Novel Mode of Microbial Energy Metabolism: Organic Carbon Oxidation Coupled to Dissimilatory Reduction of Iron or Manganese
Open accessAbstract
A dissimilatory Fe(III)- and Mn(IV)-reducing microorganism was isolated from freshwater sediments of the Potomac River, Maryland. The isolate, designated GS-15, grew in defined anaerobic medium with acetate as the sole electron donor and Fe(III), Mn(IV), or nitrate as the sole electron acceptor. GS-15 oxidized acetate to carbon dioxide with the concomitant reduction of amorphic Fe(III) oxide to magnetite (Fe(3)O(4)). When Fe(III) citrate replaced amorphic Fe(III) oxide as the electron acceptor, GS-15 grew faster and reduced all of the added Fe(III) to Fe(II). GS-15 reduced a natural amorphic Fe(III) oxide but did not significantly reduce highly crystalline Fe(III) forms. Fe(III) was reduced optimally at pH 6.7 to 7 and at 30 to 35 degrees C. Ethanol, butyrate, and propionate could also serve as electron donors for Fe(III) reduction. A variety of other organic compounds and hydrogen could not. MnO(2) was completely reduced to Mn(II), which precipitated as rhodochrosite (MnCO(3)). Nitrate was reduced to ammonia. Oxygen could not serve as an electron acceptor, and it inhibited growth with the other electron acceptors. This is the first demonstration that microorganisms can completely oxidize organic compounds with Fe(III) or Mn(IV) as the sole electron acceptor and that oxidation of organic matter coupled to dissimilatory Fe(III) or Mn(IV) reduction can yield energy for microbial growth. GS-15 provides a model for how enzymatically catalyzed reactions can be quantitatively signi…
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Froelich, P. N., Klinkhammer, G. P., Bender, M. L., Luedtke, N. A., Heath, G. R., Cullen, D., Dauphin, P., Hammond, D., Hartman, B., & Maynard, V. (1979) · Geochimica et Cosmochimica Acta · doi:10.1016/0016-7037(79)90095-4 · Cited by 3,368 · see citing works
Reduction of Ferric Iron by Heterotrophic Bacteria in Lake Sediments
Jones, J. G., Gardener, S., & Simon, B. M. (1984) · Microbiology · doi:10.1099/00221287-130-1-45 · Cited by 78 · see citing works
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Humic substances as electron acceptors for microbial respiration
Lovley, D. R., Coates, J. D., Blunt-Harris, E. L., Phillips, E. J. P., & Woodward, J. C. (1996) · Nature · doi:10.1038/382445a0 · Cited by 1,834 · see citing works
Self-citationDissimilatory Fe(III) and Mn(IV) Reduction
Lovley, D. R., Holmes, D. E., & Nevin, K. P. (2004) · Advances in Microbial Physiology · doi:10.1016/s0065-2911(04)49005-5 · Cited by 1,471 · see citing works
Self-citationMicrobial reduction of uranium
Lovley, D. R., Phillips, E. J. P., Gorby, Y. A., & Landa, E. R. (1991) · Nature · doi:10.1038/350413a0 · Cited by 1,446 · see citing works
Self-citationBacterial Manganese Reduction and Growth with Manganese Oxide as the Sole Electron Acceptor
Myers, C. R., & Nealson, K. H. (1988) · Science · doi:10.1126/science.240.4857.1319 · Cited by 1,365 · see citing works
Role of metal-reducing bacteria in arsenic release from Bengal delta sediments
Islam, F. S., Gault, A. G., Boothman, C., Polya, D. A., Charnock, J. M., Chatterjee, D., & Lloyd, J. R. (2004) · Nature · doi:10.1038/nature02638 · Cited by 1,241 · see citing works
Lovley, D. R., Giovannoni, S. J., White, D. C., Champine, J. E., Phillips, E. J. P., Gorby, Y. A., & Goodwin, S. (1993) · Archives of Microbiology · doi:10.1007/bf00290916 · Cited by 983 · see citing works
Self-citationLovley, D. R. (1993) · Annual Review of Microbiology · doi:10.1146/annurev.mi.47.100193.001403 · Cited by 1,021 · see citing works
Self-citationCaccavo, F., Lonergan, D. J., Lovley, D. R., Davis, M., Stolz, J. F., & McInerney, M. J. (1994) · Applied and Environmental Microbiology · doi:10.1128/aem.60.10.3752-3759.1994 · Cited by 896 · see citing works
Self-citationThe interplay of microbially mediated and abiotic reactions in the biogeochemical Fe cycle
Melton, E. D., Swanner, E. D., Behrens, S., Schmidt, C., & Kappler, A. (2014) · Nature Reviews Microbiology · doi:10.1038/nrmicro3347 · Cited by 899 · see citing works
Fredrickson, J. K., Zachara, J. M., Kennedy, D. W., Dong, H., Onstott, T. C., Hinman, N. W., & Li, S.-M. (1998) · Geochimica et Cosmochimica Acta · doi:10.1016/s0016-7037(98)00243-9 · Cited by 807 · see citing works
Bacterial Manganese and Iron Reduction in Aquatic Sediments
Thamdrup, B. (2000) · Advances in Microbial Ecology · doi:10.1007/978-1-4615-4187-5_2 · Cited by 659 · see citing works
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Lloyd, J. R. (2003) · FEMS Microbiology Reviews · doi:10.1016/s0168-6445(03)00044-5 · Cited by 654 · see citing works
Hansel, C. M., Benner, S. G., Neiss, J., Dohnalkova, A., Kukkadapu, R. K., & Fendorf, S. (2003) · Geochimica et Cosmochimica Acta · doi:10.1016/s0016-7037(03)00276-x · Cited by 634 · see citing works
Development of a Genetic System for <i>Geobacter sulfurreducens</i>
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Self-citationReduction of Fe(III) in sediments by sulphate-reducing bacteria
Coleman, M. L., Hedrick, D. B., Lovley, D. R., White, D. C., & Pye, K. (1993) · Nature · doi:10.1038/361436a0 · Cited by 479 · see citing works
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Self-citationPhylogenetic analysis of dissimilatory Fe(III)-reducing bacteria
Lonergan, D. J., Jenter, H. L., Coates, J. D., Phillips, E. J., Schmidt, T. M., & Lovley, D. R. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.8.2402-2408.1996 · Cited by 380 · see citing works
Self-citationCoates, J. D., Ellis, D. J., Gaw, C. V., & Lovley, D. R. (1999) · International Journal of Systematic and Evolutionary Microbiology · doi:10.1099/00207713-49-4-1615 · Cited by 382 · see citing works
Self-citationLLOYD, J. R., LEANG, C., MYERSON, A. L. H., COPPI, M. V., CUIFO, S., METHE, B., SANDLER, S. J., & LOVLEY, D. R. (2003) · Biochemical Journal · doi:10.1042/bj20020597 · Cited by 373 · see citing works
Self-citationOremland, R. S., Hollibaugh, J. T., Maest, A. S., Presser, T. S., Miller, L. G., & Culbertson, C. W. (1989) · Applied and Environmental Microbiology · doi:10.1128/aem.55.9.2333-2343.1989 · Cited by 364 · see citing works
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Nevin, K. P., & Lovley, D. R. (2002) · Geomicrobiology Journal · doi:10.1080/01490450252864253 · Cited by 330 · see citing works
Self-citationLovley, D. R., Phillips, E. J. P., & Lonergan, D. J. (1989) · Applied and Environmental Microbiology · doi:10.1128/aem.55.3.700-706.1989 · Cited by 313 · see citing works
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Kashefi, K., & Lovley, D. R. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.3.1050-1056.2000 · Cited by 292 · see citing works
Self-citationDirect and Fe(II)-Mediated Reduction of Technetium by Fe(III)-Reducing Bacteria
Lloyd, J. R., Sole, V. A., Van Praagh, C. V. G., & Lovley, D. R. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.9.3743-3749.2000 · Cited by 283 · see citing works
Self-citationGREENE, A. C., PATEL, B. K. C., & SHEEHY, A. J. (1997) · International Journal of Systematic Bacteriology · doi:10.1099/00207713-47-2-505 · Cited by 243 · see citing works
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Johnson, J. E., Webb, S. M., Ma, C., & Fischer, W. W. (2016) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2015.10.027 · Cited by 245 · see citing works
Oremland, R. S., Blum, J. S., Culbertson, C. W., Visscher, P. T., Miller, L. G., Dowdle, P., & Strohmaier, F. E. (1994) · Applied and Environmental Microbiology · doi:10.1128/aem.60.8.3011-3019.1994 · Cited by 232 · see citing works
Leang, C., Ueki, T., Nevin, K. P., & Lovley, D. R. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.02891-12 · Cited by 202 · see citing works
Self-citationReductive Precipitation of Gold by Dissimilatory Fe(III)-Reducing <i>Bacteria</i> and <i>Archaea</i>
Kashefi, K., Tor, J. M., Nevin, K. P., & Lovley, D. R. (2001) · Applied and Environmental Microbiology · doi:10.1128/aem.67.7.3275-3279.2001 · Cited by 200 · see citing works
Self-citationLloyd, J. R., Ridley, J., Khizniak, T., Lyalikova, N. N., & Macaskie, L. E. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.6.2691-2696.1999 · Cited by 187 · see citing works
Lovley, D. R., & Anderson, R. T. (2000) · Hydrogeology Journal · doi:10.1007/pl00010974 · Cited by 183 · see citing works
Self-citationLear, G., Song, B., Gault, A. G., Polya, D. A., & Lloyd, J. R. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.01654-06 · Cited by 170 · see citing works
MACY, J. M., NUNAN, K., HAGEN, K. D., DIXON, D. R., HARBOUR, P. J., CAHILL, M., & SLY, L. I. (1996) · International Journal of Systematic Bacteriology · doi:10.1099/00207713-46-4-1153 · Cited by 164 · see citing works
Biogeochemical and Environmental Factors in Fe Biomineralization: Magnetite and Siderite Formation
Roh, Y., Zhang, C.-L., Vali, H., Lauf, R. J., Zhou, J., & Phelps, T. J. (2003) · Clays and Clay Minerals · doi:10.1346/ccmn.2003.510110 · Cited by 159 · see citing works
Geovibrio ferrireducens , a phylogenetically distinct dissimilatory Fe(III)-reducing bacterium
Caccavo Jr., F., Coates, J. D., Rossello-Mora, R. A., Ludwig, W., Schleifer, K. H., Lovley, D. R., & McInerney, M. J. (1996) · Archives of Microbiology · doi:10.1007/s002030050340 · Cited by 144 · see citing works
Self-citationReduction of humic substances and Fe(III) by hyperthermophilic microorganisms
Lovley, D. R., Kashefi, K., Vargas, M., Tor, J. M., & Blunt-Harris, E. L. (2000) · Chemical Geology · doi:10.1016/s0009-2541(00)00209-6 · Cited by 124 · see citing works
Self-citationBiological Reduction and Removal of Np(V) by Two Microorganisms
Lloyd, J. R., Yong, P., & Macaskie, L. E. (2000) · Environmental Science & Technology · doi:10.1021/es990394y · Cited by 96 · see citing works
Methanogens Rapidly Transition from Methane Production to Iron Reduction
Sivan, O., Shusta, S. S., & Valentine, D. L. (2016) · Geobiology · doi:10.1111/gbi.12172 · Cited by 94 · see citing works
Inorganic synthesis of Fe–Ca–Mg carbonates at low temperature
Romanek, C. S., Jiménez-López, C., Navarro, A. R., Sánchez-Román, M., Sahai, N., & Coleman, M. (2009) · Geochimica et Cosmochimica Acta · doi:10.1016/j.gca.2009.05.065 · Cited by 94 · see citing works
Isolation of U(VI) reduction-deficient mutants of<i>Shewanella putrefaciens</i>
Wade, R., & DiChristina, T. J. (2000) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2000.tb09005.x · Cited by 93 · see citing works
PERCAK‐DENNETT, E. M., BEARD, B. L., XU, H., KONISHI, H., JOHNSON, C. M., & RODEN, E. E. (2011) · Geobiology · doi:10.1111/j.1472-4669.2011.00277.x · Cited by 83 · see citing works
Gorby, Y. A., Caccavo, & Bolton, H. (1998) · Environmental Science & Technology · doi:10.1021/es970516r · Cited by 77 · see citing works
Isolation and Characterization of a Mo <sup>6+</sup> -Reducing Bacterium
Ghani, B., Takai, M., Hisham, N. Z., Kishimoto, N., Ismail, A. K. M., Tano, T., & Sugio, T. (1993) · Applied and Environmental Microbiology · doi:10.1128/aem.59.4.1176-1180.1993 · Cited by 64 · see citing works
Yong, P., Farr, J. P. G., Harris, I. R., & Macaskie, L. E. (2002) · Biotechnology Letters · doi:10.1023/a:1014141610562 · Cited by 45 · see citing works
Differential cytochrome content and reductase activity in Geospirillum barnesii strain SeS3
Stolz, J. F., Gugliuzza, T., Blum, J. S., Oremland, R., & Murillo, F. M. (1997) · Archives of Microbiology · doi:10.1007/s002030050408 · Cited by 44 · see citing works
Microbial metal-ion reduction and Mars: extraterrestrial expectations?
Nealson, K. H., & Cox, B. L. (2002) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(02)00326-0 · Cited by 33 · see citing works
- Authors
- Lovley, D. R., & Phillips, E. J. P.
- Affiliations
- United States Geological Survey (US)
- Venue
- Applied and Environmental Microbiology
- Publisher
- American Society for Microbiology
- Published
- 1988-06
- Volume
- 54
- Issue
- 6
- Pages
- 1472-1480
- ISSN
- 0099-2240 (ISSN-L)
- 1098-5336
- PMC
- PMC202682
- OpenAlex
- W2164513556
- Cited by
- 2,395
- References
- 2
- Citations by year
- 2026: 70 · 2025: 62 · 2024: 69 · 2023: 77 · 2022: 74 · 2021: 78 · 2020: 73 · 2019: 111 · 2018: 113 · 2017: 112 · 2016: 97 · 2015: 120 · 2014: 112 · 2013: 97 · 2012: 112
- FWCI
- 32.85
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Applied and Environmental Microbiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- ScholarWorks@UMassAmherst (University of Massachusetts Amherst) (submittedVersion)
- Topics
- Physical Sciences › Environmental Science › Environmental Engineering › Microbial Fuel Cells and Bioremediation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Keywords
- dissimilatory iron reduction, organic carbon oxidation, acetate oxidation, anaerobic microorganisms, Fe(III) oxide reduction, magnetite, rhodochrosite, nitrate reduction, electron donors, freshwater sediments, Potomac River, microbial energy metabolism
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