Fold Evolution before LUCA: Common Ancestry of SH3 Domains and OB Domains
Abstract SH3 and OB are the simplest, oldest, and most common protein domains within the translation system. SH3 and OB domains are β-barrels that are structurally similar but are topologically distinct. To transform an OB domain to a SH3 domain, β-strands must be permuted in a multistep and evoluti...
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Veröffentlicht in: | Molecular biology and evolution 2021-11, Vol.38 (11), p.5134-5143 |
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creator | Alvarez-Carreño, Claudia Penev, Petar I Petrov, Anton S Williams, Loren Dean |
description | Abstract
SH3 and OB are the simplest, oldest, and most common protein domains within the translation system. SH3 and OB domains are β-barrels that are structurally similar but are topologically distinct. To transform an OB domain to a SH3 domain, β-strands must be permuted in a multistep and evolutionarily implausible mechanism. Here, we explored relationships between SH3 and OB domains of ribosomal proteins, initiation, and elongation factors using a combined sequence- and structure-based approach. We detect a common core of SH3 and OB domains, as a region of significant structure and sequence similarity. The common core contains four β-strands and a loop, but omits the fifth β-strand, which is variable and is absent from some OB and SH3 domain proteins. The structure of the common core immediately suggests a simple permutation mechanism for interconversion between SH3 and OB domains, which appear to share an ancestor. The OB domain was formed by duplication and adaptation of the SH3 domain core, or vice versa, in a simple and probable transformation. By employing the folding algorithm AlphaFold2, we demonstrated that an ancestral reconstruction of a permuted SH3 sequence folds into an OB structure, and an ancestral reconstruction of a permuted OB sequence folds into a SH3 structure. The tandem SH3 and OB domains in the universal ribosomal protein uL2 share a common ancestor, suggesting that the divergence of these two domains occurred before the last universal common ancestor. |
doi_str_mv | 10.1093/molbev/msab240 |
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SH3 and OB are the simplest, oldest, and most common protein domains within the translation system. SH3 and OB domains are β-barrels that are structurally similar but are topologically distinct. To transform an OB domain to a SH3 domain, β-strands must be permuted in a multistep and evolutionarily implausible mechanism. Here, we explored relationships between SH3 and OB domains of ribosomal proteins, initiation, and elongation factors using a combined sequence- and structure-based approach. We detect a common core of SH3 and OB domains, as a region of significant structure and sequence similarity. The common core contains four β-strands and a loop, but omits the fifth β-strand, which is variable and is absent from some OB and SH3 domain proteins. The structure of the common core immediately suggests a simple permutation mechanism for interconversion between SH3 and OB domains, which appear to share an ancestor. The OB domain was formed by duplication and adaptation of the SH3 domain core, or vice versa, in a simple and probable transformation. By employing the folding algorithm AlphaFold2, we demonstrated that an ancestral reconstruction of a permuted SH3 sequence folds into an OB structure, and an ancestral reconstruction of a permuted OB sequence folds into a SH3 structure. The tandem SH3 and OB domains in the universal ribosomal protein uL2 share a common ancestor, suggesting that the divergence of these two domains occurred before the last universal common ancestor.</description><identifier>ISSN: 0737-4038</identifier><identifier>EISSN: 1537-1719</identifier><identifier>DOI: 10.1093/molbev/msab240</identifier><identifier>PMID: 34383917</identifier><language>eng</language><publisher>United States: Oxford University Press</publisher><subject>Amino Acid Sequence ; Discoveries ; Models, Molecular ; Protein structure prediction ; Proteins ; Ribosomal Proteins - genetics ; Sequence Alignment ; src Homology Domains - genetics</subject><ispartof>Molecular biology and evolution, 2021-11, Vol.38 (11), p.5134-5143</ispartof><rights>The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. 2021</rights><rights>The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.</rights><rights>COPYRIGHT 2021 Oxford University Press</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c463t-c94c3308d394666aac5903df4f1cde7fcdc174fffe894cd878fe18afc1f523923</citedby><cites>FETCH-LOGICAL-c463t-c94c3308d394666aac5903df4f1cde7fcdc174fffe894cd878fe18afc1f523923</cites><orcidid>0000-0002-1827-8946 ; 0000-0003-3359-7299 ; 0000-0002-7215-4194 ; 0000-0002-9027-3824</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8557408/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8557408/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,1604,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34383917$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Rogers, Rebekah</contributor><creatorcontrib>Alvarez-Carreño, Claudia</creatorcontrib><creatorcontrib>Penev, Petar I</creatorcontrib><creatorcontrib>Petrov, Anton S</creatorcontrib><creatorcontrib>Williams, Loren Dean</creatorcontrib><title>Fold Evolution before LUCA: Common Ancestry of SH3 Domains and OB Domains</title><title>Molecular biology and evolution</title><addtitle>Mol Biol Evol</addtitle><description>Abstract
SH3 and OB are the simplest, oldest, and most common protein domains within the translation system. SH3 and OB domains are β-barrels that are structurally similar but are topologically distinct. To transform an OB domain to a SH3 domain, β-strands must be permuted in a multistep and evolutionarily implausible mechanism. Here, we explored relationships between SH3 and OB domains of ribosomal proteins, initiation, and elongation factors using a combined sequence- and structure-based approach. We detect a common core of SH3 and OB domains, as a region of significant structure and sequence similarity. The common core contains four β-strands and a loop, but omits the fifth β-strand, which is variable and is absent from some OB and SH3 domain proteins. The structure of the common core immediately suggests a simple permutation mechanism for interconversion between SH3 and OB domains, which appear to share an ancestor. The OB domain was formed by duplication and adaptation of the SH3 domain core, or vice versa, in a simple and probable transformation. By employing the folding algorithm AlphaFold2, we demonstrated that an ancestral reconstruction of a permuted SH3 sequence folds into an OB structure, and an ancestral reconstruction of a permuted OB sequence folds into a SH3 structure. The tandem SH3 and OB domains in the universal ribosomal protein uL2 share a common ancestor, suggesting that the divergence of these two domains occurred before the last universal common ancestor.</description><subject>Amino Acid Sequence</subject><subject>Discoveries</subject><subject>Models, Molecular</subject><subject>Protein structure prediction</subject><subject>Proteins</subject><subject>Ribosomal Proteins - genetics</subject><subject>Sequence Alignment</subject><subject>src Homology Domains - genetics</subject><issn>0737-4038</issn><issn>1537-1719</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNqFkctPAyEQxonRaK1ePRqOemiFAgvrwaTWZ9LEg3omlIdiFqhLt0n_ezGtr5PhMMzMb77M5APgCKMhRjU5C6mZ2eVZyGo2omgL9DAjfIA5rrdBD_Hyp4iIPbCf8xtCmNKq2gV7hBJBasx74P4mNQZeL1PTLXyKcGZdai2cPk_G53CSQii1cdQ2L9oVTA4-3hF4lYLyMUMVDXy4_EoPwI5TTbaHm9gHzzfXT5O7wfTh9n4yng40rchioGuqCUHCkLrsUimlWY2IcdRhbSx32mjMqXPOikIawYWzWCinsWMjUo9IH1ysdefdLFijbVy0qpHz1gfVrmRSXv7tRP8qX9JSCsY4RaIInGwE2vTelctk8FnbplHRpi7LEaswFYJwVtDhGn1RjZU-ulQUdXnGBq9TtM6X-phzRilGDP0M6Dbl3Fr3vRdG8tMwuTZMbgwrA8e_r_nGvxwqwOkaSN38P7EPOh6h2w</recordid><startdate>20211101</startdate><enddate>20211101</enddate><creator>Alvarez-Carreño, Claudia</creator><creator>Penev, Petar I</creator><creator>Petrov, Anton S</creator><creator>Williams, Loren Dean</creator><general>Oxford University Press</general><scope>TOX</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-1827-8946</orcidid><orcidid>https://orcid.org/0000-0003-3359-7299</orcidid><orcidid>https://orcid.org/0000-0002-7215-4194</orcidid><orcidid>https://orcid.org/0000-0002-9027-3824</orcidid></search><sort><creationdate>20211101</creationdate><title>Fold Evolution before LUCA: Common Ancestry of SH3 Domains and OB Domains</title><author>Alvarez-Carreño, Claudia ; Penev, Petar I ; Petrov, Anton S ; Williams, Loren Dean</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c463t-c94c3308d394666aac5903df4f1cde7fcdc174fffe894cd878fe18afc1f523923</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Amino Acid Sequence</topic><topic>Discoveries</topic><topic>Models, Molecular</topic><topic>Protein structure prediction</topic><topic>Proteins</topic><topic>Ribosomal Proteins - genetics</topic><topic>Sequence Alignment</topic><topic>src Homology Domains - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Alvarez-Carreño, Claudia</creatorcontrib><creatorcontrib>Penev, Petar I</creatorcontrib><creatorcontrib>Petrov, Anton S</creatorcontrib><creatorcontrib>Williams, Loren Dean</creatorcontrib><collection>Oxford Journals Open Access Collection</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular biology and evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Alvarez-Carreño, Claudia</au><au>Penev, Petar I</au><au>Petrov, Anton S</au><au>Williams, Loren Dean</au><au>Rogers, Rebekah</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Fold Evolution before LUCA: Common Ancestry of SH3 Domains and OB Domains</atitle><jtitle>Molecular biology and evolution</jtitle><addtitle>Mol Biol Evol</addtitle><date>2021-11-01</date><risdate>2021</risdate><volume>38</volume><issue>11</issue><spage>5134</spage><epage>5143</epage><pages>5134-5143</pages><issn>0737-4038</issn><eissn>1537-1719</eissn><abstract>Abstract
SH3 and OB are the simplest, oldest, and most common protein domains within the translation system. SH3 and OB domains are β-barrels that are structurally similar but are topologically distinct. To transform an OB domain to a SH3 domain, β-strands must be permuted in a multistep and evolutionarily implausible mechanism. Here, we explored relationships between SH3 and OB domains of ribosomal proteins, initiation, and elongation factors using a combined sequence- and structure-based approach. We detect a common core of SH3 and OB domains, as a region of significant structure and sequence similarity. The common core contains four β-strands and a loop, but omits the fifth β-strand, which is variable and is absent from some OB and SH3 domain proteins. The structure of the common core immediately suggests a simple permutation mechanism for interconversion between SH3 and OB domains, which appear to share an ancestor. The OB domain was formed by duplication and adaptation of the SH3 domain core, or vice versa, in a simple and probable transformation. By employing the folding algorithm AlphaFold2, we demonstrated that an ancestral reconstruction of a permuted SH3 sequence folds into an OB structure, and an ancestral reconstruction of a permuted OB sequence folds into a SH3 structure. The tandem SH3 and OB domains in the universal ribosomal protein uL2 share a common ancestor, suggesting that the divergence of these two domains occurred before the last universal common ancestor.</abstract><cop>United States</cop><pub>Oxford University Press</pub><pmid>34383917</pmid><doi>10.1093/molbev/msab240</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-1827-8946</orcidid><orcidid>https://orcid.org/0000-0003-3359-7299</orcidid><orcidid>https://orcid.org/0000-0002-7215-4194</orcidid><orcidid>https://orcid.org/0000-0002-9027-3824</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Amino Acid Sequence Discoveries Models, Molecular Protein structure prediction Proteins Ribosomal Proteins - genetics Sequence Alignment src Homology Domains - genetics |
title | Fold Evolution before LUCA: Common Ancestry of SH3 Domains and OB Domains |
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