Peculiar morphology of Asgard archaeal cells close to the prokaryote-eukaryote boundary

The emergence of complex eukaryotic cells from prokaryotic ancestors is a major enigma in the history of life. Current data suggest that Asgard archaea are the closest prokaryotic relatives of eukaryotes and have a genetic potential for cellular complexity, suggesting their key role in the evolution of eukaryotes. The Asgard archaeal order Hodarchaeales was recently proposed as the sister lineage of eukaryotes with a unique set of eukaryotic signature proteins. However, there is no microscopic evidence to show the cellular structure of these closest known archaeal relatives of eukaryotes. Here, we retrieved Hodarchaeales-affiliated full-length 16S rRNA sequences from marine sediments (Aarhus Bay, Denmark), representing 0.1% of the relative rRNA read abundance in sequence libraries, and designed new oligonucleotide probes specifically targeting their cells. We then employed catalyzed reporter deposition-fluorescence in situ hybridization (CARD-FISH) and imaged the labeled cells by super-resolution microscopy with appropriate controls. Hodarchaeales-affiliated cells were characterized by an elongated cell body connected to a rounded expansion at one pole with a confined central DNA localization. They were conspicuously large, with an average length of 3 µm, ranging from 1.5 to 5.2 µm. The average width was 1.1–0.8 µm in the round expansion and the cell body, respectively. The remarkable size and morphology of the detected Hodarchaeales-related cells suggest a potential for complex eukaryote-like cellular architecture in these as-yet-uncultivated Asgard archaea, which could represent a key transitional stage in eukaryogenesis.