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Evidence for rapid microscale bacterial redox cycling of iron in circumneutral environments

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Abstract

The potential for microscale bacterial Fe redox cycling was investigated in microcosms containing ferrihydrite-coated sand and a coculture of a lithotrophic Fe(II)-oxidizing bacterium (strain TW2) and a dissimilatory Fe(III)-reducing bacterium (Shewanella alga strain BrY). The Fe(II)-oxidizing organism was isolated from freshwater wetland surface sediments which are characterized by steep gradients of dissolved O2 and high concentrations of dissolved and solid-phase Fe(II) within mm of the sediment–water interface, and which support comparable numbers (105–106 mL−1) of culturable Fe(II)-oxidizing and Fe(III)-reducing reducing. The coculture systems showed minimal Fe(III) oxide accumulation at the sand-water interface, despite intensive O2 input from the atmosphere and measurable dissolved O2 to a depth of 2 mm below the sand–water interface. In contrast, a distinct layer of oxide precipitates formed in systems containing Fe(III)-reducing bacteria alone. Examination of materials from the cocultures by fluorescence in situ hybridization indicated close physical juxtapositioning of Fe(II)-oxidizing and Fe(III)-reducing bacteria in the upper few mm of sand. Our results indicate that Fe(II)-oxidizing bacteria have the potential to enhance the coupling of Fe(II) oxidation and Fe(III) reduction at redox interfaces, thereby promoting rapid microscale cycling of Fe.

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References

  • Armstrong W (1964) Oxygen diffusion from the roots of some British bog plants. Nature 204: 801–802.

    Article  CAS  Google Scholar 

  • Arnold RG, Hoffmann MR, DiChristina TJ & Picardal FW (1990) Regulation of dissimilatory Fe(III) reduction activity in Shewanella putrefaciens. Appl. Environ. Microbiol. 56: 2811–2817.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Brendel PJ & Luther GW (1995) Development of a gold amalgam voltammetric microelectrode for the determination of dissolved Fe, Mn, O-2, and S(-II) in porewaters of marine and freshwater sediments. Environ. Sci. Technol. 29: 751–761.

    Article  CAS  Google Scholar 

  • Brock TD & Gustafson J (1972) Sulfolobus: a new genus of sulfur-oxidizing bacteria living at low pH and high temperature. Arch. Microbiol. 84: 54–68.

    CAS  Google Scholar 

  • Caccavo F, Blakemore RP & Lovley DR (1992) A hydrogen-oxidizing, Fe(III)-reducing microorganism from the Great Bay estuary, New Hampshire. Appl. Environ. Microbiol. 58: 3211–3216.

    PubMed  CAS  Google Scholar 

  • Cornell RM & Schwertmann U (1996) The Iron Oxides. VCH, New York.

    Google Scholar 

  • Davison W (1993) Iron and manganese in lakes. Earth-Sci. Rev. 34: 119–163.

    Article  CAS  Google Scholar 

  • Davison W & Seed G (1983) The kinetics of the oxidation of ferrous iron in synthetic and natural waters. Geochim. Cosmochim. Acta 47: 67–79.

    Article  CAS  Google Scholar 

  • Davison W, Grime GW, Morgan JAW & Clarke K (1991) Distribution of dissolved iron in sediment pore waters at submillimetre resolution. Nature 353: 323–325.

    Article  Google Scholar 

  • DiChristina TJ & Delong EF (1993) Design and application of rRNA-targeted oligonucleotide probes for the dissimilatory iron-and manganese-reducing bacterium Shewanella putrefaciens. Appl. Environ. Microbiol. 59: 4152–4160.

    PubMed  CAS  Google Scholar 

  • Ehrenreich A & Widdel F (1994) Anaerobic oxidation of ferrous iron by purple bacteria, a new type of phototrophic metabolism. Appl. Environ. Microbiol. 60: 4517–4526.

    PubMed  CAS  Google Scholar 

  • Ehrlich HL (1995) Geomicrobiology. Marcel Dekker, Inc., New York.

    Google Scholar 

  • Emerson D (2000) Microbial oxidation of Fe(II) and Mn(II) at circumneutral pH. In: Lovley DR (Ed) Environmental Metal-Microbe Interactions (pp 31–52). ASM Press, Washington, DC.

    Google Scholar 

  • Emerson D (2002) Bacterial iron oxidation at circumneutral pH. In: Coates JD & Zhang C (Eds) Iron in the Natural Environment: Biogeochemistry, Microbial Diversity, and Bioremediation (pp submitted for publication). Kluwer.

  • Emerson D & Revsbech NP (1994) Investigation of an iron-oxidizing microbial mat community located near Aarhus, Denmark: Field studies. Appl Environ Microbiol 60: 4022–4031.

    PubMed  CAS  Google Scholar 

  • Emerson D & Moyer C (1997) Isolation and characterization of novel lithotrophic iron-oxidizing bacteria that grow at circumneutral pH. Appl. Environ. Microbiol. 63: 4784–4792.

    PubMed  CAS  Google Scholar 

  • Emerson D, Weiss JV & Megonigal JP (1999) Iron-oxidizing bacteria are associated with ferric hydroxide precipitates (Fe-plaque) on the roots of wetland plants. Appl. Environ. Microbiol. 65: 2758–2761.

    PubMed  CAS  Google Scholar 

  • Fredrickson JK, Zachara JM, Kennedy DW, Dong H, Onstott TC, Hinman NW & Li S (1998) Biogenic iron mineralization accompanying the dissimilatory reduction of hydrous ferric oxide by a groundwater bacterium. Geochim. Cosmochim. Acta 62: 3239–3257.

    Article  CAS  Google Scholar 

  • Ghiorse WC (1984) Biology of iron-and manganese-depositing bacteria. Annu. Rev. Microbiol. 38: 515–550.

    PubMed  CAS  Google Scholar 

  • Glud RN, Forster S & Huettel M (1996) Influence of radial pressure gradients on solute exchange in stirred benthic chambers. Marine Ecol. Prog. Ser. 141: 303–311.

    Google Scholar 

  • Huettel M, Ziebis W, Forster S & Luther GW (1998) Advective transport affecting metal and nutrient distributions and interfacial.597 fluxes in permeable sediments. Geochim. Cosmochim. Acta 62: 613–631.

    Article  CAS  Google Scholar 

  • Hunter KS, Wang Y & VanCappellen P (1998) Kinetic modeling of microbially-driven redox chemistry of subsurface environments: coupling transport, microbial metabolism and geochemistry. J. Hydrol. 209: 53–80.

    Article  CAS  Google Scholar 

  • Jahnke R (1985) A model for microenvironments in deep-sea sediments, formation and effects on porewater profiles. Limnol. Oceanogr. 30: 956–965.

    CAS  Google Scholar 

  • Johnson DB, McGinness S & Ghauri MA (1993) Biogeochemical cycling of iron and sulfur in leaching environments. FEMS Microbiol. Rev. 11: 63–70.

    Article  CAS  Google Scholar 

  • Jorgensen BB (1977) Bacterial sulfate reduction within reduced microniches of oxidized marine sediments. Mar. Biol. 41: 7–17.

    Article  Google Scholar 

  • Jorgensen BB (1989) Biogeochemistry of chemoautotrophic bacteria. In: Schlegel HG & Bowien B (Eds) Biochemistry of Autotrophic Bacteria (pp 117–146) Science Tech Publishers, Madison, WI.

    Google Scholar 

  • Jorgensen BB & Revsbech NP (1983) Colorless sulfur bacteria, Beggiatoa spp. and Thiovulum spp., in O2 and H2S microgradients. Appl. Environ. Microbiol. 45: 1261–1270.

    PubMed  CAS  Google Scholar 

  • Kusel K & Dorsch T (2000) Effect of supplemental electron donors on the microbial reduction of Fe(III), sulfate, and CO2 in coal mining-impacted freshwater lake sediments. Microb. Ecol. 40: 238–249.

    PubMed  CAS  Google Scholar 

  • Kusel K, Dorsch T, Acker G & Stackebrandt E (1999) Microbial reduction of Fe(III) in acidic sediments: isolation of Acidiphilium cryptum JF-5 capable of coupling the reduction of Fe(III) to the oxidation of glucose. Appl. Environ. Microbiol. 65: 3633–3640.

    PubMed  CAS  Google Scholar 

  • Lovley DR (1991) Dissimilatory Fe(III) and Mn(IV) reduction. Microbiol. Rev. 55: 259-287. Lovley DR (2000) Fe(III) and Mn(IV) reduction. In: Lovley DR (Ed) Environmental Metal-Microbe Interactions (pp 3-30). ASM Press, Washington, DC.

    PubMed  CAS  Google Scholar 

  • Lovley DR (2002) Fe(III)-and Mn(IV)-reducing prokaryotes. In: SFM Dworkin, Rosenberg E, Schleifer KH, & Stackebrandt E (Ed) The Prokaryotes (pp in press). Springer-Verlag, New York.

    Google Scholar 

  • Lovley DR & Phillips EJP (1986) Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Appl. Environ. Microbiol. 51: 683–689.

    PubMed  CAS  Google Scholar 

  • Lovley DR & Anderson RT (2000) The influence of dissimilatory metal reduction on the fate of organic and metal contaminants in the subsurface. J. Hydrol. 8: 77–88.

    CAS  Google Scholar 

  • Luther GW, Brendel PJ, Lewis BL, Sundby B, Lefrancois L, Silverberg N & Nuzzio D (1998) Simultaneous measurement of O2, Mn, Fe, I-, and S(-II) in marine pore waters with a solid-state voltammetric microelectrode. Limnol. Oceanogr. 43: 325–333.

    Article  CAS  Google Scholar 

  • Millero FJ, Sotolongo S & Izaguirre M (1987) The oxidation kinetics of Fe(II) in seawater. Geochim. Cosmochim. Acta 51: 793–801.

    Article  CAS  Google Scholar 

  • Nelson DC, Jorgensen BB & Revsbech NP (1986) Growth pattern and yield of a chemoautotrophic Beggiatoa sp. in oxygen-sulfide microgradients. Appl. Environ. Microbiol. 52: 225–233.

    PubMed  CAS  Google Scholar 

  • Nevin K & Lovley DR (2002) Mechanisms of Fe(III) oxide reduction in sedimentary environments. Geomicrobiol. J. 19: 141–159.

    Article  CAS  Google Scholar 

  • Peine A, Tritschler A, Kusel K & Peiffer S (2000) Electron flow in an iron-rich acidic sediment - evidence for an acidity-driven iron cycle. Limnol. Oceanogr. 45: 1077–1087.

    Article  CAS  Google Scholar 

  • Perfil'ev BV & Gabe DR (1969) The capillary method of studying the microflora of bottom deposits, soils and subterranean waters in microbial landscapes. Capillary Methods of Investigating Micro-Organisms (pp 13–78). University of Toronto Press, Toronto.

    Google Scholar 

  • Ratering S & Schnell S (2000) Localization of iron-reducing activity in paddy soil by profile studies. Biogeochemistry 48: 341–365.

    Article  CAS  Google Scholar 

  • Revsbech NP (1989) An oxygen microelectrode with guard cathode. Limnol. Oceanogr. 34: 472–476.

    Article  Google Scholar 

  • Roden EE & Wetzel RG (1996) Organic carbon oxidation and suppression of methane production by microbial Fe(III) oxide reduction in vegetated and unvegetated freshwater wetland sediments. Limnol. Oceanogr. 41: 1733–1748.

    Article  CAS  Google Scholar 

  • Roden EE, Sobolev D & Luther GW (2002) New insights into the biogeochemical cycling of iron in sedimentary environments: potential for a rapid microscale bacterial Fe redox cycle at the aerobic-anaerobic interface. In: Coates JD (Ed) Biogeochemical Cycling of Iron in Natural Environments (pp Submitted for publication) Kluwer.

  • Shuttleworth SM, Davison W & Hamilton-Taylor J (1999) Two-dimensional and fine structure in the concentration of iron and manganese in sediment pore-waters. Environ. Sci. Technol. 33: 4169–4175.

    Article  CAS  Google Scholar 

  • Singer PC & Stumm W (1972) Acid mine drainage - the rate limiting step. Science 167: 1121–1123.

    Google Scholar 

  • Sobolev D & Roden EE (2001) Suboxic deposition of ferric iron by bacteria in opposing gradients of Fe(II) and oxygen at circumneutral pH. Appl. Environ. Microbiol. 67: 1328–1334.

    Article  PubMed  CAS  Google Scholar 

  • Sobolev D, Emerson D & Roden E (2002) Characterization of a chemolithoautotrophic Fe(II)-oxidizing bacterium from the ß-subclass of the Proteobacteria isolated from freshwater wetland sediments. Manuscript in preparation.

  • Straub KL & Buchholz-Cleven BEE (1998) Enumeration and detection of anaerobic ferrous-iron oxidizing, nitrate-reducing bacteria from diverse European sediments. Appl. Environ. Microbiol. 64: 4846–4856.

    PubMed  CAS  Google Scholar 

  • Straub KL, Benz M, Schink B & Widdel F (1996) Anaerobic, nitrate-dependent microbial oxidation of ferrous iron. Appl. Environ. Microbiol. 62: 1458–1460.

    PubMed  CAS  Google Scholar 

  • Stumm W & Sulzberger B (1992) The cycling of iron in natural environments: Considerations based on laboratory studies of heterogeneous redox processes. Geochim. Cosmochim. Acta 56: 3233–3257.

    Article  CAS  Google Scholar 

  • Taillefert M, Bono A & Luther G (2000) Reactivity of freshly formed Fe(III) in synthetic solutions and (pore)waters: voltammetric evidence of an aging process. Environ. Sci. Technol. 34: 2169–2177.

    Article  CAS  Google Scholar 

  • Thamdrup B (2000) Bacterial manganese and iron reduction in aquatic sediments. Adv. Microb. Ecol. 16: 41–84.

    CAS  Google Scholar 

  • Thamdrup B, Fossing H & Jorgensen BB (1994) Manganese, iron, and sulfur cycling in a coastal marine sediment, Aarhus Bay, Denmark. Geochim. Cosmochim. Acta 58: 5115–5129.

    Article  CAS  Google Scholar 

  • vandenEnde FP, Meier J & vanGermerden H (1997) Syntrophic growth of sulfate-reducing bacteria and colorless sulfur bacteria during oxygen limitation. FEMS Microbiol. Ecol. 23: 65–80.

    Article  CAS  Google Scholar 

  • Weber KA, Picardal FW & Roden EE (2001) Microbially-catalyzed nitrate-dependent oxidation of biogenic solid-phase Fe(II) compounds. Environ. Sci. Technol. 35: 1644–1650.

    Article  PubMed  CAS  Google Scholar 

  • Westermann P (1993) Wetland and swamp microbiology. In: Ford TE (Ed) Aquatic Microbiology: An Ecological Approach (pp 295–302). Blackwell Scientific, Boston.

    Google Scholar 

  • Widdel F, Schnell S, Heising S, Ehrenreich A, Assmus B & Schink B (1993) Ferrous iron oxidation by anoxygenic phototrophic bacteria. Nature 362: 834–835.

    Article  CAS  Google Scholar 

  • Woomer PL (1994) Most probable number counts. In: Bigham JM (Ed) Methods of soil analysis Part 2 - Microbiological and Biochemical Properties (pp 59–79). Soil Science Society of America, Madison.

    Google Scholar 

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  1. Department of Biological Sciences, The University of Alabama, Tuscaloosa, AL, 35487-0206, USA

    Dmitri Sobolev & Eric E. Roden

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  1. Dmitri Sobolev
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  2. Eric E. Roden
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Correspondence to Eric E. Roden.

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Sobolev, D., Roden, E.E. Evidence for rapid microscale bacterial redox cycling of iron in circumneutral environments. Antonie Van Leeuwenhoek 81, 587–597 (2002). https://doi.org/10.1023/A:1020569908536

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