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 g...
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Veröffentlicht in: | Nature ecology & evolution 2022-07, Vol.6 (7), p.1007-1023 |
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creator | Grau-Bové, Xavier Navarrete, Cristina Chiva, Cristina Pribasnig, Thomas Antó, Meritxell Torruella, Guifré Galindo, Luis Javier Lang, Bernd Franz Moreira, David López-Garcia, Purificación Ruiz-Trillo, Iñaki Schleper, Christa Sabidó, Eduard Sebé-Pedrós, Arnau |
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.
Comparative genomics and proteomics of archaea and eukaryotes are used to explore the evolutionary history of eukaryotic chromatin, including modifications, catalytic functions and relationship with genomic parasites. |
doi_str_mv | 10.1038/s41559-022-01771-6 |
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Comparative genomics and proteomics of archaea and eukaryotes are used to explore the evolutionary history of eukaryotic chromatin, including modifications, catalytic functions and relationship with genomic parasites.</description><identifier>ISSN: 2397-334X</identifier><identifier>EISSN: 2397-334X</identifier><identifier>DOI: 10.1038/s41559-022-01771-6</identifier><identifier>PMID: 35680998</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/114 ; 631/181 ; 631/208/176 ; 631/208/212/748 ; 631/326/26 ; 82/58 ; Archaea ; Biological and Physical Anthropology ; Biomedical and Life Sciences ; Chromatin ; Ecology ; Eukaryotes ; Evolution ; Evolutionary Biology ; Evolutionary genetics ; Genomics ; Histones ; Life Sciences ; Paleontology ; Parasites ; Phylogenetics ; Phylogeny ; Post-translation ; Proteomics ; Zoology</subject><ispartof>Nature ecology & evolution, 2022-07, Vol.6 (7), p.1007-1023</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2022</rights><rights>2022. The Author(s), under exclusive licence to Springer Nature Limited.</rights><rights>The Author(s), under exclusive licence to Springer Nature Limited 2022.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c508t-2ebab1bd483e2e4401c13e98b5f3fd7baca0a229ca0fb36c414e942c93e7b3193</citedby><cites>FETCH-LOGICAL-c508t-2ebab1bd483e2e4401c13e98b5f3fd7baca0a229ca0fb36c414e942c93e7b3193</cites><orcidid>0000-0002-2594-7327 ; 0000-0002-9896-9746 ; 0000-0002-0927-0651 ; 0000-0003-1978-5824 ; 0000-0002-1918-2735 ; 0000-0002-6534-4758 ; 0000-0001-8150-6203 ; 0000-0003-3642-3200 ; 0000-0001-6506-7714 ; 0000-0002-4431-3784 ; 0000-0001-6547-5304 ; 0000-0002-2064-5354</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41559-022-01771-6$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41559-022-01771-6$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35680998$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-03847593$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Grau-Bové, Xavier</creatorcontrib><creatorcontrib>Navarrete, Cristina</creatorcontrib><creatorcontrib>Chiva, Cristina</creatorcontrib><creatorcontrib>Pribasnig, Thomas</creatorcontrib><creatorcontrib>Antó, Meritxell</creatorcontrib><creatorcontrib>Torruella, Guifré</creatorcontrib><creatorcontrib>Galindo, Luis Javier</creatorcontrib><creatorcontrib>Lang, Bernd Franz</creatorcontrib><creatorcontrib>Moreira, David</creatorcontrib><creatorcontrib>López-Garcia, Purificación</creatorcontrib><creatorcontrib>Ruiz-Trillo, Iñaki</creatorcontrib><creatorcontrib>Schleper, Christa</creatorcontrib><creatorcontrib>Sabidó, Eduard</creatorcontrib><creatorcontrib>Sebé-Pedrós, Arnau</creatorcontrib><title>A phylogenetic and proteomic reconstruction of eukaryotic chromatin evolution</title><title>Nature ecology & evolution</title><addtitle>Nat Ecol Evol</addtitle><addtitle>Nat Ecol Evol</addtitle><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.
Comparative genomics and proteomics of archaea and eukaryotes are used to explore the evolutionary history of eukaryotic chromatin, including modifications, catalytic functions and relationship with genomic parasites.</description><subject>631/114</subject><subject>631/181</subject><subject>631/208/176</subject><subject>631/208/212/748</subject><subject>631/326/26</subject><subject>82/58</subject><subject>Archaea</subject><subject>Biological and Physical Anthropology</subject><subject>Biomedical and Life Sciences</subject><subject>Chromatin</subject><subject>Ecology</subject><subject>Eukaryotes</subject><subject>Evolution</subject><subject>Evolutionary Biology</subject><subject>Evolutionary genetics</subject><subject>Genomics</subject><subject>Histones</subject><subject>Life Sciences</subject><subject>Paleontology</subject><subject>Parasites</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Post-translation</subject><subject>Proteomics</subject><subject>Zoology</subject><issn>2397-334X</issn><issn>2397-334X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>BENPR</sourceid><recordid>eNp9kU1P3DAQhq2qVUHAH-ihitRLewj4K_64VFqhFpAW9QISN8vxTnZDE3uxk5X493UI34eexvY88854XoS-EHxMMFMniZOq0iWmtMRESlKKD2ifMi1LxvjNx1fnPXSU0i3GE1ZpIT6jPVYJhbVW--hyUWw3911Yg4ehdYX1q2IbwwChz7cILvg0xNENbfBFaAoY_9p4HybUbWLo7dD6AnahGyfiEH1qbJfg6DEeoOvfv65Oz8vln7OL08WydBVWQ0mhtjWpV1wxoMA5Jo4w0KquGtasZG2dxZZSnUNTM-E44aA5dZqBrBnR7AD9nHW3Y93DyoEfou3MNrZ9ns4E25q3Gd9uzDrsjBSEYcazwI9ZYPOu7HyxNNNbXjHP22I7ktnvj81iuBshDaZvk4Ousx7CmAwVshJYcCUz-u0dehvG6PMqMqUqRalk0_R0plwMKUVonicg2Ezmmtlck801D-YakYu-vv7yc8mTlRlgM5Byyq8hvvT-j-w_sayxEQ</recordid><startdate>20220701</startdate><enddate>20220701</enddate><creator>Grau-Bové, Xavier</creator><creator>Navarrete, Cristina</creator><creator>Chiva, Cristina</creator><creator>Pribasnig, Thomas</creator><creator>Antó, Meritxell</creator><creator>Torruella, Guifré</creator><creator>Galindo, Luis Javier</creator><creator>Lang, Bernd Franz</creator><creator>Moreira, David</creator><creator>López-Garcia, Purificación</creator><creator>Ruiz-Trillo, Iñaki</creator><creator>Schleper, Christa</creator><creator>Sabidó, Eduard</creator><creator>Sebé-Pedrós, Arnau</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><general>Nature</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>8FE</scope><scope>8FH</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>BKSAR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M7P</scope><scope>PATMY</scope><scope>PCBAR</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PYCSY</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-2594-7327</orcidid><orcidid>https://orcid.org/0000-0002-9896-9746</orcidid><orcidid>https://orcid.org/0000-0002-0927-0651</orcidid><orcidid>https://orcid.org/0000-0003-1978-5824</orcidid><orcidid>https://orcid.org/0000-0002-1918-2735</orcidid><orcidid>https://orcid.org/0000-0002-6534-4758</orcidid><orcidid>https://orcid.org/0000-0001-8150-6203</orcidid><orcidid>https://orcid.org/0000-0003-3642-3200</orcidid><orcidid>https://orcid.org/0000-0001-6506-7714</orcidid><orcidid>https://orcid.org/0000-0002-4431-3784</orcidid><orcidid>https://orcid.org/0000-0001-6547-5304</orcidid><orcidid>https://orcid.org/0000-0002-2064-5354</orcidid></search><sort><creationdate>20220701</creationdate><title>A phylogenetic and proteomic reconstruction of eukaryotic chromatin evolution</title><author>Grau-Bové, Xavier ; 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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.
Comparative genomics and proteomics of archaea and eukaryotes are used to explore the evolutionary history of eukaryotic chromatin, including modifications, catalytic functions and relationship with genomic parasites.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>35680998</pmid><doi>10.1038/s41559-022-01771-6</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-2594-7327</orcidid><orcidid>https://orcid.org/0000-0002-9896-9746</orcidid><orcidid>https://orcid.org/0000-0002-0927-0651</orcidid><orcidid>https://orcid.org/0000-0003-1978-5824</orcidid><orcidid>https://orcid.org/0000-0002-1918-2735</orcidid><orcidid>https://orcid.org/0000-0002-6534-4758</orcidid><orcidid>https://orcid.org/0000-0001-8150-6203</orcidid><orcidid>https://orcid.org/0000-0003-3642-3200</orcidid><orcidid>https://orcid.org/0000-0001-6506-7714</orcidid><orcidid>https://orcid.org/0000-0002-4431-3784</orcidid><orcidid>https://orcid.org/0000-0001-6547-5304</orcidid><orcidid>https://orcid.org/0000-0002-2064-5354</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | 631/114 631/181 631/208/176 631/208/212/748 631/326/26 82/58 Archaea Biological and Physical Anthropology Biomedical and Life Sciences Chromatin Ecology Eukaryotes Evolution Evolutionary Biology Evolutionary genetics Genomics Histones Life Sciences Paleontology Parasites Phylogenetics Phylogeny Post-translation Proteomics Zoology |
title | A phylogenetic and proteomic reconstruction of eukaryotic chromatin evolution |
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