Duplication of Horizontally Acquired GH5_2 Enzymes Played a Central Role in the Evolution of Longhorned Beetles

Abstract The rise of functional diversity through gene duplication contributed to the adaption of organisms to various environments. Here we investigate the evolution of putative cellulases of the subfamily 2 of glycoside hydrolase family 5 (GH5_2) in the Cerambycidae (longhorned beetles), a megadiv...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Molecular biology and evolution 2022-06, Vol.39 (6)
Hauptverfasser: Shin, Na Ra, Doucet, Daniel, Pauchet, Yannick
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page
container_issue 6
container_start_page
container_title Molecular biology and evolution
container_volume 39
creator Shin, Na Ra
Doucet, Daniel
Pauchet, Yannick
description Abstract The rise of functional diversity through gene duplication contributed to the adaption of organisms to various environments. Here we investigate the evolution of putative cellulases of the subfamily 2 of glycoside hydrolase family 5 (GH5_2) in the Cerambycidae (longhorned beetles), a megadiverse assemblage of mostly xylophagous beetles. Cerambycidae originally acquired GH5_2 from a bacterial donor through horizontal gene transfer (HGT), and extant species harbor multiple copies that arose from gene duplication. We ask how these digestive enzymes contributed to the ability of these beetles to feed on wood. We analyzed 113 GH5_2, including the functional characterization of 52 of them, derived from 25 species covering most subfamilies of Cerambycidae. Ancestral gene duplications led to five well-defined groups with distinct substrate specificity, allowing these beetles to break down, in addition to cellulose, polysaccharides that are abundant in plant cell walls (PCWs), namely, xyloglucan, xylan, and mannans. Resurrecting the ancestral enzyme originally acquired by HGT, we show it was a cellulase that was able to break down glucomannan and xylan. Finally, recent gene duplications further expanded the catalytic repertoire of cerambycid GH5_2, giving rise to enzymes that favor transglycosylation over hydrolysis. We suggest that HGT and gene duplication, which shaped the evolution of GH5_2, played a central role in the ability of cerambycid beetles to use a PCW-rich diet and may have contributed to their successful radiation.
doi_str_mv 10.1093/molbev/msac128
format Article
fullrecord <record><control><sourceid>gale_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9246334</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A775003422</galeid><oup_id>10.1093/molbev/msac128</oup_id><sourcerecordid>A775003422</sourcerecordid><originalsourceid>FETCH-LOGICAL-c463t-c5ddc4d391197e0e736b1676c2dead5bd699968c0c7cd2a747790c31dce0ee353</originalsourceid><addsrcrecordid>eNqFkc1vEzEUxC1ERdPClSPyEQ5p_bFrry9IaQgNUiQQgrPl2G8TI6-drncjpX99DUkLnCofbI1_bzRPg9BbSq4oUfy6S2EN--suG0tZ8wJNaM3llEqqXqIJkeVdEd6co4ucfxFCq0qIV-ic11LwhjYTlD6Nu-CtGXyKOLV4mXp_n-JgQjjgmb0bfQ8O3y5rzfAi3h86yPhbMIciGjyHOPQm4O8pAPYRD1vAi30K46PbKsXNNvWx0DcAQ4D8Gp21JmR4c7ov0c_Pix_z5XT19fbLfLaa2krwYWpr52zluKJUSSAguVhTIYVlDoyr104opURjiZXWMSMrKRWxnDpbYOA1v0Qfj767cd1Bkf8k1bved6Y_6GS8_v8n-q3epL1WrATgVTF4fzLo090IedCdzxZCMBHSmDUTDWO1qjgt6NUR3ZgA2sc2FUdbjoPO2xSh9UWfSVkTwivG_g7YPuXcQ_uUixL9u1Z9rFWfai0D7_7d5gl_7LEAH45AGnfPmT0AU6CwvA</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2682259431</pqid></control><display><type>article</type><title>Duplication of Horizontally Acquired GH5_2 Enzymes Played a Central Role in the Evolution of Longhorned Beetles</title><source>Oxford Journals Open Access Collection</source><source>DOAJ Directory of Open Access Journals</source><source>PubMed Central</source><source>Alma/SFX Local Collection</source><source>Free Full-Text Journals in Chemistry</source><source>EZB Electronic Journals Library</source><creator>Shin, Na Ra ; Doucet, Daniel ; Pauchet, Yannick</creator><contributor>Takahashi, Aya</contributor><creatorcontrib>Shin, Na Ra ; Doucet, Daniel ; Pauchet, Yannick ; Takahashi, Aya</creatorcontrib><description>Abstract The rise of functional diversity through gene duplication contributed to the adaption of organisms to various environments. Here we investigate the evolution of putative cellulases of the subfamily 2 of glycoside hydrolase family 5 (GH5_2) in the Cerambycidae (longhorned beetles), a megadiverse assemblage of mostly xylophagous beetles. Cerambycidae originally acquired GH5_2 from a bacterial donor through horizontal gene transfer (HGT), and extant species harbor multiple copies that arose from gene duplication. We ask how these digestive enzymes contributed to the ability of these beetles to feed on wood. We analyzed 113 GH5_2, including the functional characterization of 52 of them, derived from 25 species covering most subfamilies of Cerambycidae. Ancestral gene duplications led to five well-defined groups with distinct substrate specificity, allowing these beetles to break down, in addition to cellulose, polysaccharides that are abundant in plant cell walls (PCWs), namely, xyloglucan, xylan, and mannans. Resurrecting the ancestral enzyme originally acquired by HGT, we show it was a cellulase that was able to break down glucomannan and xylan. Finally, recent gene duplications further expanded the catalytic repertoire of cerambycid GH5_2, giving rise to enzymes that favor transglycosylation over hydrolysis. We suggest that HGT and gene duplication, which shaped the evolution of GH5_2, played a central role in the ability of cerambycid beetles to use a PCW-rich diet and may have contributed to their successful radiation.</description><identifier>ISSN: 0737-4038</identifier><identifier>EISSN: 1537-1719</identifier><identifier>DOI: 10.1093/molbev/msac128</identifier><identifier>PMID: 35763818</identifier><language>eng</language><publisher>United States: Oxford University Press</publisher><subject>Analysis ; Beetles ; Cellulose ; Discoveries ; Genes ; Genetic aspects ; Hydrolysis</subject><ispartof>Molecular biology and evolution, 2022-06, Vol.39 (6)</ispartof><rights>The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. 2022</rights><rights>The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.</rights><rights>COPYRIGHT 2022 Oxford University Press</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c463t-c5ddc4d391197e0e736b1676c2dead5bd699968c0c7cd2a747790c31dce0ee353</citedby><cites>FETCH-LOGICAL-c463t-c5ddc4d391197e0e736b1676c2dead5bd699968c0c7cd2a747790c31dce0ee353</cites><orcidid>0000-0002-2918-8946</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/PMC9246334/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9246334/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,1599,27905,27906,53772,53774</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35763818$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Takahashi, Aya</contributor><creatorcontrib>Shin, Na Ra</creatorcontrib><creatorcontrib>Doucet, Daniel</creatorcontrib><creatorcontrib>Pauchet, Yannick</creatorcontrib><title>Duplication of Horizontally Acquired GH5_2 Enzymes Played a Central Role in the Evolution of Longhorned Beetles</title><title>Molecular biology and evolution</title><addtitle>Mol Biol Evol</addtitle><description>Abstract The rise of functional diversity through gene duplication contributed to the adaption of organisms to various environments. Here we investigate the evolution of putative cellulases of the subfamily 2 of glycoside hydrolase family 5 (GH5_2) in the Cerambycidae (longhorned beetles), a megadiverse assemblage of mostly xylophagous beetles. Cerambycidae originally acquired GH5_2 from a bacterial donor through horizontal gene transfer (HGT), and extant species harbor multiple copies that arose from gene duplication. We ask how these digestive enzymes contributed to the ability of these beetles to feed on wood. We analyzed 113 GH5_2, including the functional characterization of 52 of them, derived from 25 species covering most subfamilies of Cerambycidae. Ancestral gene duplications led to five well-defined groups with distinct substrate specificity, allowing these beetles to break down, in addition to cellulose, polysaccharides that are abundant in plant cell walls (PCWs), namely, xyloglucan, xylan, and mannans. Resurrecting the ancestral enzyme originally acquired by HGT, we show it was a cellulase that was able to break down glucomannan and xylan. Finally, recent gene duplications further expanded the catalytic repertoire of cerambycid GH5_2, giving rise to enzymes that favor transglycosylation over hydrolysis. We suggest that HGT and gene duplication, which shaped the evolution of GH5_2, played a central role in the ability of cerambycid beetles to use a PCW-rich diet and may have contributed to their successful radiation.</description><subject>Analysis</subject><subject>Beetles</subject><subject>Cellulose</subject><subject>Discoveries</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Hydrolysis</subject><issn>0737-4038</issn><issn>1537-1719</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><recordid>eNqFkc1vEzEUxC1ERdPClSPyEQ5p_bFrry9IaQgNUiQQgrPl2G8TI6-drncjpX99DUkLnCofbI1_bzRPg9BbSq4oUfy6S2EN--suG0tZ8wJNaM3llEqqXqIJkeVdEd6co4ucfxFCq0qIV-ic11LwhjYTlD6Nu-CtGXyKOLV4mXp_n-JgQjjgmb0bfQ8O3y5rzfAi3h86yPhbMIciGjyHOPQm4O8pAPYRD1vAi30K46PbKsXNNvWx0DcAQ4D8Gp21JmR4c7ov0c_Pix_z5XT19fbLfLaa2krwYWpr52zluKJUSSAguVhTIYVlDoyr104opURjiZXWMSMrKRWxnDpbYOA1v0Qfj767cd1Bkf8k1bved6Y_6GS8_v8n-q3epL1WrATgVTF4fzLo090IedCdzxZCMBHSmDUTDWO1qjgt6NUR3ZgA2sc2FUdbjoPO2xSh9UWfSVkTwivG_g7YPuXcQ_uUixL9u1Z9rFWfai0D7_7d5gl_7LEAH45AGnfPmT0AU6CwvA</recordid><startdate>20220628</startdate><enddate>20220628</enddate><creator>Shin, Na Ra</creator><creator>Doucet, Daniel</creator><creator>Pauchet, Yannick</creator><general>Oxford University Press</general><scope>TOX</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-2918-8946</orcidid></search><sort><creationdate>20220628</creationdate><title>Duplication of Horizontally Acquired GH5_2 Enzymes Played a Central Role in the Evolution of Longhorned Beetles</title><author>Shin, Na Ra ; Doucet, Daniel ; Pauchet, Yannick</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c463t-c5ddc4d391197e0e736b1676c2dead5bd699968c0c7cd2a747790c31dce0ee353</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Analysis</topic><topic>Beetles</topic><topic>Cellulose</topic><topic>Discoveries</topic><topic>Genes</topic><topic>Genetic aspects</topic><topic>Hydrolysis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Shin, Na Ra</creatorcontrib><creatorcontrib>Doucet, Daniel</creatorcontrib><creatorcontrib>Pauchet, Yannick</creatorcontrib><collection>Oxford Journals Open Access Collection</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>Shin, Na Ra</au><au>Doucet, Daniel</au><au>Pauchet, Yannick</au><au>Takahashi, Aya</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Duplication of Horizontally Acquired GH5_2 Enzymes Played a Central Role in the Evolution of Longhorned Beetles</atitle><jtitle>Molecular biology and evolution</jtitle><addtitle>Mol Biol Evol</addtitle><date>2022-06-28</date><risdate>2022</risdate><volume>39</volume><issue>6</issue><issn>0737-4038</issn><eissn>1537-1719</eissn><abstract>Abstract The rise of functional diversity through gene duplication contributed to the adaption of organisms to various environments. Here we investigate the evolution of putative cellulases of the subfamily 2 of glycoside hydrolase family 5 (GH5_2) in the Cerambycidae (longhorned beetles), a megadiverse assemblage of mostly xylophagous beetles. Cerambycidae originally acquired GH5_2 from a bacterial donor through horizontal gene transfer (HGT), and extant species harbor multiple copies that arose from gene duplication. We ask how these digestive enzymes contributed to the ability of these beetles to feed on wood. We analyzed 113 GH5_2, including the functional characterization of 52 of them, derived from 25 species covering most subfamilies of Cerambycidae. Ancestral gene duplications led to five well-defined groups with distinct substrate specificity, allowing these beetles to break down, in addition to cellulose, polysaccharides that are abundant in plant cell walls (PCWs), namely, xyloglucan, xylan, and mannans. Resurrecting the ancestral enzyme originally acquired by HGT, we show it was a cellulase that was able to break down glucomannan and xylan. Finally, recent gene duplications further expanded the catalytic repertoire of cerambycid GH5_2, giving rise to enzymes that favor transglycosylation over hydrolysis. We suggest that HGT and gene duplication, which shaped the evolution of GH5_2, played a central role in the ability of cerambycid beetles to use a PCW-rich diet and may have contributed to their successful radiation.</abstract><cop>United States</cop><pub>Oxford University Press</pub><pmid>35763818</pmid><doi>10.1093/molbev/msac128</doi><orcidid>https://orcid.org/0000-0002-2918-8946</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0737-4038
ispartof Molecular biology and evolution, 2022-06, Vol.39 (6)
issn 0737-4038
1537-1719
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9246334
source Oxford Journals Open Access Collection; DOAJ Directory of Open Access Journals; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry; EZB Electronic Journals Library
subjects Analysis
Beetles
Cellulose
Discoveries
Genes
Genetic aspects
Hydrolysis
title Duplication of Horizontally Acquired GH5_2 Enzymes Played a Central Role in the Evolution of Longhorned Beetles
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-17T16%3A25%3A30IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Duplication%20of%20Horizontally%20Acquired%20GH5_2%20Enzymes%20Played%20a%20Central%20Role%20in%20the%20Evolution%20of%20Longhorned%20Beetles&rft.jtitle=Molecular%20biology%20and%20evolution&rft.au=Shin,%20Na%20Ra&rft.date=2022-06-28&rft.volume=39&rft.issue=6&rft.issn=0737-4038&rft.eissn=1537-1719&rft_id=info:doi/10.1093/molbev/msac128&rft_dat=%3Cgale_pubme%3EA775003422%3C/gale_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2682259431&rft_id=info:pmid/35763818&rft_galeid=A775003422&rft_oup_id=10.1093/molbev/msac128&rfr_iscdi=true