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Volume 2012 (2012), Article ID 789278, 12 pages
http://dx.doi.org/10.1155/2012/789278
Research Article

A First Analysis of Metallome Biosignatures of Hyperthermophilic Archaea

1Department of Geosciences and Penn State Astrobiology Research Center, The Pennsylvania State University, University Park, PA 16802, USA
2School of Earth Sciences, University of Bristol, Bristol BS8 1RJ, UK

Received 12 July 2012; Revised 27 September 2012; Accepted 29 September 2012

Academic Editor: Antoine Danchin

Copyright © 2012 Vyllinniskii Cameron et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. J. R. Frausto da Silva and R. J. P. Williams, The Biological Chemistry of the Elements, vol. 2nd, Oxford University Press, Oxford, UK, 2001.
  2. R. J. P. Williams and J. J. R. Fraústo Da Silva, “Evolution was chemically constrained,” Journal of Theoretical Biology, vol. 220, no. 3, pp. 323–343, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. A. D. Anbar and A. H. Knoll, “Proterozoic ocean chemistry and evolution: a bioinorganic bridge?” Science, vol. 297, no. 5584, pp. 1137–1142, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. C. L. Dupont, S. Yang, B. Palenik, and P. E. Bourne, “Modern proteomes contain putative imprints of ancient shifts in trace metal geochemistry,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 47, pp. 17822–17827, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Kietzin and M. W. W. Adams, “Tungsten in biological systems,” FEMS Microbiology Reviews, vol. 18, no. 1, pp. 5–63, 1996. View at Publisher · View at Google Scholar · View at Scopus
  6. P. E. Cloud, “A working model of the primitive Earth,” American Journal of Science, vol. 272, pp. 537–548, 1972. View at Google Scholar
  7. D. E. Canfield, “A new model for Proterozoic ocean chemistry,” Nature, vol. 396, no. 6710, pp. 450–453, 1998. View at Publisher · View at Google Scholar · View at Scopus
  8. E. L. Stiefel, “The biogeochemistry of molybdenum and tungsten,” in Molybdenum and Tungsten: Their Roles in Biological Processes, M. Dekker, Ed., pp. 1–29, Marcel Dekker, New York, NY, USA, 2002. View at Google Scholar
  9. R. J. P. Williams and J. J. R. Fraústo da Silva, “The involvement of molybdenum in life,” Biochemical and Biophysical Research Communications, vol. 292, no. 2, pp. 293–299, 2002. View at Publisher · View at Google Scholar · View at Scopus
  10. C. R. Woese, O. Kandler, and M. L. Wheelis, “Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 12, pp. 4576–4579, 1990. View at Publisher · View at Google Scholar · View at Scopus
  11. K. O. Stetter, “Hyperthermophilic procaryotes,” FEMS Microbiology Reviews, vol. 18, no. 2-3, pp. 149–158, 1996. View at Publisher · View at Google Scholar · View at Scopus
  12. K. O. Stetter, G. Fiala, G. Huber, R. Huber, and A. Segerer, “Hyperthermophilic microorganisms,” FEMS Microbiology Reviews, vol. 75, no. 2-3, pp. 117–124, 1990. View at Google Scholar · View at Scopus
  13. D. S. Kelley, J. A. Baross, and J. R. Delaney, “Volcanoes, fluids, and life at mid-ocean ridge spreading centers,” Annual Review of Earth and Planetary Sciences, vol. 30, pp. 385–491, 2002. View at Publisher · View at Google Scholar · View at Scopus
  14. K. L. Von Damm, J. M. Edmond, B. Grant, C. I. Measures, B. Walden, and R. F. Weiss, “Chemistry of submarine hydrothermal solutions at 21°N, East Pacific Rise,” Geochimica et Cosmochimica Acta, vol. 49, no. 11, pp. 2197–2220, 1985. View at Google Scholar · View at Scopus
  15. K. L. Von Damm, J. M. Edmond, C. I. Measures, and B. Grant, “Chemistry of submarine hydrothermal solutions at Guaymas Basin, Gulf of California,” Geochimica et Cosmochimica Acta, vol. 49, no. 11, pp. 2221–2237, 1985. View at Google Scholar · View at Scopus
  16. K. W. Bruland, “Complexation of zinc by natural organic ligands in the central North Pacific,” Limnology & Oceanography, vol. 34, no. 2, pp. 269–285, 1989. View at Google Scholar · View at Scopus
  17. V. P. Edgcomb, S. J. Molyneaux, M. A. Saito et al., “Sulfide ameliorates metal toxicity for deep-sea hydrothermal vent archaea,” Applied and Environmental Microbiology, vol. 70, no. 4, pp. 2551–2555, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. J. F. Holden and M. W. W. Adams, “Microbe-metal interactions in marine hydrothermal environments,” Current Opinion in Chemical Biology, vol. 7, no. 2, pp. 160–165, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. L. J. Liermann, R. L. Guynn, A. Anbar, and S. L. Brantley, “Production of a molybdophore during metal-targeted dissolution of silicates by soil bacteria,” Chemical Geology, vol. 220, no. 3-4, pp. 285–302, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. J. B. Neilands, “Siderophores: structure and function of microbial iron transport compounds,” Journal of Biological Chemistry, vol. 270, no. 45, pp. 26723–26726, 1995. View at Google Scholar · View at Scopus
  21. S. G. Sander, A. Koschinsky, G. Massoth, M. Stott, and K. A. Hunter, “Organic complexation of copper in deep-sea hydrothermal vent systems,” Environmental Chemistry, vol. 4, no. 2, pp. 81–89, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. R. J. P. Williams, “Chemical selection of elements by cells,” Coordination Chemistry Reviews, vol. 216-217, pp. 583–595, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. F. M. M. Morel, A. J. Milligan, and M. A. Saito, “Marine bioinorganic chemistry: the role of trace metals in the oceanic cycles of major nutrients,” in Treatise on Geochemistry, H. D. Holland and K. K. Turekian, Eds., pp. 113–143, Elsevier Academic Press, London, UK, 2003. View at Google Scholar
  24. A. D. Anbar and O. Rouxel, “Metal stable isotopes in paleoceanography,” Annual Review of Earth and Planetary Sciences, vol. 35, pp. 717–746, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. C. Archer and D. Vance, “Coupled Fe and S isotope evidence for Archean microbial Fe(III) and sulfate reduction,” Geology, vol. 34, no. 3, pp. 153–156, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. B. L. Beard, C. M. Johnson, L. Cox, H. Sun, K. H. Nealson, and C. Aguilar, “Iron isotope biosignatures,” Science, vol. 285, no. 5435, pp. 1889–1891, 1999. View at Publisher · View at Google Scholar · View at Scopus
  27. A. L. Zerkle, C. H. House, and S. L. Brantley, “Biogeochemical signatures through time as inferred from whole microbial genomes,” American Journal of Science, vol. 305, no. 6-8, pp. 467–502, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. W. B. Whitman, “Validation List No.85: validation of publication of new names and new combinations previously effectively published outside the IJSEM,” International Journal of Systematic and Evolutionary Microbiology, vol. 52, no. 3, pp. 685–690, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. L. A. Finney and T. V. O'Halloran, “Transition metal speciation in the cell: insights from the chemistry of metal ion receptors,” Science, vol. 300, no. 5621, pp. 931–936, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. C. E. Outten and T. V. O'Halloran, “Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis,” Science, vol. 292, no. 5526, pp. 2488–2492, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. T. D. Rae, P. J. Schmidt, R. A. Pufahl, V. C. Culotta, and T. V. O'Halloran, “Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase,” Science, vol. 284, no. 5415, pp. 805–808, 1999. View at Publisher · View at Google Scholar · View at Scopus
  32. F. E. Jenney and M. W. W. Adams, “Hydrogenases of the model hyperthermophiles,” Annals of the New York Academy of Sciences, vol. 1125, pp. 252–266, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. F. M. M. Morel, “The co-evolution of phytoplankton and trace element cycles in the oceans,” Geobiology, vol. 6, no. 3, pp. 318–324, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Ledin, “Accumulation of metals by microorganisms—processes and importance for soil systems,” Earth Science Reviews, vol. 51, no. 1–4, pp. 1–31, 2000. View at Publisher · View at Google Scholar · View at Scopus
  35. L. J. Liermann, B. E. Kalinowski, S. L. Brantley, and J. G. Ferry, “Role of bacterial siderophores in dissolution of hornblende,” Geochimica et Cosmochimica Acta, vol. 64, no. 4, pp. 587–602, 2000. View at Publisher · View at Google Scholar · View at Scopus
  36. P. L. Croot, B. Karlson, J. T. Van Elteren, and J. J. Kroon, “Uptake and efflux of 64CU by the marine cyanobacterium Synechococcus (WH7803),” Limnology and Oceanography, vol. 48, no. 1 I, pp. 179–188, 2003. View at Google Scholar · View at Scopus
  37. F. M. M. Morel and N. M. Price, “The biogeochemical cycles of trace metals in the oceans,” Science, vol. 300, no. 5621, pp. 944–947, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. S. L. Brantley, L. J. Liermann, R. L. Guynn, A. Anbar, G. A. Icopini, and J. Barling, “Fe isotopic fractionation during mineral dissolution with and without bacteria,” Geochimica et Cosmochimica Acta, vol. 68, no. 15, pp. 3189–3204, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. K. J. Edwards, W. Bach, and D. R. Rogers, “Geomicrobiology of the ocean crust: a role for chemoautotrophic Fe-bacteria,” Biological Bulletin, vol. 204, no. 2, pp. 180–185, 2003. View at Google Scholar · View at Scopus
  40. J. R. Rogers and P. C. Bennett, “Mineral stimulation of subsurface microorganisms: release of limiting nutrients from silicates,” Chemical Geology, vol. 203, no. 1-2, pp. 91–108, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. W. W. Barker, S. A. Welch, S. Chu, and J. F. Banfield, “Experimental.observations of the effects of bacteria on aluminosilicate weathering,” American Mineralogist, vol. 83, no. 11-12, pp. 1551–1563, 1998. View at Google Scholar · View at Scopus
  42. A. Neaman, J. Chorover, and S. L. Brantley, “Element mobility patterns record organic ligands in soils on early Earth,” Geology, vol. 33, no. 2, pp. 117–120, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. B. E. Kalinowski, L. J. Liermann, S. Givens, and S. L. Brantley, “Rates of bacteria-promoted solubilization of Fe from minerals: a review of problems and approaches,” Chemical Geology, vol. 169, no. 3-4, pp. 357–370, 2000. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Douglas, “Mineralogical footprints of microbial life,” American Journal of Science, vol. 305, no. 6-8, pp. 503–525, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. I. H. Thorseth, T. Torsvik, H. Furnes, and K. Muehlenbachs, “Microbes play an important role in the alteration of oceanic crust,” Chemical Geology, vol. 126, no. 2, pp. 137–146, 1995. View at Google Scholar · View at Scopus
  46. H. L. Ehrlich, “Microbes as geologic agents: their role in mineral formation,” Geomicrobiology Journal, vol. 16, no. 2, pp. 135–153, 1999. View at Google Scholar · View at Scopus
  47. K. Kashefi and D. R. Lovley, “Reduction of Fe(III), Mn(IV), and toxic metals at 100°C by Pyrobaculum islandicum,” Applied and Environmental Microbiology, vol. 66, no. 3, pp. 1050–1056, 2000. View at Publisher · View at Google Scholar · View at Scopus
  48. W. Bach and K. J. Edwards, “Iron and sulfide oxidation within the basaltic ocean crust: implications for chemolithoautotrophic microbial biomass production,” Geochimica et Cosmochimica Acta, vol. 67, no. 20, pp. 3871–3887, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. S. E. Childers, S. Ciufo, and D. R. Lovley, “Geobacter metallireducens accesses insoluble Fe(III) oxide by chemotaxis,” Nature, vol. 416, no. 6882, pp. 767–769, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. H. Dong, J. K. Fredrickson, D. W. Kennedy, J. M. Zachara, R. K. Kukkadapu, and T. C. Onstott, “Mineral transformation associated with the microbial reduction of magnetite,” Chemical Geology, vol. 169, no. 3-4, pp. 299–318, 2000. View at Publisher · View at Google Scholar · View at Scopus
  51. P. Philippot, M. Van Zuilen, K. Lepot, C. Thomazo, J. Farquhar, and M. J. Van Kranendonk, “Early archaean microorganisms preferred elemental sulfur, not sulfate,” Science, vol. 317, no. 5844, pp. 1534–1537, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. P. Schoenheit, J. Moll, and R. K. Thauer, “Nickel, cobalt, and molybdenum requirement for growth of Methanobacterium thermoautotrophicum,” Archives of Microbiology, vol. 123, no. 1, pp. 105–107, 1979. View at Google Scholar · View at Scopus
  53. Y. Zhang, Z. Zhang, K. Suzuki, and T. Maekawa, “Uptake and mass balance of trace metals for methane producing bacteria,” Biomass and Bioenergy, vol. 25, no. 4, pp. 427–433, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. K. J. Waldron, J. C. Rutherford, D. Ford, and N. J. Robinson, “Metalloproteins and metal sensing,” Nature, vol. 460, no. 7257, pp. 823–830, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. P. J. Boston, M. V. Ivanov, and C. P. McKay, “On the possibility of chemosynthetic ecosystems in subsurface habitats on Mars,” Icarus, vol. 95, no. 2, pp. 300–308, 1992. View at Google Scholar · View at Scopus
  56. D. J. Barber and E. R. D. Scott, “Origin of supposedly biogenic magnetite in the Martian meteorite Allan Hills 84001,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 10, pp. 6556–6561, 2002. View at Publisher · View at Google Scholar · View at Scopus
  57. J. L. Kirschvink and S. R. Chang, “Ultrafine-grained magnetite in deep-sea sediments: possible bacterial magnetofossils,” Geology, vol. 12, no. 9, pp. 559–562, 1984. View at Google Scholar · View at Scopus
  58. F. Westall, A. Steele, J. Toporski et al., “Polymeric substances and biofilms as biomarkers in terrestrial materials: implications for extraterrestrial samples,” Journal of Geophysical Research E, vol. 105, no. 10, pp. 24511–24527, 2000. View at Google Scholar · View at Scopus
  59. P. R. Buseck, R. E. Dunin-Borkowski, B. Devouard et al., “Magnetite morphology and life on Mars,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 24, pp. 13490–13495, 2001. View at Publisher · View at Google Scholar · View at Scopus
  60. K. O. Konhauser, T. Hamade, R. Raiswell et al., “Could bacteria have formed the Precambrian banded iron formations?” Geology, vol. 30, no. 12, pp. 1079–1082, 2002. View at Google Scholar · View at Scopus
  61. C. J. Bjerrum and D. E. Canfield, “Ocean productivity before about 1.9 Gyr ago limited by phosphorus adsorption onto iron oxides,” Nature, vol. 417, no. 6885, pp. 159–162, 2002. View at Publisher · View at Google Scholar · View at Scopus
  62. M. A. Saito, D. M. Sigman, and F. M. M. Morel, “The bioinorganic chemistry of the ancient ocean: the co-evolution of cyanobacterial metal requirements and biogeochemical cycles at the Archean-Proterozoic boundary?” Inorganica Chimica Acta, vol. 356, pp. 308–318, 2003. View at Publisher · View at Google Scholar · View at Scopus
  63. M. Brasier, N. McLoughlin, O. Green, and D. Wacey, “A fresh look at the fossil evidence for early Archaean cellular life,” Philosophical Transactions of the Royal Society B, vol. 361, no. 1470, pp. 887–902, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. V. R. Phoenix, K. O. Konhauser, D. G. Adams, and S. H. Bottrell, “Role of biomineralization as an ultraviolet shield: implications for Archean life,” Geology, vol. 29, no. 9, pp. 823–826, 2001. View at Google Scholar · View at Scopus
  65. M. Vargas, K. Kashefi, E. L. Blunt-Harris, and D. R. Lovley, “Microbiological evidence for Fe(III) reduction on early earth,” Nature, vol. 395, no. 6697, pp. 65–67, 1998. View at Publisher · View at Google Scholar · View at Scopus
  66. U. Ermler, “On the mechanism of methyl-coenzyme M reductase,” Dalton Transactions, no. 21, pp. 3451–3458, 2005. View at Publisher · View at Google Scholar · View at Scopus
  67. G. Diekert, U. Konheiser, K. Piechulla, and R. K. Thauer, “Nickel requirement and factor F430 content of methanogenic bacteria,” Journal of Bacteriology, vol. 148, no. 2, pp. 459–464, 1981. View at Google Scholar · View at Scopus
  68. D. Fortin, G. Southam, and T. J. Beveridge, “Nickel sulfide, iron-nickel sulfide and iron sulfide precipitation by a newly isolated Desulfotomaculum species and its relation to nickel resistance,” FEMS Microbiology Ecology, vol. 14, no. 2, pp. 121–132, 1994. View at Publisher · View at Google Scholar · View at Scopus
  69. T. Y. Ho, A. Quigg, Z. V. Finkel et al., “The elemental composition of some marine phytoplankton,” Journal of Phycology, vol. 39, no. 6, pp. 1145–1159, 2003. View at Publisher · View at Google Scholar · View at Scopus
  70. W. G. Sunda and S. A. Huntsman, “Iron uptake and growth limitation in oceanic and coastal phytoplankton,” Marine Chemistry, vol. 50, no. 1–4, pp. 189–206, 1995. View at Google Scholar · View at Scopus
  71. M. A. Saito and T. J. Goepfert, “Zinc-cobalt colimitation of Phaeocystis antarctica,” Limnology and Oceanography, vol. 53, no. 1, pp. 266–275, 2008. View at Google Scholar · View at Scopus
  72. W. G. Sunda and S. A. Huntsman, “Interactions among Cu2+, Zn2+, and Mn2+ in controlling cellular Mn, Zn, and growth rate in the coastal alga Chlamydomonas,” Limnology and Oceanography, vol. 43, no. 6, pp. 1055–1064, 1998. View at Google Scholar · View at Scopus
  73. W. G. Sunda and S. A. Huntsman, “Processes regulating cellular metal accumulation and physiological effects: phytoplankton as model systems,” Science of the Total Environment, vol. 219, no. 2-3, pp. 165–181, 1998. View at Publisher · View at Google Scholar · View at Scopus
  74. W. G. Sunda and S. A. Huntsman, “Effect of Zn, Mn, and Fe on Cd accumulation in phytoplankton: implications for oceanic Cd cycling,” Limnology and Oceanography, vol. 45, no. 7, pp. 1501–1516, 2000. View at Google Scholar · View at Scopus
  75. G. Gonzalez-Gil, S. Jansen, M. H. Zandvoort, and H. P. Van Leeuwen, “Effect of yeast extract on speciation and bioavailability of nickel and cobalt in anaerobic bioreactors,” Biotechnology and Bioengineering, vol. 82, no. 2, pp. 134–142, 2003. View at Publisher · View at Google Scholar · View at Scopus
  76. A. Cvetkovic, A. L. Menon, M. P. Thorgersen et al., “Microbial metalloproteomes are largely uncharacterized,” Nature, vol. 466, no. 7307, pp. 779–782, 2010. View at Publisher · View at Google Scholar · View at Scopus
  77. P. Scherer, H. Lippert, and G. Wolff, “Composition of the major elements and trace elements of 10 methanogenic bacteria determined by inductively coupled plasma emission spectrometry,” Biological Trace Element Research, vol. 5, no. 3, pp. 149–163, 1983. View at Publisher · View at Google Scholar · View at Scopus
  78. A. Khoshmanesh, B. T. Hart, A. Duncan, and R. Beckett, “Luxury uptake of phosphorus by sediment bacteria,” Water Research, vol. 36, no. 3, pp. 774–778, 2002. View at Publisher · View at Google Scholar · View at Scopus
  79. H. Rudnick, S. Hendrich, U. Pilatus, and K. H. Blotevogel, “Phosphate accumulation and the occurence of polyphosphates and cyclic 2,3-diphosphoglycerate in Methanosarcina frisia,” Archives of Microbiology, vol. 154, no. 6, pp. 584–588, 1990. View at Google Scholar · View at Scopus
  80. K. R. Sowers and J. G. Ferry, “Trace metal and vitamin requirements of Methanococcoides methylutens grown with trimethylamine,” Archives of Microbiology, vol. 142, no. 2, pp. 148–151, 1985. View at Google Scholar · View at Scopus
  81. R. J. P. Williams, “The fundamental nature of life as a chemical system: the part played by inorganic elements,” Journal of Inorganic Biochemistry, vol. 88, no. 3-4, pp. 241–250, 2002. View at Publisher · View at Google Scholar · View at Scopus
  82. R. J. P. Williams, “Systems biology of evolution: the involvement of metal ions,” BioMetals, vol. 20, no. 2, pp. 107–112, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. E. G. Nisbet and N. H. Sleep, “The habitat and nature of early life,” Nature, vol. 409, no. 6823, pp. 1083–1091, 2001. View at Publisher · View at Google Scholar · View at Scopus
  84. M. J. Russell and W. Martin, “The rocky roots of the acetyl-CoA pathway,” Trends in Biochemical Sciences, vol. 29, no. 7, pp. 358–363, 2004. View at Publisher · View at Google Scholar · View at Scopus
  85. G. Wachtershauser, “The cradle chemistry of life—on the origin of natural-products in a pyrite-pulled chemo-autotrophic origin of life,” Pure and Applied Chemistry, vol. 65, pp. 1343–1348, 1993. View at Google Scholar
  86. K. Kishida, Y. Sohrin, K. Okamura, and J. I. Ishibashi, “Tungsten enriched in submarine hydrothermal fluids,” Earth and Planetary Science Letters, vol. 222, no. 3-4, pp. 819–827, 2004. View at Publisher · View at Google Scholar · View at Scopus
  87. S. Arnórsson and N. Óskarsson, “Molybdenum and tungsten in volcanic rocks and in surface and < 100°C ground waters in Iceland,” Geochimica et Cosmochimica Acta, vol. 71, no. 2, pp. 284–304, 2007. View at Publisher · View at Google Scholar · View at Scopus
  88. G. F. Ivanova, “Geochemistry of tungsten,” in Geology of Tungsten, A. A. Beuss, Ed., pp. 11–43, UNESCO, Paris, France, 1986. View at Google Scholar
  89. M. K. Johnson, D. C. Rees, and M. W. W. Adams, “Tungstoenzymes,” Chemical Reviews, vol. 96, no. 7, pp. 2817–2839, 1996. View at Google Scholar · View at Scopus
  90. R. Hille, “Molybdenum and tungsten in biology,” Trends in Biochemical Sciences, vol. 27, no. 7, pp. 360–367, 2002. View at Publisher · View at Google Scholar · View at Scopus
  91. J. G. Ferry, Methanogenesis: Ecology, Physiology, Biochemistry & Genetics, Chapman & Hall, New York, NY, USA, 1993.
  92. S. Frank, A. A. Brindley, E. Deery et al., “Anaerobic synthesis of vitamin B12: characterization of the early steps in the pathway,” Biochemical Society Transactions, vol. 33, no. 4, pp. 811–814, 2005. View at Publisher · View at Google Scholar · View at Scopus
  93. D. Heldt, A. D. Lawrence, M. Lindenmeyer et al., “Aerobic synthesis of vitamin B12: ring contraction and cobalt chelation,” Biochemical Society Transactions, vol. 33, no. 4, pp. 815–819, 2005. View at Publisher · View at Google Scholar · View at Scopus
  94. J. L. Rowe, G. L. Starnes, and P. T. Chivers, “Complex transcriptional control links NikABCDE-dependent nickel transport with hydrogenase expression in Escherichia coli,” Journal of Bacteriology, vol. 187, no. 18, pp. 6317–6323, 2005. View at Publisher · View at Google Scholar · View at Scopus