Oceanic nickel depletion and a methanogen famine before the Great Oxidation Event

Abstract

It has been suggested that a decrease in atmospheric methane levels triggered the progressive rise of atmospheric oxygen, the so-called Great Oxidation Event, about 2.4 Gyr ago1. Oxidative weathering of terrestrial sulphides, increased oceanic sulphate, and the ecological success of sulphate-reducing microorganisms over methanogens has been proposed as a possible cause for the methane collapse1, but this explanation is difficult to reconcile with the rock record2,3. Banded iron formations preserve a history of Precambrian oceanic elemental abundance and can provide insights into our understanding of early microbial life and its influence on the evolution of the Earth system4,5. Here we report a decline in the molar nickel to iron ratio recorded in banded iron formations about 2.7 Gyr ago, which we attribute to a reduced flux of nickel to the oceans, a consequence of cooling upper-mantle temperatures and decreased eruption of nickel-rich ultramafic rocks at the time. We measured nickel partition coefficients between simulated Precambrian sea water and diverse iron hydroxides, and subsequently determined that dissolved nickel concentrations may have reached 400 nM throughout much of the Archaean eon, but dropped below 200 nM by 2.5 Gyr ago and to modern day values6 (9 nM) by 550 Myr ago. Nickel is a key metal cofactor in several enzymes of methanogens7 and we propose that its decline would have stifled their activity in the ancient oceans and disrupted the supply of biogenic methane. A decline in biogenic methane production therefore could have occurred before increasing environmental oxygenation and not necessarily be related to it. The enzymatic reliance of methanogens on a diminishing supply of volcanic nickel links mantle evolution to the redox state of the atmosphere.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Ni/Fe mole ratios for BIF versus age, and properties of parental komatiite liquids.
Figure 2: Experimentally determined distribution coefficients for dissolved Ni.
Figure 3: Maximum dissolved Ni concentrations in sea water through time.

References

  1. 1

    Zahnle, K. J., Claire, M. W. & Catling, D. C. The loss of mass-independent fractionation of sulfur due to a Paleoproterozoic collapse of atmospheric methane. Geobiology 4, 271–283 (2006)

  2. 2

    Papineau, D., Mojzsis, S. J. & Schmitt, A. K. Multiple sulfur isotopes from Paleoproterozoic Huronian interglacial sediments and the rise of atmospheric oxygen. Earth Planet. Sci. Lett. 255, 188–212 (2007)

  3. 3

    Scott, C. et al. Tracing the stepwise oxygenation of the Proterozoic ocean. Nature 452, 456–459 (2008)

  4. 4

    Bjerrum, C. J. & Canfield, D. E. Ocean productivity before about 1.9 Gyr limited by phosphorus adsorption onto iron oxides. Nature 417, 159–162 (2002)

  5. 5

    Konhauser, K. O., Lalonde, S. V., Amskold, L. & Holland, H. D. Was there really an Archean phosphate crisis? Science 315, 1234 (2007)

  6. 6

    Drever, J. I. The Geochemistry of Natural Waters 2nd edn (Prentice Hall, 1988)

  7. 7

    Jaun, B. & Thauer, R. K. in Metal Ions in Life Sciences Vol. 2, Nickel and its Surprising Impact in Nature (eds Sigel, A., Sigel, H. & Sigel, R. K. O.) 323–356 (Wiley & Sons, 2007)

  8. 8

    Saito, M. A., Sigman, D. M. & Morel, F. M. M. The bioinorganic chemistry of the ancient ocean: the co-evolution of cyanobacterial metal requirements and biogeochemical cycles at the Archean-Proterozoic boundary? Inorg. Chim. Acta 356, 308–318 (2003)

  9. 9

    Öztürk, M. Trends of trace metal (Mn, Fe, Co, Ni, Cu, Zn, Cd and Pb) distributions at the oxic-anoxic interface and in sulfidic water of the Drammensfjord. Mar. Chem. 48, 329–342 (1995)

  10. 10

    Hannington, M. D., Santaguida, F., Kjarsgaard, I. M. & Cathles, L. M. Regional-scale hydrothermal alteration in the Central Blake River Group, western Abitibi subprovince, Canada: implications for VMS prospectivity. Mineralium Deposita 38, 393–422 (2003)

  11. 11

    Keays, R. R. The role of komatiitic and picritic magmatism and S-saturation in the formation of ore deposits. Lithos 34, 1–18 (1995)

  12. 12

    Trendall, A. F. in Precambrian Sedimentary Environments: A Modern Approach to Ancient Depositional Systems (eds Altermann, W. & Corcoran, P. L.) 33–66 (Special Publication 33, International Association of Sedimentologists, 2002)

  13. 13

    Berry, A. J., Danyushevsky, L. V., O’Neill, H. C., Newville, M. & Sutton, S. R. Oxidation state of iron in komatiite melt inclusions indicates hot Archaean mantle. Nature 455, 960–963 (2008)

  14. 14

    Barley, M. E., Krapež, B., Groves, D. I. & Kerrich, R. The Late Archaean bonanza: metallogenic and environmental consequences of the interaction between mantle plumes, lithospheric tectonics and global cyclicity. Precambr. Res. 91, 65–90 (1998)

  15. 15

    Kamber, B. S., Whitehouse, M. J., Bolhar, R. & Moorbath, S. Volcanic resurfacing and the early terrestrial crust: zircon U-Pb and REE constraints from the Isua Greenstone Belt, southern West Greenland. Earth Planet. Sci. Lett. 240, 276–290 (2005)

  16. 16

    Arndt, N. T. High Ni in Archean tholeiites. Tectonophysics 187, 411–420 (1991)

  17. 17

    Barley, M. E., Bekker, A. & Krapež, B. Late Archean to early Paleoproterozoic global tectonics, environmental change and the rise of atmospheric oxygen. Earth Planet. Sci. Lett. 238, 156–171 (2005)

  18. 18

    Nisbet, E. G. in Komatiites (eds Arndt, N.T. & Nisbet, E.G.) 501–520 (George Allen and Unwin, 1982)

  19. 19

    Arndt, N. T., Barnes, S. J. & Lesher, C. M. Komatiite (Cambridge University Press, 2008)

  20. 20

    da Silva, J. J. R. F. & Williams, R. J. P. The Biological Chemistry of the Elements: The Inorganic Chemistry of Life (Oxford University Press, 1991)

  21. 21

    Jarrell, K. F., Colvin, J. R. & Sprott, G. D. Spontaneous protoplast formation in Methanobacterium bryantii . J. Bacteriol. 149, 346–353 (1982)

  22. 22

    Diekert, G., Weber, B. & Thauer, R. K. Nickel dependence of factor F430 content in Methanobacterium thermoautotrophicum . Arch. Microbiol. 127, 273–278 (1980)

  23. 23

    Schönheit, P., Moll, J. & Thauer, R. K. Nickel, cobalt, and molybdenum requirement for growth of Methanobacterium thermoautotrophicum . Arch. Microbiol. 123, 105–107 (1979)

  24. 24

    Kida, K. et al. Influence of Ni2+ and Co2+ on methanogenic activity and the amounts of coenzymes involved in methanogenesis. J. Biosci. Bioeng. 91, 590–595 (2001)

  25. 25

    Basiliko, N. & Yavitt, J. B. Influence of Ni, Co, Fe, and Na additions on methane production in Sphagnum-dominated Northern American peatland. Biogeochemistry 52, 133–153 (2001)

  26. 26

    Shima, S. & Thauer, R. K. A third type of hydrogenase catalysing H2 activation. Chem. Rec. 7, 37–46 (2007)

  27. 27

    Hausrath, E. M., Liermann, L. J., House, C. H., Ferry, J. G. & Brantley, S. L. The effect of methanogen growth on mineral substrates: will Ni markers of methanogen-based communities be detectable in the rock record? Geobiology 5, 49–61 (2007)

  28. 28

    Saito, M. A., Moffett, J. W. & DiTullio, G. R. Cobalt and nickel in the Peru upwelling region: a major flux of labile cobalt utilized as a micronutrient. Glob. Biogeochem. Cycles 18, GB4030 (2004)

  29. 29

    Kump, L. R. & Barley, M. E. Increased subaerial volcanism and the rise of atmospheric oxygen 2.5 billion years ago. Nature 448, 1033–1036 (2007)

  30. 30

    Kharecha, P., Kasting, J. & Siefert, J. A coupled atmosphere-ecosystem model of the early Archean Earth. Geobiology 3, 53–76 (2005)

  31. 31

    Krüger, M. et al. A conspicuous nickel protein in microbial mats that oxidize methane anaerobically. Nature 426, 878–881 (2003)

  32. 32

    Catling, D. C., Claire, M. W. & Zahnle, K. J. Anaerobic methanotrophy and the rise of atmospheric oxygen. Phil. Trans. R. Soc. A 365, 1867–1888 (2007)

  33. 33

    McLennan, S. M., Taylor, S. R. & Eriksson, K. A. Geochemistry of Archean shales from Pilbara Supergroup, Western Australia. Geochim. Cosmochim. Acta 47, 1211–1222 (1983)

  34. 34

    Taylor, S. R. & McLennan, S. M. The Continental Crust: Its Composition and Evolution (Blackwell, 1985)

  35. 35

    Condie, K. C. Chemical composition and evolution of the upper continental crust: contrasting results from surface samples and shales. J. Chem. Geol. 104, 1–37 (1993)

  36. 36

    Chester, R. Marine Geochemistry (Blackwell, 2000)

  37. 37

    McLennan, S. M. in Geochemistry and Mineralogy of Rare Earth Elements (eds Lipin, B. R. & McKay, G. A.) 169–200 (Mineral Society of America, 1989)

  38. 38

    Kamber, B. S. & Webb, G. E. The geochemistry of late Archaean microbial carbonate: implications for ocean chemistry and continental erosion history. Geochim. Cosmochim. Acta 65, 2509–2525 (2001)

  39. 39

    Maliva, R. G., Knoll, A. H. & Simonson, B. M. Secular change in the Precambrian silica cycle: insights from chert petrology. Geol. Soc. Am. Bull. 117, 835–845 (2005)

  40. 40

    Tréguer, P. et al. The silica balance in the world ocean: a reestimate. Science 268, 375–379 (1995)

Download references

Acknowledgements

We thank M. Labbe for sample preparation, G. Chen and A. Simonetti for assistance with LA-ICP-MS analyses in the Radiogenic Isotope Facility at the University of Alberta, and S. Matveev for assistance with electron microprobe analyses. Field assistance by W. Mueller is acknowledged for Hunter Mine Group samples. Samples from the Loch Maree Group were provided by A. Wright. Funding was provided by the Natural Science and Engineering Research Council of Canada (NSERC) to K.O.K., the Canada Research Chairs Program to B.S.K., the Australian Research Council (ARC) to M.E.B., and NASA Exobiology and Evolutionary Biology Program individually to D.P. and K.Z. This manuscript was improved by discussions with R. Buick, J. Kasting and M. Lesher, and reviews by R. Frei and M. Saito.

Author Contributions BIF samples were provided by K.O.K., E.P., B.S.K. and D.P. E.P. performed LA-ICP-MS and electron microprobe analysis and S.V.L. conducted sorption experiments. K.O.K., S.V.L., E.P. and B.S.K. produced the manuscript with significant contributions from all co-authors. Specifically, insights into komatiites were provided by E.G.N., N.T.A. and M.E.B.; early Earth tectonics by M.E.B. and B.S.K.; and GOE and methanogens by D.P. and K.Z.

Author information

Correspondence to Kurt O. Konhauser.

Supplementary information

Supplementary Information

This file contains Supplementary Figures S1-S5 with Legends, Supplementary Tables S1-S3, a Supplementary Discussion and Supplementary References. (PDF 2070 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Konhauser, K., Pecoits, E., Lalonde, S. et al. Oceanic nickel depletion and a methanogen famine before the Great Oxidation Event. Nature 458, 750–753 (2009). https://doi.org/10.1038/nature07858

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.