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Evidence for arsenic metabolism and cycling by microorganisms 2.7 billion years ago

Nature Geoscience volume 7, pages 811–815 (2014)Cite this article

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Abstract

The ability of microbes to metabolize arsenic may have emerged more than 3.4 billion years ago1,2. Some of the modern environments in which prominent arsenic metabolism occurs are anoxic3,4, as were the Precambrian oceans. Early oceans may also have had a relatively high abundance of arsenic5. However, it is unclear whether arsenic cycling occurred in ancient environments. Here we assess the chemistry and nature of cell-like globules identified in salt-encrusted portions of 2.72-billion-year-old fossil stromatolites from Western Australia. We use Raman spectroscopy and X-ray fluorescence to show that the globules are composed of organic carbon and arsenic (As). We argue that our data are best explained by the occurrence of a complete arsenic cycle at this site, with As(III) oxidation and As(V) reduction by microbes living in permanently anoxic conditions. We therefore suggest that arsenic cycling could have occurred more widely in marine environments in the several hundred million years before the Earth’s atmosphere and shallow oceans were oxygenated.

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Figure 1: Imaging of the 2.72-Gyr-old Tumbiana stromatolite.
Figure 2: Imaging of Tumbiana stromatolite.
Figure 3: Metal distribution patterns in the Tumbiana stromatolite.
Figure 4: As-rich organic globules.

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References

  1. Lebrun, E. et al. Arsenite oxidase, an ancient bioenergetic enzyme. Mol. Biol. Evol. 20, 686–693 (2003).

    Article  Google Scholar 

  2. Duval, S., Ducluzeau, A-L., Nitschke, W. & Schoepp-Cothenet, B. Enzyme phylogenies as markers for the oxidation state of the environment: The case of respiratory arsenate reductase and related enzymes. BMC Evol. Biol. 8, 206–219 (2008).

    Article  Google Scholar 

  3. Kulp, T. R. et al. Arsenic (III) fuels anoxygenic photosynthesis in hot springs biofilms from Mono Lake, California. Science 321, 967–970 (2008).

    Article  Google Scholar 

  4. Oremland, R. S. et al. Anaerobic oxidation of arsenite in Mono Lake water and by a facultative, arsenite-oxidizing chemoautotroph, strain MLHE-1. Appl. Environ. Microbiol. 68, 4795–4802 (2002).

    Article  Google Scholar 

  5. Bergman, I. A. & Kolesov, G. M. Arsenic, antimony, and bismuth as indicators of the genesis of ore material in Early Precambrian ferrous quartzite formations. Geochem. Int. 50, 816–831 (2012).

    Article  Google Scholar 

  6. Philippot, P. et al. Early traces of life investigations in drilling Archean hydrothermal and sedimentary rocks of the Pilbara Craton, Western Australia and Barberton Greenstone Belt, South Africa. C. R. Palevol 8, 649–663 (2009).

    Article  Google Scholar 

  7. Lepot, K., Benzerara, K., Brown, G. E. Jr & Philippot, P. Microbially influenced formation of 2.724-million-year-old stromatolites. Nature Geosci. 11, 18–121 (2008).

    Google Scholar 

  8. Lepot, K. et al. Organic matter heterogeneities in 2.72 Ga stromatolites: Alteration versus preservation by sulfur incorporation. Geochim. Cosmochim. Acta 73, 6579–6599 (2009).

    Article  Google Scholar 

  9. Buick, R. The antiquity of oxygenic photosynthesis: Evidence from stromatolites in sulphate-deficient Archaean lakes. Science 255, 74–77 (1992).

    Article  Google Scholar 

  10. Bolhar, R. & Van Kranendonk, M. J. A non-marine depositional setting for the northern Fortescue Group, Pilbara Craton, inferred from trace element geochemistry of stromatolitic carbonates. Precambr. Res. 155, 229–250 (2007).

    Article  Google Scholar 

  11. Stolz, J. F., Basu, P., Santini, J. M. & Oremland, R. S. Arsenic and selenium in microbial metabolism. Annu. Rev. Microbiol. 60, 107–130 (2006).

    Article  Google Scholar 

  12. Braissant, O. et al. Exopolymeric substances of sulfate-reducing bacteria: Interactions with calcium at alkaline pH and implication for formation of carbonate minerals. Geobiology 5, 401–411 (2007).

    Article  Google Scholar 

  13. Buick, R. When did oxygenic photosynthesis evolve? Phil. Trans. R. Soc. Lond. 363, 2731–2743 (2008).

    Article  Google Scholar 

  14. Hayes, J. M. in Early Life on Earth (ed Bengston, S.) 220–236 (Columbia Univ. Press, 1994).

    Google Scholar 

  15. Eigenbrode, J. L. & Freeman, K. H. Late Archean rise of aerobic microbial ecosystems. Proc. Natl Acad. Sci. USA 103, 15759–15764 (2006).

    Article  Google Scholar 

  16. Hinrichs, K. U. Microbial fixation of methane carbon at 2.7 Ga: Was an anaerobic mechanism possible? Geochem. Geophys. Geosyst. 3, 1–10 (2002).

    Article  Google Scholar 

  17. Thomazo, C., Ader, M., Farquhar, J. & Philippot, P. Methanotrophs regulated atmospheric sulfur isotope anomalies during the Mesoarchean (Tumbiana Formation, Western Australia). Earth Planet. Sci. Lett. 279, 65–75 (2009).

    Article  Google Scholar 

  18. Thomazo, C., Ader, M. & Philippot, P. Extreme 15N-enrichments in 2.72-Gyr-old sediments: Evidence for a turning point in the nitrogen cycle. Geobiology 9, 107–120 (2011).

    Article  Google Scholar 

  19. Griffin, B. M., Schott, J. & Schink, B. Nitrite, an electron donor for anoxygenic photosynthesis. Science 316, 1870 (2007).

    Article  Google Scholar 

  20. Schoepp-Cothenet, B. et al. Menaquinone as pool quinone in a purple bacterium. Proc. Natl Acad. Sci. USA 106, 8549–8554 (2009).

    Article  Google Scholar 

  21. Oremland, R. S., Saltikov, C. W., Wolfe-Simon, F. & Stolz, J. F. Arsenic in the evolution of Earth and extraterrestrial ecosystems. Geomicrobiol. J. 26, 522–536 (2009).

    Article  Google Scholar 

  22. Oremland, R. S., Stolz, J. F. & Hollibaugh, J. T. The microbial arsenic cycle in Mono Lake, California. FEMS Microbiol. Ecol. 48, 15–27 (2004).

    Article  Google Scholar 

  23. Hoeft, S. E., Kulp, T. R., Han, S., Lanoil, B. & Oremland, R. S. Coupled arsenotrophy in a hot spring photosynthetic biofilm at Mono Lake, California. Appl. Environ. Microbiol. 76, 4633–4639 (2010).

    Article  Google Scholar 

  24. Van Lis, R., Nitschke, W., Duval, S. & Schoepp-Cothenet, B. Arsenics as bioenergetic substrates. Biochim. Biophys. Acta 1827, 176–188 (2013).

    Article  Google Scholar 

  25. Oremland, R. S. et al. A microbial arsenic cycle in a salt-saturated, extreme environment. Science 308, 1305–1308 (2005).

    Article  Google Scholar 

  26. Miller, L. G., Jellison, R., Oremland, R. S. & Culbertson, C. W. Meromixis in hypersaline Mono Lake, California. 3. Biogeochemical response to stratification and overturn. Limnol. Oceanogr. 38, 1040–1051 (1993).

    Article  Google Scholar 

  27. Farías, M. E. et al. The discovery of stromatolites developing at 3570 m above sea level in a high-altitude volcanic lake Socompa, Argentinean Andes. PLoS ONE 8, e53497 (2013).

    Article  Google Scholar 

  28. Lara, J. et al. Enrichment of arsenic transforming and resistant heterotrophic bacteria from sediments of two salt lakes in Northern Chile. Extremophiles 16, 523–538 (2012).

    Article  Google Scholar 

Download references

Acknowledgements

The authors are grateful to D. Paterson, M. De Jonge (AS), C. Ryan (CSIRO), D. Grolimund, C. Borca (SLS) and F. Segura-Ruiz (ESRF) for their help during SR-XRF experiments. We thank the Institut de Physique du Globe de Paris and the Geological Survey of Western Australia for supporting the PDP. This work was supported by a grant from the Agence Nationale de la Recherche project ‘eLIFE2’ to P.P. and the UnivEarths Labex programme at Sorbonne Paris Cité (ANR-10-LABX-0023 and ANR-11-IDEX-0005-02). This is IPGP contribution number 3559.

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Authors and Affiliations

  1. Géobiosphère Actuelle & Primitive, Institut de Physique du Globe de Paris, Sorbonne Paris Cité, Université Paris Diderot, CNRS, 75238 Paris, France

    Marie Catherine Sforna, Pascal Philippot & Mark A. van Zuilen

  2. Synchrotron Soleil, BP 48, Saint-Aubin, 91192 Gif-sur-Yvette, France

    Andrea Somogyi & Kadda Medjoubi

  3. Laboratoire de Bioénergétique et Ingénierie des Protéines UMR 7281 CNRS/AMU, FR3479, F-13402 Marseille Cedex 20, France

    Barbara Schoepp-Cothenet & Wolfgang Nitschke

  4. Department of Marine Sciences, University of Connecticut, Groton, Connecticut 06340, USA

    Pieter T. Visscher

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  1. Marie Catherine Sforna
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Contributions

M.C.S., A.S., P.P., M.A.v.Z. and K.M. carried out the synchrotron and Raman experiments and treated the data. P.P., M.C.S. and A.S. wrote the paper with input from all authors.

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Correspondence to Marie Catherine Sforna or Pascal Philippot.

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Sforna, M., Philippot, P., Somogyi, A. et al. Evidence for arsenic metabolism and cycling by microorganisms 2.7 billion years ago. Nature Geosci 7, 811–815 (2014). https://doi.org/10.1038/ngeo2276

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