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Unique mobile elements and scalable gene flow at the prokaryote–eukaryote boundary revealed by circularized Asgard archaea genomes

Wu, Fabai and Speth, Daan R. and Philosof, Alon and Crémière, Antoine and Narayanan, Aditi and Barco, Roman A. and Connon, Stephanie A. and Amend, Jan P. and Antoshechkin, Igor A. and Orphan, Victoria J. (2022) Unique mobile elements and scalable gene flow at the prokaryote–eukaryote boundary revealed by circularized Asgard archaea genomes. Nature Microbiology, 7 (2). pp. 200-212. ISSN 2058-5276. doi:10.1038/s41564-021-01039-y. https://resolver.caltech.edu/CaltechAUTHORS:20220118-973186300

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[img] Image (JPEG) (Extended Data Fig. 1: The emergence of Ca. Heimdallarchaeum endolithica belonging to the Ancient Archaea Group of Heimdallarchaeota in a series of incubations derived from the same rock originated from Pescadero basin) - Supplemental Material
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Abstract

Eukaryotic genomes are known to have garnered innovations from both archaeal and bacterial domains but the sequence of events that led to the complex gene repertoire of eukaryotes is largely unresolved. Here, through the enrichment of hydrothermal vent microorganisms, we recovered two circularized genomes of Heimdallarchaeum species that belong to an Asgard archaea clade phylogenetically closest to eukaryotes. These genomes reveal diverse mobile elements, including an integrative viral genome that bidirectionally replicates in a circular form and aloposons, transposons that encode the 5,000 amino acid-sized proteins Otus and Ephialtes. Heimdallaechaeal mobile elements have garnered various genes from bacteria and bacteriophages, likely playing a role in shuffling functions across domains. The number of archaea- and bacteria-related genes follow strikingly different scaling laws in Asgard archaea, exhibiting a genome size-dependent ratio and a functional division resembling the bacteria- and archaea-derived gene repertoire across eukaryotes. Bacterial gene import has thus likely been a continuous process unaltered by eukaryogenesis and scaled up through genome expansion. Our data further highlight the importance of viewing eukaryogenesis in a pan-Asgard context, which led to the proposal of a conceptual framework, that is, the Heimdall nucleation–decentralized innovation–hierarchical import model that accounts for the emergence of eukaryotic complexity.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s41564-021-01039-yDOIArticle
https://www.ncbi.nlm.nih.gov/bioproject/PRJNA721962Related ItemData
https://github.com/dspeth/bioinfo_scripts/tree/master/phylogenyRelated ItemCode
https://github.com/wufabai/genomicsRelated ItemCode
ORCID:
AuthorORCID
Wu, Fabai0000-0001-5812-5621
Speth, Daan R.0000-0002-2361-5935
Philosof, Alon0000-0003-2684-8678
Crémière, Antoine0000-0001-7382-2097
Amend, Jan P.0000-0003-4953-7776
Antoshechkin, Igor A.0000-0002-9934-3040
Orphan, Victoria J.0000-0002-5374-6178
Additional Information:© The Author(s) 2022. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 12 May 2021; Accepted 29 November 2021; Published 13 January 2022. We thank W. Fischer for critical comments on the manuscript, L. Kelly for advice on viral sequence analysis, A. Roger for discussions on phylogenetic methods and K. Makarova and E. Koonin for discussions on CRISPR–Cas systems. We thank the pilots, crew and participants on the cruises to the southern Pescadero Basin, FK181031 on R/V Falkor operated by the Schmidt Ocean Institute and NA091 on E/V Nautilus operated by the Ocean Exploration Trust, with NA091 supported by the Dalio Foundation and Woods Hole Oceanographic Institute. This research used samples provided by the Ocean Exploration Trust’s Nautilus Exploration Program, cruise NA091. We thank chief scientists S. Wankel and A. Michel for the opportunity to sail on NA091, Co-Chief Scientists D. Caress and R. Zierenberg on FK181031, and S. Wankel, A. Foulk and L. Marsh, R. Zierenberg and D. Cardace for assistance with shipboard processing of rock samples and J. Magyar and S. Goffredi for shipboard processing of sediment samples. Illumina library construction and Nanopore sequencing were performed at the Millard and Muriel Jacobs Genetics and Genomics Laboratory at Caltech. F.W. was supported by the Netherlands Organisation for Scientific Research Rubicon Award no. 019.162LW.037 and a Human Frontiers Science Program Long-term Fellowship no. LT000468/2017. D.R.S. was supported by the Netherlands Organisation for Scientific Research Rubicon Award no. 019.153LW.039 and the Caltech GPS Division Texaco Postdoctoral Fellowship. J.P.A. is funded by the National Science Foundation (NSF) no. OCE-1431598. V.J.O. is a Canadian Institute for Advanced Science fellow in the Earth 4D program. This research was supported by a Caltech Center for Evolutionary Science Pilot Grant (F.W. and V.J.O.), the NOMIS Foundation (V.J.O.), the Simons Foundation Principles of Microbial Ecosystems project (V.J.O.) and the NSF Center for Dark Energy Biosphere Investigations (no. OCE-0939564, V.J.O. and J.P.A.). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. Data availability: The assembled genomes and raw metagenomic sequencing reads can be found on the National Center for Biotechnology Information database under BioProject no. PRJNA721962. Source data are provided with this paper. Code availability: The custom script for recoding of amino acid sequences to four-state SR4 can be found at https://github.com/dspeth/bioinfo_scripts/tree/master/phylogeny. Other custom scripts can be found at https://github.com/wufabai/genomics. Author Contributions: F.W., D.R.S., A.C. and V.J.O. conceived the project. D.R.S. and V.J.O. collected the hydrothermal vent samples. F.W., D.R.S., A.C. and S.A.C. carried out the microbial incubations, periodic sampling, DNA extraction, sulphide analyses and amplicon sequencing. I.A.A. and A.N. prepared the Illumina sequencing libraries. I.A.A. performed the Oxford Nanopore sequencing. F.W., I.A.A. and A.P. assembled the Asgard archaea genomes. D.R.S. performed the phylogenomic analyses, protein clustering and overall bioinformatics platform support. R.A.B. performed the ANI/AAI analyses and taxonomic evaluation. F.W., D.R.S. and A.P. annotated the genomes. F.W. performed the PacBio HiFi 16S sequencing, protein phylogenetic analyses, marker HMM construction, comparative genomics, CRISPR/mobilome discovery, statistical analyses and wrote the paper. V.J.O. revised the paper. D.R.S., A.P., A.C., R.A.B. and J.P.A. provided critical comments on the paper. All authors read and approved the manuscript. V.J.O. and J.P.A. supervised the work. The authors declare no competing interests. Peer review information: Nature Microbiology thanks Brett Baker and the other, anonymous, reviewers for their contribution to the peer review of this work. Peer reviewer reports are available.
Funders:
Funding AgencyGrant Number
Dalio FoundationUNSPECIFIED
Woods Hole Oceanographic InstitutionUNSPECIFIED
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO)019.162LW.037
Human Frontier Science ProgramLT000468/2017
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO)019.153LW.039
Caltech Division of Geological and Planetary SciencesUNSPECIFIED
NSFOCE-1431598
Canadian Institute for Advanced Research (CIFAR)UNSPECIFIED
Caltech Center for Evolutionary ScienceUNSPECIFIED
NOMIS FoundationUNSPECIFIED
Simons FoundationUNSPECIFIED
NSFOCE-0939564
Subject Keywords:Ecology; Evolution
Issue or Number:2
DOI:10.1038/s41564-021-01039-y
Record Number:CaltechAUTHORS:20220118-973186300
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20220118-973186300
Official Citation:Wu, F., Speth, D.R., Philosof, A. et al. Unique mobile elements and scalable gene flow at the prokaryote–eukaryote boundary revealed by circularized Asgard archaea genomes. Nat Microbiol 7, 200–212 (2022). https://doi.org/10.1038/s41564-021-01039-y
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:112948
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:18 Jan 2022 22:36
Last Modified:08 Feb 2022 22:11

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