Applied and Environmental Microbiology, May 2002, p. 2294-2299, Vol. 68, No. 5
0099-2240/02/$04.00+0 DOI: 10.1128/AEM.68.5.2294-2299.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.
Mechanisms for Accessing Insoluble Fe(III) Oxide during Dissimilatory Fe(III) Reduction by Geothrix fermentans
Kelly P. Nevin and Derek R. Lovley*
Department of Microbiology, University of Massachusetts, Amherst, Massachusetts 01003
Received 15 October 2001/
Accepted 12 February 2002
Mechanisms for Fe(III) oxide reduction were investigated in Geothrix fermentans, a dissimilatory Fe(III)-reducing microorganism found within the Fe(III) reduction zone of subsurface environments. Culture filtrates of G. fermentans stimulated the reduction of poorly crystalline Fe(III) oxide by washed cell suspensions, suggesting that G. fermentans released one or more extracellular compounds that promoted Fe(III) oxide reduction. In order to determine if G. fermentans released electron-shuttling compounds, poorly crystalline Fe(III) oxide was incorporated into microporous alginate beads, which prevented contact between G. fermentans and the Fe(III) oxide. G. fermentans reduced the Fe(III) within the beads, suggesting that one of the compounds that G. fermentans releases is an electron-shuttling compound that can transfer electrons from the cell to Fe(III) oxide that is not in contact with the organism. Analysis of culture filtrates by thin-layer chromatography suggested that the electron shuttle has characteristics similar to those of a water-soluble quinone. Analysis of filtrates by ion chromatography demonstrated that there was as much as 250 µM dissolved Fe(III) in cultures of G. fermentans growing with Fe(III) oxide as the electron acceptor, suggesting that G. fermentans released one or more compounds capable of chelating and solubilizing Fe(III). Solubilizing Fe(III) is another strategy for alleviating the need for contact between cells and Fe(III) oxide for Fe(III) reduction. This is the first demonstration of a microorganism that, in defined medium without added electron shuttles or chelators, can reduce Fe(III) derived from Fe(III) oxide without directly contacting the Fe(III) oxide. These results are in marked contrast to those with Geobacter metallireducens, which does not produce electron shuttles or Fe(III) chelators. These results demonstrate that phylogenetically distinct Fe(III)-reducing microorganisms may use significantly different strategies for Fe(III) reduction. Thus, it is important to know which Fe(III)-reducing microorganisms predominate in a given environment in order to understand the mechanisms for Fe(III) reduction in the environment of interest.
* Corresponding author. Mailing address: Department of Microbiology, University of Massachusetts, Amherst, MA 01003. Phone: 413-545-9651. Fax: 413-545-1578. E-mail: dlovley{at}microbio.umass.edu.
Applied and Environmental Microbiology, May 2002, p. 2294-2299, Vol. 68, No. 5
0099-2240/02/$04.00+0 DOI: 10.1128/AEM.68.5.2294-2299.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.
This article has been cited by other articles:
-
von Canstein, H., Ogawa, J., Shimizu, S., Lloyd, J. R.
(2008). Secretion of Flavins by Shewanella Species and Their Role in Extracellular Electron Transfer. Appl. Environ. Microbiol.
74: 615-623
[Abstract]
[Full Text]
-
Chatfield, C. H., Cianciotto, N. P.
(2007). The Secreted Pyomelanin Pigment of Legionella pneumophila Confers Ferric Reductase Activity. Infect. Immun.
75: 4062-4070
[Abstract]
[Full Text]
-
Korenevsky, A., Beveridge, T. J.
(2007). The surface physicochemistry and adhesiveness of Shewanella are affected by their surface polysaccharides. Microbiology
153: 1872-1883
[Abstract]
[Full Text]
-
Reguera, G., Pollina, R. B., Nicoll, J. S., Lovley, D. R.
(2007). Possible Nonconductive Role of Geobacter sulfurreducens Pilus Nanowires in Biofilm Formation. J. Bacteriol.
189: 2125-2127
[Abstract]
[Full Text]
-
Hori, T., Noll, M., Igarashi, Y., Friedrich, M. W., Conrad, R.
(2007). Identification of Acetate-Assimilating Microorganisms under Methanogenic Conditions in Anoxic Rice Field Soil by Comparative Stable Isotope Probing of RNA. Appl. Environ. Microbiol.
73: 101-109
[Abstract]
[Full Text]
-
Kwon, M. J., Finneran, K. T.
(2006). Microbially Mediated Biodegradation of Hexahydro-1,3,5-Trinitro-1,3,5- Triazine by Extracellular Electron Shuttling Compounds. Appl. Environ. Microbiol.
72: 5933-5941
[Abstract]
[Full Text]
-
McLean, J. E., Dupont, R. R., Sorensen, D. L.
(2006). Iron and arsenic release from aquifer solids in response to biostimulation.. J. Environ. Qual.
35: 1193-1203
[Abstract]
[Full Text]
-
Ruebush, S. S., Brantley, S. L., Tien, M.
(2006). Reduction of Soluble and Insoluble Iron Forms by Membrane Fractions of Shewanella oneidensis Grown under Aerobic and Anaerobic Conditions. Appl. Environ. Microbiol.
72: 2925-2935
[Abstract]
[Full Text]
-
Mahadevan, R., Bond, D. R., Butler, J. E., Esteve-Nunez, A., Coppi, M. V., Palsson, B. O., Schilling, C. H., Lovley, D. R.
(2006). Characterization of Metabolism in the Fe(III)-Reducing Organism Geobacter sulfurreducens by Constraint-Based Modeling. Appl. Environ. Microbiol.
72: 1558-1568
[Abstract]
[Full Text]
-
Feinberg, L. F., Holden, J. F.
(2006). Characterization of Dissimilatory Fe(III) versus NO3- Reduction in the Hyperthermophilic Archaeon Pyrobaculum aerophilum. J. Bacteriol.
188: 525-531
[Abstract]
[Full Text]
-
Mehta, T., Coppi, M. V., Childers, S. E., Lovley, D. R.
(2005). Outer Membrane c-Type Cytochromes Required for Fe(III) and Mn(IV) Oxide Reduction in Geobacter sulfurreducens. Appl. Environ. Microbiol.
71: 8634-8641
[Abstract]
[Full Text]
-
Islam, F. S., Boothman, C., Gault, A. G., Polya, D. A., Lloyd, J. R.
(2005). Potential role of the Fe(III)-reducing bacteria Geobacter and Geothrix in controlling arsenic solubility in Bengal delta sediments. Mineral Mag
69: 865-875
[Abstract]
[Full Text]
-
Leang, C., Adams, L. A., Chin, K.-J., Nevin, K. P., Methe, B. A., Webster, J., Sharma, M. L., Lovley, D. R.
(2005). Adaptation to Disruption of the Electron Transfer Pathway for Fe(III) Reduction in Geobacter sulfurreducens. J. Bacteriol.
187: 5918-5926
[Abstract]
[Full Text]
-
Lies, D. P., Hernandez, M. E., Kappler, A., Mielke, R. E., Gralnick, J. A., Newman, D. K.
(2005). Shewanella oneidensis MR-1 Uses Overlapping Pathways for Iron Reduction at a Distance and by Direct Contact under Conditions Relevant for Biofilms. Appl. Environ. Microbiol.
71: 4414-4426
[Abstract]
[Full Text]
-
Nevin, K. P., Holmes, D. E., Woodard, T. L., Hinlein, E. S., Ostendorf, D. W., Lovley, D. R.
(2005). Geobacter bemidjiensis sp. nov. and Geobacter psychrophilus sp. nov., two novel Fe(III)-reducing subsurface isolates. Int. J. Syst. Evol. Microbiol.
55: 1667-1674
[Abstract]
[Full Text]
-
Leang, C., Lovley, D. R.
(2005). Regulation of two highly similar genes, omcB and omcC, in a 10 kb chromosomal duplication in Geobacter sulfurreducens. Microbiology
151: 1761-1767
[Abstract]
[Full Text]
-
Methe, B. A., Webster, J., Nevin, K., Butler, J., Lovley, D. R.
(2005). DNA Microarray Analysis of Nitrogen Fixation and Fe(III) Reduction in Geobacter sulfurreducens. Appl. Environ. Microbiol.
71: 2530-2538
[Abstract]
[Full Text]
-
Bond, D. R., Lovley, D. R.
(2005). Evidence for Involvement of an Electron Shuttle in Electricity Generation by Geothrix fermentans. Appl. Environ. Microbiol.
71: 2186-2189
[Abstract]
[Full Text]
-
DiChristina, T. J., Fredrickson, J. K., Zachara, J. M.
(2005). Enzymology of Electron Transport: Energy Generation With Geochemical Consequences. Reviews in Mineralogy and Geochemistry
59: 27-52
[Full Text]
-
Kappler, A., Straub, K. L.
(2005). Geomicrobiological Cycling of Iron. Reviews in Mineralogy and Geochemistry
59: 85-108
[Full Text]
-
Chin, K.-J., Esteve-Nunez, A., Leang, C., Lovley, D. R.
(2004). Direct Correlation between Rates of Anaerobic Respiration and Levels of mRNA for Key Respiratory Genes in Geobacter sulfurreducens. Appl. Environ. Microbiol.
70: 5183-5189
[Abstract]
[Full Text]
-
Myers, C. R., Myers, J. M.
(2004). Shewanella oneidensis MR-1 Restores Menaquinone Synthesis to a Menaquinone-Negative Mutant. Appl. Environ. Microbiol.
70: 5415-5425
[Abstract]
[Full Text]
-
Butler, J. E., Kaufmann, F., Coppi, M. V., Nunez, C., Lovley, D. R.
(2004). MacA, a Diheme c-Type Cytochrome Involved in Fe(III) Reduction by Geobacter sulfurreducens. J. Bacteriol.
186: 4042-4045
[Abstract]
[Full Text]
-
Kashefi, K., Holmes, D. E., Baross, J. A., Lovley, D. R.
(2003). Thermophily in the Geobacteraceae: Geothermobacter ehrlichii gen. nov., sp. nov., a Novel Thermophilic Member of the Geobacteraceae from the "Bag City" Hydrothermal Vent. Appl. Environ. Microbiol.
69: 2985-2993
[Abstract]
[Full Text]
-
Leang, C., Coppi, M. V., Lovley, D. R.
(2003). OmcB, a c-Type Polyheme Cytochrome, Involved in Fe(III) Reduction in Geobacter sulfurreducens. J. Bacteriol.
185: 2096-2103
[Abstract]
[Full Text]
-
Bond, D. R., Lovley, D. R.
(2003). Electricity Production by Geobacter sulfurreducens Attached to Electrodes. Appl. Environ. Microbiol.
69: 1548-1555
[Abstract]
[Full Text]
-
Holmes, D. E., Finneran, K. T., O'Neil, R. A., Lovley, D. R.
(2002). Enrichment of Members of the Family Geobacteraceae Associated with Stimulation of Dissimilatory Metal Reduction in Uranium-Contaminated Aquifer Sediments. Appl. Environ. Microbiol.
68: 2300-2306
[Abstract]
[Full Text]
Copyright © 2002 by the American Society for Microbiology. All rights reserved.