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Oldest thylakoids in fossil cells directly evidence oxygenic photosynthesis

Nature volume 625, pages 529–534 (2024)Cite this article

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Abstract

Today oxygenic photosynthesis is unique to cyanobacteria and their plastid relatives within eukaryotes. Although its origin before the Great Oxidation Event is still debated1,2,3,4, the accumulation of O2 profoundly modified the redox chemistry of the Earth and the evolution of the biosphere, including complex life. Understanding the diversification of cyanobacteria is thus crucial to grasping the coevolution of our planet and life, but their early fossil record remains ambiguous5. Extant cyanobacteria include the thylakoid-less Gloeobacter-like group and the remainder of cyanobacteria that acquired thylakoid membranes6,7. The timing of this divergence is indirectly estimated at between 2.7 and 2.0 billion years ago (Ga) based on molecular clocks and phylogenies8,9,10,11 and inferred from the earliest undisputed fossil record of Eoentophysalis belcherensis, a 2.018–1.854 Ga pleurocapsalean cyanobacterium preserved in silicified stromatolites12,13. Here we report the oldest direct evidence of thylakoid membranes in a parallel-to-contorted arrangement within the enigmatic cylindrical microfossils Navifusa majensis from the McDermott Formation, Tawallah Group, Australia (1.78–1.73 Ga), and in a parietal arrangement in specimens from the Grassy Bay Formation, Shaler Supergroup, Canada (1.01–0.9 Ga). This discovery extends their fossil record by at least 1.2 Ga and provides a minimum age for the divergence of thylakoid-bearing cyanobacteria at roughly 1.75 Ga. It allows the unambiguous identification of early oxygenic photosynthesizers and a new redox proxy for probing early Earth ecosystems, highlighting the importance of examining the ultrastructure of fossil cells to decipher their palaeobiology and early evolution.

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Fig. 1: Images of N. majensis microfossils.
Fig. 2: TEM images of N. majensis from the McDermott Formation, Australia, and the Grassy Bay Formation, Canada.
Fig. 3: TEM images of N. majensis from the Grassy Bay Formation, Canada, and the BIIc6 Formation, DRC.
Fig. 4: Raman microspectroscopy of isolated N. majensis specimens.

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Data availability

All raw data are deposited in ULiege institutional open archive ORBi and can be accessed at https://hdl.handle.net/2268/308458. The folder ‘morphometry’ contains a table with measurements of microfossil lengths and widths; the folder ‘Raman_RawData’ contains raw maps; the folder ‘Raman_TreatedData_Temperatures’ contains tables with the treated data used to obtain temperatures (palaeothermometry - Raman reflectance T°C Rmc Ro); the folder ‘Raw_TEM_images’ contains raw TEM images of microfossil ultrastructure with scales. All tables are in .txt format.

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Acknowledgements

We thank the Royal Museum for Central Africa (Tervuren, Belgium) and D. Baudet for access to the Kanshi SB13 drill core; S. Spinks and M. Kunzmann (CSIRO Mineral Resources, Australia) for samples from the GSD7 drill core at the Darwin core facility (Australia); and the Geological Survey of Canada’s Geomapping for Energy and Minerals programme, G. Halverson (McGill University, Canada), R. Rainbird (GSC, Canada), E. Turner (Laurentian University, Canada), T. Gibson (McGill University, Canada) and C. Loron (ULiege, Belgium and University of Edinburgh, UK) for sampling the Shaler Supergroup in the Northwest Territories of Arctic Canada. We thank M. Giraldo at the Early Life Traces & Evolution–Astrobiology laboratory and C. López-Iglesias and H. Duimel at the Microscopy CORE Lab (University of Maastricht) for technical support. FRS-FNRS-FWO EOS ET-Home (grant no. 30442502), ERC Stg ELiTE FP7/308074, an Agouron Institute geobiology grant and BELSPO BRAIN project B2/212/PI/PORTAL supported this project.

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Authors and Affiliations

  1. Early Life Traces & Evolution-Astrobiology, UR Astrobiology, University of Liège, Liège, Belgium

    Catherine F. Demoulin, Yannick J. Lara, Alexandre Lambion & Emmanuelle J. Javaux

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Contributions

C.F.D., Y.J.L. and E.J.J. conceived the study and interpreted the data. A.L. performed acid demineralization and prepared microfossil slides. C.F.D. and E.J.J. performed TEM sample preparation and observations. C.F.D. and E.J.J. prepared samples for Raman spectroscopy. C.F.D., Y.J.L. and E.J.J. performed Raman analyses. C.F.D., Y.J.L. and E.J.J. wrote the paper. E.J.J. supervised the project.

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Correspondence to Catherine F. Demoulin or Emmanuelle J. Javaux.

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Extended data figures and tables

Extended Data Fig. 1 TEM pictures of a specimen of Navifusa majensis, from the Grassy Bay Formation (Shaler Supergroup, Canada).

Pictures a, c and d show the width and limits of each layer interpreted as stacked thylakoidal membranes that were measured. Measurements are compiled in Extended Data Table 1 below. Picture b is a zoom of the section through the microfossil rounded end in a (black box). The parietal arrangement is clearly visible (dotted black lines), as well as the variable thicknesses of stacked thylakoidal membranes, due to merging of several thylakoids during burial, compression and diagenesis, dotted yellow lines show possible limits of several layers in the ticker one. These TEM pictures are from the same specimen illustrated in Fig. 2c,d; 3a,b.

Extended Data Fig. 2 TEM pictures of the second specimen of Navifusa majensis from the Grassy Bay Formation (Shaler Supergroup, Canada).

Pictures a and b show some positions where thickness of layers were measured and clearly illustrate the limits of each layer interpreted as stacked thylakoidal membranes. Measures are summarized in the Extended Data Table 1 below. Picture c shows knife marks (dotted lines) creating artefacts on ultrathin sections. These knife marks are clearly distinguishable from limits of stacked thylakoidal layers. Picture c also shows that on a same ultrathin section, the limits between layers may be less clear, due to merging during burial and compression. n = 2 N. majensis for Grassy Bay Formation. “n” represents the number of specimens observed by TEM.

Extended Data Fig. 3 TEM picture of a specimen of Navifusa majensis from the McDermott Formation (Tawallah Group, Australia).

This picture shows the positions where the thylakoidal membranes are measured. Measurements are compiled in table S4 below. n = 2 N. majensis for McDermott Formation. “n” represents the number of specimens observed by TEM.

Extended Data Fig. 4 Schematic drawings showing how compressed microfossils were cut transversally for TEM observations.

a represents a whole flattened specimen of Navifusa majensis, with transversal section shown (black line). b represents a transversal TEM ultrathin section through the microfossil. The length of the ultrathin section in b corresponds to the width of the microfossil (red line in a and b), while the thickness of the ultrathin section corresponds to the thickness of the compressed microfossil (T in a and b). L: length of the whole microfossil; W: width; T: thickness.

Extended Data Table 1 Measurements of thickness of layers interpreted as stacked thylakoids in Navifusa majensis from both Shaler Supergroup (Extended Data Figs. 1 and 2) and Tawallah Group (Extended Data Fig. 3)
Full size table

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Demoulin, C.F., Lara, Y.J., Lambion, A. et al. Oldest thylakoids in fossil cells directly evidence oxygenic photosynthesis. Nature 625, 529–534 (2024). https://doi.org/10.1038/s41586-023-06896-7

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