Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1996 Apr;178(8):2402–2408. doi: 10.1128/jb.178.8.2402-2408.1996

Phylogenetic analysis of dissimilatory Fe(III)-reducing bacteria.

D J Lonergan 1, H L Jenter 1, J D Coates 1, E J Phillips 1, T M Schmidt 1, D R Lovley 1
PMCID: PMC177952  PMID: 8636045

Abstract

Evolutionary relationships among strictly anaerobic dissimilatory Fe(III)-reducing bacteria obtained from a diversity of sedimentary environments were examined by phylogenetic analysis of 16S rRNA gene sequences. Members of the genera Geobacter, Desulfuromonas, Pelobacter, and Desulfuromusa formed a monophyletic group within the delta subdivision of the class Proteobacteria. On the basis of their common ancestry and the shared ability to reduce Fe(III) and/or S0, we propose that this group be considered a single family, Geobacteraceae. Bootstrap analysis, characteristic nucleotides, and higher-order secondary structures support the division of Geobacteraceae into two subgroups, designated the Geobacter and Desulfuromonas clusters. The genus Desulfuromusa and Pelobacter acidigallici make up a distinct branch within the Desulfuromonas cluster. Several members of the family Geobacteraceae, none of which reduce sulfate, were found to contain the target sequences of probes that have been previously used to define the distribution of sulfate-reducing bacteria and sulfate-reducing bacterium-like microorganisms. The recent isolations of Fe(III)-reducing microorganisms distributed throughout the domain Bacteria suggest that development of 16S rRNA probes that would specifically target all Fe(III) reducers may not be feasible. However, all of the evidence suggests that if a 16S rRNA sequence falls within the family Geobacteraceae, then the organism has the capacity for Fe(III) reduction. The suggestion, based on geological evidence, that Fe(III) reduction was the first globally significant process for oxidizing organic matter back to carbon dioxide is consistent with the finding that acetate-oxidizing Fe(III) reducers are phylogenetically diverse.

Full Text

The Full Text of this article is available as a PDF (278.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Amann R. I., Binder B. J., Olson R. J., Chisholm S. W., Devereux R., Stahl D. A. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol. 1990 Jun;56(6):1919–1925. doi: 10.1128/aem.56.6.1919-1925.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Amann R. I., Krumholz L., Stahl D. A. Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol. 1990 Feb;172(2):762–770. doi: 10.1128/jb.172.2.762-770.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Amann R. I., Ludwig W., Schleifer K. H. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev. 1995 Mar;59(1):143–169. doi: 10.1128/mr.59.1.143-169.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Amann R. I., Stromley J., Devereux R., Key R., Stahl D. A. Molecular and microscopic identification of sulfate-reducing bacteria in multispecies biofilms. Appl Environ Microbiol. 1992 Feb;58(2):614–623. doi: 10.1128/aem.58.2.614-623.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Balashova V. V. Ispol'zovanie molekuliarnoi sery v kachestve okislitelia H2 fakul'tativno-anaerobnym Pseudomonasom. Mikrobiologiia. 1985 Mar-Apr;54(2):324–326. [PubMed] [Google Scholar]
  6. Blumentals I. I., Itoh M., Olson G. J., Kelly R. M. Role of Polysulfides in Reduction of Elemental Sulfur by the Hyperthermophilic Archaebacterium Pyrococcus furiosus. Appl Environ Microbiol. 1990 May;56(5):1255–1262. doi: 10.1128/aem.56.5.1255-1262.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Boone D. R., Liu Y., Zhao Z. J., Balkwill D. L., Drake G. R., Stevens T. O., Aldrich H. C. Bacillus infernus sp. nov., an Fe(III)- and Mn(IV)-reducing anaerobe from the deep terrestrial subsurface. Int J Syst Bacteriol. 1995 Jul;45(3):441–448. doi: 10.1099/00207713-45-3-441. [DOI] [PubMed] [Google Scholar]
  8. Caccavo F., Blakemore R. P., Lovley D. R. A Hydrogen-Oxidizing, Fe(III)-Reducing Microorganism from the Great Bay Estuary, New Hampshire. Appl Environ Microbiol. 1992 Oct;58(10):3211–3216. doi: 10.1128/aem.58.10.3211-3216.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Caccavo F., Jr, Lonergan D. J., Lovley D. R., Davis M., Stolz J. F., McInerney M. J. Geobacter sulfurreducens sp. nov., a hydrogen- and acetate-oxidizing dissimilatory metal-reducing microorganism. Appl Environ Microbiol. 1994 Oct;60(10):3752–3759. doi: 10.1128/aem.60.10.3752-3759.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Coates J. D., Lonergan D. J., Philips E. J., Jenter H., Lovley D. R. Desulfuromonas palmitatis sp. nov., a marine dissimilatory Fe(III) reducer that can oxidize long-chain fatty acids. Arch Microbiol. 1995 Dec;164(6):406–413. [PubMed] [Google Scholar]
  11. DeLong E. F., Wickham G. S., Pace N. R. Phylogenetic stains: ribosomal RNA-based probes for the identification of single cells. Science. 1989 Mar 10;243(4896):1360–1363. doi: 10.1126/science.2466341. [DOI] [PubMed] [Google Scholar]
  12. Devereux R., Delaney M., Widdel F., Stahl D. A. Natural relationships among sulfate-reducing eubacteria. J Bacteriol. 1989 Dec;171(12):6689–6695. doi: 10.1128/jb.171.12.6689-6695.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Devereux R., He S. H., Doyle C. L., Orkland S., Stahl D. A., LeGall J., Whitman W. B. Diversity and origin of Desulfovibrio species: phylogenetic definition of a family. J Bacteriol. 1990 Jul;172(7):3609–3619. doi: 10.1128/jb.172.7.3609-3619.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Eden P. A., Schmidt T. M., Blakemore R. P., Pace N. R. Phylogenetic analysis of Aquaspirillum magnetotacticum using polymerase chain reaction-amplified 16S rRNA-specific DNA. Int J Syst Bacteriol. 1991 Apr;41(2):324–325. doi: 10.1099/00207713-41-2-324. [DOI] [PubMed] [Google Scholar]
  15. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol. 1981;17(6):368–376. doi: 10.1007/BF01734359. [DOI] [PubMed] [Google Scholar]
  16. Finster K., Bak F. Complete oxidation of propionate, valerate, succinate, and other organic compounds by newly isolated types of marine, anaerobic, mesophilic, gram-negative, sulfur-reducing eubacteria. Appl Environ Microbiol. 1993 May;59(5):1452–1460. doi: 10.1128/aem.59.5.1452-1460.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Giovannoni S. J., DeLong E. F., Olsen G. J., Pace N. R. Phylogenetic group-specific oligodeoxynucleotide probes for identification of single microbial cells. J Bacteriol. 1988 Feb;170(2):720–726. doi: 10.1128/jb.170.2.720-726.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Laverman A. M., Blum J. S., Schaefer J. K., Phillips E., Lovley D. R., Oremland R. S. Growth of Strain SES-3 with Arsenate and Other Diverse Electron Acceptors. Appl Environ Microbiol. 1995 Oct;61(10):3556–3561. doi: 10.1128/aem.61.10.3556-3561.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Liesack W., Bak F., Kreft J. U., Stackebrandt E. Holophaga foetida gen. nov., sp. nov., a new, homoacetogenic bacterium degrading methoxylated aromatic compounds. Arch Microbiol. 1994;162(1-2):85–90. doi: 10.1007/BF00264378. [DOI] [PubMed] [Google Scholar]
  20. Lovley D. R. Bioremediation of organic and metal contaminants with dissimilatory metal reduction. J Ind Microbiol. 1995 Feb;14(2):85–93. doi: 10.1007/BF01569889. [DOI] [PubMed] [Google Scholar]
  21. Lovley D. R. Dissimilatory Fe(III) and Mn(IV) reduction. Microbiol Rev. 1991 Jun;55(2):259–287. doi: 10.1128/mr.55.2.259-287.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lovley D. R. Dissimilatory metal reduction. Annu Rev Microbiol. 1993;47:263–290. doi: 10.1146/annurev.mi.47.100193.001403. [DOI] [PubMed] [Google Scholar]
  23. Lovley D. R., Giovannoni S. J., White D. C., Champine J. E., Phillips E. J., Gorby Y. A., Goodwin S. Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch Microbiol. 1993;159(4):336–344. doi: 10.1007/BF00290916. [DOI] [PubMed] [Google Scholar]
  24. Lovley D. R., Lonergan D. J. Anaerobic Oxidation of Toluene, Phenol, and p-Cresol by the Dissimilatory Iron-Reducing Organism, GS-15. Appl Environ Microbiol. 1990 Jun;56(6):1858–1864. doi: 10.1128/aem.56.6.1858-1864.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lovley D. R., Phillips E. J., Caccavo F., Jr Acetate oxidation by dissimilatory Fe(III) reducers. Appl Environ Microbiol. 1992 Sep;58(9):3205–3208. doi: 10.1128/aem.58.9.3205-3208.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lovley D. R., Phillips E. J., Lonergan D. J. Hydrogen and Formate Oxidation Coupled to Dissimilatory Reduction of Iron or Manganese by Alteromonas putrefaciens. Appl Environ Microbiol. 1989 Mar;55(3):700–706. doi: 10.1128/aem.55.3.700-706.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lovley D. R., Phillips E. J., Lonergan D. J., Widman P. K. Fe(III) and S0 reduction by Pelobacter carbinolicus. Appl Environ Microbiol. 1995 Jun;61(6):2132–2138. doi: 10.1128/aem.61.6.2132-2138.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lovley D. R., Phillips E. J. Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microbiol. 1988 Jun;54(6):1472–1480. doi: 10.1128/aem.54.6.1472-1480.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Maidak B. L., Larsen N., McCaughey M. J., Overbeek R., Olsen G. J., Fogel K., Blandy J., Woese C. R. The Ribosomal Database Project. Nucleic Acids Res. 1994 Sep;22(17):3485–3487. doi: 10.1093/nar/22.17.3485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Muyzer G., de Waal E. C., Uitterlinden A. G. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol. 1993 Mar;59(3):695–700. doi: 10.1128/aem.59.3.695-700.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Myers C. R., Nealson K. H. Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science. 1988 Jun 3;240(4857):1319–1321. doi: 10.1126/science.240.4857.1319. [DOI] [PubMed] [Google Scholar]
  32. Myers R. M., Maniatis T., Lerman L. S. Detection and localization of single base changes by denaturing gradient gel electrophoresis. Methods Enzymol. 1987;155:501–527. doi: 10.1016/0076-6879(87)55033-9. [DOI] [PubMed] [Google Scholar]
  33. Nealson K. H., Saffarini D. Iron and manganese in anaerobic respiration: environmental significance, physiology, and regulation. Annu Rev Microbiol. 1994;48:311–343. doi: 10.1146/annurev.mi.48.100194.001523. [DOI] [PubMed] [Google Scholar]
  34. Olsen G. J., Lane D. J., Giovannoni S. J., Pace N. R., Stahl D. A. Microbial ecology and evolution: a ribosomal RNA approach. Annu Rev Microbiol. 1986;40:337–365. doi: 10.1146/annurev.mi.40.100186.002005. [DOI] [PubMed] [Google Scholar]
  35. Olsen G. J., Matsuda H., Hagstrom R., Overbeek R. fastDNAmL: a tool for construction of phylogenetic trees of DNA sequences using maximum likelihood. Comput Appl Biosci. 1994 Feb;10(1):41–48. doi: 10.1093/bioinformatics/10.1.41. [DOI] [PubMed] [Google Scholar]
  36. Pfennig N., Biebl H. Desulfuromonas acetoxidans gen. nov. and sp. nov., a new anaerobic, sulfur-reducing, acetate-oxidizing bacterium. Arch Microbiol. 1976 Oct 11;110(1):3–12. doi: 10.1007/BF00416962. [DOI] [PubMed] [Google Scholar]
  37. Risatti J. B., Capman W. C., Stahl D. A. Community structure of a microbial mat: the phylogenetic dimension. Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):10173–10177. doi: 10.1073/pnas.91.21.10173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Roden E. E., Lovley D. R. Dissimilatory Fe(III) Reduction by the Marine Microorganism Desulfuromonas acetoxidans. Appl Environ Microbiol. 1993 Mar;59(3):734–742. doi: 10.1128/aem.59.3.734-742.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  40. Stahl D. A., Flesher B., Mansfield H. R., Montgomery L. Use of phylogenetically based hybridization probes for studies of ruminal microbial ecology. Appl Environ Microbiol. 1988 May;54(5):1079–1084. doi: 10.1128/aem.54.5.1079-1084.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Stahl D. A., Lane D. J., Olsen G. J., Pace N. R. Analysis of hydrothermal vent-associated symbionts by ribosomal RNA sequences. Science. 1984 Apr 27;224(4647):409–411. doi: 10.1126/science.224.4647.409. [DOI] [PubMed] [Google Scholar]
  42. Walker J. C. Suboxic diagenesis in banded iron formations. Nature. 1984 May 24;309:340–342. doi: 10.1038/309340a0. [DOI] [PubMed] [Google Scholar]
  43. Walker J. C. Was the Archaean biosphere upside down? Nature. 1987 Oct 22;329:710–712. doi: 10.1038/329710a0. [DOI] [PubMed] [Google Scholar]
  44. Weisburg W. G., Barns S. M., Pelletier D. A., Lane D. J. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol. 1991 Jan;173(2):697–703. doi: 10.1128/jb.173.2.697-703.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Woese C. R. Bacterial evolution. Microbiol Rev. 1987 Jun;51(2):221–271. doi: 10.1128/mr.51.2.221-271.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES