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.

Early fungi from the Proterozoic era in Arctic Canada

Nature volume 570, pages 232–235 (2019)Cite this article

Subjects

An Author Correction to this article was published on 04 July 2019

This article has been updated

Abstract

Fungi are crucial components of modern ecosystems. They may have had an important role in the colonization of land by eukaryotes, and in the appearance and success of land plants and metazoans1,2,3. Nevertheless, fossils that can unambiguously be identified as fungi are absent from the fossil record until the middle of the Palaeozoic era4,5. Here we show, using morphological, ultrastructural and spectroscopic analyses, that multicellular organic-walled microfossils preserved in shale of the Grassy Bay Formation (Shaler Supergroup, Arctic Canada), which dates to approximately 1,010–890 million years ago, have a fungal affinity. These microfossils are more than half a billion years older than previously reported unambiguous occurrences of fungi, a date which is consistent with data from molecular clocks for the emergence of this clade6,7. In extending the fossil record of the fungi, this finding also pushes back the minimum date for the appearance of eukaryotic crown group Opisthokonta, which comprises metazoans, fungi and their protist relatives8,9.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

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

Fig. 1: Microphotographs of O. giraldae specimens.
Fig. 2: Spectra obtained with FTIR microspectroscopy.
Fig. 3: Simplified phylogenetic relationships of main eukaryotic supergroups.

Data availability

All processed data are included in Supplementary Tables 1 and 2. Raw data are available from the corresponding authors upon reasonable request. Microfossil specimens are accessible at the Early Life Traces and Evolution–Astrobiology Laboratory.

Change history

  • 04 July 2019

    An amendment to this paper has been published and can be accessed via a link at the top of the paper.

References

  1. Kenrick, P. & Crane, P. R. The origin and early evolution of plants on land. Nature 389, 33–39 (1997).

    Article  CAS  ADS  Google Scholar 

  2. Jeffries, P., Gianinazzi, S., Perotto, S., Turnau, K. & Barea, J. M. The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol. Fertil. Soils 37, 1–16 (2003).

    Google Scholar 

  3. Berbee, M. L., James, T. Y. & Strullu-Derrien, C. Early diverging fungi: diversity and impact at the dawn of terrestrial life. Annu. Rev. Microbiol. 71, 41–60 (2017).

    Article  CAS  Google Scholar 

  4. Taylor, T. N., Krings, M. & Taylor, E. L. Fossil Fungi (Academic, Amsterdam, 2014).

    Google Scholar 

  5. Redecker, D., Kodner, R. & Graham, L. E. Glomalean fungi from the Ordovician. Science 289, 1920–1921 (2000).

    Article  CAS  ADS  Google Scholar 

  6. Berbee, M. L. & Taylor, J. W. Dating the molecular clock in fungi–how close are we? Fungal Biol. Rev. 24, 1–16 (2010).

    Article  Google Scholar 

  7. Watkinson, S. C., Boddy, L. & Money, N. The Fungi (Academic, London, 2015).

    Google Scholar 

  8. Parfrey, L. W., Lahr, D. J., Knoll, A. H. & Katz, L. A. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc. Natl Acad. Sci. USA 108, 13624–13629 (2011).

    Article  CAS  ADS  Google Scholar 

  9. Eme, L., Sharpe, S. C., Brown, M. W. & Roger, A. J. On the age of eukaryotes: evaluating evidence from fossils and molecular clocks. Cold Spring Harb. Perspect. Biol. 6, a016139 (2014).

    Article  Google Scholar 

  10. Butterfield, N. J. Probable proterozoic fungi. Paleobiology 31, 165–182 (2005).

    Article  Google Scholar 

  11. Retallack, G. J. Ediacaran life on land. Nature 493, 89–92 (2013).

    Article  ADS  Google Scholar 

  12. Graham, L. E., Trest, M. T. & Cook, M. E. Acetolysis resistance of modern fungi: testing attributions of enigmatic Proterozoic and Early Paleozoic fossils. Int. J. Plant Sci. 178, 330–339 (2017).

    Article  Google Scholar 

  13. Marshall, C. P., Javaux, E. J., Knoll, A. H. & Walter, M. R. Combined micro-Fourier transform infrared (FTIR) spectroscopy and micro-Raman spectroscopy of Proterozoic acritarchs: a new approach to palaeobiology. Precambr. Res. 138, 208–224 (2005).

    Article  CAS  ADS  Google Scholar 

  14. Loron, C. C., Rainbird, R. H., Turner, E. C., Greenman, J. W. & Javaux, E. J. Organic-walled microfossils from the late Mesoproterozoic to early Neoproterozoic lower Shaler Supergroup (Arctic Canada): diversity and biostratigraphic significance. Precambr. Res. 321, 349–374 (2019).

    Article  CAS  ADS  Google Scholar 

  15. Rainbird, R. H., Jefferson, C. W. & Young, G. M. The early Neoproterozoic sedimentary succession B of northwestern Laurentia: correlations and paleogeographic significance. Geol. Soc. Am. Bull. 108, 454–470 (1996).

    Article  ADS  Google Scholar 

  16. Greenman, J. W. & Rainbird, R. H. Stratigraphy of the Upper Nelson Head, Aok, Grassy Bay, and Boot Inlet Formations in the Brock Inlier, Northwest Territories (NTS 97-A, D). Geological Survey of Canada Open File 8394 (Canada Geological Survey, Natural Resources Canada, 2018).

    Book  Google Scholar 

  17. van Acken, D., Thomson, D., Rainbird, R. H. & Creaser, R. A. Constraining the depositional history of the Neoproterozoic Shaler Supergroup, Amundsen Basin, NW Canada: rhenium–osmium dating of black shales from the Wynniatt and Boot Inlet Formations. Precambr. Res. 236, 124–131 (2013).

    Article  ADS  Google Scholar 

  18. Rainbird, R. H. et al. Zircon provenance data record the lateral extent of pancontinental, early Neoproterozoic rivers and erosional unroofing history of the Grenville orogen. Geol. Soc. Am. Bull. 129, 1408–1423 (2017).

    Google Scholar 

  19. Javaux, E. J., Knoll, A. H. & Walter, M. Recognizing and interpreting the fossils of early eukaryotes. Orig. Life Evol. Biosph. 33, 75–94 (2003).

    Article  CAS  ADS  Google Scholar 

  20. Baludikay, B. K. et al. Raman microspectroscopy, bitumen reflectance and illite crystallinity scale: comparison of different geothermometry methods on fossiliferous Proterozoic sedimentary basins (DR Congo, Mauritania and Australia). Int. J. Coal Geol. 191, 80–94 (2018).

    Article  CAS  Google Scholar 

  21. Mohaček-Grošev, V., Božac, R. & Puppels, G. J. Vibrational spectroscopic characterization of wild growing mushrooms and toadstools. Spectrochim. Acta A 57, 2815–2829 (2001).

    Article  ADS  Google Scholar 

  22. Kačuráková, M., Capek, P., Sasinková, V., Wellner, N. & Ebringerová, A. FT-IR study of plant cell wall model compounds: pectic polysaccharides and hemicelluloses. Carbohydr. Polym. 43, 195–203 (2000).

    Article  Google Scholar 

  23. Riquelme, M. & Sánchez-León, E. The Spitzenkörper: a choreographer of fungal growth and morphogenesis. Curr. Opin. Microbiol. 20, 27–33 (2014).

    Article  CAS  Google Scholar 

  24. Spatafora, J. W. et al. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108, 1028–1046 (2016).

    Article  CAS  Google Scholar 

  25. Webster, J. & Weber, R. Introduction to Fungi (Cambridge Univ. Press, Cambridge, 2007).

    Book  Google Scholar 

  26. Mélida, H., Sandoval-Sierra, J. V., Diéguez-Uribeondo, J. & Bulone, V. Analyses of extracellular carbohydrates in oomycetes unveil the existence of three different cell wall types. Eukaryot. Cell 12, 194–203 (2013).

    Article  Google Scholar 

  27. Richards, T. A., Leonard, G. & Wideman, J. G. What defines the “kingdom” fungi? Microbiol. Spectr. 5, FUNK-0044-2017 (2017).

    Article  Google Scholar 

  28. Wanjun, T., Cunxin, W. & Donghua, C. Kinetic studies on the pyrolysis of chitin and chitosan. Polym. Degrad. Stabil. 87, 389–394 (2005).

    Article  Google Scholar 

  29. Muzzarelli, R. A. A. in Chitin: Formation and Diagenesis (Topics in Geobiology Vol. 34) (ed. Gupta, N. S.) 1–34 (Springer Science and Business Media, New York, 2010).

  30. Taylor, J. W. & Berbee, M. L. Dating divergences in the fungal tree of life: review and new analyses. Mycologia 98, 838–849 (2006).

    Article  Google Scholar 

  31. Javaux, E. J. & Knoll, A. H. Micropaleontology of the lower Mesoproterozoic Roper Group, Australia, and implications for early eukaryotic evolution. J. Paleontol. 91, 199–229 (2017).

    Article  Google Scholar 

  32. Grey, K. A Modified Palynological Preparation Technique for the Extraction of Large Neoproterozoic Acanthomorph Acritarchs and Other Acid-Soluble Microfossils. (Geological Survey of Western Australian, Department of Minerals and Energy, Perth, 1999).

  33. 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  CAS  ADS  Google Scholar 

  34. Liu, D. H. et al. Sample maturation calculated using Raman spectroscopic parameters for solid organics: methodology and geological applications. Chin. Sci. Bull. 58, 1285–1298 (2013).

    Article  CAS  Google Scholar 

  35. Sauerer, B., Craddock, P. R., AlJohani, M. D., Alsamadony, K. L. & Abdallah, W. Fast and accurate shale maturity determination by Raman spectroscopy measurement with minimal sample preparation. Int. J. Coal Geol. 173, 150–157 (2017).

    Article  CAS  Google Scholar 

  36. Paulino, A. T., Simionato, J. I., Garcia, J. C. & Nozaki, J. Characterization of chitosan and chitin produced from silkworm crysalides. Carbohydr. Polym. 64, 98–103 (2006).

    Article  CAS  Google Scholar 

  37. Movasaghi, Z., Rehman, S. & Rehman, D. I. Fourier transform infrared (FTIR) spectroscopy of biological tissues. Appl. Spectrosc. Rev. 43, 134–179 (2008).

    Article  CAS  ADS  Google Scholar 

  38. Michell, A. J. & Scurfield, G. Composition of extracted fungal cell walls as indicated by infrared spectroscopy. Arch. Biochem. Biophys. 120, 628–637 (1967).

    Article  CAS  Google Scholar 

  39. Bahmed, K., Quilès, F., Bonaly, R. & Coulon, J. Fluorescence and infrared spectrometric study of cell walls from Candida, Kluyveromyces, Rhodotorula and Schizosaccharomyces yeasts in relation with their chemical composition. Biomacromolecules 4, 1763–1772 (2003).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the Agouron Institute, the FRS-FNRS-FWO EOS ET-Home grant 30442502 and the ERC Stg ELiTE FP7/308074. We thank M. Giraldo, M.-C. Sforna, Y. Cornet and S. Smeets (University of Liège) for technical support and the Geological Survey of Canada’s Geomapping for Energy and Minerals Program for fieldwork logistics.

Reviewer information

Nature thanks Linda Graham and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author information

Authors and Affiliations

  1. Early Life Traces & Evolution–Astrobiology Laboratory, UR Astrobiology, Geology Department, University of Liège, Liège, Belgium

    Corentin C. Loron, Camille François & Emmanuelle J. Javaux

  2. Geological Survey of Canada, Ottawa, Ontario, Canada

    Robert H. Rainbird

  3. Harquail School of Earth Sciences, Laurentian University, Sudbury, Ontario, Canada

    Elizabeth C. Turner

  4. UMR 7154 CNRS, Institut de Physique du Globe de Paris, Paris, France

    Stephan Borensztajn

Authors
  1. Corentin C. Loron
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Camille François
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert H. Rainbird
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elizabeth C. Turner
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stephan Borensztajn
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Emmanuelle J. Javaux
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

C.C.L. and E.J.J. conceived the study and interpreted the data. C.F. and C.C.L performed the Raman and FTIR analyses. C.C.L., C.F. and S.B. performed the TEM and SEM sample preparation and observations. R.H.R. and E.C.T. sampled the rocks and collected the geological data. C.C.L. and E.J.J. wrote the paper with contribution from all the authors. E.J.J. supervised the project.

Corresponding authors

Correspondence to Corentin C. Loron or Emmanuelle J. Javaux.

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.

Extended data figures and tables

Extended Data Fig. 1 Location of the study area in northwestern Canada, highlighting the Brock Inlier.

The white cross indicates the location at which the samples were extracted (68° 55′ 42′′ N, 121° 44′ 17′′ W). The stratigraphic column and geology have previously been published14,15,16. The map is modified after a previous publication14.

Extended Data Fig. 2 Additional SEM images.

a, b, O. giraldae (whole specimen) with right-angled branching hyphae (indicated with arrows). d–g, Detailed images of microfibrils on the surface of the specimen shown in Fig. 1h.

Extended Data Fig. 3 Additional spectra of O. giraldae, showing a more-advanced state of degradation.

The typical peaks of chitin and chitosan are present, but at a lower intensity than in the standard. The region of the saccharides (wavenumber of 1,200–800 cm−1), which is necessary for polymer recognition, is very weak in intensity. Each measurement was repeated three times with similar results.

Supplementary information

Supplementary Information

This file contains three tables: “Average values of characteristic Raman parameters”; “FTIR assignment of absoption bands”; and the data used for Fig. 3. Supplementary note includes a list of Precambrian microfossils previously interpreted as possible fungi; information on FTIR micro-spectroscopy and additional references.

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Loron, C.C., François, C., Rainbird, R.H. et al. Early fungi from the Proterozoic era in Arctic Canada. Nature 570, 232–235 (2019). https://doi.org/10.1038/s41586-019-1217-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41586-019-1217-0

This article is cited by

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.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

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