A phylogenetic and proteomic reconstruction of eukaryotic chromatin evolution
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 (for example, 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.
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Nature Publishing Group
2022-06-09
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| Subjects: | Archaea, Comparative genomics, Computational biology and bioinformatics, Epigenetics, Evolution, |
| Online Access: | http://hdl.handle.net/10261/279333 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100002809 http://dx.doi.org/10.13039/501100004837 http://dx.doi.org/10.13039/501100000038 |
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dig-ibe-es-10261-2793332022-12-23T10:44:32Z A phylogenetic and proteomic reconstruction of eukaryotic chromatin evolution Grau-Bové, Xavier Navarrete, Cristina Chiva, Cristina Pribasnig, Thomas Antó, Meritxell Torruella, Guifré Galindo, Luis Lang, B. Franz Moreira, David López-García, Purificación Ruiz-Trillo, Iñaki Schleper, Christa Sabidó, Eduard Sebé-Pedrós, Arnau European Commission Ministerio de Ciencia e Innovación (España) Generalitat de Catalunya Natural Sciences and Engineering Research Council of Canada Archaea Comparative genomics Computational biology and bioinformatics Epigenetics Evolution 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 (for example, 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. Research in the A.S.-P. group was supported by the European Research Council (ERC) under the European Union’s Horizon 2020 Research and Innovation Programme (grant agreement no. 851647) and the Spanish Ministry of Science and Innovation (PGC2018-098210-A-I00). We also acknowledge support of the Spanish Ministry of Science and Innovation to the EMBL partnership, the Centro de Excelencia Severo Ochoa and the CERCA Programme (Generalitat de Catalunya). C.N. is supported by an FPI PhD fellowship from the Spanish Ministry of Economy, Industry and Competitiveness (MEIC). X.G.-B. is supported by a Juan de la Cierva fellowship (FJC2018-036282-I) from MEIC. I.R.-T. was supported by a European Research Council (grant no. 616960). B.F.L. was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC; RGPIN-2017-05411) and by the ‘Fonds de Recherche Nature et Technologie’, Quebec. P.L.-G. and D.M. were supported by a Moore and Simons foundations grant (GBMF9739) and by European Research Council advanced grants (322669, 787904). Research in the C.S. group was supported by the ERC through project TACKLE (advanced grant no. 695192). Peer reviewed 2022-09-19T07:55:53Z 2022-09-19T07:55:53Z 2022-06-09 2022-09-19T07:55:53Z artículo doi: 10.1038/s41559-022-01771-6 issn: 2397-334X Nature Ecology and Evolution 6: 1007-1023 (2022) http://hdl.handle.net/10261/279333 10.1038/s41559-022-01771-6 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100002809 http://dx.doi.org/10.13039/501100004837 http://dx.doi.org/10.13039/501100000038 #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PGC2018-098210-A-I00/ES/UNA APROXIMACION GENOMICA Y PROTEOMICA AL ORIGEN Y EVOLUCION DE LA CROMATINA EUCARIOTA/ info:eu-repo/grantAgreement/EC/H2020/851647 info:eu-repo/grantAgreement/EC/H2020/322669 info:eu-repo/grantAgreement/EC/H2020/787904 info:eu-repo/grantAgreement/EC/H2020/695192 http://doi.org/10.1038/s41559-022-01771-6 Sí none Nature Publishing Group |
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Archaea Comparative genomics Computational biology and bioinformatics Epigenetics Evolution Archaea Comparative genomics Computational biology and bioinformatics Epigenetics Evolution |
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Archaea Comparative genomics Computational biology and bioinformatics Epigenetics Evolution Archaea Comparative genomics Computational biology and bioinformatics Epigenetics Evolution Grau-Bové, Xavier Navarrete, Cristina Chiva, Cristina Pribasnig, Thomas Antó, Meritxell Torruella, Guifré Galindo, Luis Lang, B. Franz Moreira, David López-García, Purificación Ruiz-Trillo, Iñaki Schleper, Christa Sabidó, Eduard Sebé-Pedrós, Arnau A phylogenetic and proteomic reconstruction of eukaryotic chromatin evolution |
| description |
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 (for example, 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. |
| author2 |
European Commission |
| author_facet |
European Commission Grau-Bové, Xavier Navarrete, Cristina Chiva, Cristina Pribasnig, Thomas Antó, Meritxell Torruella, Guifré Galindo, Luis Lang, B. Franz Moreira, David López-García, Purificación Ruiz-Trillo, Iñaki Schleper, Christa Sabidó, Eduard Sebé-Pedrós, Arnau |
| format |
artículo |
| topic_facet |
Archaea Comparative genomics Computational biology and bioinformatics Epigenetics Evolution |
| author |
Grau-Bové, Xavier Navarrete, Cristina Chiva, Cristina Pribasnig, Thomas Antó, Meritxell Torruella, Guifré Galindo, Luis Lang, B. Franz Moreira, David López-García, Purificación Ruiz-Trillo, Iñaki Schleper, Christa Sabidó, Eduard Sebé-Pedrós, Arnau |
| author_sort |
Grau-Bové, Xavier |
| title |
A phylogenetic and proteomic reconstruction of eukaryotic chromatin evolution |
| title_short |
A phylogenetic and proteomic reconstruction of eukaryotic chromatin evolution |
| title_full |
A phylogenetic and proteomic reconstruction of eukaryotic chromatin evolution |
| title_fullStr |
A phylogenetic and proteomic reconstruction of eukaryotic chromatin evolution |
| title_full_unstemmed |
A phylogenetic and proteomic reconstruction of eukaryotic chromatin evolution |
| title_sort |
phylogenetic and proteomic reconstruction of eukaryotic chromatin evolution |
| publisher |
Nature Publishing Group |
| publishDate |
2022-06-09 |
| url |
http://hdl.handle.net/10261/279333 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100002809 http://dx.doi.org/10.13039/501100004837 http://dx.doi.org/10.13039/501100000038 |
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