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Asgard archaea illuminate the origin of eukaryotic cellular complexity

Author

Listed:
  • Katarzyna Zaremba-Niedzwiedzka

    (Science for Life Laboratory, Uppsala University)

  • Eva F. Caceres

    (Science for Life Laboratory, Uppsala University)

  • Jimmy H. Saw

    (Science for Life Laboratory, Uppsala University)

  • Disa Bäckström

    (Science for Life Laboratory, Uppsala University)

  • Lina Juzokaite

    (Science for Life Laboratory, Uppsala University)

  • Emmelien Vancaester

    (Science for Life Laboratory, Uppsala University
    †Present address: Department of Plant Systems Biology, VIB and Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 927, B-9052 Ghent, Belgium.)

  • Kiley W. Seitz

    (University of Texas-Austin, Marine Science Institute, Port Aransas)

  • Karthik Anantharaman

    (Policy, and Management, University of California)

  • Piotr Starnawski

    (Section for Microbiology and Center for Geomicrobiology, Aarhus University)

  • Kasper U. Kjeldsen

    (Section for Microbiology and Center for Geomicrobiology, Aarhus University)

  • Matthew B. Stott

    (GNS Science, Extremophile Research Group, Private Bag 2000)

  • Takuro Nunoura

    (Research and Development Center for Marine Biosciences, Japan Agency for Marine-Earth Science and Technology)

  • Jillian F. Banfield

    (Policy, and Management, University of California)

  • Andreas Schramm

    (Section for Microbiology and Center for Geomicrobiology, Aarhus University)

  • Brett J. Baker

    (University of Texas-Austin, Marine Science Institute, Port Aransas)

  • Anja Spang

    (Science for Life Laboratory, Uppsala University)

  • Thijs J. G. Ettema

    (Science for Life Laboratory, Uppsala University)

Abstract

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. Here 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. Notably, 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, indicating that the archaeal host cell already contained many key components that govern eukaryotic cellular complexity.

Suggested Citation

  • Katarzyna Zaremba-Niedzwiedzka & Eva F. Caceres & Jimmy H. Saw & Disa Bäckström & Lina Juzokaite & Emmelien Vancaester & Kiley W. Seitz & Karthik Anantharaman & Piotr Starnawski & Kasper U. Kjeldsen &, 2017. "Asgard archaea illuminate the origin of eukaryotic cellular complexity," Nature, Nature, vol. 541(7637), pages 353-358, January.
    • Handle: RePEc:nat:nature:v:541:y:2017:i:7637:d:10.1038_nature21031
    DOI: 10.1038/nature21031
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    Cited by:

    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. Pedro Leão & Mary E. Little & Kathryn E. Appler & Daphne Sahaya & Emily Aguilar-Pine & Kathryn Currie & Ilya J. Finkelstein & Valerie Anda & Brett J. Baker, 2024. "Asgard archaea defense systems and their roles in the origin of eukaryotic immunity," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    6. David Moi & Shunsuke Nishio & Xiaohui Li & Clari Valansi & Mauricio Langleib & Nicolas G. Brukman & Kateryna Flyak & Christophe Dessimoz & Daniele de Sanctis & Kathryn Tunyasuvunakool & John Jumper & , 2022. "Discovery of archaeal fusexins homologous to eukaryotic HAP2/GCS1 gamete fusion proteins," Nature Communications, Nature, vol. 13(1), pages 1-18, 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. Florent Waltz & Thalia Salinas-Giegé & Robert Englmeier & Herrade Meichel & Heddy Soufari & Lauriane Kuhn & Stefan Pfeffer & Friedrich Förster & Benjamin D. Engel & Philippe Giegé & Laurence Drouard &, 2021. "How to build a ribosome from RNA fragments in Chlamydomonas mitochondria," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    10. Jason E. Cournoyer & Sarah D. Altman & Yang-le Gao & Catherine L. Wallace & Dianwen Zhang & Guo-Hsuen Lo & Noah T. Haskin & Angad P. Mehta, 2022. "Engineering artificial photosynthetic life-forms through endosymbiosis," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    11. Carolien Bastiaanssen & Pilar Bobadilla Ugarte & Kijun Kim & Giada Finocchio & Yanlei Feng & Todd A. Anzelon & Stephan Köstlbacher & Daniel Tamarit & Thijs J. G. Ettema & Martin Jinek & Ian J. MacRae , 2024. "RNA-guided RNA silencing by an Asgard archaeal Argonaute," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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