Anaerobic Respiratory Iron(II) Oxidation

J. Cameron Thrash; Sarir Ahmadi; John D. Coates

doi:10.1128/9781555817190.ch9

Chapter 9 : Anaerobic Respiratory Iron(II) Oxidation

Authors: J. Cameron Thrash¹, Sarir Ahmadi², John D. Coates³

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720; 2: Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720; 3: Department of Plant and Microbial Biology, University of California, and Earth Sciences Division, Ernest Orlando Lawrence Berkeley National Laboratory, Berkeley, CA 94720

Content Type: Monograph

Publication Year: 2011

Category: Applied and Industrial Microbiology; Environmental Microbiology

Book DOI: 10.1128/9781555817190

Chapter DOI: 10.1128/9781555817190.ch9

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

Anaerobic Respiratory Iron(II) Oxidation, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555817190/9781555815363_Chap09-1.gif /docserver/preview/fulltext/10.1128/9781555817190/9781555815363_Chap09-2.gif

Abstract:

This chapter explores what is known about anaerobic, mesophilic Fe(II) oxidation in environmental samples and pure cultures. It includes an investigation of the mechanism of Fe(II) oxidation by dissimilatory (per)chlorate-reducing bacteria (DPRB), and a discussion on the oxidation products formed by the biomineralization processes, and emerging applications for the metabolism. Isolation and study of pure cultures have provided the needed starting points for investigating the presence of organisms in environmental samples and examining the microbial ecology of nitrate-dependent Fe(II) oxidation. The selective anaerobic bio-oxidation of added Fe(II) in situ could be used as an effective means of “capping off ” and completing the attenuation of heavy metals and radionuclides in a reducing environment. Two recent studies have also demonstrated the ability of both pure and mixed cultures to successfully adsorb arsenic to iron(III) oxides generated during this process. Genome sequences of several known nitrate-dependent Fe(II)-oxidizing microorganisms (FOM) are now available or in the process of completion, and comparative genomics should yield potential targets for further genetic study of the metabolism. The variety of culture-independent techniques now in use for assessment of microbial ecology will inevitably lead to a better understanding of the prevalence, biogeography, and diversity of FOM in natural and contaminated settings. The combined efforts of types of studies will help develop more accurate models regarding the role of FOM in the biogeochemical cycling of nitrogen, iron, and carbon.

Citation: Cameron Thrash J, Ahmadi S, Coates J. 2011. Anaerobic Respiratory Iron(II) Oxidation, p 157-171. In Stolz J, Oremland R (ed), Microbial Metal and Metalloid Metabolism. ASM Press, Washington, DC. doi: 10.1128/9781555817190.ch9

Key Concept Ranking

Denaturing Gradient Gel Electrophoresis: 0.4450077
Microbial Ecology: 0.42198664

0.4450077

Highlighted Text: Show | Hide

Full text loading...

Figures

Anaerobic Respiratory Iron(II) Oxidation

[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555817190.ch09-1,webId=/content/author/10.1128/9781555817190.ch09-1,properties={foaf_givenname=J., foaf_name=J. Cameron Thrash, foaf_surname=Cameron Thrash, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555817190.ch09-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555817190.ch09-2,webId=/content/author/10.1128/9781555817190.ch09-2,properties={foaf_givenname=Sarir, foaf_name=Sarir Ahmadi, foaf_surname=Ahmadi, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555817190.ch09-aff2]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555817190.ch09-3,webId=/content/author/10.1128/9781555817190.ch09-3,properties={foaf_givenname=John D., foaf_name=John D. Coates, foaf_surname=Coates, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555817190.ch09-aff3]]}]]

/content/10.1128/9781555817190.ch09.ch09fig01

FIGURE 1

The microbially mediated iron redox cycle. Over the past two decades it has been unambiguously demonstrated that microorganisms play a central role in the environmental geochemical redox cycle of iron. Microbial Fe(III) reduction is mediated primarily through the activity of dissimilatory metal-reducing bacteria under anaerobic conditions, while Fe(II) oxidation can occur through the activity of both photolithotrophic Fe(II) oxidizers using Fe(II) as an electron source for CO2 reduction, or chemolithotrophic respiratory Fe(II)-oxidizing bacteria (aerobic and anaerobic) using Fe(II) as an energy and electron source for carbon assimilation with a variety of alternative electron acceptors. Both Fe(III)-reducing and Fe(II)-oxidizing microorganisms have been shown to use either soluble or solid-phase iron sources, thus extending the biogeochemical cycle of iron to beyond the soluble form. 10.1128/9781555817190.ch9.f1

10.1128/9781555817190/f0159-01_thmb.gif

10.1128/9781555817190/f0159-01.gif

FIGURE 1

/content/10.1128/9781555817190.ch09.ch09fig02

FIGURE 2

Phylogenetic diversity of anaerobic Fe(II)-oxidizing microorganisms. Available quality 16S rRNA gene sequences were aligned with MUSCLE ( Edgar, 2004 ) and phylogeny was computed with MrBayes 3.2 ( Ronquist and Huelsenbeck, 2003 ). Scale bar indicates 0.2 changes per position. 10.1128/9781555817190.ch9.f2

10.1128/9781555817190/f0160-01_thmb.gif

10.1128/9781555817190/f0160-01.gif

FIGURE 2

/content/10.1128/9781555817190.ch09.ch09fig03

FIGURE 3

Effect of Fe(II) and Fe(III) on heterotrophic growth of strain VDY. ■, cells with added Fe(II); ●, cells with added Fe(III); ○, cells with no added iron; ▲, (ClO4 –) for cells with added Fe(II); ◆, (ClO4 –) for cells with added Fe(III); ☐, (ClO4 –) for cells with no added iron. 10.1128/9781555817190.ch9.f3

10.1128/9781555817190/f0167-01_thmb.gif

10.1128/9781555817190/f0167-01.gif

FIGURE 3

/content/10.1128/9781555817190.ch09.ch09fig04

FIGURE 4

Model for possible iterations of iron with the perchlorate-reduction pathway of strain VDY. Both Fe(II) and Fe(III) are postulated to inhibit chlorite dismutase (Cld). This prevents the formation and subsequent reduction of oxygen, disabling the creation of a proton motive force. Cld inhibition would also cause a buildup of chlorite, which is toxic to the cell and can also abiotically react with iron(II). OM, outer membrane; PM, periplasmic membrane; Pcr, perchlorate reductase. 10.1128/9781555817190.ch9.f4

10.1128/9781555817190/f0168-01_thmb.gif

10.1128/9781555817190/f0168-01.gif

FIGURE 4

References

/content/book/10.1128/9781555817190.ch09

1. Ainsworth, C.,, J. Pilon,, P. Gassman, and, W. Van der Sluys. 1994. Cobalt, cadmium, and lead sorption to hydrous iron oxide: residence time effect. Soil Sci. Soc. Am. J. 58: 1615– 1623.

2. Ames, L.,, J. McGarrah,, B. Walker, and, P. Salter. 1983. Uranium and radium sorption on amorphous ferric oxyhydroxide. Chem. Geol. 40: 135– 148.

3. Beller, H. 2005. Anaerobic, nitrate-dependent oxidation of U(IV) oxide minerals by the chemolithoautotrophic bacterium Thiobacillus denitrificans. Appl. Environ. Microbiol. 71: 2170– 2174.

4. Benz, M.,, A. Brune, and, B. Schink. 1998. Anaerobic and aerobic oxidation of ferrous iron at neutral pH by chemoheterotrophic nitrate-reducing bacteria. Arch. Microbiol. 169: 159– 165.

5. Blothe, M.,, and E. Roden. 2008. Microbial iron redox cycling in a circumneutral-pH groundwater seep. Appl. Environ. Microbiol. 75: 468– 473.

6. Blothe, M.,, and E. Roden. 2009. Composition and activity of an autotrophic Fe(II)-oxidizing, nitrate-reducing enrichment culture. Appl. Environ. Microbiol. 75: 6937– 6940.

7. Bopp, L. H.,, and H. L. Ehrlich. 1988. Chromate resistance and reduction in Pseudomonas fluorescens strain lb300. Arch. Microbiol. 150: 426– 431.

8. Bruce, R. A.,, L. A. Achenbach, and, J. D. Coates. 1999. Reduction of (per)chlorate by a novel organism isolated from a paper mill waste. Environ. Microbiol. 1: 319– 331.

9. Buffle, J. 1988. Complexation Reactions in Aquatic Systems. Wiley, New York, NY.

10. Byrne-Bailey, K. G.,, K. A. Weber,, A. H. Chair,, S. Bose,, T. Knox,, T. L. Spanbauer,, O. Chertkov, and, J. D. Coates. 2009. Completed genome sequence of the anaerobic iron oxidizing bacterium Acidovorax ebreus strain TPSY. J. Bacteriol. 92: 1475– 1476.

11. Charlet, L.,, and A. Manceau. 1992. X-ray absorption spectroscopic study of the sorption of Cr(III) at the oxide-water interface. J. Colloid Interface Sci. 148: 443– 457.

12. Chaudhuri, S. K.,, J. G. Lack, and, J. D. Coates. 2001. Biogenic magnetite formation through anaerobic biooxidation of Fe(II). Appl. Environ. Microbiol. 67: 2844– 2848.

13. Coates, J. D.,, and L. A. Achenbach. 2004. Microbial perchlorate reduction: rocket-fuelled metabolism. Nat. Rev. Microbiol. 2: 569– 580.

14. Coates, J. D.,, and L. A. Achenbach. 2006. The microbiology of perchlorate reduction and its bioremediative application, p. 279–291. In B. Gu and, J. D. Coates (ed.), Perchlorate, Environmental Occurrence, Interactions, and Treatment. Springer, Berlin, Germany.

15. Coates, J. D.,, and R. Chakraborty. 2003. Anaerobic bioremediation—an emerging resource for environmental cleanup, p. 227–257. In I. Singleton,, M. G. Milner, and, I. M. Head (ed.), Bioremediation: a Critical Review. Horizon Press, Norfolk, United Kingdom.

16. Coates, J. D.,, R. Chakraborty,, S. M. O’Connor,, C. Schmidt, and, J. Thieme. 2001. The geochemical effects of microbial humic substances reduction. Acta Hydrochim. Hydrobiol. 28: 420– 427.

17. Cornell, R. M.,, and U. Schwertmann. 2003. The Iron Oxides: Structure, Properties, Reactions, Occurrences and Uses. Wiley-VCH, Weinheim, Germany.

18. Craft, E. S.,, A. W. Abu-Qare,, M. M. Flaherty,, M. C. Garofolo,, H. L. Rincavage, and, M. B. Abou-Donia. 2004. Depleted and natural uranium: chemistry and toxicological effects. J. Toxicol. Environ. Health B Crit. Rev. 7: 297– 317.

19. Drever, J. L. 1997. The Geochemistry of Natural Waters. Prentice Hall, Upper Saddle River, NJ.

20. Dzombak, D. A.,, and F. M. M. Morel. 1990. Surface Complexation Modeling: Hydrous Ferric Oxide. John Wiley and Sons, New York, NY.

21. Edgar, R. 2004. Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792– 1797.

22. Edwards, K. J.,, D. R. Rogers,, C. O. Wirsen, and, T. M. McCollom. 2003. Isolation and characterization of novel psychrophilic, neutrophilic, Fe-oxidizing, chemolithoautotrophic α-and γ- Proteobacteria from the deep sea. Appl. Environ. Microbiol. 69: 2906– 2913.

23. Emerson, D.,, and C. L. Moyer. 1997. Isolation and characterization of novel iron-oxidizing bacteria that grow at circumneutral pH. Appl. Environ. Microbiol. 63: 4784– 4792.

24. Finneran, K. T.,, M. E. Housewright, and, D. R. Lovley. 2002. Multiple influences of nitrate on uranium solubility during bioremediation of uranium-contaminated subsurface sediments. Environ. Microbiol. 4: 510– 516.

25. Ghiorse, W. C. 1984. Biology of iron-depositing and manganese-depositing bacteria. Annu. Rev. Microbiol. 38: 515– 550.

26. Gorby, Y. A.,, F. Caccavo, Jr., and, H. Bolton, Jr. 1998. Microbial reduction of cobalt iiiedta - in the presence and absence of manganese(IV) oxide. Environ. Sci. Technol. 32: 244- 250.

27. Gorby, Y. A.,, and D. R. Lovley. 1992. Enzymatic uranium precipitation. Environ. Sci. Technol. 26: 205– 207.

28. Hafenbradl, D.,, M. Keller,, R. Dirmeier,, R. Rachel,, P. Rossnagel,, S. Burggraf,, H. Huber, and, K. O. Stetter. 1996. Ferroglobus placidus gen. Nov., sp. Nov., a novel hyperthermophilic archaeum that oxidizes Fe 2+ at neutral pH under anoxic conditions. Arch. Microbiol. 166: 308– 314.

29. Hansel, C. M.,, M. J. La Force,, S. Fendorf, and, S. Sutton. 2002. Spatial and temporal association of As and Fe species on aquatic plant roots. Environ. Sci. Technol. 36: 1988– 1994.

30. Harrison, A. P. 1984. The acidophilic thiobacilli and other acidophilic bacteria that share their habitat. Annu. Rev. Microbiol. 38: 265– 292.

31. Hecht, M. H.,, S. P. Kounaves,, R. C. Quinn,, S. J. West,, S. M. M. Young,, D. W. Ming,, D. C. Catling,, B. C. Clark,, W. V. Boynton,, J. Hoffman,, L. P. DeFlores,, K. Gospodinova,, J. Kapit, and, P. H. Smith. 2009. Detection of perchlorate and the soluble chemistry of Martian soil at the phoenix lander site. Science 325: 64– 67.

32. Hegler, F.,, N. Posth,, J. Jiang, and, A. Kappler. 2008. Physiology of phototrophic iron(II)-oxidizing bacteria: implications for modern and ancient environments. FEMS Microbiol. Ecol. 66: 250– 260.

33. Hohl, H.,, and W. Stumm. 1976. Interaction of Pb 2+ with hydrous Al 3O 3. J. Colloid Interface Sci. 55: 281– 288.

34. Hohmann, C.,, E. Winkler,, G. Morin, and, A. Kappler. 2009. Anaerobic fe(ii)-oxidizing bacteria show as resistance and immobilize as during Fe(III) mineral precipitation. Environ. Sci. Technol. 44: 94– 101.

35. Ishibashi, Y.,, C. Cervantes, and, S. Silver. 1990. Chromium reduction in Pseudomonas putida. Appl. Environ. Microbiol. 56: 2268– 2270.

36. Jorgensen, J. C.,, O. S. Jacobsen,, B. Elberling, and, J. Aamand. 2009. Microbial oxidation of pyrite coupled to nitrate reduction in anoxic groundwater sediment. Environ. Sci. Technol. 43: 4851– 4857.

37. Kappler, A.,, B. Schink, and, D. Newman. 2005. Fe(III) mineral formation and cell encrustation by the nitrate-dependent Fe(II)-oxidizer strain BOFEN-1. Geobiology 3: 235– 245.

38. Kumaraswamy, R.,, K. Sjollema,, G. Kuenen,, M. Loosdrecht, and, G. Muyzer. 2006. Nitrate-dependent [Fe(II)EDTA] 2– oxidation by Paracoccus ferrooxidans sp. Nov., isolated from a denitrifying bioreactor. Syst. Appl. Microbiol. 29: 276– 286.

39. Lack, J.,, S. Chaudhuri,, R. Chakraborty,, L. Achenbach, and, J. Coates. 2002. Anaerobic biooxidation of Fe(II) by Dechlorosoma suillum. Microb. Ecol. 43: 424– 431.

40. Lack, J. G. 2002. Immobilization of radionuclides and heavy metals through anaerobic biooxidation of Fe(II). Appl. Environ. Microbiol. 68: 2704– 2710.

41. Lloyd, J. R. 2003. Microbial reduction of metals and radionuclides. FEMS Microbiol. Rev. 27: 411– 425.

42. Lovley, D. R.,, E. J. P. Phillips,, Y. A. Gorby, and, E. R. Landa. 1991. Microbial reduction of uranium. Nature 350: 413– 416.

43. Means, J. L.,, D. A. Crerar, and, M. P. Borcsik. 1978. Adsorption of Co and selected actinides by Mn and Fe oxides in soils and sediments. Geochim. Cosmochim. Acta 42: 1763– 1773.

44. Miot, J.,, K. Benzerara,, G. Morin,, S. Bernard,, O. Beyssac,, E. Larquet,, A. Kappler, and, F. Guyot. 2009a. Transformation of vivianite by anaerobic nitrate-reducing iron-oxidizing bacteria. Geobiology 7: 373– 384.

45. Miot, J.,, K. Benzerara,, G. Morin,, A. Kappler,, S. Bernard,, M. Obst,, C. Ferard,, F. Skouripanet,, J. Guigner, and, N. Posth. 2009b. Iron biomineralization by anaerobic neutrophilic iron-oxidizing bacteria. Geochim. Cosmochim. Acta 73: 696– 711.

46. Moulin, V.,, and C. Moulin. 1995. Fate of actinides in the presence of humic substances under conditions relevant to nuclear waste disposal. Appl. Geochem. 10: 573– 580.

47. Muehe, E.,, S. Gerhardt,, B. Schink, and, A. Kappler. 2009. Ecophysiology and the energetic benefit of mixotrophic Fe(II) oxidation by various strains of nitrate-reducing bacteria. FEMS Microbiol. Ecol. 70: 3– 11.

48. Mumma, M. J.,, G. L. Villanueva,, R. E. Novak,, T. Hewagama,, B. P. Bonev,, M. A. DiSanti,, A. M. Mandell, and, M. D. Smith. 2009. Strong release of methane on Mars in northern summer 2003. Science 332: 1041– 1045.

49. Nielsen, J. L.,, and P. H. Nielsen. 1998. Microbial nitrate-dependent oxidation of ferrous iron in activated sludge. Environ. Sci. Technol. 32: 3556– 3561.

50. O’Connor, S. M.,, and J. D. Coates. 2002. A universal immuno-probe for (per)chlorate-reducing bacteria. Appl. Environ. Microbiol. 68: 3108– 3113.

51. Oremland, R. S.,, S. E. Hoeft,, J. A. Santini,, N. Bano,, R. A. Hollibaugh, and, J. T. Hollibaugh. 2002. Anaerobic oxidation of arsenite in mono lake water and by the facultative, arsenite-oxidizing chemoautotroph, strain mlhe-1. Appl. Environ. Microbiol. 68: 4795– 4802.

52. Poulain, A.,, and D. Newman. 2009. Rhodobacter capsulatus catalyzes light-dependent Fe(II) oxidation under anaerobic conditions as a potential detoxification mechanism. Appl. Environ. Microbiol. 75: 6639– 6646.

53. Rajagopalan, S.,, T. Anderson,, S. Cox,, G. Harvey,, Q. Cheng, and, W. A. Jackson. 2009. Perchlorate in wet deposition across North America. Environ. Sci. Technol. 43: 616– 622.

54. Rajagopalan, S.,, T. A. Anderson,, L. Fahlquist,, K. A. Rainwater,, M. Ridley, and, W. A. Jackson. 2006. Widespread presence of naturally occurring perchlorate in high plains of Texas and New Mexico. Environ. Sci. Technol. 40: 3156– 3162.

55. Rao, B.,, T. A. Anderson,, G. J. Orris,, K. A. Rainwater,, S. Rajagopalan,, R. M. Sandvig,, B. R. Scanlon,, D. A. Stonestrom,, M. A. Walvoord, and, W. A. Jackson. 2007. Widespread natural perchlorate in unsaturated zones of the southwest United States. Environ. Sci. Technol. 41: 4522– 4528.

56. Ratering, S.,, and S. Schnell. 2001. Nitrate-dependent iron(II) oxidation in paddy soil. Environ. Microbiol. 3: 100– 109.

57. Ronquist, F.,, and J. P. Huelsenbeck. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572– 1574.

58. Salomons, W.,, and U. Forstner. 1984. Metals in the Hydrocycle. Springer-Verlag, New York, NY.

59. Saunders, J. A.,, M. A. Pritchett, and, R. B. Cook. 1997. Geochemistry of biogenic pyrite and ferromanganese coatings from a small watershed: a bacterial connection. Geomicrobiol. J. 14: 203– 217.

60. Scanlon, B. R.,, R. C. Reedy,, W. A. Jackson, and, B. Rao. 2008. Mobilization of naturally occurring perchlorate related to land-use change in the southern high plains, Texas. Environ. Sci. Technol. 42: 8648– 8653.

61. Schadler, S.,, C. Burkhardt,, F. Hegler,, K. Straub,, J. Miot,, K. Benzerara, and, A. Kappler. 2009. Formation of cell-iron-mineral aggregates by phototrophic and nitrate-reducing anaerobic Fe(II)-oxidizing bacteria. Geomicrobiol. J. 26: 93– 103.

62. Shelobolina, E.,, C. Vanpraagh, and, D. Lovley. 2003. Use of ferric and ferrous iron containing minerals for respiration by Desulfitobacterium frappieri. Geomicrobiol. J. 20: 143– 156.

63. Smedley, P. L.,, and D. G. Kinniburgh. 2002. A review of the source behavior and distribution of arsenic in natural waters. Appl. Geochem. 17: 517– 568.

64. Straub, K.,, and B. E. Buchholz-Cleven. 1998. Enumeration and detection of anaerobic ferrous iron-oxidizing, nitrate-reducing bacteria from diverse European sediments. Appl. Environ. Microbiol. 64: 4846– 4856.

65. Straub, K.,, M. Hanzlik, and, B. E. Buchholz-Cleven. 1998. The use of biologically produced ferrihydrite for the isolation of novel iron-reducing bacteria. Syst. Appl. Microbiol. 21: 442– 449.

66. Straub, K.,, W. A. Schonhuber,, B. Buchholz-Cleven, and, B. Schink. 2004. Diversity of ferrous iron-oxidizing, nitrate-reducing bacteria and their involvement in oxygen-independent iron cycling. Geomicrobiol. J. 21: 371– 378.

67. Straub, K. L.,, M. Benz,, B. Schink, and, F. Widdel. 1996. Anaerobic, nitrate-dependent microbial oxidation of ferrous iron. Appl. Environ. Microbiol. 62: 1458– 1460.

68. Stumm, W.,, and J. J. Morgan. 1996. Aquatic Chemistry: Chemical Equilibria and Rates in Natural Waters. John Wiley & Sons, New York, NY.

69. Sun, W.,, R. Sierra-Alvarez,, L. Milner,, R. Oremland, and, J. A. Field. 2009. Arsenite and ferrous iron oxidation linked to chemolithotrophic denitrification for the immobilization of arsenic in anoxic environments. Environ. Sci. Technol. 43: 6585– 6591.

70. Sun, Y. 2008. Physiology of microbial perchlorate reduction. Ph.D. thesis. Plant and Microbial Biology. University of California, Berkeley, CA.

71. Thrash, J. C.,, B. J. Baker,, S. Ahmadi,, T. Torok, and, J. D. Coates. 2010a. Magnetospirillum bellicus sp. nov., a novel dissimilatory perchlorate-reducing alphaproteobacterium isolated from a bioelectrical reactor. Appl. Environ. Microbiol. 76: 4730– 4737.

72. Thrash, J. C.,, J. Pollock,, T. Torok, and, J. D. Coates. 2010b. Description of the novel perchlorate-reducing bacteria Dechlorobacter hydrogenophilus gen. Nov., sp. Nov., and Propionivibrio militaris, sp. Nov. Appl. Microbiol. Biotechnol. 86: 335– 343.

73. Thurman, E. M. 1985. Organic Geochemistry of Natural Waters. Springer, Boston, MA.

74. Tyson, G.,, J. Chapman,, P. Hugenholtz,, E. E. Allen,, R. J. Ram,, P. M. Richardson,, V. V. Solovyev,, E. M. Rubin,, D. S. Rokhsar, and, J. F. Banfield. 2004. Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428: 37– 43.

75. Urbansky, E. T. 1998. Perchlorate chemistry: implications for analysis and remediation. Bioremed. J. 2: 81– 95.

76. Weber, K. A.,, L. A. Achenbach, and, J. D. Coates. 2006a. Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat. Rev. Microbiol. 4: 752– 764.

77. Weber, K. A.,, D. B. Hedrick,, A. D. Peacock,, J. C. Thrash,, D. C. White,, L. A. Achenbach, and, J. D. Coates. 2009. Physiological and taxonomic description of the novel autotrophic, metal oxidizing bacterium, Pseudogulbenkiania sp. strain 2002. Appl. Microbiol. Biotechnol. 83: 555– 565.

78. Weber, K. A.,, F. W. Picardal, and, E. E. Roden. 2001. Microbially catalyzed nitrate-dependent oxidation of biogenic solid-phase Fe(II) compounds. Environ. Sci. Technol. 35: 1644– 1650.

79. Weber, K. A.,, J. Pollock,, K. A. Cole,, S. M. O’Connor,, L. A. Achenbach, and, J. D. Coates. 2006b. Anaerobic nitrate-dependent iron(II) bio-oxidation by a novel lithoautotrophic betaproteobacterium, strain 2002. Appl. Environ. Microbiol. 72: 686– 694.

80. Weber, K. A.,, M. M. Urrutia,, P. F. Churchill,, R. K. Kukkadapu, and, E. E. Roden. 2006c. Anaerobic redox cycling of iron by freshwater sediment microorganisms. Environ. Microbiol. 8: 100– 113.

81. Widdel, F.,, S. Schnell,, S. Heising,, A. Ehrenreich,, B. Assmus, and, B. Schink. 1993. Ferrous iron oxidation by anoxygenic phototrophic bacteria. Nature 362: 834– 836.