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Comparative proteogenomics deciphers the origin and evolution of eukaryotic chromatin

View ORCID ProfileXavier Grau-Bové, View ORCID ProfileCristina Navarrete, View ORCID ProfileCristina Chiva, View ORCID ProfileThomas Pribasnig, Meritxell Antó, View ORCID ProfileGuifré Torruella, View ORCID ProfileLuis Javier Galindo, View ORCID ProfileBernd Franz Lang, View ORCID ProfileDavid Moreira, View ORCID ProfilePurificación López-Garcia, View ORCID ProfileIñaki Ruiz-Trillo, View ORCID ProfileChrista Schleper, View ORCID ProfileEduard Sabidó, View ORCID ProfileArnau Sebé-Pedrós
doi: https://doi.org/10.1101/2021.11.30.470311
Xavier Grau-Bové
1Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Barcelona 08003, Catalonia, Spain
2Universitat Pompeu Fabra (UPF), Barcelona 08003, Catalonia, Spain
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  • ORCID record for Xavier Grau-Bové
Cristina Navarrete
1Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Barcelona 08003, Catalonia, Spain
2Universitat Pompeu Fabra (UPF), Barcelona 08003, Catalonia, Spain
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Cristina Chiva
2Universitat Pompeu Fabra (UPF), Barcelona 08003, Catalonia, Spain
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  • ORCID record for Cristina Chiva
Thomas Pribasnig
3Department of Functional and Evolutionary Ecology, Archaea Biology Unit, University of Vienna, Djerassi-platz 1, 1030 Vienna, Austria
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Meritxell Antó
4Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta, 37-49, Barcelona 08003, Catalonia, Spain.
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Guifré Torruella
5Unité d’Ecologie Systématique et Evolution, CNRS, Université Paris-Saclay, AgroParisTech, Orsay, France
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Luis Javier Galindo
5Unité d’Ecologie Systématique et Evolution, CNRS, Université Paris-Saclay, AgroParisTech, Orsay, France
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Bernd Franz Lang
6Department of Biochemistry, Robert Cedergren Centre, Université de Montréal, Montréal, Quebec H3C 3J7, Canada
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David Moreira
5Unité d’Ecologie Systématique et Evolution, CNRS, Université Paris-Saclay, AgroParisTech, Orsay, France
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Purificación López-Garcia
5Unité d’Ecologie Systématique et Evolution, CNRS, Université Paris-Saclay, AgroParisTech, Orsay, France
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Iñaki Ruiz-Trillo
4Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta, 37-49, Barcelona 08003, Catalonia, Spain.
7ICREA, Pg. Lluís Companys 23, Barcelona 08010, Catalonia, Spain.
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Christa Schleper
3Department of Functional and Evolutionary Ecology, Archaea Biology Unit, University of Vienna, Djerassi-platz 1, 1030 Vienna, Austria
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Eduard Sabidó
1Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Barcelona 08003, Catalonia, Spain
2Universitat Pompeu Fabra (UPF), Barcelona 08003, Catalonia, Spain
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Arnau Sebé-Pedrós
1Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Barcelona 08003, Catalonia, Spain
2Universitat Pompeu Fabra (UPF), Barcelona 08003, Catalonia, Spain
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  • For correspondence: arnau.sebe@crg.eu
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Abstract

Histones and associated chromatin proteins have essential functions in eukaryotic genome organization and regulation. Despite this fundamental role in eukaryotic cell biology, we lack a phylogenetically-comprehensive understanding of chromatin evolution. Here, we combine comparative proteomics and genomics analysis of chromatin in eukaryotes and archaea. Proteomics uncovers the existence of histone post-translational modifications in Archaea. However, archaeal histone modifications are scarce, in contrast with the highly conserved and abundant marks we identify across eukaryotes. Phylogenetic analysis reveals that chromatin-associated catalytic functions (e.g., methyltransferases) have pre-eukaryotic origins, whereas histone mark readers and chaperones are eukaryotic innovations. We show that further chromatin evolution is characterized by expansion of readers, including capture by transposable elements and viruses. Overall, our study infers detailed evolutionary history of eukaryotic chromatin: from its archaeal roots, through the emergence of nucleosome-based regulation in the eukaryotic ancestor, to the diversification of chromatin regulators and their hijacking by genomic parasites.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://github.com/sebepedroslab/chromatin-evolution-analysis

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted December 01, 2021.
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Comparative proteogenomics deciphers the origin and evolution of eukaryotic chromatin
Xavier Grau-Bové, Cristina Navarrete, Cristina Chiva, Thomas Pribasnig, Meritxell Antó, Guifré Torruella, Luis Javier Galindo, Bernd Franz Lang, David Moreira, Purificación López-Garcia, Iñaki Ruiz-Trillo, Christa Schleper, Eduard Sabidó, Arnau Sebé-Pedrós
bioRxiv 2021.11.30.470311; doi: https://doi.org/10.1101/2021.11.30.470311
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Comparative proteogenomics deciphers the origin and evolution of eukaryotic chromatin
Xavier Grau-Bové, Cristina Navarrete, Cristina Chiva, Thomas Pribasnig, Meritxell Antó, Guifré Torruella, Luis Javier Galindo, Bernd Franz Lang, David Moreira, Purificación López-Garcia, Iñaki Ruiz-Trillo, Christa Schleper, Eduard Sabidó, Arnau Sebé-Pedrós
bioRxiv 2021.11.30.470311; doi: https://doi.org/10.1101/2021.11.30.470311

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