Early fungi from the Proterozoic era in Arctic Canada

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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

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. 1.

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

  2. 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).

  3. 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).

  4. 4.

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

  5. 5.

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

  6. 6.

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

  7. 7.

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

  8. 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).

  9. 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).

  10. 10.

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

  11. 11.

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

  12. 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).

  13. 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).

  14. 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).

  15. 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).

  16. 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).

  17. 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).

  18. 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).

  19. 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).

  20. 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).

  21. 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).

  22. 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).

  23. 23.

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

  24. 24.

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

  25. 25.

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

  26. 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).

  27. 27.

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

  28. 28.

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

  29. 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. 30.

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

  31. 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).

  32. 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. 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).

  34. 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).

  35. 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).

  36. 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).

  37. 37.

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

  38. 38.

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

  39. 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).

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

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.

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). dg, 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

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.