1. Key points

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Cultivation of us Eukaryotes’ closest prokaryotic (microbial) relative from deep-sea sediments

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This prokaryote belongs to microbial lineage known as “Archaea”, possesses many genes thought to have been unique to Eukaryotes, depends on symbioses, and produces unique tentacle-like features.

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Based on the structure and physiology, we propose a new theory (E³ model) for the evolutionary origin of Eukaryotes

2．Overview

Dr. Hiroyuki Imachi of the Japan Agency for Marine-Earth Science and Technology (JAMSTEC) and Dr. Masaru K. Nobu of the National Institute of Advanced Industrial Science and Technology (AIST), and colleagues accomplished the first cultivation and characterization of us Eukaryotes’ closest prokaryotic relative and revealed unprecedented insight into the origin of Eukaryotes.

Eukaryotes (complex organisms including animals, plants, fungi, and amoeba) are thought to have evolved from Prokaryotes (structurally simple and unicellular organisms), yet, “how” this took place remains a major mystery. Prokaryotes can be divided into two groups: Bacteria and Archaea. Current data suggests that the first Eukaryote emerged through an “archaeon” engulfing a “bacterium” and fusing into a single biological entity. The hosting archaeon is hypothesized to have belonged to a group of Archaea known as Asgard archaea. However, the appearance, way of life, and evolutionary story of these organisms remained unknown without living cells that could be studied in the laboratory.

This JAMSTEC-AIST collaboration succeeded capturing the first archaeon of this group. Cultivation was accomplished through combining the new and old – artificially recreating the deep-sea sediment environment in a unique reactor, monitoring growth using modern DNA sequencing technology, and purification through traditional cultivation techniques. A culture of the archaeon was finally reached through 12 years of strategic experimentation. The strain was named “Prometheoarchaeum syntrophicum MK-D1” after the Greek god, Prometheus, who created mankind from mud.

Though closely related to the ancestor of Eukaryotes, MK-D1 displayed many biological and physical features distinct from Eukaryotes. MK-D1 grew slowly, relied on symbiosis with other prokaryotes to grow on amino acids as energy sources, and could only grow in the absence of oxygen. Physically, MK-D1 cells were extremely small (~550 nm diameter; roughly 1/2000 of a millimeter) and simple on the inside, lacking any complex internal structures. On the other hand, MK-D1 possessed a structure never observed in prokaryotes before – branching tentacle-like protrusions extending from the cell surface.

Based on the physical, biological, and genomic characteristics unveiled by this work, the researchers propose a novel theory for the origin of eukaryotes: the “Entangle-Engulf-Endogenize (E³) model”. With the advent of photosynthesis, oxygen levels rose on Earth and created an opportunity for high-energy respiration. In the theory, the Eukaryotes’ ancestor archaeon formed symbiosis with an oxygen-respiring bacterium (the free-living ancestor of the mitochondrion), used tentacle-like protrusions and vesicles (like those observed in MK-D1) to engulf the bacterium, further developed the symbiosis internally, and matured into a single biological entity capable of digesting amino acids and breathing oxygen. This represents a primordial ancestor of us Eukaryotes.

Further research of this archaeon and its relatives will illuminate the evolutionary path structurally simple Prokaryotes took to evolve into Eukaryotes.

This study was partially supported by grants from the Japan Society for the Promotion of Science (JSPS) (KAKENHI Grants 18687006, 21687006, 24687011, 15H02419, 19H01005, 18H03367, 26710012, 18H02426, 18H05295, 16J10845, 18H04468, 18K18795), Advanced Bioimaging Support (ABiS) funded by JSPS KAKENHI Grant Number JP16H06280, and the Cooperative Study Program (19-504) of National Institute for Physiological Sciences.

The study was published in the international journal Nature on 15 January 2020 at 13:00 (EST).

Title：Isolation of an archaeon at the prokaryote-eukaryote interface
Authors: Hiroyuki Imachi^1*, Masaru K. Nobu^2,1*, Nozomi Nakahara^1,2,3, Yuki Morono⁴, Miyuki Ogawara¹, Yoshihiro Takaki¹, Yoshinori Takano⁵, Katsuyuki Uematsu⁶, Tetsuro Ikuta⁷, Motoo Ito⁴, Yohei Matsui⁸, Masayuki Miyazaki¹, Kazuyoshi Murata⁹, Yumi Saito¹, Sanae Sakai¹, Chihong Song⁹, Eiji Tasumi¹, Yuko Yamanaka¹, Takashi Yamaguchi³, Yoichi Kamagata², Hideyuki Tamaki² and Ken Takai^1,10
1Institute for Extra-cutting-edge Science and Technology Avant-garde Research (X-star), JAMSTEC ²Bioproduction Research Institute, AIST ³Department of Civil and Environmental Engineering, Nagaoka University of Technology ⁴Kochi Institute for Core Sample Research, X-star, JAMSTEC ⁵Biogeochemistry Program, Research Institute for Marine Resources Utilization, JAMSTEC ⁶Department of Marine and Earth Sciences, Marine Work Japan Ltd ⁷Research Institute for Global Change, JAMSTEC ⁸Research Institute for Marine Resources Utilization, JAMSTEC ⁹National Institute for Physiological Sciences, National Institute for Natural Sciences (NINS) ¹⁰Exploratory Research Center on Life and Living Systems (ExCELLS), NINS
*These authors contributed equally to this study.