Antonie van Leeuwenhoek

, Volume 81, Issue 1–4, pp 215–222 | Cite as

Breathing metals as a way of life: geobiology in action

  • Kenneth H. NealsonEmail author
  • Andrea Belz
  • Brent McKee


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.

anaerobic respiration dissimilatory metabolism metal reduction solubilization of metals Shewanella transition metals 


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  1. 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
  2. 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.PubMedGoogle Scholar
  3. Aller RC (1990) Bioturbation and manganese cycling in hemipelagic sediments. Phil. Trans. R. Soc. Lond. A. 331: 51–68.Google Scholar
  4. Aller RC, Aller J, Mackin NJ & Rude P (1991) Biogeochemical processes in Amazon shelf sediments. Oceanog. April: 27-32.Google Scholar
  5. 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).Google Scholar
  6. Belz AP, Ahn CC, Andrews MY & Nealson KH (2002a) Effects of solution chemistry in manganese reduction by Shewanella oneidensis Envir. Sci. Technol. (in press).Google Scholar
  7. Belz AP, Ahn CC & Nealson KH (2002b) Characterization of manganese oxides using electron energy loss spectrometry Amer. Mineralog. (in press).Google Scholar
  8. 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.Google Scholar
  9. Burdige DJ & Nealson KH (1986) Chemical and microbiological studies of sulfide-mediated manganese reduction. Geomicrobiol. J. 4: 361–387.CrossRefGoogle Scholar
  10. Burdige DJ, Dhakar SP & Nealson KH (1992) Effects of Mn oxide mineralogy on microbial and chemical Mn reduction. Geomicrobiol. J. 10: 27–48.Google Scholar
  11. 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.PubMedCrossRefGoogle Scholar
  12. Das A & Caccavo F (2001) Adhesion of dissimilatory Fe(III) reducing bacteria S. algae to crystalline Fe(III) oxides Curr. Microbiol. 42: 151–154.PubMedCrossRefGoogle Scholar
  13. Das A & Caccavo F (2000) Dissimilatory iron oxide reduction by S. algae BrY requires adhesion. Curr. Microbiol. 40: 344–347.PubMedCrossRefGoogle Scholar
  14. 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
  15. 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.CrossRefGoogle Scholar
  16. Gorby YA & Lovley DR (1992) Enzymatic uranium precipitation. Envir. Sci. Technol. 26: 205–207.CrossRefGoogle Scholar
  17. Hernandez ME & Newman DK (2001) Extracellular electron transfer. Cell. Mol. Life Sci. 58: 1562–1571.PubMedCrossRefGoogle Scholar
  18. 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
  19. 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.Google Scholar
  20. 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.PubMedGoogle Scholar
  21. 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
  22. 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.CrossRefGoogle Scholar
  23. MacGregor B, Moser D, Nealson KH & Stahl DA (1997) Crenarchaeota in Lake Michigan sediments. Appl. Environ. Microbiol. 63: 1178–1181.PubMedGoogle Scholar
  24. 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.PubMedCrossRefGoogle Scholar
  25. Myers C & Nealson KH (1988a) Bacterial Mn reduction and growth with Mn oxdie as the sole electron acceptor. Science 240: 1319–1321.PubMedGoogle Scholar
  26. Myers C & Nealson KH (1988b) Microbial reduction of Mn oxides: interactions with iron and sulfur. Geochim. Cosmochim. Acta 52: 2727–2732.CrossRefGoogle Scholar
  27. Nealson KH (1997) Sediment bacteria: who's there, what are they doing, and what's new? Annu. Rev. Earth Planet. Sci. 25: 403–434.PubMedCrossRefGoogle Scholar
  28. Nealson KH & Little B (1997) Breathing Mn and Fe: solid state respiration. Adv. Appl. Microbiol. 45: 213–239.CrossRefGoogle Scholar
  29. 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
  30. Newman DK & Kolter R (2000) A role for excreted quinones in extracellular electron transfer. Nature 405: 94–97.PubMedCrossRefGoogle Scholar
  31. 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.CrossRefGoogle Scholar
  32. 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.PubMedCrossRefGoogle Scholar
  33. Stone AT & Morgan JJ (1984a) Reduction and dissolution of Mn oxides by organics (I). Env. Sci. Technol. 18: 450–460.CrossRefGoogle Scholar
  34. Stone AT & Morgan JJ (1984b) Reduction and dissolution of Mn oxides by organics (II). Env. Sci. Technol. 18: 617–624.CrossRefGoogle Scholar
  35. Stumm W & Morgan JJ (1996) Aquatic Chemistry 3rd edn. John Wiley, NY.Google Scholar
  36. Thamdrup B, Glud RN & Hansen JW (1994) Manganese oxidation and in situ manganese fluxes from a coastal sediment. Geochim. Cosmochim. Acta 58: 2577–2583.CrossRefGoogle Scholar
  37. 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.CrossRefGoogle Scholar
  38. 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.CrossRefGoogle Scholar
  39. 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.CrossRefGoogle Scholar
  40. 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.CrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  1. 1.Department of Earth SciencesUniversity of Southern CaliforniaLos AngelesUSA
  2. 2.Environmental EngineeringCalifornia Institute of TechnologyPasadenaUSA
  3. 3.Department of GeologyTulane UniversityNew OrleansUSA

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