Asgard archaea illuminate the origin of eukaryotic cellular complexity

Zaremba-Niedzwiedzka, Katarzyna; Caceres, Eva F.; Saw, Jimmy H.; Bäckström, Disa; Juzokaite, Lina; Vancaester, Emmelien; Seitz, Kiley W.; Anantharaman, Karthik; Starnawski, Piotr; Kjeldsen, Kasper U.; Stott, Matthew B.; Nunoura, Takuro; Banfield, Jillian F.; Schramm, Andreas; Baker, Brett J.; Spang, Anja; Ettema, Thijs J.  G.

doi:10.1038/nature21031

Asgard archaea illuminate the origin of eukaryotic cellular complexity

Journal Article · Wed Jan 11 00:00:00 EST 2017 · Nature (London)

DOI:https://doi.org/10.1038/nature21031· OSTI ID:1580084

Zaremba-Niedzwiedzka, Katarzyna ^[1]; Caceres, Eva F. ^[1]; Saw, Jimmy H. ^[1]; Bäckström, Disa ^[1]; Juzokaite, Lina ^[1]; Vancaester, Emmelien ^[2]; Seitz, Kiley W. ^[3]; Anantharaman, Karthik ^[4]; Starnawski, Piotr ^[5]; Kjeldsen, Kasper U. ^[5]; Stott, Matthew B. ^[6]; Nunoura, Takuro ^[7]; Banfield, Jillian F. ^[4]; Schramm, Andreas ^[5]; Baker, Brett J. ^[3]; Spang, Anja ^[1]; Ettema, Thijs J. G. ^[1]

Uppsala Univ. (Sweden). Dept. of Cell and Molecular Biology, Science for Life Lab.
Uppsala Univ. (Sweden). Dept. of Cell and Molecular Biology, Science for Life Lab.; Ghent Univ. (Belgium). Dept. of Plant Systems Biology, VIB and Dept. of Plant Biotechnology and Bioinformatics
Univ. of Texas-Austin, Port Aransas, TX (United States). Dept. of Marine Science, Marine Science Inst.
Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Sciences and Dept. of Environmental Science, Policy, and Management
Aarhus Univ. (Denmark). Dept. of Bioscience, Section for Microbiology and Center for Geomicrobiology
GNS Science, Taupō (New Zealand). Extremophile Research Group
Japan Agency for Marine-Earth Science and Technology, Yokosuka (Japan). Research and Development Center for Marine Biosciences

The origin and cellular complexity of eukaryotes represent a major enigma in biology. Current data support scenarios in which an archaeal host cell and an alphaproteobacterial (mitochondrial) endosymbiont merged together, resulting in the first eukaryotic cell. The host cell is related to Lokiarchaeota, an archaeal phylum with many eukaryotic features. The emergence of the structural complexity that characterizes eukaryotic cells remains unclear. In this report we describe the 'Asgard' superphylum, a group of uncultivated archaea that, as well as Lokiarchaeota, includes Thor-, Odin- and Heimdallarchaeota. Asgard archaea affiliate with eukaryotes in phylogenomic analyses, and their genomes are enriched for proteins formerly considered specific to eukaryotes. Interestingly, thorarchaeal genomes encode several homologues of eukaryotic membrane-trafficking machinery components, including Sec23/24 and TRAPP domains. Furthermore, we identify thorarchaeal proteins with similar features to eukaryotic coat proteins involved in vesicle biogenesis. Our results expand the known repertoire of 'eukaryote-specific' proteins in Archaea, suggesting that the archaeal host cell already contained many key components that govern eukaryotic cellular complexity.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1580084

Journal Information:: Nature (London), Journal Name: Nature (London) Journal Issue: 7637 Vol. 541; ISSN 0028-0836

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Additional file 3 of Genomic reconstruction of fossil and living microorganisms in ancient Siberian permafrost Liang, Renxing; Li, Zhou; Vetter, Maggie C. Y. Lau figshare https://doi.org/10.6084/m9.figshare.14608591	dataset	January 2021
Additional file 4 of Genomic reconstruction of fossil and living microorganisms in ancient Siberian permafrost Liang, Renxing; Li, Zhou; Vetter, Maggie C. Y. Lau figshare https://doi.org/10.6084/m9.figshare.14608594	dataset	January 2021
Additional file 5 of Genomic reconstruction of fossil and living microorganisms in ancient Siberian permafrost Liang, Renxing; Li, Zhou; Vetter, Maggie C. Y. Lau figshare https://doi.org/10.6084/m9.figshare.14608597	dataset	January 2021
Additional file 7 of Genomic reconstruction of fossil and living microorganisms in ancient Siberian permafrost Liang, Renxing; Li, Zhou; Vetter, Maggie C. Y. Lau figshare https://doi.org/10.6084/m9.figshare.14608603.v1	dataset	January 2021
Additional file 8 of Genomic reconstruction of fossil and living microorganisms in ancient Siberian permafrost Liang, Renxing; Li, Zhou; Vetter, Maggie C. Y. Lau figshare https://doi.org/10.6084/m9.figshare.14608606	dataset	January 2021
Additional file 2 of Linking genomic and physiological characteristics of psychrophilic Arthrobacter to metagenomic data to explain global environmental distribution Shen, Liang; Liu, Yongqin; Allen, Michelle A. figshare https://doi.org/10.6084/m9.figshare.14775424.v1	dataset	January 2021
Additional file 3 of Linking genomic and physiological characteristics of psychrophilic Arthrobacter to metagenomic data to explain global environmental distribution Shen, Liang; Liu, Yongqin; Allen, Michelle A. figshare https://doi.org/10.6084/m9.figshare.14775427.v1	dataset	January 2021
Additional file 4 of Linking genomic and physiological characteristics of psychrophilic Arthrobacter to metagenomic data to explain global environmental distribution Shen, Liang; Liu, Yongqin; Allen, Michelle A. figshare https://doi.org/10.6084/m9.figshare.14775430.v1	dataset	January 2021
Additional file 5 of Linking genomic and physiological characteristics of psychrophilic Arthrobacter to metagenomic data to explain global environmental distribution Shen, Liang; Liu, Yongqin; Allen, Michelle A. figshare https://doi.org/10.6084/m9.figshare.14775433	dataset	January 2021
Additional file 6 of Linking genomic and physiological characteristics of psychrophilic Arthrobacter to metagenomic data to explain global environmental distribution Shen, Liang; Liu, Yongqin; Allen, Michelle A. figshare https://doi.org/10.6084/m9.figshare.14775436	dataset	January 2021
Additional file 7 of Linking genomic and physiological characteristics of psychrophilic Arthrobacter to metagenomic data to explain global environmental distribution Shen, Liang; Liu, Yongqin; Allen, Michelle A. figshare https://doi.org/10.6084/m9.figshare.14775439.v1	dataset	January 2021
Additional file 8 of Linking genomic and physiological characteristics of psychrophilic Arthrobacter to metagenomic data to explain global environmental distribution Shen, Liang; Liu, Yongqin; Allen, Michelle A. figshare https://doi.org/10.6084/m9.figshare.14775442	dataset	January 2021
Additional file 1 of Functional differentiation determines the molecular basis of the symbiotic lifestyle of Ca. Nanohaloarchaeota Xie, Yuan-Guo; Luo, Zhen-Hao; Fang, Bao-Zhu figshare https://doi.org/10.6084/m9.figshare.21340502	dataset	January 2022
Additional file 4 of Functional differentiation determines the molecular basis of the symbiotic lifestyle of Ca. Nanohaloarchaeota Xie, Yuan-Guo; Luo, Zhen-Hao; Fang, Bao-Zhu figshare https://doi.org/10.6084/m9.figshare.21340511.v1	dataset	January 2022
Additional file 1 of Metagenomic insights into Heimdallarchaeia clades from the deep-sea cold seep and hydrothermal vent Liu, Rui; Cai, Ruining; Wang, Minxiao figshare https://doi.org/10.6084/m9.figshare.26085143.v1	dataset	January 2024
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The structure and evolution of eukaryotic chaperonin-containing TCP-1 and its mechanism that folds actin into a protein spring Willison, Keith Robert Biochemical Journal, Vol. 475, Issue 19 https://doi.org/10.1042/bcj20170378	journal	October 2018
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Asgard archaea are diverse, ubiquitous, and transcriptionally active microbes Cai, Mingwei; Liu, Yang; Zhou, Zhichao https://doi.org/10.1101/374165	posted_content	July 2018
Marine deep biosphere microbial communities assemble in near-surface sediments in Aarhus Bay Petro, Caitlin; Zäncker, Birthe; Starnawski, Piotr https://doi.org/10.1101/557041	posted_content	February 2019
Timing the origin of eukaryotic cellular complexity with ancient duplications Vosseberg, Julian; van Hooff, Jolien J. E.; Marcet-Houben, Marina https://doi.org/10.1101/823484	posted_content	July 2020
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Common ancestry of heterodimerizing TALE homeobox transcription factors across Metazoa and Archaeplastida Joo, Sunjoo; Wang, Ming Hsiu; Lui, Gary BMC Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s12915-018-0605-5	journal	November 2018
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Breath-giving cooperation: critical review of origin of mitochondria hypotheses: Major unanswered questions point to the importance of early ecology Zachar, István; Szathmáry, Eörs Biology Direct, Vol. 12, Issue 1 https://doi.org/10.1186/s13062-017-0190-5	journal	August 2017
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Characterization of Bathyarchaeota genomes assembled from metagenomes of biofilms residing in mesophilic and thermophilic biogas reactors Maus, Irena; Rumming, Madis; Bergmann, Ingo Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1162-4	journal	June 2018
IS982 and kin: new insights into an old IS family Fayad, Nancy; Kallassy Awad, Mireille; Mahillon, Jacques Mobile DNA, Vol. 11, Issue 1 https://doi.org/10.1186/s13100-020-00221-z	journal	July 2020
Genomes from uncultivated prokaryotes: a comparison of metagenome-assembled and single-amplified genomes Alneberg, Johannes; Karlsson, Christofer M. G.; Divne, Anna-Maria Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0550-0	journal	September 2018
Life on the fringe: microbial adaptation to growth on carbon monoxide Robb, Frank T.; Techtmann, Stephen M. F1000Research, Vol. 7 https://doi.org/10.12688/f1000research.16059.1	journal	January 2018
Pore timing: the evolutionary origins of the nucleus and nuclear pore complex Field, Mark C.; Rout, Michael P. F1000Research, Vol. 8 https://doi.org/10.12688/f1000research.16402.1	journal	January 2019
The deep(er) roots of Eukaryotes and Akaryotes Harish, Ajith; Morrison, David F1000Research, Vol. 9 https://doi.org/10.12688/f1000research.22338.1	journal	January 2020
The deep(er) roots of Eukaryotes and Akaryotes Harish, Ajith; Morrison, David F1000Research, Vol. 9 https://doi.org/10.12688/f1000research.22338.2	journal	January 2020
Asgard archaea are the closest prokaryotic relatives of eukaryotes Spang, Anja; Eme, Laura; Saw, Jimmy H. PLOS Genetics, Vol. 14, Issue 3 https://doi.org/10.1371/journal.pgen.1007080	journal	March 2018
Asgard archaea do not close the debate about the universal tree of life topology Da Cunha, Violette; Gaia, Morgan; Nasir, Arshan PLOS Genetics, Vol. 14, Issue 3 https://doi.org/10.1371/journal.pgen.1007215	journal	March 2018
The last universal common ancestor between ancient Earth chemistry and the onset of genetics Weiss, Madeline C.; Preiner, Martina; Xavier, Joana C. PLOS Genetics, Vol. 14, Issue 8 https://doi.org/10.1371/journal.pgen.1007518	journal	August 2018
Structure and function of archaeal histones Henneman, Bram; van Emmerik, Clara; van Ingen, Hugo PLOS Genetics, Vol. 14, Issue 9 https://doi.org/10.1371/journal.pgen.1007582	journal	September 2018
Functional Innovation in the Evolution of the Calcium-Dependent System of the Eukaryotic Endoplasmic Reticulum Schäffer, Daniel E.; Iyer, Lakshminarayan M.; Burroughs, A. Maxwell Frontiers in Genetics, Vol. 11 https://doi.org/10.3389/fgene.2020.00034	journal	February 2020
Casting light on Asgardarchaeota metabolism in a sunlit microoxic niche Bulzu, Paul-Adrian; Andrei, Adrian-Ştefan; Salcher, Michaela M. Nature Publishing Group https://doi.org/10.5167/uzh-183773	text	January 2019
What is an archaeon and are the Archaea really unique? Harish, Ajith PeerJ, Vol. 6 https://doi.org/10.7717/peerj.5770	journal	January 2018

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