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Asgard Archaea Illuminate the Origin of Eukaryotic Cellular Complexity Katarzyna Zaremba-Niedzwiedzka1*, Eva F

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Asgard Archaea Illuminate the Origin of Eukaryotic Cellular Complexity Katarzyna Zaremba-Niedzwiedzka1*, Eva F ARTICLE doi:10.1038/nature21031 Asgard archaea illuminate the origin of eukaryotic cellular complexity Katarzyna Zaremba-Niedzwiedzka1*, Eva F. Caceres1*, Jimmy H. Saw1*, Disa Bäckström1, Lina Juzokaite1, Emmelien Vancaester1†, Kiley W. Seitz2, Karthik Anantharaman3, Piotr Starnawski4, Kasper U. Kjeldsen4, Matthew B. Stott5, Takuro Nunoura6, Jillian F. Banfield3, Andreas Schramm4, Brett J. Baker2, Anja Spang1 & Thijs J. G. Ettema1 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. The origin of the eukaryotic cell is regarded as one of the major evolu- metabolism21,22, leading to renewed efforts to explain the origin and tionary innovations in the history of life on our planet. Yet, the emer- early evolution of eukaryotes. Though insightful, these deductions are gence of the complex and compartmentalized nature of eukaryotic preliminary as they are based, so far, on a single genomic data set. Here cells represents a major conundrum in modern biology1–3. Most we describe the metagenomic discovery of the Asgard superphylum, recent insights support symbiogenic scenarios of eukaryotic which, as well as Lokiarchaeota, includes several new uncultivated evolution3,4—that the emergence of the first eukaryotic cell was triggered archaeal lineages that reside in a wide variety of environments. We by a merger between an archaeal host cell5–9 and an alphaproteobacterial show that these lineages comprise novel phylum-level groups that rep- (mitochondrial) endosymbiont10. Whereas the alphaproteobacterial resent the closest archaeal relatives of eukaryotes. Detailed analyses of provenance of mitochondria is overwhelming, the identity and nature their reconstructed genomes provide new insights into the identity and of the archaeal host cell have remained elusive until recently. The iden- genetic nature of the archaeal ancestor of eukaryotes and the primal tification and genomic characterization of Lokiarchaeota, a clade of stages of eukaryogenesis. archaea found in deep marine sediments, has provided several crucial insights into the archaeal origin of eukaryotes11. First, phylogenomic Metagenomic discovery of Asgard archaea analyses of carefully selected genomic data sets placed Lokiarchaeota To gain insight into the archaea-to-eukaryote transition, we aimed to as the most closely related group to eukaryotes, providing further com- identify and characterize novel archaeal lineages related to the recently pelling evidence for the two-domain tree of life12, in which eukaryotes described Lokiarchaeota11, an archaeal clade that was previously shown branch from within the archaeal domain. Furthermore, a careful analy- to be more closely related to eukaryotes than any other prokaryotic sis of genome content of the composite Lokiarchaeum genome revealed lineage. We sampled aquatic sediments from seven geographically that it encodes a multitude of genes that were previously regarded separated sites which differed markedly with respect to their biological specific to eukaryotes11. These so-called eukaryotic signature proteins13 and chemical parameters: Loki’s Castle, Yellowstone National Park, included several cytoskeletal components (actin homologues and gel- Aarhus Bay, an aquifer near Colorado River, Radiata Pool, Taketomi solin-domain proteins), ESCRT complex proteins (including ESCRT-I, Island Vent and the White Oak River estuary (Extended Data Fig. 1a, -II and -III components), and a wide variety of small GTPases11, Supplementary Table 1). Total DNA was extracted from all samples and including Gtr/Rag family GTPase orthologues14,15—proteins that in sequenced, resulting in a total of 644.88 gigabase pairs (Gbp) of paired eukaryotes are involved in various regulatory processes including end reads. Sequence assembly generated a total of 3.28 Gbp of conti- cytoskeleton remodelling, signal transduction, nucleocytoplasmic guous sequences (contigs) ≥5 kb (Supplementary Table 2). To assess the transport and vesicular trafficking. The discovery of Lokiarchaeota presence of potential Lokiarchaeota-related lineages, contigs containing has reignited debates about the nature of the archaeal host cell from at least six genes of a conserved 15-ribosomal protein (RP15) gene which eukaryotes emerged. For example, on the basis of analyses of the cluster were extracted and subjected to phylogenomic analysis. This available lokiarchaeal genome data, inferences have been made about its analysis revealed the presence of numerous archaeal contigs that were level of cellular complexity14,16–19 its membrane composition20 and its relatively closely related to the previously described Lokiarchaeota11 1Department of Cell and Molecular Biology, Science for Life Laboratory, Uppsala University, SE-75123 Uppsala, Sweden. 2Department of Marine Science, University of Texas-Austin, Marine Science Institute, Port Aransas, Texas 78373, USA. 3Department of Earth and Planetary Sciences, and Department of Environmental Science, Policy, and Management, University of California, Berkeley, California, USA. 4Section for Microbiology and Center for Geomicrobiology, Department of Bioscience, Aarhus University, DK-8000 Aarhus, Denmark. 5GNS Science, Extremophile Research Group, Private Bag 2000, Taupoˉ 3352, New Zealand. 6Research and Development Center for Marine Biosciences, Japan Agency for Marine-Earth Science and Technology, Yokosuka 237-0061, Japan. †Present address: Department of Plant Systems Biology, VIB and Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 927, B-9052 Ghent, Belgium. * These authors contributed equally to this work. 00 MONTH 2017 | VOL 000 | NATURE | 1 © 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved. RESEARCH ARTICLE a Odinarchaeota ta Odinarchaeote LCB_4 Thorarchaeo Heimdallarchaeote T Heimdallarchaeote LC_2 Thorarchaeote WOR_ Thorarchaeote imdallarchaeo horarchaeote e Lokiarcha 5 H AB_2 Thorarchaeote ta Heimdallarchaeote LC_3 c W OR_8 AB_125 e ote CR_4 ote 84 45 3 100 97 100 74 41 100 94 100 100 TACK 82 100 Bathyarchaeota 100 91 Odinarchaeote RP_19 Korarchaeota 87 Odinarchaeote LCB_4 Crenarchaeota 85 AigarchaeotaThaumarchaeota Euryarchaeota 52 Figure 1 | Identification and phylogenomics of Asgard archaea. LC Lokiar LCB a 28 100 LokiarchaeoteLokiarchaeum CR_4 sp. GC14_75 , Maximum-likelihood tree, inferred with RAxML and PROTCATLG CR model, based on metagenomic contigs containing conserved ribosomal WOR 46 RP proteins (see Methods) revealing the Asgard superphylum. Slow, non- chaeota 42 AB, 0.25 m.b.s.f. parametric maximum-likelihood bootstrap support values above 50 and 0.3 AB, 0.5 m.b.s.f. 90 are indicated with empty and filled circles, respectively. Abbreviations AB, 1.25 m.b.s.f. Thorarchaeote AB_25 AB, 1.75 m.b.s.f. of the sites mentioned are as follows: LC, Loki’s Castle; CR, Colorado100 River aquifer (USA); LCB, Lower Culex Basin (Yellowstone National Park, Thorarchaeote WOR_83 USA); WOR, White Oak River (USA); AB: Aarhus Bay (Denmark); RP, 0.1 Radiata Pool (New Zealand); m.b.s.f., metres below sea floor. b Heimdallarchaeote LC_3 inference of 55 concatenated archaeo-eukaryotic ribosomal proteins Heimdallarchaeote AB_125 inferred with PhyloBayes and CAT-GTR model (b likelihood analysis of concatenated small and large subunit rRNA gene Heimdallarchaeote LC_2 Lokiarchaeum d and Thorarchaeota sp. GC14_75 that were only distantly related but still part of the same archaeal clade ( Fig. 1a). We decided to name this archaeal clade Asgard, after the realm of the gods in Norse mythology. Apart from Lokiarchaeota- and Thorarchaeota-related lineages, we could define two additional b candidate phyla in the Asgard clade, which we hereafter refer to as Odinarchaeota and Heimdallarchaeota (Supplementary Table 3, Lokiarchaeum sp. GC14_75 Supplementary Discussion 1). Whereas contigs from Odinarchaeota Lokiarchaeote CR_4 0.94 0.99 were exclusively identified in hot spring metagenomes (Yellowstone Odinarchaeote LCB_4 National Park and Radiata Pool), contigs from Heimdallarchaeota were Thorarchaeote AB_25 0.94 detected in marine sediments (Loki’s Castle and Aarhus© 2017 Bay; Fig. Macmillan 1a). Publishers Limited, part of Springer Nature. All rights reserved.Eukarya Thorarchaeote WOR_45 0.98 23 1 1 novel Asgard lineages, contigs were binned into metagenome- Thorarchaeote WOR_83 To analyse the genomic content and evolutionary history
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