A diverse Palaeoproterozoic microbial ecosystem implies early eukaryogenesis

Microbial interactions may lead to major events in life and planetary evolution, such as eukaryogenesis, the birth of complex nucleated cells. In synergy with microbiology, cellular palaeobiology may shed some light on this very ancient and debated affair and its circumstances. The 1.78-1.73 Ga McDermott Formation, McArthur Basin (Australia), preserves a microfossil assemblage that provides unique insights into the evolution of early eukaryotes. The fossil cells display a level of morphological complexity, disparity and plasticity requiring a complex cytoskeleton and an endomembrane system, pushing back the minimum age of uncontested eukaryotic fossils by more than 100 million years (Ma). They also document an earlier appearance of reproduction by budding, simple multicellularity and diverse programmed openings of cyst wall implying a life cycle, as well as possible evidence for microbial symbiosis and behaviour, including eukaryovory and ectosymbiosis. This microbial community that also includes cyanobacterial cells preserving thylakoids, microbial mats and other microfossils, thrived in supratidal to intertidal marine environments with heterogeneous but mostly suboxic to anoxic redox conditions. Taken together, these observations imply early eukaryogenesis, including mitochondrial endosymbiosis in micro-/nano-oxic niches, and suggest a >1.75 Ga minimum age for the Last Eukaryotic Common Ancestor (LECA), preceded by a deeper history of the domain Eukarya, consistent with several molecular clocks and the fossil record.This article is part of the discussion meeting issue 'Chance and purpose in the evolution of biospheres'.