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Microbiological evidence for Fe(III) reduction on early Earth

Abstract

It is generally considered1 that sulphur reduction was one of the earliest forms of microbial respiration, because the known microorganisms that are most closely related to the last common ancestor of modern life are primarily anaerobic, sulphur-reducing hyperthermophiles2,3,4. However, geochemical evidence indicates that Fe(III) is more likely than sulphur to have been the first external electron acceptor of global significance in microbial metabolism5,6,7. Here we show that Archaea and Bacteria that are most closely related to the last common ancestor can reduce Fe(III) to Fe(II) and conserve energy to support growth from this respiration. Surprisingly, even Thermotoga maritima, previously considered to have only a fermentative metabolism, could grow as a respiratory organism when Fe(III) was provided as an electron acceptor. These results provide microbiological evidence that Fe(III) reduction could have been an important process on early Earth and suggest that microorganisms might contribute to Fe(III) reduction in modern hot biospheres. Furthermore, our discovery that hyperthermophiles that had previously been thought to require sulphur for cultivation can instead be grown without the production of toxic and corrosive sulphide, should aid biochemical investigations of these poorly understood organisms.

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References

  1. Madigan, M. T., Martinko, J. M. & Parker, J. Biology of Microorganisms (Prentice Hall, Upper Saddle River, New Jersey, (1997)).

    Google Scholar 

  2. Pace, N. R. Origin of life — facing up to the physical setting. Cell 65, 531–533 (1991).

    Article  CAS  Google Scholar 

  3. Adams, M. W. W. Enzymes and proteins from organisms that grow near and above 100 °C. Annu. Rev. Microbiol. 47, 627–658 (1993).

    Article  CAS  Google Scholar 

  4. Stetter, K. O. Hyperthermophilic procaryotes. FEMS Microbiol. Rev. 18, 149–158 (1996).

    Article  CAS  Google Scholar 

  5. de Duve, C. Vital Dust 1–362 (Basic Books, New York, (1995)).

    Google Scholar 

  6. Walker, J. C. G. Was the Archaean biosphere upside down? Nature 329, 710–712 (1987).

    Article  ADS  CAS  Google Scholar 

  7. Cairns-Smith, A. G., Hall, A. J. & Russell, M. J. Mineral theories of the origin of life and an iron sulfide example. Orig. Life Evol. Biosph. 22, 161–180 (1992).

    Article  ADS  CAS  Google Scholar 

  8. Walker, J. C. G. & Brimblecombe, P. Iron and sulfur in the pre-biologic ocean. Precambr. Res. 28, 205–222 (1985).

    Article  ADS  CAS  Google Scholar 

  9. Kasting, J. F. Earth's early atmosphere. Science 259, 920–926 (1993).

    Article  ADS  CAS  Google Scholar 

  10. De Ronde, C. E. J., De Wit, M. J. & Spooner, E. T. C. Early Archean (<3.2 Ga) Fe-oxide-rich, hydrothermal discharge vents in the Barberton greenstone belt, South Africa. Geol. Soc. Am. Bull. 106, 86–104 (1984).

    Article  Google Scholar 

  11. Holm, N. G. Why are hydrothermal systems proposed as plausible environments for the origin of life? Origins Life Evol. Biosphere 22, 5–14 (1992).

    Article  ADS  Google Scholar 

  12. Barns, S. M. & Nierzwicki-Bauer, S. A. Microbial diversity in ocean, surface, and subsurface environments. Rev. Mineral. 35, 35–79 (1997).

    CAS  Google Scholar 

  13. Lonergan, D. J. et al. Phylogenetic analysis of dissimilatory Fe(III)-reducing bacteria. J. Bacteriol. 178, 2402–2408 (1996).

    Article  CAS  Google Scholar 

  14. Lovley, D. R., Coates, J. D., Saffarini, D. A. & Lonergan, D. J. in Iron and Related Transition Metals in Microbial Metabolism (eds Winkelman, G. & Carrano, C. J.) 187–215 (Harwood, Switzerland, (1997)).

    Google Scholar 

  15. Boone, D. R. et al. Bacillus infernus sp. nov., an Fe(III)- and Mn(IV)-reducing anaerobe from the deep terrestrial subsurface. Int. J. Sys. Bacteriol. 45, 441–448 (1995).

    Article  CAS  Google Scholar 

  16. Slobodkin, A., Reysenbach, A.-, Strutz, N., Dreier, M. & Wiegel, J. Thermoterrabacterium ferrireducens gen. nov., sp. nov., a thermophilic anaerobic dissimilatory Fe(III)-reducing bacterium from a continental hot spring. Int. J. System. Bacteriol. 47, 541–547 (1997).

    Article  CAS  Google Scholar 

  17. Greene, A. C., Patel, B. K. C. & Sheehy, A. J. Deferribacter thermophilus gen. nov., sp. nov., a novel thermophilic manganese- and iron-reducing bacterium isolated from a petroleum reservoir. Int. J. System. Bacteriol. 47, 505–509 (1997).

    Article  CAS  Google Scholar 

  18. Liu, S. V. et al. Thermophilic Fe(III)-reducing bacteria from the deep subsurface: the evolutionary implications. Science 277, 1106–1109 (1997).

    Article  CAS  Google Scholar 

  19. Lovley, D. R., Stolz, J. F., Nord, G. L. & Phillips, E. J. P. Anaerobic production of magnetite by a dissimilatory iron-reducing microorganism. Nature 330, 252–254 (1987).

    Article  ADS  CAS  Google Scholar 

  20. Lovley, D. R. in Iron Biominerals (eds Frankel, R. B. & Blakemore, R. P.) 151–166 (Plenum, New York, (1990)).

    Google Scholar 

  21. McKay, D. S. et al. Search for past life on Mars: possible relic biogenic activity in Martian meteorite ALH84001. Science 273, 924–930 (1996).

    Article  ADS  CAS  Google Scholar 

  22. Gold, T. The deep, hot biosphere. Proc. Natl Acad. Sci. USA 89, 6045–6049 (1992).

    Article  ADS  CAS  Google Scholar 

  23. Huber, R. et al. Thermotoga maritima sp. nov. represents a new genus of unique extremely thermophilic eubacteria growing up to 90 °C. Arch. Microbiol. 144, 324–333 (1986).

    Article  CAS  Google Scholar 

  24. Ravot, G. et al. Thiosulfate reduction, an important physiological feature shared by members of the order Thermotogales. Appl. Environ. Microbiol. 61, 2053–2055 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Childers, S., Vargas, M. & Noll, K. M. Improved methods for cultivation of the extremely thermophilic bacterium Thermotoga neapolitana. Appl. Environ. Microbiol. 58, 3949–3953 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Lovley, D. R. & Phillips, E. J. P. Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Appl. Environ. Microbiol. 51, 683–689 (1986).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Hobbie, J. E., Daley, R. J. & Jasper, S. Use of Nuclepore filters for counting bacteria by fluorescence microscopy. Appl. Environ. Microbiol. 33, 1225–1228 (1977).

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by a grant from the LExEN program of the NSF.

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Correspondence to Derek R. Lovley.

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Vargas, M., Kashefi, K., Blunt-Harris, E. et al. Microbiological evidence for Fe(III) reduction on early Earth. Nature 395, 65–67 (1998). https://doi.org/10.1038/25720

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