[en] Today oxygenic photosynthesis is unique to cyanobacteria and their plastid relatives within eukaryotes. Although its origin before the Great Oxidation Event is still debated1-4, 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 phylogenies8-11 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.
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.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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