Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Microbial life and biogeochemical cycling on land 3,220 million years ago

An Author Correction to this article was published on 08 October 2018

This article has been updated

Abstract

The colonization of emergent continental landmass by microbial life was an evolutionary step of paramount importance in Earth history. Here we report direct fossil evidence for life on land 3,220 million years ago (Ma) in the form of terrestrial microbial mats draping fluvial conglomerates and gravelly sandstones of the Moodies Group, South Africa. Combined field, petrographic, carbon isotope and Raman spectroscopic analyses confirm the synsedimentary origin and biogenicity of these unique fossil mats as well as their fluvial habitat. The carbon isotope compositions of organic matter (δ13Corg) from these mats define a narrow range centred on −21‰, in contrast to fossil mats of marine origin from nearby tidal deposits that show δ13Corg values as low as −34‰. Bulk nitrogen isotope compositions (2 < δ15N < 5‰) are also significantly different from their marine counterparts (0 < δ15N < 3‰), which we interpret as reflecting denitrification in the terrestrial habitat, possibly of an atmospheric source of nitrate. Our results support the antiquity of a thriving terrestrial biosphere during the Palaeoarchaean and suggest that a complex and microbially driven redox landscape existed during the deposition of the Moodies Group, with distinct biogeochemical cycling occurring on land by 3,220 Ma.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Field photographs of fluvial sandstones and conglomerates hosting fossil terrestrial mats from the 3,220-Myr-old Moodies Group.
Fig. 2: Reflected and transmitted light photomicrographs of the terrestrial microbial mats of the Moodies Group.
Fig. 3: Images of the kerogenous laminae and filamentous microstructures.
Fig. 4: Carbon isotope composition of organic matter and bulk nitrogen isotope composition from terrestrial and marine microbial mats of the Palaeoarchaean Moodies Group.

Similar content being viewed by others

Change history

  • 08 October 2018

    In the version of this Article originally published, author Magali Ader was wrongly linked to affiliation 3; it should have been affiliation 2. This error has now been corrected in the online versions.

References

  1. Nutman, A. P., Bennett, V. C., Friend, C. R. L., Van Kranendonk, M. J. & Chivas, A. R. Rapid emergence of life shown by discovery of 3,700-million-year-old microbial structures. Nature 537, 535–538 (2016).

    Article  Google Scholar 

  2. Allwood, A. C., Walter, M. R., Kamber, B. S., Marshall, C. P. & Burch, I. W. Stromatolite reef from the Early Archaean era of Australia. Nature 441, 714–718 (2006).

    Article  Google Scholar 

  3. Tice, M. M. & Lowe, D. R. Photosynthetic microbial mats in the 3,416-Myr-old ocean. Nature 431, 549–552 (2004).

    Article  Google Scholar 

  4. Wacey, D., Kilburn, M. R., Saunders, M., Cliff, J. & Brasier, M. D. Microfossils of sulphur-metabolizing cells in 3.4-billion-year-old rocks of Western Australia. Nat. Geosci. 4, 698–702 (2011).

    Article  Google Scholar 

  5. Dodd, M. S. et al. Evidence for early life in Earth’s oldest hydrothermal vent precipitates. Nature 543, 60–64 (2017).

    Article  Google Scholar 

  6. Flament, N., Coltice, N. & Rey, P. F. The evolution of the 87Sr/86Sr of marine carbonates does not constrain continental growth. Precambrian Res. 229, 177–188 (2013).

    Article  Google Scholar 

  7. Beraldi-Campesi, H. Early life on land and the first terrestrial ecosystems. Ecol. Process. 2, 1 (2013).

    Article  Google Scholar 

  8. Wellman, C. H. & Strother, P. K. The terrestrial biota prior to the origin of land plants (embryophytes): a review of the evidence. Palaeontology 58, 601–627 (2015).

    Article  Google Scholar 

  9. Watanabe, Y., Martini, J. E. & Ohmoto, H. Geochemical evidence for terrestrial ecosystems 2.6 billion years ago. Nature 408, 574–578 (2000).

    Article  Google Scholar 

  10. Rye, R. & Holland, H. D. Life associated with a 2.76 Ga ephemeral pond? Evidence from Mount Roe #2 paleosol. Geology 28, 483–486 (2000).

    Article  Google Scholar 

  11. Crowe, S. A. et al. Atmospheric oxygenation three billion years ago. Nature 501, 535–538 (2013).

    Article  Google Scholar 

  12. Mukhopadhyay, J. et al. Oxygenation of the Archean atmosphere: new paleosol constraints from eastern India. Geology 42, 923–926 (2014).

    Article  Google Scholar 

  13. Nabhan, S., Wiedenbeck, M., Milke, R. & Heubeck, C. Biogenic overgrowth on detrital pyrite in ca. 3.2 Ga Archean paleosols. Geology 44, 763–766 (2016).

    Article  Google Scholar 

  14. Djokic, T., Van Kranendonk, M. J., Campbell, K. A., Walter, M. R. & Ward, C. R. Earliest signs of life on land preserved in ca. 3.5 Ga hot spring deposits. Nat. Commun. 8, 15263 (2017).

    Article  Google Scholar 

  15. Javaux, E. J., Marshall, C. P. & Bekker, A. Organic-walled microfossils in 3.2-billion-year-old shallow-marine siliciclastic deposits. Nature 463, 934–938 (2010).

    Article  Google Scholar 

  16. Noffke, N., Eriksson, K. A., Hazen, R. M. & Simpson, E. L. A new window into Early Archean life: microbial mats in Earth’s oldest siliciclastic tidal deposits (3.2 Ga Moodies Group, South Africa). Geology 34, 253 (2006).

    Article  Google Scholar 

  17. Heubeck, C. An early ecosystem of Archean tidal microbial mats (Moodies Group, South Africa, ca. 3.2 Ga). Geology 37, 931–934 (2009).

    Article  Google Scholar 

  18. Homann, M., Heubeck, C., Airo, A. & Tice, M. M. Morphological adaptations of 3.22 Ga-old tufted microbial mats to Archean coastal habitats (Moodies Group, Barberton Greenstone Belt, South Africa). Precambrian Res. 266, 47–64 (2015).

    Article  Google Scholar 

  19. Homann, M. et al. Evidence for cavity-dwelling microbial life in 3.22 Ga tidal deposits. Geology 44, 51–54 (2016).

    Article  Google Scholar 

  20. Eriksson, K. A., Simpson, E. L. & Mueller, W. U. An unusual fluvial to tidal transition in the mesoarchean Moodies Group, South Africa: a response to high tidal range and active tectonics. Sediment. Geol. 190, 13–24 (2006).

    Article  Google Scholar 

  21. Heubeck, C. et al. Geological constraints on Archean (3.22 Ga) coastal-zone processes from the Dycedale Syncline, Barberton Greenstone Belt. South Afr. J. Geol. 119, 495–518 (2016).

    Article  Google Scholar 

  22. De Ronde, C. E. J. & Kamo, S. L. An Archaean arc–arc collisional event: a short-lived (ca 3 Myr) episode, Weltevreden area, Barberton greenstone belt, South Africa. J. Afr. Earth Sci. 30, 219–248 (2000).

    Article  Google Scholar 

  23. Heubeck, C. et al. Timing of deposition and deformation of the Moodies Group (Barberton Greenstone Belt, South Africa): very-high-resolution of Archaean surface processes. Precambrian Res. 231, 236–262 (2013).

    Article  Google Scholar 

  24. Farber, K., Dziggel, A., Trumbull, R. B., Meyer, F. M. & Wiedenbeck, M. Tourmaline B-isotopes as tracers of fluid sources in silicified Palaeoarchaean oceanic crust of the Mendon Formation, Barberton greenstone belt, South Africa. Chem. Geol. 417, 134–147 (2015).

    Article  Google Scholar 

  25. Xie, X., Byerly, G. R. & Ferrell, R. E. Jr. IIb trioctahedral chlorite from the Barberton greenstone belt: crystal structure and rock composition constraints with implications to geothermometry. Contrib. Mineral. Petrol. 126, 275–291 (1997).

    Article  Google Scholar 

  26. Tice, M. M., Bostick, B. C. & Lowe, D. R. Thermal history of the 3.5–3.2 Ga Onverwacht and Fig Tree Groups, Barberton greenstone belt, South Africa, inferred by Raman microspectroscopy of carbonaceous material. Geology 32, 37 (2004).

    Article  Google Scholar 

  27. Popp, B. N. et al. Effect of phytoplankton cell geometry on carbon isotopic fractionation. Geochim. Cosmochim. Acta 62, 69–77 (1998).

    Article  Google Scholar 

  28. Hayes, J. M., Strauss, H. & Kaufman, A. J. The abundance of in marine organic matter and isotopic fractionation in the global biogeochemical cycle of carbon during the past 800 Ma. Chem. Geol. 161, 103–125 (1999).

    Article  Google Scholar 

  29. Driese, S. G. et al. Neoarchean paleoweathering of tonalite and metabasalt: Implications for reconstructions of 2.69 Ga early terrestrial ecosystems and paleoatmospheric chemistry. Precambrian Res. 189, 1–17 (2011).

    Article  Google Scholar 

  30. Laws, E. A., Popp, B. N., Cassas, N. & Tanimoto, J. 13C discrimination patterns in oceanic phytoplankton: likely influence of CO2 concentrating mechanisms, and implications for palaeoreconstructions. Funct. Plant Biol. 29, 323–333 (2002).

    Article  Google Scholar 

  31. Schidlowski, M. A 3,800-million-year isotopic record of life from carbon in sedimentary rocks. Nature 333, 313–318 (1988).

    Article  Google Scholar 

  32. 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 

  33. Stüeken, E. E. & Buick, R. Environmental control on microbial diversification and methane production in the Mesoarchean. Precambrian Res. 304, 64–72 (2018).

    Article  Google Scholar 

  34. Slotznick, S. P. & Fischer, W. W. Examining Archean methanotrophy. Earth Planet. Sci. Lett. 441, 52–59 (2016).

    Article  Google Scholar 

  35. Havig, J. R., Hamilton, T. L., Bachan, A. & Kump, L. R. Sulfur and carbon isotopic evidence for metabolic pathway evolution and a four-stepped Earth system progression across the Archean and Paleoproterozoic. Earth Sci. Rev. 174, 1–21 (2017).

    Article  Google Scholar 

  36. Baumgartner, L. K. et al. Sulfate reducing bacteria in microbial mats: changing paradigms, new discoveries. Sediment. Geol. 185, 131–145 (2006).

    Article  Google Scholar 

  37. Hoehler, T. M., Bebout, B. M. & Des Marais, D. J. The role of microbial mats in the production of reduced gases on the early Earth. Nature 412, 324–327 (2001).

    Article  Google Scholar 

  38. Lovley, D. R. & Klug, M. J. Sulfate reducers can outcompete methanogens at freshwater sulfate concentrations. Appl. Environ. Microbiol. 45, 187–192 (1983).

    Google Scholar 

  39. Nabhan, S., Luber, T., Scheffler, F. & Heubeck, C. Climatic and geochemical implications of Archean pedogenic gypsum in the Moodies Group (<3.2 Ga), Barberton Greenstone Belt, South Africa. Precambrian Res. 275, 119–134 (2016).

    Article  Google Scholar 

  40. Tice, M. M. & Lowe, D. R. Hydrogen-based carbon fixation in the earliest known photosynthetic organisms. Geology 34, 37 (2006).

    Article  Google Scholar 

  41. Bandyopadhyay, A., Stöckel, J., Min, H., Sherman, L. A. & Pakrasi, H. B. High rates of photobiological H2 production by a cyanobacterium under aerobic conditions. Nat. Commun. 1, 139 (2010).

    Article  Google Scholar 

  42. Ader, M. et al. Interpretation of the nitrogen isotopic composition of Precambrian sedimentary rocks: assumptions and perspectives. Chem. Geol. 429, 93–110 (2016).

    Article  Google Scholar 

  43. Ader, M. et al. Nitrogen isotopic evolution of carbonaceous matter during metamorphism: methodology and preliminary results. Chem. Geol. 232, 152–169 (2006).

    Article  Google Scholar 

  44. Stüeken, E. E. A test of the nitrogen-limitation hypothesis for retarded eukaryote radiation: nitrogen isotopes across a Mesoproterozoic basinal profile. Geochim. Cosmochim. Acta 120, 121–139 (2013).

    Article  Google Scholar 

  45. Papineau, D. et al. High primary productivity and nitrogen cycling after the Paleoproterozoic phosphogenic event in the Aravalli Supergroup, India. Precambrian Res. 171, 37–56 (2009).

    Article  Google Scholar 

  46. Kasting, J. F. & Walker, J. C. G. Limits on oxygen concentration in the prebiological atmosphere and the rate of abiotic fixation of nitrogen. J. Geophys. Res. 86, 1147 (1981).

    Article  Google Scholar 

  47. Navarro-gonz, R., Molina, M. J. & Molina, L. T. Nitrogen fixation by volcanic lightning in the early Earth. Geophys. Res. Lett. 25, 3123–3126 (1998).

    Article  Google Scholar 

  48. Stüeken, E. E., Kipp, M. A., Koehler, M. C. & Buick, R. The evolution of Earth’s biogeochemical nitrogen cycle. Earth Sci. Rev. 160, 220–239 (2016).

    Article  Google Scholar 

  49. Joye, S. B. & Paerl, H. W. Nitrogen cycling in microbial mats—rates and patterns of denitrification and nitrogen-fixation. Mar. Biol. 119, 285–295 (1994).

    Article  Google Scholar 

  50. Sforna, M. C., van Zuilen, M. A. & Philippot, P. Structural characterization by Raman hyperspectral mapping of organic carbon in the 3.46 billion-year-old Apex chert, Western Australia. Geochim. Cosmochim. Acta 124, 18–33 (2014).

    Article  Google Scholar 

  51. Beyssac, O., Goffé, B., Chopin, C. & Rouzaud, J. N. Raman spectra of carbonaceous material in metasediments: a new geothermometer. J. Metamorph. Geol. 20, 859–871 (2002).

    Article  Google Scholar 

  52. Kouketsu, Y. et al. A new approach to develop the Raman carbonaceous material geothermometer for low-grade metamorphism using peak width. Isl. Arc 23, 33–50 (2014).

    Article  Google Scholar 

  53. Stüeken, E. E., Zaloumis, J., Meixnerová, J. & Buick, R. Differential metamorphic effects on nitrogen isotopes in kerogen extracts and bulk rocks. Geochim. Cosmochim. Acta 217, 80–94 (2017).

    Article  Google Scholar 

  54. Ader, M., Boudou, J.-P., Javoy, M., Goffe, B. & Daniels, E. Isotope study on organic nitrogen of Westphalian anthracites from the Western Middle field of Pennsylvania (U.S.A.) and from the Bramsche Massif (Germany). Org. Geochem. 29, 315–323 (1998).

    Article  Google Scholar 

  55. Li, L., Cartigny, P. & Ader, M. Kinetic nitrogen isotope fractionation associated with thermal decomposition of NH3: experimental results and potential applications to trace the origin of N2 in natural gas and hydrothermal systems. Geochim. Cosmochim. Acta 73, 6282–6297 (2009).

    Article  Google Scholar 

Download references

Acknowledgements

This work was greatly supported by LabexMER ANR-10-LABX-19 and Prestige COFUND-GA-2013-609102 to M.H., and Deutsche Forschungsgemeinschaft (DFG) grant He2418/13–1 to C.H. S.V.L. and M.V.Z. acknowledge support from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement n° 716515 for S.V.L. and grant agreement n° 646894 for M.V.Z.). We thank N. and D. Oosthuizen for access to the private Mountainlands nature reserve, S. Bläsing and M. Grund for assistance with sample collection, J.-P. Oldra for thin section preparation, and O. Lebeau, C. Tanvet, C. Liorzou, M.-L. Rouget and B. Gueguen for assistance with isotopic and elemental analysis.

Author information

Authors and Affiliations

Authors

Contributions

M.H. and C.H. carried out fieldwork and collected samples in South Africa. P.S., M.A. and S.V.L. helped with the acquisition and interpretation of elemental and isotopic data. M.V.Z. and J.G. performed Raman analysis. B.K., I.S.F., A.A. and M.J.V.K. contributed to the discussion of the data. M.H. wrote the manuscript with contributions from all co-authors.

Corresponding author

Correspondence to Martin Homann.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary material.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Homann, M., Sansjofre, P., Van Zuilen, M. et al. Microbial life and biogeochemical cycling on land 3,220 million years ago. Nature Geosci 11, 665–671 (2018). https://doi.org/10.1038/s41561-018-0190-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41561-018-0190-9

This article is cited by

Search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology