Evolutionary diversification of paleoproterozoic prokaryotes: New microfossil records in 1.88 Ga Gunflint Formation

The evolutionary history of early prokaryotes is recorded in Paleoproterozoic sedimentary rocks. The ca. 1.88 Ga Gunflint Formation is considered key to constrain the course of Paleoproterozoic microbial evolution. However, whether the multicellularity of prokaryote and eukaryote was already present by the Gunflint age remains uncertain. Here, we report novel morphotypes of prokaryotes including colonial, ellipsoidal, spherical, with intracellular inclusions (ICIs), spinous-type, and tail-bearing type, in the Gunflint stromatolitic chert. Biogenicity of such morphotypes was indicated based on their unique microstructures with the parallel C, N, and S distributions and lack of evidence of their post-depositional artifact origin. The new finding of colonial-type microbes in the Gunflint Formation indicates global flourishment of the colonial-type in this age. Moreover, unknown spherical cell-like structures with ICIs were identified, along with microfossils bearing strong similarities to cyanobacterial akinetes. ICIs were more enriched in N-bearing organic compounds than cell wall organic matter. Those ICIs were interpreted as biological contracted protoplasts. These new findings suggest that Paleoproterozoic prokaryotes were more diverse and complex than previously considered and had already acquired adaptability to survive drastic environmental changes. Furthermore, the protruding appendages in the novel spine- and tail-bearing type microfossils likely provided them with advantages in nutrient access and motility respectively, resulting in the promotion of the intercellular interactions. This suggests that functional evolution toward eukaryotes had already started in the Gunflint age.