Datum: 17.01.2020

Isolation of an archaeon at the prokaryote–eukaryote interface

Hiroyuki Imachi, Masaru K. Nobu, Nozomi Nakahara, Yuki Morono, Miyuki Ogawara, Yoshihiro Takaki, Yoshinori Takano, Katsuyuki Uematsu, Tetsuro Ikuta, Motoo Ito, Yohei Matsui, Masayuki Miyazaki, Kazuyoshi Murata, Yumi Saito, Sanae Sakai, Chihong Song, Eiji Tasumi, Yuko Yamanaka, Takashi Yamaguchi, Yoichi Kamagata, Hideyuki Tamaki & Ken Takai

The origin of eukaryotes remains unclear. Current data suggest that eukaryotes may have emerged from an archaeal lineage known as ‘Asgard’ archaea. Despite the eukaryote-like genomic features that are found in these archaea, the evolutionary transition from archaea to eukaryotes remains unclear, owing to the lack of cultured representatives and corresponding physiological insights. Here we report the decade-long isolation of an Asgard archaeon related to Lokiarchaeota from deep marine sediment. The archaeon—‘Candidatus Prometheoarchaeum syntrophicum’ strain MK-D1—is an anaerobic, extremely slow-growing, small coccus (around 550 nm in diameter) that degrades amino acids through syntrophy. Although eukaryote-like intracellular complexes have been proposed for Asgard archaea, the isolate has no visible organelle-like structure. Instead, Ca. P. syntrophicum is morphologically complex and has unique protrusions that are long and often branching. On the basis of the available data obtained from cultivation and genomics, and reasoned interpretations of the existing literature, we propose a hypothetical model for eukaryogenesis, termed the entangle–engulf–endogenize (also known as E3) model.

How the first eukaryotic cell emerged remains unclear. Among various competing evolutionary models, the most widely accepted are symbiogenic models in which an archaeal host cell and an alphaproteobacterial endosymbiont merged to become the first eukaryotic cell. Recent metagenomic characterization of deep-sea archaeal group/marine benthic group-B (also known as Lokiarchaeota) and the Asgard archaea superphylum led to the theory that eukaryotes originated from an archaeon that was closely related to these lineages5,6. The genomes of Asgard archaea encode a repertoire of proteins that are only found in Eukarya (eukaryotic signature proteins), including those involved in membrane trafficking, vesicle formation and/or transportation, ubiquitin and cytoskeleton formation6. Subsequent metagenomic studies have suggested that Asgard archaea have a wide variety of physiological properties, including hydrogen-dependent anaerobic autotrophy7, peptide or short-chain hydrocarbon-dependent organotrophy and rhodopsin-based phototrophy. However, no representative of the Asgard archaea has been cultivated and, thus, the physiology and cell biology of this clade remains unclear. In an effort to close this knowledge gap, we successfully isolated an archaeon of this clade, report its physiological and genomic characteristics, and propose a new model for eukaryogenesis.

Imachi H., Nobu M.K., Nakahara N. et al. Isolation of an archaeon at the prokaryote–eukaryote interface. Nature (2020). doi:10.1038/s41586-019-1916-6

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