Three-dimensional genome architecture persists in a 52,000-year-old woolly mammoth skin sample.

Hi-C X inactivation ancient DNA chromatin loops fossil genome architecture genome assembly glass transition vitrification woolly mammoth

Journal

Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066

Informations de publication

Date de publication:
11 Jul 2024
Historique:
received: 30 06 2023
revised: 07 03 2024
accepted: 03 06 2024
medline: 13 7 2024
pubmed: 13 7 2024
entrez: 12 7 2024
Statut: ppublish

Résumé

Analyses of ancient DNA typically involve sequencing the surviving short oligonucleotides and aligning to genome assemblies from related, modern species. Here, we report that skin from a female woolly mammoth (†Mammuthus primigenius) that died 52,000 years ago retained its ancient genome architecture. We use PaleoHi-C to map chromatin contacts and assemble its genome, yielding 28 chromosome-length scaffolds. Chromosome territories, compartments, loops, Barr bodies, and inactive X chromosome (Xi) superdomains persist. The active and inactive genome compartments in mammoth skin more closely resemble Asian elephant skin than other elephant tissues. Our analyses uncover new biology. Differences in compartmentalization reveal genes whose transcription was potentially altered in mammoths vs. elephants. Mammoth Xi has a tetradic architecture, not bipartite like human and mouse. We hypothesize that, shortly after this mammoth's death, the sample spontaneously freeze-dried in the Siberian cold, leading to a glass transition that preserved subfossils of ancient chromosomes at nanometer scale.

Identifiants

pubmed: 38996487
pii: S0092-8674(24)00642-1
doi: 10.1016/j.cell.2024.06.002
pii:
doi:

Substances chimiques

Chromatin 0
DNA, Ancient 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

3541-3562.e51

Informations de copyright

Copyright © 2024 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests E.L.A., M.T.P.G., and L.D. are on the scientific advisory board of Colossal Biosciences and hold stock options. From 2021 to 2023, M.A.M.-R. received consulting honoraria from Acuity Spatial Genomics. E.L.A. and O.D. are inventors on US provisional patent applications 16/308,386 (E.L.A. and O.D., filed 12/7/2018), 16/247,502 (E.L.A. and O.D., 1/14/2019), and PCT/US2020/064704 (E.L.A., 12/11/2020) by the Baylor College of Medicine and the Broad Institute, relating to the assembly methods in this manuscript.

Auteurs

Marcela Sandoval-Velasco (M)

Center for Evolutionary Hologenomics, University of Copenhagen, DK-1353 Copenhagen, Denmark.

Olga Dudchenko (O)

The Center for Genome Architecture and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA; Center for Theoretical Biological Physics, Rice University, Houston, TX 77030, USA. Electronic address: olga.dudchenko@bcm.edu.

Juan Antonio Rodríguez (JA)

Center for Evolutionary Hologenomics, University of Copenhagen, DK-1353 Copenhagen, Denmark; Centre Nacional d'Anàlisi Genòmica, CNAG, 08028 Barcelona, Spain.

Cynthia Pérez Estrada (C)

The Center for Genome Architecture and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA; Center for Theoretical Biological Physics, Rice University, Houston, TX 77030, USA.

Marianne Dehasque (M)

Centre for Palaeogenetics, SE-106 91 Stockholm, Sweden; Department of Bioinformatics and Genetics, Swedish Museum of Natural History, 10405 Stockholm, Sweden; Department of Zoology, Stockholm University, SE-106 91 Stockholm, Sweden.

Claudia Fontsere (C)

Center for Evolutionary Hologenomics, University of Copenhagen, DK-1353 Copenhagen, Denmark.

Sarah S T Mak (SST)

Center for Evolutionary Hologenomics, University of Copenhagen, DK-1353 Copenhagen, Denmark.

Ruqayya Khan (R)

The Center for Genome Architecture and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

Vinícius G Contessoto (VG)

Center for Theoretical Biological Physics, Rice University, Houston, TX 77030, USA.

Antonio B Oliveira Junior (AB)

Center for Theoretical Biological Physics, Rice University, Houston, TX 77030, USA.

Achyuth Kalluchi (A)

Department of Genetics, Cell Biology and Anatomy, University of Nebraska Medical Center, Omaha, NE 68198, USA.

Bernardo J Zubillaga Herrera (BJ)

Department of Physics, Northeastern University, Boston, MA 02115, USA; Center for Theoretical Biological Physics, Northeastern University, Boston, MA 02215, USA.

Jiyun Jeong (J)

The Center for Genome Architecture and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

Renata P Roy (RP)

The Center for Genome Architecture and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA; Center for Theoretical Biological Physics, Rice University, Houston, TX 77030, USA; Departments of Biology and Physics, Texas Southern University, Houston, TX 77004, USA.

Ishawnia Christopher (I)

The Center for Genome Architecture and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

David Weisz (D)

The Center for Genome Architecture and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

Arina D Omer (AD)

The Center for Genome Architecture and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

Sanjit S Batra (SS)

The Center for Genome Architecture and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

Muhammad S Shamim (MS)

The Center for Genome Architecture and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

Neva C Durand (NC)

The Center for Genome Architecture and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA; Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA.

Brendan O'Connell (B)

Department of Biomolecular Engineering, University of California, Santa Cruz, Santa Cruz, CA 95064, USA; Department of Molecular and Medical Genetics, Oregon Health & Science University, Portland, OR 97239, USA.

Alfred L Roca (AL)

Department of Animal Sciences and Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.

Maksim V Plikus (MV)

Department of Developmental and Cell Biology, University of California, Irvine, Irvine, CA 92697, USA.

Mariya A Kusliy (MA)

Institute of Molecular and Cellular Biology SB RAS, Novosibirsk 630090, Russia.

Svetlana A Romanenko (SA)

Institute of Molecular and Cellular Biology SB RAS, Novosibirsk 630090, Russia.

Natalya A Lemskaya (NA)

Institute of Molecular and Cellular Biology SB RAS, Novosibirsk 630090, Russia.

Natalya A Serdyukova (NA)

Institute of Molecular and Cellular Biology SB RAS, Novosibirsk 630090, Russia.

Svetlana A Modina (SA)

Institute of Molecular and Cellular Biology SB RAS, Novosibirsk 630090, Russia.

Polina L Perelman (PL)

Institute of Molecular and Cellular Biology SB RAS, Novosibirsk 630090, Russia.

Elena A Kizilova (EA)

Institute of Cytology and Genetics SB RAS, Novosibirsk 630090, Russia.

Sergei I Baiborodin (SI)

Institute of Cytology and Genetics SB RAS, Novosibirsk 630090, Russia.

Nikolai B Rubtsov (NB)

Institute of Cytology and Genetics SB RAS, Novosibirsk 630090, Russia.

Gur Machol (G)

The Center for Genome Architecture and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

Krisha Rath (K)

The Center for Genome Architecture and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

Ragini Mahajan (R)

The Center for Genome Architecture and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA; Center for Theoretical Biological Physics, Rice University, Houston, TX 77030, USA; Department of Biosciences, Rice University, Houston, TX 77005, USA.

Parwinder Kaur (P)

UWA School of Agriculture and Environment, University of Western Australia, Perth, WA 6009, Australia.

Andreas Gnirke (A)

Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA.

Isabel Garcia-Treviño (I)

San Antonio Zoo, San Antonio, TX 78212, USA.

Rob Coke (R)

San Antonio Zoo, San Antonio, TX 78212, USA.

Joseph P Flanagan (JP)

Houston Zoo, Houston, TX 77030, USA.

Kelcie Pletch (K)

Houston Zoo, Houston, TX 77030, USA.

Aurora Ruiz-Herrera (A)

Departament de Biologia Cel·lular, Fisiologia i Immunologia and Genome Integrity and Instability Group, Institut de Biotecnologia i Biomedicina, Universitat Autònoma de Barcelona, 08193 Cerdanyola del Vallès, Spain.

Valerii Plotnikov (V)

Academy of Sciences of Sakha Republic, Yakutsk 677000, Russia.

Innokentiy S Pavlov (IS)

Academy of Sciences of Sakha Republic, Yakutsk 677000, Russia.

Naryya I Pavlova (NI)

Institute of Biological Problems of Cryolitezone SB RAS, Yakutsk 677000, Russia.

Albert V Protopopov (AV)

Academy of Sciences of Sakha Republic, Yakutsk 677000, Russia; North-Eastern Federal University, Yakutsk 677027, Russia.

Michele Di Pierro (M)

Department of Physics, Northeastern University, Boston, MA 02115, USA; Center for Theoretical Biological Physics, Northeastern University, Boston, MA 02215, USA.

Alexander S Graphodatsky (AS)

Institute of Molecular and Cellular Biology SB RAS, Novosibirsk 630090, Russia.

Eric S Lander (ES)

Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Department of Systems Biology, Harvard Medical School, Boston, MA 02115, USA; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.

M Jordan Rowley (MJ)

Department of Genetics, Cell Biology and Anatomy, University of Nebraska Medical Center, Omaha, NE 68198, USA.

Peter G Wolynes (PG)

Center for Theoretical Biological Physics, Rice University, Houston, TX 77030, USA; Department of Biosciences, Rice University, Houston, TX 77005, USA; Departments of Physics, Astronomy, & Chemistry, Rice University, Houston, TX 77005, USA.

José N Onuchic (JN)

Center for Theoretical Biological Physics, Rice University, Houston, TX 77030, USA; Department of Biosciences, Rice University, Houston, TX 77005, USA; Departments of Physics, Astronomy, & Chemistry, Rice University, Houston, TX 77005, USA.

Love Dalén (L)

Centre for Palaeogenetics, SE-106 91 Stockholm, Sweden; Department of Bioinformatics and Genetics, Swedish Museum of Natural History, 10405 Stockholm, Sweden; Department of Zoology, Stockholm University, SE-106 91 Stockholm, Sweden.

Marc A Marti-Renom (MA)

Centre Nacional d'Anàlisi Genòmica, CNAG, 08028 Barcelona, Spain; Centre for Genomic Regulation, The Barcelona Institute for Science and Technology, 08003 Barcelona, Spain; ICREA, 08010 Barcelona, Spain; Universitat Pompeu Fabra, 08002 Barcelona, Spain. Electronic address: martirenom@cnag.eu.

M Thomas P Gilbert (MTP)

Center for Evolutionary Hologenomics, University of Copenhagen, DK-1353 Copenhagen, Denmark; University Museum NTNU, 7012 Trondheim, Norway. Electronic address: tgilbert@sund.ku.dk.

Erez Lieberman Aiden (EL)

The Center for Genome Architecture and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA; Center for Theoretical Biological Physics, Rice University, Houston, TX 77030, USA; Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA. Electronic address: erez@erez.com.

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