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Breathing metals as a way of life: geobiology in action

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Abstract

Many microbes have the ability to reduce transition metals, coupling this reduction to the oxidation of energy sources in a dissimilatory fashion. Because of their abundance, iron and manganese have been extensively studied, and it is well established that reduction of Mn and Fe account for significant turnover of organic carbon in many environments. In addition, many of the dissimilatory metal reducing bacteria (DMRB) also reduce other metals, including toxic metals like Cr(VI), and radioactive contaminants like U(VI), raising the expectations that these processes can be used for bioremediation. The processes involved in metal reduction remain mysterious, and often progress is slow, as nearly all iron and manganese oxides are solids, which offer particular challenges with regard to imaging and chemical measurements. In particular, the interactions that occur at the bacteria-mineral interfaces are not yet clearly elucidated. One DMRB, Shewanella oneidensis MR-1 offers the advantage that its genome has recently been sequenced, and with the availability of its genomic sequence, several aspects of its metal reducing abilities are now beginning to be seen. As these studies progress, it should be possible to separate several processes involved with metal reduction, including surface recognition, attachment, metal destabilization and reduction, and secondary mineral formation.

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References

  • Aguilar C & Nealson KH (1993) Mn reduction in Oneida Lake, NY: estimates of spatial and temporal Mn flux. Can. J. Fish. Aquat. Sci. 51: 185–196.

    Google Scholar 

  • Aguilar C & Nealson KH (1998) Biogeochemical cycling of Mn in Oneida Lake, NY: whole lake studies of Mn. J. Great Lakes Res. 24: 93–104.

    PubMed  CAS  Google Scholar 

  • Aller RC (1990) Bioturbation and manganese cycling in hemipelagic sediments. Phil. Trans. R. Soc. Lond. A. 331: 51–68.

    CAS  Google Scholar 

  • Aller RC, Aller J, Mackin NJ & Rude P (1991) Biogeochemical processes in Amazon shelf sediments. Oceanog. April: 27-32.

  • Beliaev A, Thompson DK, Giometti CS, Brandt CC, Li G, Yates J, Nealson KH, Tiedje JM, Murray AE, Heidelberg JF & Zhou J (2002) Gene and protein expression profiles of Shewanella oneidensis during anaerobic growth with different electron acceptors OMICS: A J. of Integ. Bio. 6: (in press).

  • Belz AP, Ahn CC, Andrews MY & Nealson KH (2002a) Effects of solution chemistry in manganese reduction by Shewanella oneidensis Envir. Sci. Technol. (in press).

  • Belz AP, Ahn CC & Nealson KH (2002b) Characterization of manganese oxides using electron energy loss spectrometry Amer. Mineralog. (in press).

  • Brettar I & Hoeffle M (1993) Nitrous oxide producing heterotrophic bacteria from the water column of the central Baltic: abundance and molecular identification Mar. Ecol. Prog. Ser. 94: 253–265.

    CAS  Google Scholar 

  • Burdige DJ & Nealson KH (1986) Chemical and microbiological studies of sulfide-mediated manganese reduction. Geomicrobiol. J. 4: 361–387.

    Article  CAS  Google Scholar 

  • Burdige DJ, Dhakar SP & Nealson KH (1992) Effects of Mn oxide mineralogy on microbial and chemical Mn reduction. Geomicrobiol. J. 10: 27–48.

    CAS  Google Scholar 

  • Canfield DE, Thamdrup B & Hansen JW (1993) The anaerobic oxidation of organic matter in Danish coastal sediments: iron reduction, manganese reduction, and sulfate reduction. Geochim. Cosmochim. Acta 57: 3867–3885.

    Article  PubMed  CAS  Google Scholar 

  • Das A & Caccavo F (2001) Adhesion of dissimilatory Fe(III) reducing bacteria S. algae to crystalline Fe(III) oxides Curr. Microbiol. 42: 151–154.

    Article  PubMed  CAS  Google Scholar 

  • Das A & Caccavo F (2000) Dissimilatory iron oxide reduction by S. algae BrY requires adhesion. Curr. Microbiol. 40: 344–347.

    Article  PubMed  CAS  Google Scholar 

  • DeChristina T & DeLong E (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.

    Google Scholar 

  • Dollhopf M, Nealson KH, Simon D & Luther G (2000) Kinetics of Fe(III) and Mn(IV) reduction by the Black Sea strain of Shewanella putrefaciens using in situ solid state voltammetric Au/Hg electrodes. Mar. Chem. 70: 171–180.

    Article  CAS  Google Scholar 

  • Gorby YA & Lovley DR (1992) Enzymatic uranium precipitation. Envir. Sci. Technol. 26: 205–207.

    Article  CAS  Google Scholar 

  • Hernandez ME & Newman DK (2001) Extracellular electron transfer. Cell. Mol. Life Sci. 58: 1562–1571.

    Article  PubMed  CAS  Google Scholar 

  • Hoeffle M & Brettar I (1996) Genotyping of heterotrophic bacteria from the central Baltic Sea by low-molecular weight RNA profiles. Appl. Environ. Microbiol. 62: 1383–1390.

    Google Scholar 

  • Larsen I, Little B, Nealson KH, Ray R, Stone A & Tian J (1998) Manganite reduction by S. putrefaciens MR-4. Amer. Mineral. 83: 1564–1573.

    CAS  Google Scholar 

  • Lonergan DJ, Jenter HL, Coates JD, Phillips EJP, Schmidt T & Lovley DR (1996) Phylogenetic analysis of dissimilatory Fe(III) reducing bacteria. J. Bact. 178: 2402–2408.

    PubMed  CAS  Google Scholar 

  • Lovley DJ & Phillips EJP (1988) Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl. Env. Microbiol. 51: 683–689.

    Google Scholar 

  • Lovley DR, Coates JD, Blunt-Harris EL, Phillips EJP & Woodward JC (1996) Humic substances as a mediator for microbially catalyzed metal reduction. Nature 382: 445–448.

    Article  CAS  Google Scholar 

  • MacGregor B, Moser D, Nealson KH & Stahl DA (1997) Crenarchaeota in Lake Michigan sediments. Appl. Environ. Microbiol. 63: 1178–1181.

    PubMed  CAS  Google Scholar 

  • Murray A, Lies D, Li G, Nealson K, Zhou J & Tiedje JM (2001) DNA/DNA hybridization to microarrays reveals gene-specific differences between closely related microbial genomes. Proc. Nat. Acad. Sci. USA 98: 9853–9858.

    Article  PubMed  CAS  Google Scholar 

  • Myers C & Nealson KH (1988a) Bacterial Mn reduction and growth with Mn oxdie as the sole electron acceptor. Science 240: 1319–1321.

    CAS  PubMed  Google Scholar 

  • Myers C & Nealson KH (1988b) Microbial reduction of Mn oxides: interactions with iron and sulfur. Geochim. Cosmochim. Acta 52: 2727–2732.

    Article  CAS  Google Scholar 

  • Nealson KH (1997) Sediment bacteria: who's there, what are they doing, and what's new? Annu. Rev. Earth Planet. Sci. 25: 403–434.

    Article  PubMed  CAS  Google Scholar 

  • Nealson KH & Little B (1997) Breathing Mn and Fe: solid state respiration. Adv. Appl. Microbiol. 45: 213–239.

    Article  CAS  Google Scholar 

  • Nealson KH, Myers CR & Wimpee B (1991) Isolation and identification of Mn-reducing bacteria and estimates of microbial Mn reducing potential in the Black Sea. Deep Sea Res. 38: 907–920.

    Google Scholar 

  • Newman DK & Kolter R (2000) A role for excreted quinones in extracellular electron transfer. Nature 405: 94–97.

    Article  PubMed  CAS  Google Scholar 

  • Roden E & Zachara J (1996) Microbial reduction of crystalline Fe oxides: influences of oxide surface area and potential for cell growth. Env. Sci. Technol. 30: 1618–1628.

    Article  CAS  Google Scholar 

  • Stein L, LaDuc M, Grundl T & Nealson KH (2001) Bacterial and Archaeal populations associated with freshwater ferromanganese micronodules and sediments. Environ. Microbiol. 3: 10–18.

    Article  PubMed  CAS  Google Scholar 

  • Stone AT & Morgan JJ (1984a) Reduction and dissolution of Mn oxides by organics (I). Env. Sci. Technol. 18: 450–460.

    Article  CAS  Google Scholar 

  • Stone AT & Morgan JJ (1984b) Reduction and dissolution of Mn oxides by organics (II). Env. Sci. Technol. 18: 617–624.

    Article  CAS  Google Scholar 

  • Stumm W & Morgan JJ (1996) Aquatic Chemistry 3rd edn. John Wiley, NY.

    Google Scholar 

  • Thamdrup B, Glud RN & Hansen JW (1994) Manganese oxidation and in situ manganese fluxes from a coastal sediment. Geochim. Cosmochim. Acta 58: 2577–2583.

    Article  Google Scholar 

  • Urrutia MM, Roden EE & Zachara JM (1999) Influence of aqueous and solid-phase Fe(II) complexants on microbial reduction of crystalline iron(III) oxides. Environ. Sci. Tech. 33: 4022–4028.

    Article  CAS  Google Scholar 

  • Urrutia MM, Roden EE, Fredrickson JK & Zachara JM (1998) Microbial and surface chemistry controls on reduction of synthetic Fe(III) oxide minerals by the dissimilatory iron-reducing bacterium Shewanella alga. Geomicrobiol. J. 15: 269–291.

    Article  CAS  Google Scholar 

  • Venkateswaren K, Dollhopf ME, Aller R, Stackebrandt E & Nealson KH (1998) Shewanella amazonensis sp. nov., a metal-reducing facultative anaerobe from Amazonian shelf muds. Int. J. Syst. Bact. 48: 965–972.

    Article  Google Scholar 

  • Venkateswaren K, Moser DP, Dollhopf ME, Lies DP, Saffarini DA, MacGregor BJ, Ringelberg DB, White DC, Nishijima M, Sano H, Burghardt J, Stackebrandt E & Nealson KH (1999). Polyphasic taxonomy of the genus Shewanella: description of Shewanella oneidensis sp. nov. Int. J. Syst. Bacteriol. 49: 705–724.

    Article  Google Scholar 

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Correspondence to Kenneth H. Nealson.

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Nealson, K.H., Belz, A. & McKee, B. Breathing metals as a way of life: geobiology in action. Antonie Van Leeuwenhoek 81, 215–222 (2002). https://doi.org/10.1023/A:1020518818647

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