05ID14517. Partial financial support was provided by a grant from the Inland Northwest Research Alliance (INRA) under contract MSU 002.
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Gerlach, R., Field, E.K., Viamajala, S. et al. Influence of carbon sources and electron shuttles on ferric iron reduction by Cellulomonas sp. strain ES6. Biodegradation 22, 983–995 (2011). https://doi.org/10.1007/s10532-011-9457-1
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DOI: https://doi.org/10.1007/s10532-011-9457-1