Vanadate and acetate biostimulation of contaminated sediments decreases diversity, selects for specific taxa, and decreases aqueous V5+ concentration

Environmental Science and Technology

Volumn 47, Issue 12, 2013, Pages 6500-6509

  Yelton, Alexis P ^a,e   Williams, Kenneth H ^b   Fournelle, John ^c   Wrighton, Kelly C ^d   Handley, Kim M ^d,f   Banfield, Jillian F ^a,b,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e Massachusetts Institute of Technology Cambridge   (United States)

^f UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA GENE SEQUENCING; AQUIFER SEDIMENTS; CONTAMINATED SEDIMENT; FOSSIL FUEL COMBUSTION; GROUNDWATER WELLS; MICROBIAL RESPONSE; MOST PROBABLE NUMBER; NATURAL GROUNDWATER;

AQUIFERS; BIOREMEDIATION; BIOTECHNOLOGY; FUELS; GROUNDWATER RESOURCES; POLLUTION; RNA; VANADIUM;

VOLATILE FATTY ACIDS;

ACETIC ACID; GROUND WATER; RNA 16S; VANADIC ACID; VANADIUM;

ACETATE; BIOREMEDIATION; CONCENTRATION (COMPOSITION); FLOODPLAIN; REMOVAL EXPERIMENT; RNA; SEDIMENT POLLUTION; VANADATE GROUP;

AQUIFER; ARTICLE; ATOMIC EMISSION SPECTROMETRY; BIOREMEDIATION; COMMUNITY STRUCTURE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DNA ISOLATION; FLOODPLAIN; GENE SEQUENCE; HEAVY METAL REMOVAL; ION PAIR CHROMATOGRAPHY; MICROBIAL COMMUNITY; MINE TAILINGS; NONHUMAN; RIVER; SCANNING ELECTRON MICROSCOPY; SEDIMENT; SPECIES RICHNESS; UNITED STATES; WATER CONTAMINATION;

ACETATES; BIODEGRADATION, ENVIRONMENTAL; VANADATES;

COLORADO RIVER [NORTH AMERICA];

EID: 84879215448     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es4006674     Document Type: Article

References (90)

1. Environmental Protection Agency. http://www.epa.gov/superfund/ (Nov 2008)
2. Rehder, D. Bioinorganic Vanadium Chemistry, 2nd ed.; John Wiley & Sons, Ltd: West Sussex, U. K., 2008; p 224.
3. Valko, M. M. H.; Cronin, M. T. D. Metals, toxicity and oxidative stress Curr. Med. Chem. 2005, 12 (10) 1161-1208
4. Cortizo, A. M.; Bruzzone, L.; Molinuevo, S.; Etcheverry, S. B. A possible role of oxidative stress in the vanadium-induced cytotoxicity in the MC3T3E1 osteoblast and UMR106 osteosarcoma cell lines Toxicology 2000, 147 (2) 89-99
5. Sabbioni, E.; Pozzi, G.; Pintar, A.; Casella, L.; Garattini, S. Cellular retention, cytotoxicity and morphological transformation by vanadium (IV) and vanadium(V) in BALB/3T3 cell-lines Carcinogenesis 1991, 12 (1) 47-52
6. Shi, X. L.; Jiang, H. G.; Mao, Y.; Ye, J. P.; Saffiotti, U. Vanadium(IV)-mediated free radical generation and related 2'-deoxyguanosine hydroxylation and DNA damage Toxicology 1996, 106 (1-3) 27-38
7. Soares, S. S.; Martins, H.; Gutierrez-Merino, C.; Aureliano, M. Vanadium and cadmium in vivo effects in teleost cardiac muscle: Metal accumulation and oxidative stress markers Comp. Biochem. Physiol., Part C: Toxicol. Pharmacol. 2008, 147 (2) 168-178
8. Zychlinski, L.; Byczkowski, J. Z.; Kulkarni, A. P. Toxic effects of long-term intratracheal administration of vanadium pentoxide in rats Arch. Environ. Contam. Toxicol. 1991, 20, 295-298
9. Zaporowska, H.; Wasilewski, W. Haematological effects of vanadium on living organisms Comp. Biochem. Physiol., Part C: Toxicol. Pharmacol. 1992, 102 (2) 223-231
10. Stohs, S.; Bagchi, D. Oxidative mechanisms in the toxicity of metal ions Free Radical Biol. Med. 1995, 18, 321-336
11. Domingo, J. Vanadium: a review of the reproductive and development toxicity Reprod. Toxicol. 1996, 10, 175-182
12. Crans, D. C. A.; Keramidas, A. D. Chemistry of relevance to vanadium in the environment. In Vanadium in the Environment. Part I: Chemistry and Biochemistry, Nriagu, J. O., Ed.; John Wiley & Sons, Inc.: New York, 1998; pp 73-95.
13. Peacock, C. L.; Sherman, D. M. Vanadium(V) adsorption onto goethite (alpha-FeOOH) at pH 1.5 to 12: A surface complexation model based on ab initio molecular geometries and EXAFS spectroscopy Geochim. Cosmochim. Acta 2004, 68 (8) 1723-1733
14. Ortiz-Bernad, I.; Anderson, R. T.; Vrionis, H. A.; Lovley, D. R. Vanadium respiration by Geobacter metallireducens: Novel strategy for in situ removal of vanadium from groundwater Appl. Environ. Microbiol. 2004, 70 (5) 3091-3095
15. Carpentier, W.; Sandra, K.; De Smet, I.; Brige, A.; De Smet, L.; Van Beeumen, J. Microbial reduction and precipitation of vanadium by Shewanella oneidensis Appl. Environ. Microbiol. 2003, 69 (6) 3636-3639
16. Carpentier, W.; De Smet, L.; Van Beeumen, J.; Brige, A. Respiration and growth of Shewanella oneidensis MR-1 using vanadate as the sole electron acceptor J. Bacteriol. 2005, 187 (10) 3293-3301
17. Yurkova, N. A.; Lyalikova, N. N. New facultative chemolithotrophic bacteria reducing vanadate Microbiology 1990, 59 (6) 672-677
18. Woolfolk, C. A.; Whiteley, H. R. Reduction of inorganic compounds with molecular hydrogen by Micrococcus lactilyticus. 1. Stoichiometry with compounds of arsenic, selenium, tellurium, transition and other elements J. Bacteriol. 1962, 84 (4) 647-&
19. Van Marwijk, J.; Opperman, D. J.; Piater, L. A.; Van Heerden, E. Reduction of vanadium(V) by Enterobacter cloacae EV-SA01 isolated from a South African deep gold mine Biotechnol. Lett. 2009, 31 (6) 845-849
20. Ogg, C. D.; Patel, B. K. C. Fervidicella metallireducens gen. nov., sp nov., a thermophilic, anaerobic bacterium from geothermal waters Int. J. Syst. Evol. Microbiol. 2010, 60, 1394-1400
21. Aendekerk, S.; Ghysels, B.; Cornelis, P.; Baysse, C. Characterization of a new efflux pump, MexGHI-OpmD, from Pseudomonas aeruginosa that confers resistance to vanadium Microbiology (SGM) 2002, 148, 2371-2381
22. Denayer, S.; Matthijs, S.; Cornelis, P. Resistance to vanadium in Pseudomonas fluorescens ATCC 17400 caused by mutations in TCA cycle enzymes FEMS Microbiol. Lett. 2006, 264 (1) 59-64
23. Hernandez, A.; Mellado, R. P.; Martinez, J. L. Metal accumulation and vanadium-induced multidrug resistance by environmental isolates of Escherichia hermannii and Enterobacter cloacae Appl. Environ. Microbiol. 1998, 64 (11) 4317-4320
24. Bella, J. M. L.; Philp, J. C.; Kuyukina, M. S.; Ivshina, I. B.; Dunbar, S. A.; Cunningham, C. J.; Anderson, P. Methods evaluating vanadium tolerance in bacteria isolated from crude oil contaminated land J. Microbiol. Methods 2004, 58 (1) 87-100
25. Kamika, I.; Momba, M. N. B. Comparing the Tolerance Limits of Selected Bacterial and Protozoan Species to Vanadium in Wastewater Systems Water Air Soil Pollut. 2012, 223 (5) 2525-2539
26. Final Site Observational Work Plan for the UMTRA Project Old Rifle Site. In USDOE, Grand Junction, CO, 1999.
27. Anderson, R. T.; Vrionis, H. A.; Ortiz-Bernad, I.; Resch, C. T.; Long, P. E.; Dayvault, R.; Karp, K.; Marutzky, S.; Metzler, D. R.; Peacock, A.; White, D. C.; Lowe, M.; Lovley, D. R. Stimulating the in situ activity of Geobacter species to remove uranium from the groundwater of a uranium-contaminated aquifer Appl. Environ. Microbiol. 2003, 69 (10) 5884-5891
28. Giloteaux, L. H. D.; Williams, K. H.; Wrighton, K. C.; Wilkins, M. J.; Montgomery, A. P.; Smith, J. A.; Orellana, R.; Thompson, C. A.; Roper, T. J.; Long, P. E.; Lovley, D. R. Characterization and transcription of arsenic respiration and resistance genes during in situ uranium bioremediation. ISME J. 2012, in press, DOI: 10.1038/ismej.2012.109.
29. Sandell, E. B. Determination of chromium, vanadium, and molybdenum in silicate rocks Ind. Eng. Chem., Anal. Ed. 1936, 8, 336-341
30. Handley, K. M.; Wrighton, K. C.; Piceno, Y. M.; Andersen, G. L.; DeSantis, T. Z.; Williams, K. H.; Wilkins, M. J.; N'Guessan, A. L.; Peacock, A.; Bargar, J.; Long, P. E.; Banfield, J. F. High-density PhyloChip profiling of stimulated aquifer microbial communities reveals a complex response to acetate amendment FEMS Microbiol. Ecol. 2012, 81 (1) 188-204
31. Handley, K. M.; VerBerkmoes, N. C.; Steefel, C. I.; Williams, K. H.; Sharon, I.; Miller, C. S.; Frischkorn, K. R.; Chourey, K.; Thomas, B. C.; Shah, M. B.; Long, P. E.; Hettich, R. L.; Banfield, J. F. Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community ISME J. 2013, 7 (4) 800-816
32. Williams, K. H.; Long, P. E.; Davis, J. A.; Wilkins, M. J.; N'Guessan, A. L.; Steefel, C. I.; Yang, L.; Newcomer, D.; Spane, F. A.; Kerkhof, L. J.; McGuinness, L.; Dayvault, R.; Lovley, D. R. Acetate Availability and its Influence on Sustainable Bioremediation of Uranium-Contaminated Groundwater Geomicrobiol. J. 2011, 28 (5-6) 519-539
33. Lovley, D. R.; Phillips, E. J. P. Novel mode of microbial energy metabolism: Organic carbon oxidation coupled to dissimilatory reduction of iron or manganese Appl. Environ. Microbiol. 1988, 54 (6) 1472-1480
34. de Man, J. MPN tables, corrected Appl. Microbiol. Biotechnol. 1983, 17, 301-305
35. Cochran, W. G. Estimation of bacterial densities by means of the most probably number Biometrics 1950, 6 (2) 105-116
36. Miller, C. S.; Baker, B. J.; Thomas, B. C.; Singer, S. W.; Banfield, J. F. EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data Genome Biol. 2011, 12 (5) R44
37. Nawrocki, E. P.; Kolbe, D. L.; Eddy, S. R. Infernal 1.0: inference of RNA alignments Bioinformatics 2009, 25 (10) 1335-1337
38. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST Bioinformatics 2010, 26 (19) 2460-2461
39. Price, M. N.; Dehal, P. S.; Arkin, A. P. FastTree: Computing large minimum evolution trees with profiles instead of a distance matrix Mol. Biol. Evol. 2009, 26 (7) 1641-1650
40. Price, M. N.; Dehal, P. S.; Arkin, A. P. FastTree 2-Approximately maximum-likelihood trees for large alignments PLoS One 2010, 5 (3) e9490
41. R: A Language and Environment for Statistical Computing. http://www.R-project.org/.
42. Dixon, P. VEGAN, a package of R functions for community ecology J. Veg. Sci. 2003, 14 (6) 927-930
43. Kembel, S. W.; Cowan, P. D.; Helmus, M. R.; Cornwell, W. K.; Morlon, H.; Ackerly, D. D.; Blomberg, S. P.; Webb, C. O. Picante: R tools for integrating phylogenies and ecology Bioinformatics 2010, 26 (11) 1463-1464
44. Kanamori, K. T. Kiyoshi. Inorganic Chemistry of Vanadium. In Vanadium: Biochemical and Molecular Biological Approaches; Michibata, H., Ed.; Springer: New York, 2012; p 19.
45. Jost, L. Entropy and diversity Oikos 2006, 113 (2) 363-375
46. Webb, C. O. Exploring the phylogenetic structure of ecological communities: An example for rain forest trees Am. Nat. 2000, 156 (2) 145-155
47. Chou, J.-H.; Chou, Y.-J.; Arun, A. B.; Young, C.-C.; Chen, C. A.; Wang, J.-T.; Chen, W.-M. Vogesella lacus sp nov., isolated from a soft-shell turtle culture pond Int. J. Syst. Evol. Microbiol. 2009, 59, 2629-2632
48. Chou, Y.-J.; Chou, J.-H.; Lin, M.-C.; Arun, A. B.; Young, C.-C.; Chen, W.-M. Vogesella perlucida sp nov., a non-pigmented bacterium isolated from spring water Int. J. Syst. Evol. Microbiol. 2008, 58, 2677-2681
49. Grimes, D. J.; Woese, C. R.; MacDonell, M. T.; Colwell, R. R. Systematic study of the genus Vogesella gen. nov. and its type species, Vogesella indigofera comb. nov Int. J. Syst. Bacteriol. 1997, 47 (1) 19-27
50. Jorgensen, N. O. G.; Brandt, K. K.; Nybroe, O.; Hansen, M. Vogesella mureinivorans sp. nov., a peptidoglycan-degrading bacterium from lake water Int. J. Syst. Evol. Microbiol. 2010, 60, 2467-2472
51. Ziv-El, M.; Delgado, A. G.; Yao, Y.; Kang, D.-W.; Nelson, K. G.; Halden, R. U.; Krajmalnik-Brown, R. Development and characterization of DehaloR boolean AND 2, a novel anaerobic microbial consortium performing rapid dechlorination of TCE to ethene Appl. Microbiol. Biotechnol. 2011, 92 (5) 1063-1071
52. Vrionis, H. A.; Anderson, R. T.; Ortiz-Bernad, I.; O'Neill, K. R.; Resch, C. T.; Peacock, A. D.; Dayvault, R.; White, D. C.; Long, P. E.; Lovley, D. R. Microbiological and geochemical heterogeneity in an in situ uranium bioremediation field site Appl. Environ. Microbiol. 2005, 71 (10) 6308-6318
53. Holmes, D. E.; O'Neil, R. A.; Vrionis, H. A.; N'Guessan, L. A.; Ortiz-Bernad, I.; Larrahondo, M. J.; Adams, L. A.; Ward, J. A.; Nicoll, J. S.; Nevin, K. P.; Chavan, M. A.; Johnson, J. P.; Long, P. E.; Lovley, D. R. Subsurface clade of Geobacteraceae that predominates in a diversity of Fe(III)-reducing subsurface environments ISME J. 2007, 1 (8) 663-677
54. North, N. N.; Dollhopf, S. L.; Petrie, L.; Istok, J. D.; Balkwill, D. L.; Kostka, J. E. Change in bacterial community structure during in situ Biostimulation of subsurface sediment cocontaminated with uranium and nitrate Appl. Environ. Microbiol. 2004, 70 (8) 4911-4920
55. Chang, Y. J.; Long, P. E.; Geyer, R.; Peacock, A. D.; Resch, C. T.; Sublette, K.; Pfiffner, S.; Smithgall, A.; Anderson, R. T.; Vrionis, H. A.; Stephen, J. R.; Dayvault, R.; Ortiz-Bernad, I.; Lovley, D. R.; White, D. C. Microbial incorporation of C-13-labeled acetate at the field scale: Detection of microbes responsible for reduction of U(VI) Environ. Sci. Technol. 2005, 39 (23) 9039-9048
56. Northrop, H. R.; Goldhaber, M. B.; Landis, G. P.; Unruh, J. W.; Reynolds, R. L.; Campbell, J. A.; Wanty, R. B.; Grauch, R. I.; Whitney, G.; Rye, R. O. Genesis of the tabular-type vanadium-uranium deposits of the Henry Basin, Utah. 1. Geochemical and mineralogical evidence for the sources of the ore-forming fluids. 2. Mechanisms of ore and gague mineral formation at the interface between brine and meteoric water. 3. Evidence from the mineralogy and geochemistry of clay-minerals Econ. Geol. Bull. Soc. Econ. Geol. 1990, 85 (2) 215-269
57. Wanty, R. B.; Goldhaber, M. B. Thermodynamics and kinetics of reactions involving vanadium in natural systems-Accumulation of vanadium in sedimentary rocks Geochim. Cosmochim. Acta 1992, 56 (4) 1471-1483
58. Wanty, R. B.; Goldhaber, M. B.; Northrop, H. R. Geochemistry of vanadium in an epigenetic, sandstone-hosted vanadium-uranium deposit, Henry Basin, Utah Econ. Geol. Bull. Soc. Econ. Geol. 1990, 85 (2) 270-284
59. Breit, G. N. Origin of clay-minerals associated with V-U deposits in the Entrada Sandstone, Placerville mining district, Southwestern Colorado Econ. Geol. Bull. Soc. Econ. Geol. 1995, 90 (2) 407-419
60. Schwertmann, U.; Pfab, G. Structural vanadium and chromium in lateritic iron oxides: Genetic implications Geochim. Cosmochim. Acta 1996, 60 (21) 4279-4283
61. Yabusaki, S. B.; Fang, Y.; Long, P. E.; Resch, C. T.; Peacock, A. D.; Komlos, J.; Jaffe, P. R.; Morrison, S. J.; Dayvault, R. D.; White, D. C.; Anderson, R. T. Uranium removal from groundwater via in situ biostimulation: Field-scale modeling of transport and biological processes J. Contam. Hydrol. 2007, 93 (1-4) 216-235
62. Li, L.; Steefel, C. I.; Kowalsky, M. B.; Englert, A.; Hubbard, S. S. Effects of physical and geochemical heterogeneities on mineral transformation and biomass accumulation during biostimulation experiments at Rifle, Colorado J. Contam. Hydrol. 2010, 112 (1-4) 45-63
63. N'Guessan, A. L.; Vrionis, H. A.; Resch, C. T.; Long, P. E.; Lovley, D. R. Sustained removal of uranium from contaminated groundwater following stimulation of dissimilatory metal reduction Environ. Sci. Technol. 2008, 42 (8) 2999-3004
64. Massa, S.; Grandi, M.; Poda, G.; Cesaroni, D.; Cangamella, F.; Trovatelli, L. D. Coliform detection from river waters-Comparison between MPN and MF techniques Water Air Soil Pollut. 1989, 43 (1-2) 135-145
65. Sievert, S. M.; Brinkhoff, T.; Muyzer, G.; Ziebis, V.; Kuever, J. Spatial heterogeneity of bacterial populations along an environmental gradient at a shallow submarine hydrothermal vent near Milos Island (Greece) Appl. Environ. Microbiol. 1999, 65 (9) 3834-3842
66. Guerinot, M. L.; Colwell, R. R. Enumeration, isolation, and characterization of N-2 fixing bacteria from seawater Appl. Environ. Microbiol. 1985, 50 (2) 350-355
67. Petrie, L.; North, N. N.; Dollhopf, S. L.; Balkwill, D. L.; Kostka, J. E. Enumeration and characterization of iron(III)-reducing microbial communities from acidic subsurface sediments contaminated with uranium(VI) Appl. Environ. Microbiol. 2003, 69 (12) 7467-7479
68. Holmes, D. E.; Finneran, K. T.; O'Neil, R. A.; Lovley, D. R. Enrichment of members of the family Geobacteraceae associated with stimulation of dissimilatory metal reduction in uranium-contaminated aquifer sediments Appl. Environ. Microbiol. 2002, 68 (5) 2300-2306
69. Islam, E.; Dhal, P. K.; Kazy, S. K.; Sar, P. Molecular analysis of bacterial communities in uranium ores and surrounding soils from Banduhurang open cast uranium mine, India: A comparative study J. Environ. Sci. Health, Part A: Toxic/Hazard. Subst. Environ. Eng. 2011, 46 (3) 271-280
70. Islam, E.; Sar, P. Molecular assessment on impact of uranium ore contamination in soil bacterial diversity Int. Biodeterior. Biodegrad. 2011, 65 (7) 1043-1051
71. Wrighton, K. C.; Virdis, B.; Clauwaert, P.; Read, S. T.; Daly, R. A.; Boon, N.; Piceno, Y.; Andersen, G. L.; Coates, J. D.; Rabaey, K. Bacterial community structure corresponds to performance during cathodic nitrate reduction ISME J. 2010, 4 (11) 1443-1455
72. Webb, C. O.; Ackerly, D. D.; McPeek, M. A.; Donoghue, M. J. Phylogenies and community ecology Annu. Rev. Ecol. Syst. 2002, 33, 475-505
73. Horner-Devine, M. C.; Bohannan, B. J. M. Phylogenetic clustering and overdispersion in bacterial communities Ecology 2006, 87 (7) S100-S108
74. Pontarp, M.; Sjostedt, J.; Lundberg, P. Experimentally induced habitat filtering in marine bacterial communities Mar. Ecol.: Prog. Ser. 2013, 477, 77-U406
75. Boto, L. Horizontal gene transfer in evolution: facts and challenges Proc. R. Soc. London, Ser. B 2010, 277 (1683) 819-827
76. Suzuki, S.; Kimura, M.; Agusa, T.; Rahman, H. M. Vanadium accelerates horizontal transfer of tet(M) gene from marine Photobacterium to Escherichia coli FEMS Microbiol. Lett. 2012, 336 (1) 52-56
77. Mouser, P. J.; N'Guessan, A. L.; Elifantz, H.; Holmes, D. E.; Williams, K. H.; Wilkins, M. J.; Long, P. E.; Lovley, D. R. Influence of Heterogeneous Ammonium Availability on Bacterial Community Structure and the Expression of Nitrogen Fixation and Ammonium Transporter Genes during in Situ Bioremediation of Uranium-Contaminated Groundwater Environ. Sci. Technol. 2009, 43 (12) 4386-4392
78. Wrighton, K. C.; Thomas, B. C.; Sharon, I.; Miller, C. S.; Castelle, C. J.; VerBerkmoes, N. C.; Wilkins, M. J.; Hettich, R. L.; Lipton, M. S.; Williams, K. H.; Long, P. E.; Banfield, J. F. Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla Science 2012, 337 (6102) 1661-1665
79. Finneran, K. T.; Johnsen, C. V.; Lovley, D. R. Rhodoferax ferrireducens sp nov., a psychrotolerant, facultatively anaerobic bacterium that oxidizes acetate with the reduction of Fe(III) Int. J. Syst. Evol. Microbiol. 2003, 53, 669-673
80. Hartman, M. J. Hanford Site Groundwater Monitoring: Setting, Sources and Methods; USDOE, U.S. Department of Commerce: Springfield, VA, 2000; p 142.
81. USDOE Hanford Site: First Five Year Review Report; The U.S. Environmental Protection Agency, R., Hanford Project Office; USDOE: Richland, WA, 2001.
82. Lin, X. J.; Kennedy, D.; Fredrickson, J.; Bjornstad, B.; Konopka, A. Vertical stratification of subsurface microbial community composition across geological formations at the Hanford Site Environ. Microbiol. 2012, 14 (2) 414-425
83. Lin, X. J.; McKinley, J.; Resch, C. T.; Kaluzny, R.; Lauber, C. L.; Fredrickson, J.; Knight, R.; Konopka, A. Spatial and temporal dynamics of the microbial community in the Hanford unconfined aquifer ISME J. 2012, 6 (9) 1665-1676
84. Lovley, D. R.; Giovannoni, S. J.; White, D. C.; Champine, J. E.; Phillips, E. J. P.; 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
85. Caccavo, F.; Lonergan, D. J.; Lovley, D. R.; Davis, M.; Stolz, J. F.; McInerney, M. J. Geobacter sulfurreducens sp. nov, a hydrogen-oxidizing and acetate-oxidizing dissimilatory metal-reducing microorganism Appl. Environ. Microbiol. 1994, 60 (10) 3752-3759
86. Coates, J. D.; Bhupathiraju, V. K.; Achenbach, L. A.; McInerney, M. J.; Lovley, D. R. Geobacter hydrogenophilus, Geobacter chapellei and Geobacter grbiciae, three new, strictly anaerobic, dissimilatory Fe(III)-reducers Int. J. Syst. Evol. Microbiol. 2001, 51, 581-588
87. Lovley, D. R. Effect of Geobacter species on the fate of metal and organic contaminants in the subsurface Abstr. Pap.-Am. Chem. Soc. 2000, 220, U346-U346
88. Nevin, K. P.; Holmes, D. E.; Woodard, T. L.; Hinlein, E. S.; Ostendorf, D. W.; Lovley, D. R. Geobacter bemidjiensis sp. nov and Geobacter psychrophilus sp. nov., two novel Fe(III)-reducing subsurface isolates Int. J. Syst. Evol. Microbiol. 2005, 55, 1667-1674
89. Shelobolina, E. S.; Vrionis, H. A.; Findlay, R. H.; Lovley, D. R. Geobacter uraniireducens sp. nov., isolated from subsurface sediment undergoing uranium bioremediation Int. J. Syst. Evol. Microbiol. 2008, 58, 1075-1078
90. Zhuang, K.; Izallalen, M.; Mouser, P.; Richter, H.; Risso, C.; Mahadevan, R.; Lovley, D. R. Genome-scale dynamic modeling of the competition between Rhodoferax and Geobacter in anoxic subsurface environments ISME J. 2011, 5 (2) 305-316