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The Role of Bacterial Spores in Metal Cycling and Their Potential Application in Metal Contaminant Bioremediation

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  • Authors: Cristina N. Butterfield1, Sung-Woo Lee2, Bradley M. Tebo3
  • Editors: Patrick Eichenberger4, Adam Driks5
    Affiliations: 1: Division of Environmental and Biomolecular Systems, Institute of Environmental Health, Oregon Health & Science University, Portland, OR 97239; 2: Division of Environmental and Biomolecular Systems, Institute of Environmental Health, Oregon Health & Science University, Portland, OR 97239; 3: Division of Environmental and Biomolecular Systems, Institute of Environmental Health, Oregon Health & Science University, Portland, OR 97239; 4: New York University, New York, NY; 5: Loyola University Medical Center, Maywood, IL
  • Source: microbiolspec April 2016 vol. 4 no. 2 doi:10.1128/microbiolspec.TBS-0018-2013
  • Received 16 April 2013 Accepted 29 February 2016 Published 01 April 2016
  • Bradley M. Tebo, [email protected]
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  • Abstract:

    Bacteria are one of the premier biological forces that, in combination with chemical and physical forces, drive metal availability in the environment. Bacterial spores, when found in the environment, are often considered to be dormant and metabolically inactive, in a resting state waiting for favorable conditions for them to germinate. However, this is a highly oversimplified view of spores in the environment. The surface of bacterial spores represents a potential site for chemical reactions to occur. Additionally, proteins in the outer layers (spore coats or exosporium) may also have more specific catalytic activity. As a consequence, bacterial spores can play a role in geochemical processes and may indeed find uses in various biotechnological applications. The aim of this review is to introduce the role of bacteria and bacterial spores in biogeochemical cycles and their potential use as toxic metal bioremediation agents.

  • Citation: Butterfield C, Lee S, Tebo B. 2016. The Role of Bacterial Spores in Metal Cycling and Their Potential Application in Metal Contaminant Bioremediation. Microbiol Spectrum 4(2):TBS-0018-2013. doi:10.1128/microbiolspec.TBS-0018-2013.


1. Gray HB. 2003. Biological inorganic chemistry at the beginning of the 21st century. Proc Natl Acad Sci USA 100:3563–3568. http://dx.doi.org/10.1073/pnas.0730378100. [PubMed][CrossRef]
2. Bond PL, Hugenholtz P, Keller J, Blackall LL. 1995. Bacterial community structures of phosphate-removing and non-phosphate-removing activated sludges from sequencing batch reactors. Appl Environ Microbiol 61:1910–1916. [PubMed]
3. Beswick PH, Hall GH, Hook AJ, Little K, McBrien DC, Lott KA. 1976. Copper toxicity: evidence for the conversion of cupric to cuprous copper in vivo under anaerobic conditions. Chem Biol Interact 14:347–356. http://dx.doi.org/10.1016/0009-2797(76)90113-7. [CrossRef]
4. Outten FW, Huffman DL, Hale JA, O’Halloran TV. 2001. The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J Biol Chem 276:30670–30677. http://dx.doi.org/10.1074/jbc.M104122200. [CrossRef]
5. Changela A, Chen K, Xue Y, Holschen J, Outten CE, O’Halloran TV, Mondragón A. 2003. Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science 301:1383–1387. http://dx.doi.org/10.1126/science.1085950. [CrossRef]
6. Chacón KN, Mealman TD, McEvoy MM, Blackburn NJ. 2014. Tracking metal ions through a Cu/Ag efflux pump assigns the functional roles of the periplasmic proteins. Proc Natl Acad Sci USA 111:15373–15378. http://dx.doi.org/10.1073/pnas.1411475111. [CrossRef]
7. Bagai I, Rensing C, Blackburn NJ, McEvoy MM. 2008. Direct metal transfer between periplasmic proteins identifies a bacterial copper chaperone. Biochemistry 47:11408–11414. http://dx.doi.org/10.1021/bi801638m. [CrossRef]
8. Andrès Y, Redercher S, Gerente C, Thouand G. 2001. Contribution of biosorption to the behavior of radionuclides in the environment. J Radioanal Nucl Chem 247:89–93. http://dx.doi.org/10.1023/A:1006763030854. [CrossRef]
9. Song Z, Kenney JPL, Fein JB, Bunker BA. 2012. An X-ray absorption fine structure study of Au adsorbed onto the non-metabolizing cells of two soil bacterial species. Geochim Cosmochim Acta 86:103–117. http://dx.doi.org/10.1016/j.gca.2012.02.030. [CrossRef]
10. Beveridge TJ, Murray RGE. 1976. Uptake and retention of metals by cell walls of Bacillus subtilis. J Bacteriol 127:1502–1518. [PubMed]
11. Fein JB, Daughney CJ, Yee N, Davis TA. 1997. A chemical equilibrium model for metal adsorption onto bacterial surfaces. Geochim Cosmochim Acta 61:3319–3328. http://dx.doi.org/10.1016/S0016-7037(97)00166-X. [CrossRef]
12. Ishibashi Y, Cervantes C, Silver S. 1990. Chromium reduction in Pseudomonas putida. Appl Environ Microbiol 56:2268–2270. [PubMed]
13. Switzer Blum J, Burns Bindi A, Buzzelli J, Stolz JF, Oremland RS. 1998. Bacillus arsenicoselenatis, sp. nov., and Bacillus selenitireducens, sp. nov.: two haloalkaliphiles from Mono Lake, California that respire oxyanions of selenium and arsenic. Arch Microbiol 171:19–30. http://dx.doi.org/10.1007/s002030050673. [PubMed][CrossRef]
14. Lortie L, Gould WD, Rajan S, McCready RGL, Cheng KJ. 1992. Reduction of selenate and selenite to elemental selenium by a Pseudomonas stutzeri isolate. Appl Environ Microbiol 58:4042–4044. [PubMed]
15. Hashim MA, Mukhopadhyay S, Sahu JN, Sengupta B. 2011. Remediation technologies for heavy metal contaminated groundwater. J Environ Manage 92:2355–2388. http://dx.doi.org/10.1016/j.jenvman.2011.06.009. [PubMed][CrossRef]
16. Izaki K, Tashiro Y, Funaba T. 1974. Mechanism of mercuric chloride resistance in microorganisms. 3. Purification and properties of a mercuric ion reducing enzyme from Escherichia coli bearing R factor. J Biochem 75:591–599. [PubMed]
17. Schottel JL. 1978. The mercuric and organomercurial detoxifying enzymes from a plasmid-bearing strain of Escherichia coli. J Biol Chem 253:4341–4349. [PubMed]
18. Furukawa K, Tonomura K. 1972. Induction of metallic mercury-releasing enzyme in mercury-resistant Pseudomonas. Agric Biol Chem 36:2441–2448. http://dx.doi.org/10.1271/bbb1961.36.2441. [CrossRef]
19. Chen S, Wilson DB. 1997. Construction and characterization of Escherichia coli genetically engineered for bioremediation of Hg(2+)-contaminated environments. Appl Environ Microbiol 63:2442–2445. [PubMed]
20. Deng X, Wilson DB. 2001. Bioaccumulation of mercury from wastewater by genetically engineered Escherichia coli. Appl Microbiol Biotechnol 56:276–279. http://dx.doi.org/10.1007/s002530100620. [PubMed][CrossRef]
21. Brim H, McFarlan SC, Fredrickson JK, Minton KW, Zhai M, Wackett LP, Daly MJ. 2000. Engineering Deinococcus radiodurans for metal remediation in radioactive mixed waste environments. Nat Biotechnol 18:85–90. http://dx.doi.org/10.1038/71986. [PubMed][CrossRef]
22. Brim H, Venkateswaran A, Kostandarithes HM, Fredrickson JK, Daly MJ. 2003. Engineering Deinococcus geothermalis for bioremediation of high-temperature radioactive waste environments. Appl Environ Microbiol 69:4575–4582. http://dx.doi.org/10.1128/AEM.69.8.4575-4582.2003. [PubMed][CrossRef]
23. Bizily SP, Rugh CL, Meagher RB. 2000. Phytodetoxification of hazardous organomercurials by genetically engineered plants. Nat Biotechnol 18:213–217. http://dx.doi.org/10.1038/72678. [PubMed][CrossRef]
24. Bizily SP, Rugh CL, Summers AO, Meagher RB. 1999. Phytoremediation of methylmercury pollution: merB expression in Arabidopsis thaliana confers resistance to organomercurials. Proc Natl Acad Sci USA 96:6808–6813. http://dx.doi.org/10.1073/pnas.96.12.6808. [PubMed][CrossRef]
25. Deckwer WD, Becker FU, Ledakowicz S, Wagner-Döbler I. 2004. Microbial removal of ionic mercury in a three-phase fluidized bed reactor. Environ Sci Technol 38:1858–1865. http://dx.doi.org/10.1021/es0300517. [PubMed][CrossRef]
26. Zhang K, Li F. 2011. Isolation and characterization of a chromium-resistant bacterium Serratia sp. Cr-10 from a chromate-contaminated site. Appl Microbiol Biotechnol 90:1163–1169. http://dx.doi.org/10.1007/s00253-011-3120-y. [PubMed][CrossRef]
27. Bowen De León K, Young ML, Camilleri LB, Brown SD, Skerker JM, Deutschbauer AM, Arkin AP, Fields MW. 2012. Draft genome sequence of Pelosinus fermentans JBW45, isolated during in situ stimulation for Cr(VI) reduction. J Bacteriol 194:5456–5457. http://dx.doi.org/10.1128/JB.01224-12. [PubMed][CrossRef]
28. VanEngelen MR, Peyton BM, Mormile MR, Pinkart HC. 2008. Fe(III), Cr(VI), and Fe(III) mediated Cr(VI) reduction in alkaline media using a Halomonas isolate from Soap Lake, Washington. Biodegradation 19:841–850. http://dx.doi.org/10.1007/s10532-008-9187-1. [PubMed][CrossRef]
29. Suzuki T, Miyata N, Horitsu H, Kawai K, Takamizawa K, Tai Y, Okazaki M. 1992. NAD(P)H-dependent chromium (VI) reductase of Pseudomonas ambigua G-1: a Cr(V) intermediate is formed during the reduction of Cr(VI) to Cr(III). J Bacteriol 174:5340–5345. [PubMed]
30. Park CH, Keyhan M, Wielinga B, Fendorf S, Matin A. 2000. Purification to homogeneity and characterization of a novel Pseudomonas putida chromate reductase. Appl Environ Microbiol 66:1788–1795. http://dx.doi.org/10.1128/AEM.66.5.1788-1795.2000. [PubMed][CrossRef]
31. Bae W, Chen W, Mulchandani A, Mehra RK. 2000. Enhanced bioaccumulation of heavy metals by bacterial cells displaying synthetic phytochelatins. Biotechnol Bioeng 70:518–524. http://dx.doi.org/10.1002/1097-0290(20001205)70:5<518::AID-BIT6>3.0.CO;2-5. [PubMed][CrossRef]
32. Bopp LH, Ehrlich HL. 1988. Chromate resistance and reduction in Pseudomonas fluorescens strain LB300. Arch Microbiol 150:426–431. http://dx.doi.org/10.1007/BF00422281. [CrossRef]
33. Lovley DR, Phillips EJP. 1994. Reduction of chromate by Desulfovibrio vulgaris and its C3 cytochrome. Appl Environ Microbiol 60:726–728. [PubMed]
34. Jeyasingh J, Somasundaram V, Philip L, Bhallamudi SM. 2011. Pilot scale studies on the remediation of chromium contaminated aquifer using bio-barrier and reactive zone technologies. Chem Eng J 167:206–214. http://dx.doi.org/10.1016/j.cej.2010.12.024. [CrossRef]
35. Kennedy MJ, Reader SL, Swierczynski LM. 1994. Preservation records of micro-organisms: evidence of the tenacity of life. Microbiology 140:2513–2529. http://dx.doi.org/10.1099/00221287-140-10-2513. [PubMed][CrossRef]
36. Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P. 2000. Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev 64:548–572. http://dx.doi.org/10.1128/MMBR.64.3.548-572.2000. [PubMed][CrossRef]
37. Sneath PHA. 1962. Longevity of micro-organisms. Nature 195:643–646. http://dx.doi.org/10.1038/195643a0. [CrossRef]
38. He LM, Tebo BM. 1998. Surface charge properties of and Cu(II) adsorption by spores of the marine Bacillus sp. strain SG-1. Appl Environ Microbiol 64:1123–1129. [PubMed]
39. Turekian KK, Wedepohl KH. 1961. Distribution of the elements in some major units of the earth’s crust. Bull Geol Soc Am 72:175–192. http://dx.doi.org/10.1130/0016-7606(1961)72[175:DOTEIS]2.0.CO;2. [CrossRef]
40. Post JE. 1999. Manganese oxide minerals: crystal structures and economic and environmental significance. Proc Natl Acad Sci USA 96:3447–3454 http://dx.doi.org/10.1073/pnas.96.7.3447. [PubMed][CrossRef]
41. Towler PH, Smith JD, Dixon DR. 1996. Magnetic recovery of radium, lead and polonium from seawater samples after preconcentration on a magnetic adsorbent of manganese dioxide coated magnetite. Anal Chim Acta 328:53–59. http://dx.doi.org/10.1016/0003-2670(96)00080-3. [CrossRef]
42. Todd JF, Elsinger RJ, Moore WS. 1988. The distributions of uranium, radium and thorium isotopes in two anoxic fjords: Framvaren Fjord (Norway) and Saanich Inlet (British Columbia). Mar Chem 23:393–415. http://dx.doi.org/10.1016/0304-4203(88)90107-7. [CrossRef]
43. Wei C-L, Murray JW. 1991. 234Th/ 238U disequilibria in the Black Sea. Deep-Sea Res 38:S855–S873. http://dx.doi.org/10.1016/S0198-0149(10)80013-5. [CrossRef]
44. Goldberg ED. 1954. Marine geochemistry I. Chemical scavengers of the sea. J Geol 62:249–265. http://dx.doi.org/10.1086/626161. [CrossRef]
45. Prasad VS, Chaudhuri M. 1995. Removal of bacteria and turbidity from water by chemically treated manganese and iron ores. Aqua Lond 44:80–82. http://www.ircwash.org/resources/removal-bacteria-and-turbidity-water-chemically-treated-manganese-and-iron-ores.
46. Stone AT, Morgan JJ. 1984. Reduction and dissolution of manganese(III) and manganese(IV) oxides by organics: 2. Survey of the reactivity of organics. Environ Sci Technol 18:617–624. http://dx.doi.org/10.1021/es00126a010. [PubMed][CrossRef]
47. Stone AT, Morgan JJ. 1984. Reduction and dissolution of manganese(III) and manganese(IV) oxides by organics. 1. Reaction with hydroquinone. Environ Sci Technol 18:450–456. http://dx.doi.org/10.1021/es00124a011. [PubMed][CrossRef]
48. Lehmann RG, Cheng HH, Harsh JB. 1987. Oxidation of phenolic acids by soil iron and manganese oxides. Soil Sci Soc Am J 51:352–356. http://dx.doi.org/10.2136/sssaj1987.03615995005100020017x. [CrossRef]
49. Sunda WG, Kieber DJ. 1994. Oxidation of humic substances by manganese oxides yields low-molecular-weight organic substrates. Nature 367:62–64. http://dx.doi.org/10.1038/367062a0. [CrossRef]
50. Scott MJ, Morgan JJ. 1996. Reactions at oxide surfaces. 2. Oxidation of Se(IV) by synthetic birnessite. Environ Sci Technol 30:1990–1996. http://dx.doi.org/10.1021/es950741d. [CrossRef]
51. Manceau A, Charlet L. 1992. X-ray absorption spectroscopic study of the sorption of Cr(III) at the oxide-water interface. I. Molecular mechanism of Cr(III) oxidation on Mn oxides. J Colloid Interface Sci 148:425–442. http://dx.doi.org/10.1016/0021-9797(92)90181-K. [CrossRef]
52. Huang PM. 1991. Kinetics of redox reactions on manganese oxides and its impact on environmental quality, p 191–230. In Sparks DL, Suarez DL (ed), Rates of Soil Chemical Processes. Soil Science Society of America, Inc, Madison, WI.
53. Lin K, Liu W, Gant J. 2009. Oxidative removal of bisphenol A by manganese dioxide: efficacy, products, and pathways. Environ Sci Technol 43:3860–3864. http://dx.doi.org/10.1021/es900235f. [PubMed][CrossRef]
54. Stone AT. 1987. Reductive dissolution of manganese(III/IV) oxides by substituted phenols. Environ Sci Technol 21:979–988. http://dx.doi.org/10.1021/es50001a011. [PubMed][CrossRef]
55. Ulrich HJ, Stone AT. 1989. Oxidation of chlorophenols adsorbed to manganese oxide surfaces. Environ Sci Technol 23:421–428. http://dx.doi.org/10.1021/es00181a006. [CrossRef]
56. Tebo BM, Bargar JR, Clement BG, Dick GJ, Murray KJ, Parker D, Verity R, Webb SM. 2004. Biogenic manganese oxides: properties and mechanisms of formation. Annu Rev Earth Planet Sci 32:287–328. http://dx.doi.org/10.1146/annurev.earth.32.101802.120213. [CrossRef]
57. Park JW, Dec J, Kim JE, Bollag JM. 1999. Effect of humic constituents on the transformation of chlorinated phenols and anilines in the presence of oxidoreductive enzymes or birnessite. Environ Sci Technol 33:2028–2034. http://dx.doi.org/10.1021/es9810787. [CrossRef]
58. Cheney MA, Sposito G, McGrath AE, Criddle RS. 1996. Abiotic degradation of 2,4-D (dichlorophenoxyacetic acid) on synthetic birnessite: a calorespirometric method. Colloids Surf A Physicochem Eng Asp 107:131–140. http://dx.doi.org/10.1016/0927-7757(95)03385-8. [CrossRef]
59. Nasser A, Sposito G, Cheney MA. 2000. Mechanochemical degradation of 2,4-D adsorbed on synthetic birnessite. Colloids Surf A Physicochem Eng Asp 163:117–123. http://dx.doi.org/10.1016/S0927-7757(99)00297-6. [CrossRef]
60. Cheney MA, Shin JY, Crowley DE, Alvey S, Malengreau N, Sposito G. 1998. Atrazine dealkylation on a manganese oxide surface. Colloids Surf A Physicochem Eng Asp 137:267–273. http://dx.doi.org/10.1016/S0927-7757(97)00368-3. [CrossRef]
61. Stone AT. 1987. Microbial metabolites and the reductive dissolution of manganese oxides: oxalate and pyruvate. Geochim Cosmochim Acta 51:919–925. http://dx.doi.org/10.1016/0016-7037(87)90105-0. [CrossRef]
62. Laha S, Luthy RG. 1990. Oxidation of aniline and other primary aromatic amines by manganese dioxide. Environ Sci Technol 24:363–373. http://dx.doi.org/10.1021/es00073a012. [CrossRef]
63. Morgan JJ. 2000. Manganese in natural waters and earth’s crust: Its availability to organisms, p 1–33. In Sigel A, Sigel H (ed), Metal Ions in Biological Systems, vol 37. Manganese and Its Role in Biological Processes. Marcel Dekker, New York.
64. Hastings D, Emerson S. 1986. Oxidation of manganese by spores of a marine bacillus: kinetic and thermodynamic considerations. Geochim Cosmochim Acta 50:1819–1824. http://dx.doi.org/10.1016/0016-7037(86)90141-9. [CrossRef]
65. Richardson LL, Aguilar C, Nealson KH. 1988. Manganese oxidation in pH and O2 microenvironments produced by phytoplankton. Limnol Oceanogr 33:352–363. http://dx.doi.org/10.4319/lo.1988.33.3.0352. [PubMed][CrossRef]
66. Hullo MF, Moszer I, Danchin A, Martin-Verstraete I. 2001. CotA of Bacillus subtilis is a copper-dependent laccase. J Bacteriol 183:5426–5430. http://dx.doi.org/10.1128/JB.183.18.5426-5430.2001. [PubMed][CrossRef]
67. Nealson KH. 1978. The isolation and characterization of marine bacteria which catalyze manganese oxidation, p 847–858. In Krumbein WE (ed), Environmental Biogeochemistry and Geomicrobiology. vol 3: Methods, Metals and Assessment. Ann Arbor Science Publishers Inc., Ann Arbor, MI.
68. Rosson RA, Nealson KH. 1982. Manganese binding and oxidation by spores of a marine bacillus. J Bacteriol 151:1027–1034. [PubMed]
69. Dick GJ. 2006. Molecular Biogeochemistry of Mn(II) Oxidation: Deep-sea Hydrothermal Plumes, Enzymes, and Genomes. Ph.D. dissertation. University of California, San Diego.
70. Francis CA, Tebo BM. 2002. Enzymatic manganese(II) oxidation by metabolically dormant spores of diverse Bacillus species. Appl Environ Microbiol 68:874–880. http://dx.doi.org/10.1128/AEM.68.2.874-880.2002. [PubMed][CrossRef]
71. Lee Y. 1994. Microbial Oxidation of Cobalt: Characterization and Its Significance in Marine Environments. Ph.D. dissertation. University of California, San Diego.
72. Templeton AS, Staudigel H, Tebo BM. 2005. Diverse Mn(II) oxidizing bacteria isolated from submarine basalts at Loihi Seamount. Geomicrobiol J 22:127–139. http://dx.doi.org/10.1080/01490450590945951. [CrossRef]
73. Dick GJ, Lee YE, Tebo BM. 2006. Manganese(II)-oxidizing Bacillus spores in Guaymas Basin hydrothermal sediments and plumes. Appl Environ Microbiol 72:3184–3190. http://dx.doi.org/10.1128/AEM.72.5.3184-3190.2006. [PubMed][CrossRef]
74. Cowen JP, Hui Li Y. 1991. The influence of a changing bacterial community on trace metal scavenging in a deep-sea particle plume. J Mar Res 49:517–542. http://dx.doi.org/10.1357/002224091784995800. [CrossRef]
75. Cowen JP, Massoth GJ, Baker ET. 1986. Bacterial scavenging of Mn and Fe in a mid- to far-field hydrothermal particle plume. Nature 322:169–171. http://dx.doi.org/10.1038/322169a0. [CrossRef]
76. Cowen JP, Massoth GJ, Feely RA. 1990. Scavenging rates of dissolved manganese in a hydrothermal vent plume. Deep-Sea Res A, Oceanogr Res Pap 37:1619–1637. http://dx.doi.org/10.1016/0198-0149(90)90065-4. [CrossRef]
77. Murray KJ, Webb SM, Bargar JR, Tebo BM. 2007. Indirect oxidation of Co(II) in the presence of the marine Mn(II)-oxidizing bacterium Bacillus sp. strain SG-1. Appl Environ Microbiol 73:6905–6909. http://dx.doi.org/10.1128/AEM.00971-07. [PubMed][CrossRef]
78. Murray KJ, Tebo BM. 2007. Cr(III) is indirectly oxidized by the Mn(II)-oxidizing bacterium Bacillus sp. strain SG-1. Environ Sci Technol 41:528–533. http://dx.doi.org/10.1021/es0615167. [PubMed][CrossRef]
79. Fredrickson JK, Zachara JM, Kennedy DW, Liu C, Duff MC, Hunter DB, Dohnalkova A. 2002. Influence of Mn oxides on the reduction of uranium(VI) by the metal-reducing bacterium Shewanellaputrefaciens. Geochim Cosmochim Acta 66:3247–3262. http://dx.doi.org/10.1016/S0016-7037(02)00928-6. [CrossRef]
80. Fendorf SE, Zasoski RJ. 1992. Chromium(III) oxidation by δ-MnO2. 1. Characterization. Environ Sci Technol 26:79–85. http://dx.doi.org/10.1021/es00025a006. [CrossRef]
81. Chinni S, Anderson CR, Ulrich KU, Giammar DE, Tebo BM. 2008. Indirect UO2 oxidation by Mn(II)-oxidizing spores of Bacillus sp. strain SG-1 and the effect of U and Mn concentrations. Environ Sci Technol 42:8709–8714. http://dx.doi.org/10.1021/es801388p. [PubMed][CrossRef]
82. Bargar JR, Tebo BM, Villinski JE. 2000. In situ characterization of Mn(II) oxidation by spores of the marine Bacillus sp. strain SG-1. Geochim Cosmochim Acta 64:2775–2778. http://dx.doi.org/10.1016/S0016-7037(00)00368-9. [CrossRef]
83. van Waasbergen LG, Hoch JA, Tebo BM. 1993. Genetic analysis of the marine manganese-oxidizing Bacillus sp. strain SG-1: protoplast transformation, Tn917 mutagenesis, and identification of chromosomal loci involved in manganese oxidation. J Bacteriol 175:7594–7603. [PubMed]
84. van Waasbergen LG, Hildebrand M, Tebo BM. 1996. Identification and characterization of a gene cluster involved in manganese oxidation by spores of the marine Bacillus sp. strain SG-1. J Bacteriol 178:3517–3530. [PubMed]
85. Dick GJ, Torpey JW, Beveridge TJ, Tebo BM. 2008. Direct identification of a bacterial manganese(II) oxidase, the multicopper oxidase MnxG, from spores of several different marine Bacillus species. Appl Environ Microbiol 74:1527–1534. http://dx.doi.org/10.1128/AEM.01240-07. [PubMed][CrossRef]
86. Moeller R, Schuerger AC, Reitz G, Nicholson WL. 2012. Protective role of spore structural components in determining Bacillus subtilis spore resistance to simulated mars surface conditions. Appl Environ Microbiol 78:8849–8853. http://dx.doi.org/10.1128/AEM.02527-12. [PubMed][CrossRef]
87. Martins LO, Soares CM, Pereira MM, Teixeira M, Costa T, Jones GH, Henriques AO. 2002. Molecular and biochemical characterization of a highly stable bacterial laccase that occurs as a structural component of the Bacillus subtilis endospore coat. J Biol Chem 277:18849–18859. http://dx.doi.org/10.1074/jbc.M200827200. [CrossRef]
88. Solomon EI, Sundaram UM, Machonkin TE. 1996. Multicopper oxidases and oxygenases. Chem Rev 96:2563–2606. http://dx.doi.org/10.1021/cr950046o. [PubMed][CrossRef]
89. Butterfield CN, Soldatova AV, Lee SW, Spiro TG, Tebo BM. 2013. Mn(II,III) oxidation and MnO 2 mineralization by an expressed bacterial multicopper oxidase. Proc Natl Acad Sci USA 110:11731–11735. http://dx.doi.org/10.1073/pnas.1303677110. [PubMed][CrossRef]
90. Butterfield CN.2014. Characterizing the Mn(II) oxidizing enzyme from the marine Bacillus sp. PL-12 spore. Dissertation. Oregon Health & Science University, Portland, OR.
91. Butterfield CN, Tao L, Chacón KN, Spiro TG, Blackburn NJ, Casey WH, Britt RD, Tebo BM. 2015. Multicopper manganese oxidase accessory proteins bind Cu and Heme. Biochim Biophys Acta 1854:1853–1859. http:/dx.doi.org/10.1016/j.bbapap.2015.08.012 [PubMed][CrossRef]
92. Learman DR, Wankel SD, Webb SM, Martinez N, Madden AS, Hansel CM. 2011. Coupled biotic-abiotic Mn(II) oxidation pathway mediates the formation and structural evolution of biogenic Mn oxides. Geochim Cosmochim Acta 75:6048–6063. http://dx.doi.org/10.1016/j.gca.2011.07.026. [CrossRef]
93. Luther GW III. 2010. The role of one- and two-electron transfer reactions in forming thermodynamically unstable intermediates as barriers in multi-electron redox reactions. Aquat Geochem 16:395–420. http://dx.doi.org/10.1007/s10498-009-9082-3. [CrossRef]
94. Luther GW III. 2005. Manganese(II) oxidation and Mn(IV) reduction in the environment - Two one-electron transfer steps versus a single two-electron step. Geomicrobiol J 22:195–203. http://dx.doi.org/10.1080/01490450590946022. [CrossRef]
95. Bargar JR, Tebo BM, Bergmann U, Webb SM, Glatzel P, Chiu VQ, Villalobos M. 2005. Biotic and abiotic products of Mn(II) oxidation by spores of the marine Bacillus sp. strain SG-1. Am Mineral 90:143–154. http://dx.doi.org/10.2138/am.2005.1557. [CrossRef]
96. Villalobos M, Toner B, Bargar J, Sposito G. 2003. Characterization of the manganese oxide produced by Pseudomonas putida strain MnB1. Geochim Cosmochim Acta 67:2649–2662. http://dx.doi.org/10.1016/S0016-7037(03)00217-5. [CrossRef]
97. Webb SM, Dick GJ, Bargar JR, Tebo BM. 2005. Evidence for the presence of Mn(III) intermediates in the bacterial oxidation of Mn(II). Proc Natl Acad Sci USA 102:5558–5563. http://dx.doi.org/10.1073/pnas.0409119102. [PubMed][CrossRef]
98. Soldatova AV, Butterfield C, Oyerinde OF, Tebo BM, Spiro TG. 2012. Multicopper oxidase involvement in both Mn(II) and Mn(III) oxidation during bacterial formation of MnO(2). J Biol Inorg Chem 17:1151–1158. http://dx.doi.org/10.1007/s00775-012-0928-6. [CrossRef]
99. Honarmand Ebrahimi K, Bill E, Hagedoorn PL, Hagen WR. 2012. The catalytic center of ferritin regulates iron storage via Fe(II)-Fe(III) displacement. Nat Chem Biol 8:941–948. http://dx.doi.org/10.1038/nchembio.1071. [PubMed][CrossRef]
100. Tao L, Stich TA, Butterfield CN, Romano CA, Spiro TG, Tebo BM, Casey WH, Britt RD. 2015. Mn(II) binding and subsequent oxidation by the multicopper oxidase mnxg investigated by electron paramagnetic resonance spectroscopy. J Am Chem Soc 137:10563–10575. [PubMed][CrossRef]
101. Parker DL, Sposito G, Tebo BM. 2004. Manganese(III) binding to a pyoverdine siderophore produced by a manganese(II)-oxidizing bacterium. Geochim Cosmochim Acta 68:4809–4820. http://dx.doi.org/10.1016/j.gca.2004.05.038. [CrossRef]
102. Glenn JK, Akileswaran L, Gold MH. 1986. Mn(II) oxidation is the principal function of the extracellular Mn-peroxidase from Phanerochaete chrysosporium. Arch Biochem Biophys 251:688–696. http://dx.doi.org/10.1016/0003-9861(86)90378-4. [PubMed][CrossRef]
103. Perez J, Jeffries TW. 1992. Roles of manganese and organic acid chelators in regulating lignin degradation and biosynthesis of peroxidases by Phanerochaete chrysosporium. Appl Environ Microbiol 58:2402–2409. [PubMed]
104. Höfer C, Schlosser D. 1999. Novel enzymatic oxidation of Mn2+ to Mn3+ catalyzed by a fungal laccase. FEBS Lett 451:186–190. http://dx.doi.org/10.1016/S0014-5793(99)00566-9. [PubMed][CrossRef]
105. Schlosser D, Höfer C. 2002. Laccase-catalyzed oxidation of Mn(2+) in the presence of natural Mn(3+) chelators as a novel source of extracellular H(2)O(2) production and its impact on manganese peroxidase. Appl Environ Microbiol 68:3514–3521. http://dx.doi.org/10.1128/AEM.68.7.3514-3521.2002. [PubMed][CrossRef]
106. Kostka JE, Luther GW III, Nealson KH. 1995. Chemical and biological reduction of Mn (III)-pyrophosphate complexes: potential importance of dissolved Mn (III) as an environmental oxidant. Geochim Cosmochim Acta 59:885–894. http://dx.doi.org/10.1016/0016-7037(95)00007-0. [CrossRef]
107. Luther GW III, Ruppel DT, Burkhard C. 1998. Reactivity of dissolved Mn(III) complexes and Mn(IV) species with reductants: Mn redox chemistry without a dissolution step, p 265–280. In Sparks DL, Grundl TJ (ed), Mineral-Water Interfacial Reactions: Kinetics and Mechanisms, ACS Symposium Series, vol 715. American Chemical Society, Washington, DC.
108. Klewicki JK, Morgan JJ. 1999. Dissolution of β-MnOOH particles by ligands: pyrophosphate, ethylenediaminetetraacetate, and citrate. Geochim Cosmochim Acta 63:3017–3024. http://dx.doi.org/10.1016/S0016-7037(99)00229-X. [CrossRef]
109. Klewicki JK, Morgan JJ. 1998. Kinetic behavior of Mn(III) complexes of pyrophosphate, EDTA, and citrate. Environ Sci Technol 32:2916–2922. http://dx.doi.org/10.1021/es980308e. [CrossRef]
110. Wall JD, Krumholz LR. 2006. Uranium reduction. Annu Rev Microbiol 60:149–166. [PubMed][CrossRef]
111. Anderson RT, Vrionis HA, Ortiz-Bernad I, Resch CT, Long PE, Dayvault R, Karp K, Marutzky S, Metzler DR, Peacock A, White DC, Lowe M, Lovley DR. 2003. Stimulating the in situ activity of Geobacter species to remove uranium from the groundwater of a uranium-contaminated aquifer. Appl Environ Microbiol 69:5884–5891. http://dx.doi.org/10.1128/AEM.69.10.5884-5891.2003. [PubMed][CrossRef]
112. Wu WM, Carley J, Fienen M, Mehlhorn T, Lowe K, Nyman J, Luo J, Gentile ME, Rajan R, Wagner D, Hickey RF, Gu B, Watson D, Cirpka OA, Kitanidis PK, Jardine PM, Criddle CS. 2006. Pilot-scale in situ bioremediation of uranium in a highly contaminated aquifer. 1. Conditioning of a treatment zone. Environ Sci Technol 40:3978–3985. http://dx.doi.org/10.1021/es051954y. [CrossRef]
113. Fredrickson JK, Zachara JM, Balkwill DL, Kennedy D, Li SMW, Kostandarithes HM, Daly MJ, Romine MF, Brockman FJ. 2004. Geomicrobiology of high-level nuclear waste-contaminated vadose sediments at the Hanford site, Washington state. Appl Environ Microbiol 70:4230–4241. http://dx.doi.org/10.1128/AEM.70.7.4230-4241.2004. [CrossRef]
114. Markich SJ. 2002. Uranium speciation and bioavailability in aquatic systems: an overview. ScientificWorldJournal 2:707–729. http://dx.doi.org/10.1100/tsw.2002.130. [PubMed][CrossRef]
115. Craft E, Abu-Qare A, Flaherty M, Garofolo M, Rincavage H, Abou-Donia M. 2004. Depleted and natural uranium: chemistry and toxicological effects. J Toxicol Environ Health B Crit Rev 7:297–317. http://dx.doi.org/10.1080/10937400490452714. [PubMed][CrossRef]
116. Kauffman JW, Laughlin WC, Baldwin RA. 1986. Microbiological treatment of uranium mine waters. Environ Sci Technol 20:243–248. http://dx.doi.org/10.1021/es00145a003. [PubMed][CrossRef]
117. Gorby YA, Lovley DR. 1992. Enzymatic uranium precipitation. Environ Sci Technol 26:205–207. http://dx.doi.org/10.1021/es00025a026. [CrossRef]
118. Lovley DR, Phillips EJP. 1992. Reduction of uranium by Desulfovibrio desulfuricans. Appl Environ Microbiol 58:850–856. [PubMed]
119. Lovley DR, Phillips EJP, Gorby YA, Landa ER. 1991. Microbial reduction of uranium. Nature 350:413–416. http://dx.doi.org/10.1038/350413a0. [CrossRef]
120. Marshall MJ, Beliaev AS, Dohnalkova AC, Kennedy DW, Shi L, Wang Z, Boyanov MI, Lai B, Kemner KM, McLean JS, Reed SB, Culley DE, Bailey VL, Simonson CJ, Saffarini DA, Romine MF, Zachara JM, Fredrickson JK. 2006. c-Type cytochrome-dependent formation of U(IV) nanoparticles by Shewanella oneidensis. PLoS Biol 4:e268. http://dx.doi.org/10.1371/journal.pbio.0040268. [PubMed][CrossRef]
121. Sanford RA, Wu Q, Sung Y, Thomas SH, Amos BK, Prince EK, Löffler FE. 2007. Hexavalent uranium supports growth of Anaeromyxobacter dehalogenans and Geobacter spp. with lower than predicted biomass yields. Environ Microbiol 9:2885–2893. http://dx.doi.org/10.1111/j.1462-2920.2007.01405.x. [CrossRef]
122. Fletcher KE, Boyanov MI, Thomas SH, Wu Q, Kemner KM, Löffler FE. 2010. U(VI) reduction to mononuclear U(IV) by Desulfitobacterium species. Environ Sci Technol 44:4705–4709. http://dx.doi.org/10.1021/es903636c. [PubMed][CrossRef]
123. Tebo BM, Obraztsova AY. 1998. Sulfate-reducing bacterium grows with Cr(VI), U(VI), Mn(IV), and Fe(III) as electron acceptors. FEMS Microbiol Lett 162:193–198. http://dx.doi.org/10.1111/j.1574-6968.1998.tb12998.x. [CrossRef]
124. Brodie EL, Desantis TZ, Joyner DC, Baek SM, Larsen JT, Andersen GL, Hazen TC, Richardson PM, Herman DJ, Tokunaga TK, Wan JM, Firestone MK. 2006. Application of a high-density oligonucleotide microarray approach to study bacterial population dynamics during uranium reduction and reoxidation. Appl Environ Microbiol 72:6288–6298. http://dx.doi.org/10.1128/AEM.00246-06. [PubMed][CrossRef]
125. Suzuki Y, Kelly SD, Kemner KM, Banfield JF. 2003. Microbial populations stimulated for hexavalent uranium reduction in uranium mine sediment. Appl Environ Microbiol 69:1337–1346. http://dx.doi.org/10.1128/AEM.69.3.1337-1346.2003. [PubMed][CrossRef]
126. Wu WM, Carley J, Luo J, Ginder-Vogel MA, Cardenas E, Leigh MB, Hwang C, Kelly SD, Ruan C, Wu L, Van Nostrand J, Gentry T, Lowe K, Mehlhorn T, Carroll S, Luo W, Fields MW, Gu B, Watson D, Kemner KM, Marsh T, Tiedje J, Zhou J, Fendorf S, Kitanidis PK, Jardine PM, Criddle CS. 2007. In situ bioreduction of uranium (VI) to submicromolar levels and reoxidation by dissolved oxygen. Environ Sci Technol 41:5716–5723. http://dx.doi.org/10.1021/es062657b. [PubMed][CrossRef]
127. Paredes CJ, Alsaker KV, Papoutsakis ET. 2005. A comparative genomic view of clostridial sporulation and physiology. Nat Rev Microbiol 3:969–978. http://dx.doi.org/10.1038/nrmicro1288. [PubMed][CrossRef]
128. Preuss A, Fimpel J, Diekert G. 1993. Anaerobic transformation of 2,4,6-trinitrotoluene (TNT). Arch Microbiol 159:345–353. http://dx.doi.org/10.1007/BF00290917. [PubMed][CrossRef]
129. Lewis TA, Goszczynski S, Crawford RL, Korus RA, Admassu W. 1996. Products of anaerobic 2,4,6-trinitrotoluene (TNT) transformation by Clostridium bifermentans. Appl Environ Microbiol 62:4669–4674. [PubMed]
130. Sembries S, Crawford RL. 1997. Production of Clostridium bifermentans spores as inoculum for bioremediation of nitroaromatic contaminants. Appl Environ Microbiol 63:2100–2104. [PubMed]
131. Gao W, Francis AJ. 2008. Reduction of uranium(VI) to uranium(IV) by clostridia. Appl Environ Microbiol 74:4580–4584. http://dx.doi.org/10.1128/AEM.00239-08. [PubMed][CrossRef]
132. Francis AJ, Dodge CJ, Lu F, Halada GP, Clayton CR. 1994. XPS and XANES studies of uranium reduction by Clostridium sp. Environ Sci Technol 28:636–639. http://dx.doi.org/10.1021/es00053a016. [PubMed][CrossRef]
133. Zhang S, Yin L, Liu Y, Zhang D, Luo X, Cheng J, Cheng F, Dai J. 2011. Cometabolic biotransformation of fenpropathrin by Clostridium species strain ZP3. Biodegradation 22:869–875. http://dx.doi.org/10.1007/s10532-010-9444-y. [PubMed][CrossRef]
134. Hammill TB, Crawford RL. 1996. Degradation of 2-sec-butyl-4,6-dinitrophenol (dinoseb) by Clostridium bifermentans KMR-1. Appl Environ Microbiol 62:1842–1846. [PubMed]
135. Lal R, Pandey G, Sharma P, Kumari K, Malhotra S, Pandey R, Raina V, Kohler HPE, Holliger C, Jackson C, Oakeshott JG. 2010. Biochemistry of microbial degradation of hexachlorocyclohexane and prospects for bioremediation. Microbiol Mol Biol Rev 74:58–80. http://dx.doi.org/10.1128/MMBR.00029-09. [PubMed][CrossRef]
136. N’Guessan AL, Vrionis HA, Resch CT, Long PE, Lovley DR. 2008. Sustained removal of uranium from contaminated groundwater following stimulation of dissimilatory metal reduction. Environ Sci Technol 42:2999–3004. http://dx.doi.org/10.1021/es071960p. [PubMed][CrossRef]
137. Tapia-Rodriguez A, Tordable-Martinez V, Sun W, Field JA, Sierra-Alvarez R. 2011. Uranium bioremediation in continuously fed upflow sand columns inoculated with anaerobic granules. Biotechnol Bioeng 108:2583–2591. http://dx.doi.org/10.1002/bit.23225. [PubMed][CrossRef]
138. Vecchia ED, Veeramani H, Suvorova EI, Wigginton NS, Bargar JR, Bernier-Latmani R. 2010. U(VI) reduction by spores of Clostridium acetobutylicum. Res Microbiol 161:765–771. http://dx.doi.org/10.1016/j.resmic.2010.08.001. [PubMed][CrossRef]
139. Nölling J, Breton G, Omelchenko MV, Makarova KS, Zeng Q, Gibson R, Lee HM, Dubois J, Qiu D, Hitti J, Wolf YI, Tatusov RL, Sabathe F, Doucette-Stamm L, Soucaille P, Daly MJ, Bennett GN, Koonin EV, Smith DR, GTC Sequencing Center Production, Finishing, and Bioinformatics Teams. 2001. Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum. J Bacteriol 183:4823–4838. http://dx.doi.org/10.1128/JB.183.16.4823-4838.2001. [CrossRef]
140. Hu S, Zheng H, Gu Y, Zhao J, Zhang W, Yang Y, Wang S, Zhao G, Yang S, Jiang W. 2011. Comparative genomic and transcriptomic analysis revealed genetic characteristics related to solvent formation and xylose utilization in Clostridium acetobutylicum EA 2018. BMC Genomics 12:93. http://dx.doi.org/10.1186/1471-2164-12-93. [PubMed][CrossRef]
141. Bao G, Wang R, Zhu Y, Dong H, Mao S, Zhang Y, Chen Z, Li Y, Ma Y. 2011. Complete genome sequence of Clostridium acetobutylicum DSM 1731, a solvent-producing strain with multireplicon genome architecture. J Bacteriol 193:5007–5008. http://dx.doi.org/10.1128/JB.05596-11. [PubMed][CrossRef]
142. Nakotte S, Schaffer S, Böhringer M, Dürre P. 1998. Electroporation of, plasmid isolation from and plasmid conservation in Clostridium acetobutylicum DSM 792. Appl Microbiol Biotechnol 50:564–567. http://dx.doi.org/10.1007/s002530051335. [PubMed][CrossRef]
143. Feustel L, Nakotte S, Dürre P. 2004. Characterization and development of two reporter gene systems for Clostridium acetobutylicum. Appl Environ Microbiol 70:798–803. http://dx.doi.org/10.1128/AEM.70.2.798-803.2004. [PubMed][CrossRef]
144. Inui M, Suda M, Kimura S, Yasuda K, Suzuki H, Toda H, Yamamoto S, Okino S, Suzuki N, Yukawa H. 2008. Expression of Clostridium acetobutylicum butanol synthetic genes in Escherichia coli. Appl Microbiol Biotechnol 77:1305–1316. http://dx.doi.org/10.1007/s00253-007-1257-5. [PubMed][CrossRef]
145. Green EM, Boynton ZL, Harris LM, Rudolph FB, Papoutsakis ET, Bennett GN. 1996. Genetic manipulation of acid formation pathways by gene inactivation in Clostridium acetobutylicum ATCC 824. Microbiology 142:2079–2086. http://dx.doi.org/10.1099/13500872-142-8-2079. [PubMed][CrossRef]
146. Junier P, Frutschi M, Wigginton NS, Schofield EJ, Bargar JR, Bernier-Latmani R. 2009. Metal reduction by spores of Desulfotomaculum reducens. Environ Microbiol 11:3007–3017. http://dx.doi.org/10.1111/j.1462-2920.2009.02003.x. [PubMed][CrossRef]
147. Newman DK, Kennedy EK, Coates JD, Ahmann D, Ellis DJ, Lovley DR, Morel FMM. 1997. Dissimilatory arsenate and sulfate reduction in Desulfotomaculum auripigmentum sp. nov. Arch Microbiol 168:380–388. http://dx.doi.org/10.1007/s002030050512. [PubMed][CrossRef]
148. Radhika V, Subramanian S, Natarajan KA. 2006. Bioremediation of zinc using Desulfotomaculum nigrificans: bioprecipitation and characterization studies. Water Res 40:3628–3636. http://dx.doi.org/10.1016/j.watres.2006.06.013. [PubMed][CrossRef]
149. Fortin D, Southam G, Beveridge TJ. 1994. Nickel sulfide, iron-nickel sulfide and iron sulfide precipitation by a newly isolated Desulfotomaculum species and its relation to nickel resistance. FEMS Microbiol Ecol 14:121–132. http://dx.doi.org/10.1111/j.1574-6941.1994.tb00099.x. [CrossRef]
150. Chang YJ, Peacock AD, Long PE, Stephen JR, McKinley JP, Macnaughton SJ, Hussain AK, Saxton AM, White DC. 2001. Diversity and characterization of sulfate-reducing bacteria in groundwater at a uranium mill tailings site. Appl Environ Microbiol 67:3149–3160. http://dx.doi.org/10.1128/AEM.67.7.3149-3160.2001. [PubMed][CrossRef]
151. Nevin KP, Finneran KT, Lovley DR. 2003. Microorganisms associated with uranium bioremediation in a high-salinity subsurface sediment. Appl Environ Microbiol 69:3672–3675. http://dx.doi.org/10.1128/AEM.69.6.3672-3675.2003. [PubMed][CrossRef]
152. Bernier-Latmani R, Veeramani H, Vecchia ED, Junier P, Lezama-Pacheco JS, Suvorova EI, Sharp JO, Wigginton NS, Bargar JR. 2010. Non-uraninite products of microbial U(VI) reduction. Environ Sci Technol 44:9456–9462. http://dx.doi.org/10.1021/es101675a. [PubMed][CrossRef]
153. Hernandez ME, Newman DK. 2001. Extracellular electron transfer. Cell Mol Life Sci 58:1562–1571. http://dx.doi.org/10.1007/PL00000796. [PubMed][CrossRef]
154. Finneran KT, Anderson RT, Nevin KP, Lovley DR. 2002. Potential for bioremediation of uranium-contaminated aquifers with microbial U(VI) reduction. Soil Sediment Contam 11:339–357. http://dx.doi.org/10.1080/20025891106781. [CrossRef]
155. von Canstein H, Ogawa J, Shimizu S, Lloyd JR. 2008. Secretion of flavins by Shewanella species and their role in extracellular electron transfer. Appl Environ Microbiol 74:615–623. http://dx.doi.org/10.1128/AEM.01387-07. [PubMed][CrossRef]
156. Marsili E, Baron DB, Shikhare ID, Coursolle D, Gralnick JA, Bond DR. 2008. Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci USA 105:3968–3973. http://dx.doi.org/10.1073/pnas.0710525105. [PubMed][CrossRef]
157. Sivaswamy V, Boyanov MI, Peyton BM, Viamajala S, Gerlach R, Apel WA, Sani RK, Dohnalkova A, Kemner KM, Borch T. 2011. Multiple mechanisms of uranium immobilization by Cellulomonas sp. strain ES6. Biotechnol Bioeng 108:264–276. http://dx.doi.org/10.1002/bit.22956. [PubMed][CrossRef]
158. Lovley DR, Coates JD, Blunt-Harris EL, Phillips EJP, Woodward JC. 1996. Humic substances as electron acceptors for microbial respiration. Nature 382:445–448. http://dx.doi.org/10.1038/382445a0. [CrossRef]
159. Ahmed B, Cao B, McLean JS, Ica T, Dohnalkova A, Istanbullu O, Paksoy A, Fredrickson JK, Beyenal H. 2012. Fe(III) reduction and U(VI) immobilization by Paenibacillus sp. strain 300A, isolated from Hanford 300A subsurface sediments. Appl Environ Microbiol 78:8001–8009. http://dx.doi.org/10.1128/AEM.01844-12. [PubMed][CrossRef]
160. Junier P, Junier T, Podell S, Sims DR, Detter JC, Lykidis A, Han CS, Wigginton NS, Gaasterland T, Bernier-Latmani R. 2010. The genome of the Gram-positive metal- and sulfate-reducing bacterium Desulfotomaculum reducens strain MI-1. Environ Microbiol 12:2738–2754. [PubMed][CrossRef]
161. Junier P, Vecchia ED, Bernier-Latmani R. 2011. The response of desulfotomaculum reducens MI-1 to U(VI) exposure: a transcriptomic study. Geomicrobiol J 28:483–496. http://dx.doi.org/10.1080/01490451.2010.512031. [CrossRef]
162. Bonde GJ. 1981. Bacillus from marine habitats: allocation to phena established by numerical techniques, p 181–215. In Berkeley RCW, Goodfellow M (ed), The Aerobic Endospore-Forming Bacteria: Classification and Identification. Academic Press, New York.
163. Hong HA, To E, Fakhry S, Baccigalupi L, Ricca E, Cutting SM. 2009. Defining the natural habitat of Bacillus spore-formers. Res Microbiol 160:375–379. http://dx.doi.org/10.1016/j.resmic.2009.06.006. [CrossRef]
164. Langerhuus AT, Røy H, Lever MA, Morono Y, Inagaki F, Jørgensen BB, Lomstein BA. 2012. Endospore abundance and D:L-amino acid modeling of bacterial turnover in holocene marine sediment (Aarhus Bay). Geochim Cosmochim Acta 99:87–99. http://dx.doi.org/10.1016/j.gca.2012.09.023. [CrossRef]
165. Lomstein BA, Langerhuus AT, D’Hondt S, Jørgensen BB, Spivack AJ. 2012. Endospore abundance, microbial growth and necromass turnover in deep sub-seafloor sediment. Nature 484:101–104. http://dx.doi.org/10.1038/nature10905. [PubMed][CrossRef]
166. Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, Richardson PM, Solovyev VV, Rubin EM, Rokhsar DS, Banfield JF. 2004. Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:37–43. http://dx.doi.org/10.1038/nature02340. [PubMed][CrossRef]
167. Rahm BG, Richardson RE. 2008. Dehalococcoides’ gene transcripts as quantitative bioindicators of tetrachloroethene, trichloroethene, and cis-1,2-dichloroethene dehalorespiration rates. Environ Sci Technol 42:5099–5105. http://dx.doi.org/10.1021/es702912t. [PubMed][CrossRef]
168. Han JI, Semrau JD. 2004. Quantification of gene expression in methanotrophs by competitive reverse transcription-polymerase chain reaction. Environ Microbiol 6:388–399. http://dx.doi.org/10.1111/j.1462-2920.2004.00572.x. [PubMed][CrossRef]
169. Anderson CR, Davis RE, Bandolin NS, Baptista AM, Tebo BM. 2011. Analysis of in situ manganese(II) oxidation in the Columbia River and offshore plume: linking Aurantimonas and the associated microbial community to an active biogeochemical cycle. Environ Microbiol 13:1561–1576. http://dx.doi.org/10.1111/j.1462-2920.2011.02462.x. [CrossRef]
170. Wilkins MJ, Verberkmoes NC, Williams KH, Callister SJ, Mouser PJ, Elifantz H, N’guessan AL, Thomas BC, Nicora CD, Shah MB, Abraham P, Lipton MS, Lovley DR, Hettich RL, Long PE, Banfield JF. 2009. Proteogenomic monitoring of Geobacter physiology during stimulated uranium bioremediation. Appl Environ Microbiol 75:6591–6599. http://dx.doi.org/10.1128/AEM.01064-09. [PubMed][CrossRef]
171. Tebo BM, Ghiorse WC, van Waasbergen LG, Siering PL, Caspi R. 1997. Bacterially-mediated mineral formation: Insights into manganese(II) oxidation from molecular genetic and biochemical studies, p 225–266. In Banfield JF, Nealson KH (ed), Geomicrobiology: Interactions Between Microbes and Minerals, vol 35. Mineralogical Society of America, Washington, D.C.
172. Park TJ, Choi SK, Jung HC, Lee SY, Pan JG. 2009. Spore display using Bacillus thuringiensis exosporium protein InhA. J Microbiol Biotechnol 19:495–501. http://dx.doi.org/10.4014/jmb.0802.163. [PubMed][CrossRef]
173. Okazaki M, Sugita T, Shimizu M, Ohode Y, Iwamoto K, de Vrind-de Jong EW, de Vrind JPM, Corstjens PLAM. 1997. Partial purification and characterization of manganese-oxidizing factors of Pseudomonas fluorescens GB-1. Appl Environ Microbiol 63:4793–4799. [PubMed]
174. Caspi R, Haygood MG, Tebo BM. 1996. Unusual ribulose-1,5-bisphosphate carboxylase/oxygenase genes from a marine manganese-oxidizing bacterium. Microbiology 142:2549–2559. http://dx.doi.org/10.1099/00221287-142-9-2549. [CrossRef]
175. Boogerd FC, de Vrind JPM. 1987. Manganese oxidation by Leptothrix discophora. J Bacteriol 169:489–494. [PubMed]
176. Ridge JP, Lin M, Larsen EI, Fegan M, McEwan AG, Sly LI. 2007. A multicopper oxidase is essential for manganese oxidation and laccase-like activity in Pedomicrobium sp. ACM 3067. Environ Microbiol 9:944–953. http://dx.doi.org/10.1111/j.1462-2920.2006.01216.x. [CrossRef]
177. Hansel CM, Francis CA. 2006. Coupled photochemical and enzymatic Mn(II) oxidation pathways of a planktonic Roseobacter-Like bacterium. Appl Environ Microbiol 72:3543–3549. http://dx.doi.org/10.1128/AEM.72.5.3543-3549.2006. [CrossRef]
178. Emerson D, Rentz JA, Lilburn TG, Davis RE, Aldrich H, Chan C, Moyer CL. 2007. A novel lineage of proteobacteria involved in formation of marine Fe-oxidizing microbial mat communities. PLoS One 2:e667. http://dx.doi.org/10.1371/journal.pone.0000667. [CrossRef]
179. Emerson D, Moyer C. 1997. Isolation and characterization of novel iron-oxidizing bacteria that grow at circumneutral pH. Appl Environ Microbiol 63:4784–4792. [PubMed]
180. Hallbeck L, Pedersen K. 1991. Autotrophic and mixotrophic growth of Gallionella ferruginea. J Gen Microbiol 137:2657–2661. http://dx.doi.org/10.1099/00221287-137-11-2657. [CrossRef]
181. Straub KL, Benz M, Schink B, Widdel F. 1996. Anaerobic, nitrate-dependent microbial oxidation of ferrous iron. Appl Environ Microbiol 62:1458–1460. [PubMed]
182. Oremland RS, Blum JS, Culbertson CW, Visscher PT, Miller LG, Dowdle P, Strohmaier FE. 1994. Isolation, growth, and metabolism of an obligately anaerobic, selenate-respiring bacterium, strain SES-3. Appl Environ Microbiol 60:3011–3019. [PubMed]
183. Debieux CM, Dridge EJ, Mueller CM, Splatt P, Paszkiewicz K, Knight I, Florance H, Love J, Titball RW, Lewis RJ, Richardson DJ, Butler CS. 2011. A bacterial process for selenium nanosphere assembly. Proc Natl Acad Sci USA 108:13480–13485. http://dx.doi.org/10.1073/pnas.1105959108. [PubMed][CrossRef]
184. Tomei FA, Barton LL, Lemanski CL, Zocco TG. 1992. Reduction of selenate and selenite to elemental selenium by Wolinella succinogenes. Can J Microbiol 38:1328–1333. http://dx.doi.org/10.1139/m92-219. [CrossRef]
185. Burgos WD, McDonough JT, Senko JM, Zhang G, Dohnalkova AC, Kelly SD, Gorby Y, Kemner KM. 2008. Characterization of uraninite nanoparticles produced by Shewanella oneidensis MR-1. Geochim Cosmochim Acta 72:4901–4915. http://dx.doi.org/10.1016/j.gca.2008.07.016. [CrossRef]
186. Wu Q, Sanford RA, Löffler FE. 2006. Uranium(VI) reduction by Anaeromyxobacter dehalogenans strain 2CP-C. Appl Environ Microbiol 72:3608–3614. http://dx.doi.org/10.1128/AEM.72.5.3608-3614.2006. [PubMed][CrossRef]
187. Horitsu H, Futo S, Miyazawa Y, Ogai S, Kawai K. 1987. Enzymatic reduction of hexavalent chromium by hexavalent chromium tolerant Pseudomonas ambigua G-1. Agric Biol Chem 51:2417–2420. http://dx.doi.org/10.1271/bbb1961.51.2417. [CrossRef]
188. Llovera S, Bonet R, Simon-Pujol MD, Congregado F. 1993. Chromate reduction by resting cells of Agrobacterium radiobacter EPS-916. Appl Environ Microbiol 59:3516–3518. [PubMed]
189. Wang PC, Mori T, Komori K, Sasatsu M, Toda K, Ohtake H. 1989. Isolation and characterization of an Enterobacter cloacae strain that reduces hexavalent chromium under anaerobic conditions. Appl Environ Microbiol 55:1665–1669. [PubMed]
190. Lloyd JR, Ridley J, Khizniak T, Lyalikova NN, Macaskie LE. 1999. Reduction of technetium by Desulfovibrio desulfuricans: biocatalyst characterization and use in a flowthrough bioreactor. Appl Environ Microbiol 65:2691–2696. [PubMed]
191. Lloyd JR, Nolting HF, Solé VA, Bosecker K, Macaskie LE. 1998. Technetium reduction and precipitation by sulfate-reducing bacteria. Geomicrobiol J 15:45–58. http://dx.doi.org/10.1080/01490459809378062. [CrossRef]
192. Martinez RJ, Beazley MJ, Taillefert M, Arakaki AK, Skolnick J, Sobecky PA. 2007. Aerobic uranium (VI) bioprecipitation by metal-resistant bacteria isolated from radionuclide- and metal-contaminated subsurface soils. Environ Microbiol 9:3122–3133. http://dx.doi.org/10.1111/j.1462-2920.2007.01422.x. [PubMed][CrossRef]
193. Pan-Hou HSK, Imura N. 1981. Role of hydrogen sulfide in mercury resistance determined by plasmid of Clostridium cochlearium T-2. Arch Microbiol 129:49–52. http://dx.doi.org/10.1007/BF00417179. [PubMed][CrossRef]

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Bacteria are one of the premier biological forces that, in combination with chemical and physical forces, drive metal availability in the environment. Bacterial spores, when found in the environment, are often considered to be dormant and metabolically inactive, in a resting state waiting for favorable conditions for them to germinate. However, this is a highly oversimplified view of spores in the environment. The surface of bacterial spores represents a potential site for chemical reactions to occur. Additionally, proteins in the outer layers (spore coats or exosporium) may also have more specific catalytic activity. As a consequence, bacterial spores can play a role in geochemical processes and may indeed find uses in various biotechnological applications. The aim of this review is to introduce the role of bacteria and bacterial spores in biogeochemical cycles and their potential use as toxic metal bioremediation agents.

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Schematic diagrams of remediation by bacterial inoculation and biobarrier installation (top) and remediation by pump and treat method (bottom).

Source: microbiolspec April 2016 vol. 4 no. 2 doi:10.1128/microbiolspec.TBS-0018-2013
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Transmission electron micrograph sp. SG-1 spore with spiny MnO oxides localized to the exosporium from reference 68 (bar = 0.25 µm) .

Source: microbiolspec April 2016 vol. 4 no. 2 doi:10.1128/microbiolspec.TBS-0018-2013
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Proposed Mn(II) oxidation mechanism by spp. multicopper oxidase MnxG (adapted from reference 98 ).

Source: microbiolspec April 2016 vol. 4 no. 2 doi:10.1128/microbiolspec.TBS-0018-2013
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Examples of oxidation and sorption of metals by bacterial spores.

Source: microbiolspec April 2016 vol. 4 no. 2 doi:10.1128/microbiolspec.TBS-0018-2013
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Examples of elements precipitated by bacteria

Source: microbiolspec April 2016 vol. 4 no. 2 doi:10.1128/microbiolspec.TBS-0018-2013

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