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Isolation of an archaeon at the prokaryote-eukaryote interface

View ORCID ProfileHiroyuki Imachi, View ORCID ProfileMasaru K. Nobu, View ORCID ProfileNozomi Nakahara, View ORCID ProfileYuki Morono, Miyuki Ogawara, Yoshihiro Takaki, View ORCID ProfileYoshinori Takano, Katsuyuki Uematsu, View ORCID ProfileTetsuro Ikuta, View ORCID ProfileMotoo 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
doi: https://doi.org/10.1101/726976
Hiroyuki Imachi
Institute for Extra-cutting-edge Science and Technology Avant-garde Research (X-star), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Japan
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  • ORCID record for Hiroyuki Imachi
  • For correspondence: imachi@jamstec.go.jp m.nobu@aist.go.jp
Masaru K. Nobu
Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Japan
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  • ORCID record for Masaru K. Nobu
  • For correspondence: imachi@jamstec.go.jp m.nobu@aist.go.jp
Nozomi Nakahara
Institute for Extra-cutting-edge Science and Technology Avant-garde Research (X-star), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, JapanDepartment of Civil and Environmental Engineering, Nagaoka University of Technology, Nagaoka, Japan
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Yuki Morono
Kochi Institute for Core Sample Research, X-star, JAMSTEC, Nankoku, Japan
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  • ORCID record for Yuki Morono
Miyuki Ogawara
Institute for Extra-cutting-edge Science and Technology Avant-garde Research (X-star), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Japan
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Yoshihiro Takaki
Institute for Extra-cutting-edge Science and Technology Avant-garde Research (X-star), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Japan
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Yoshinori Takano
Biogeochemistry Program, Research Institute for Marine Resources Utilization, JAMSTEC, Yokosuka, Japan
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  • ORCID record for Yoshinori Takano
Katsuyuki Uematsu
Department of Marine and Earth Sciences, Marine Work Japan Ltd, Yokosuka, Japan
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Tetsuro Ikuta
Research Institute for Global Change, JAMSTEC, Yokosuka, Japan
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Motoo Ito
Kochi Institute for Core Sample Research, X-star, JAMSTEC, Nankoku, Japan
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  • ORCID record for Motoo Ito
Yohei Matsui
Research Institute for Marine Resources Utilization, JAMSTEC, Yokosuka, Japan
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Masayuki Miyazaki
Institute for Extra-cutting-edge Science and Technology Avant-garde Research (X-star), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Japan
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Kazuyoshi Murata
National Institute for Physiological Sciences, Okazaki, Japan
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Yumi Saito
Institute for Extra-cutting-edge Science and Technology Avant-garde Research (X-star), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Japan
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Sanae Sakai
Institute for Extra-cutting-edge Science and Technology Avant-garde Research (X-star), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Japan
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Chihong Song
National Institute for Physiological Sciences, Okazaki, Japan
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Eiji Tasumi
Institute for Extra-cutting-edge Science and Technology Avant-garde Research (X-star), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Japan
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Yuko Yamanaka
Institute for Extra-cutting-edge Science and Technology Avant-garde Research (X-star), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Japan
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Takashi Yamaguchi
Department of Civil and Environmental Engineering, Nagaoka University of Technology, Nagaoka, Japan
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Yoichi Kamagata
Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Japan
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Hideyuki Tamaki
Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Japan
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Ken Takai
Institute for Extra-cutting-edge Science and Technology Avant-garde Research (X-star), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Japan
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Abstract

The origin of eukaryotes remains enigmatic. Current data suggests that eukaryotes may have risen from an archaeal lineage known as “Asgard archaea”. Despite the eukaryote-like genomic features found in these archaea, the evolutionary transition from archaea to eukaryotes remains unclear due to the lack of cultured representatives and corresponding physiological insight. Here we report the decade-long isolation of a Lokiarchaeota-related Asgard archaeon from deep marine sediment. The archaeon, “Candidatus Prometheoarchaeum syntrophicum strain MK-D1”, is an anaerobic, extremely slow-growing, small cocci (∼550 nm), that degrades amino acids through syntrophy. Although eukaryote-like intracellular complexities have been proposed for Asgard archaea, the isolate has no visible organella-like structure. Ca. P. syntrophicum instead displays morphological complexity – unique long, and often, branching protrusions. Based on cultivation and genomics, we propose an “Entangle-Engulf-Enslave (E3) model” for eukaryogenesis through archaea-alphaproteobacteria symbiosis mediated by the physical complexities and metabolic dependency of the hosting archaeon.

Footnotes

  • Figure 4a revised

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Posted August 08, 2019.
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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
bioRxiv 726976; doi: https://doi.org/10.1101/726976
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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
bioRxiv 726976; doi: https://doi.org/10.1101/726976

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