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Isolation of an archaeon at the prokaryote–eukaryote interface

Author

Listed:
  • Hiroyuki Imachi

    (Japan Agency for Marine-Earth Science and Technology (JAMSTEC))

  • Masaru K. Nobu

    (National Institute of Advanced Industrial Science and Technology (AIST))

  • Nozomi Nakahara

    (Japan Agency for Marine-Earth Science and Technology (JAMSTEC)
    National Institute of Advanced Industrial Science and Technology (AIST)
    Nagaoka University of Technology)

  • Yuki Morono

    (Kochi Institute for Core Sample Research, X-star, JAMSTEC)

  • Miyuki Ogawara

    (Japan Agency for Marine-Earth Science and Technology (JAMSTEC))

  • Yoshihiro Takaki

    (Japan Agency for Marine-Earth Science and Technology (JAMSTEC))

  • Yoshinori Takano

    (Research Institute for Marine Resources Utilization, JAMSTEC)

  • Katsuyuki Uematsu

    (Marine Work Japan)

  • Tetsuro Ikuta

    (Research Institute for Global Change, JAMSTEC)

  • Motoo Ito

    (Kochi Institute for Core Sample Research, X-star, JAMSTEC)

  • Yohei Matsui

    (Research Institute for Marine Resources Utilization, JAMSTEC)

  • Masayuki Miyazaki

    (Japan Agency for Marine-Earth Science and Technology (JAMSTEC))

  • Kazuyoshi Murata

    (National Institute for Physiological Sciences)

  • Yumi Saito

    (Japan Agency for Marine-Earth Science and Technology (JAMSTEC))

  • Sanae Sakai

    (Japan Agency for Marine-Earth Science and Technology (JAMSTEC))

  • Chihong Song

    (National Institute for Physiological Sciences)

  • Eiji Tasumi

    (Japan Agency for Marine-Earth Science and Technology (JAMSTEC))

  • Yuko Yamanaka

    (Japan Agency for Marine-Earth Science and Technology (JAMSTEC))

  • Takashi Yamaguchi

    (Nagaoka University of Technology)

  • Yoichi Kamagata

    (National Institute of Advanced Industrial Science and Technology (AIST))

  • Hideyuki Tamaki

    (National Institute of Advanced Industrial Science and Technology (AIST))

  • Ken Takai

    (Japan Agency for Marine-Earth Science and Technology (JAMSTEC)
    National Institute of Natural Sciences)

Abstract

The origin of eukaryotes remains unclear1–4. Current data suggest that eukaryotes may have emerged from an archaeal lineage known as ‘Asgard’ archaea5,6. 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 archaea6, 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.

Suggested Citation

  • Hiroyuki Imachi & Masaru K. Nobu & Nozomi Nakahara & Yuki Morono & Miyuki Ogawara & Yoshihiro Takaki & Yoshinori Takano & Katsuyuki Uematsu & Tetsuro Ikuta & Motoo Ito & Yohei Matsui & Masayuki Miyaza, 2020. "Isolation of an archaeon at the prokaryote–eukaryote interface," Nature, Nature, vol. 577(7791), pages 519-525, January.
  • Handle: RePEc:nat:nature:v:577:y:2020:i:7791:d:10.1038_s41586-019-1916-6
    DOI: 10.1038/s41586-019-1916-6
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    Citations

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    Cited by:

    1. Giovanni Scarinci & Jan-Luca Ariens & Georgia Angelidou & Sebastian Schmidt & Timo Glatter & Nicole Paczia & Victor Sourjik, 2024. "Enhanced metabolic entanglement emerges during the evolution of an interkingdom microbial community," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Tara A. Mahendrarajah & Edmund R. R. Moody & Dominik Schrempf & Lénárd L. Szánthó & Nina Dombrowski & Adrián A. Davín & Davide Pisani & Philip C. J. Donoghue & Gergely J. Szöllősi & Tom A. Williams & , 2023. "ATP synthase evolution on a cross-braced dated tree of life," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    3. Tomoyuki Hatano & Saravanan Palani & Dimitra Papatziamou & Ralf Salzer & Diorge P. Souza & Daniel Tamarit & Mehul Makwana & Antonia Potter & Alexandra Haig & Wenjue Xu & David Townsend & David Rochest, 2022. "Asgard archaea shed light on the evolutionary origins of the eukaryotic ubiquitin-ESCRT machinery," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    4. Zhongyi Lu & Runyue Xia & Siyu Zhang & Jie Pan & Yang Liu & Yuri I. Wolf & Eugene V. Koonin & Meng Li, 2024. "Evolution of optimal growth temperature in Asgard archaea inferred from the temperature dependence of GDP binding to EF-1A," Nature Communications, Nature, vol. 15(1), pages 1-7, December.
    5. Luis E. Valentin-Alvarado & Kathryn E. Appler & Valerie Anda & Marie C. Schoelmerich & Jacob West-Roberts & Veronika Kivenson & Alexander Crits-Christoph & Lynn Ly & Rohan Sachdeva & Chris Greening & , 2024. "Asgard archaea modulate potential methanogenesis substrates in wetland soil," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    6. Matthew Herdman & Buse Isbilir & Andriko Kügelgen & Ulrike Schulze & Alan Wainman & Tanmay A. M. Bharat, 2024. "Cell cycle dependent coordination of surface layer biogenesis in Caulobacter crescentus," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    7. Zhiguang Qiu & Li Yuan & Chun-Ang Lian & Bin Lin & Jie Chen & Rong Mu & Xuejiao Qiao & Liyu Zhang & Zheng Xu & Lu Fan & Yunzeng Zhang & Shanquan Wang & Junyi Li & Huiluo Cao & Bing Li & Baowei Chen & , 2024. "BASALT refines binning from metagenomic data and increases resolution of genome-resolved metagenomic analysis," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    8. Jonathan Filée & Hubert F. Becker & Lucille Mellottee & Rima Zein Eddine & Zhihui Li & Wenlu Yin & Jean-Christophe Lambry & Ursula Liebl & Hannu Myllykallio, 2023. "Bacterial origins of thymidylate metabolism in Asgard archaea and Eukarya," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    9. Michele Castelli & Tiago Nardi & Leandro Gammuto & Greta Bellinzona & Elena Sabaneyeva & Alexey Potekhin & Valentina Serra & Giulio Petroni & Davide Sassera, 2024. "Host association and intracellularity evolved multiple times independently in the Rickettsiales," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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