Ancient endosymbiont‐mediated transmission of a selfish gene provides a model for overcoming barriers to gene transfer into animal mitochondrial genomes
In contrast to bilaterian animals, non‐bilaterian mitochondrial genomes contain atypical genes, often attributed to horizontal gene transfer (HGT) as an ad hoc explanation. Although prevalent in plants, HGT into animal mitochondrial genomes is rare, lacking suitable explanatory models for their occu...
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description | In contrast to bilaterian animals, non‐bilaterian mitochondrial genomes contain atypical genes, often attributed to horizontal gene transfer (HGT) as an ad hoc explanation. Although prevalent in plants, HGT into animal mitochondrial genomes is rare, lacking suitable explanatory models for their occurrence. HGT of the mismatch DNA repair gene (mtMutS) from giant viruses to octocoral (soft corals and their kin) mitochondrial genomes provides a model for how barriers to HGT to animal mitochondria may be overcome. A review of the available literature suggests that this HGT was mediated by an alveolate endosymbiont infected with a lysogenic phycodnavirus that enabled insertion of the homing endonuclease containing mtMutS into octocoral mitochondrial genomes. We posit that homing endonuclease domains and similar selfish elements play a crucial role in such inter‐domain gene transfers. Understanding the role of selfish genetic elements in HGT has the potential to aid development of tools for manipulating animal mitochondrial DNA.
Alveolate endosymbiont infected with lysogenic phycodnavirus was able to transfer mitochondrial DNA mismatch repair gene (mtMutS) to the octocoral mitochondrial genome. This ancient and rare horizontal gene transfer (HGT) event was facilitated by a selfish genetic element. The model presented here provides novel insights into the mechanisms of HGT into animal mitochondrial genomes. |
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Alveolate endosymbiont infected with lysogenic phycodnavirus was able to transfer mitochondrial DNA mismatch repair gene (mtMutS) to the octocoral mitochondrial genome. This ancient and rare horizontal gene transfer (HGT) event was facilitated by a selfish genetic element. The model presented here provides novel insights into the mechanisms of HGT into animal mitochondrial genomes.</description><identifier>ISSN: 0265-9247</identifier><identifier>EISSN: 1521-1878</identifier><identifier>DOI: 10.1002/bies.202200190</identifier><identifier>PMID: 36412071</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>Animals ; Corals ; Deoxyribonucleic acid ; DNA ; DNA repair ; DNA, Mitochondrial - genetics ; Domains ; Endonuclease ; endosymbiont gene transfer ; Evolution, Molecular ; Gene transfer ; Gene Transfer, Horizontal - genetics ; Genome, Mitochondrial - genetics ; Genomes ; giant viruses ; Homing ; Homing endonuclease ; horizontal gene transfer ; Horizontal transfer ; Literature reviews ; Mitochondria ; Mitochondria - genetics ; Mitochondrial DNA ; mitochondrial genome ; mtMutS ; octocorals ; Phycodnaviridae ; Phylogeny ; Repetitive Sequences, Nucleic Acid - genetics ; Viruses</subject><ispartof>BioEssays, 2023-02, Vol.45 (2), p.e2200190-n/a</ispartof><rights>2022 Wiley Periodicals LLC.</rights><rights>2023 Wiley Periodicals LLC.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3280-a3464357886b80ac9d73f2e1fd2b2b620f1cfa37cbda121c3ddc7273b64497143</cites><orcidid>0000-0002-9554-3125</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fbies.202200190$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fbies.202200190$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36412071$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Shimpi, Gaurav G.</creatorcontrib><creatorcontrib>Bentlage, Bastian</creatorcontrib><title>Ancient endosymbiont‐mediated transmission of a selfish gene provides a model for overcoming barriers to gene transfer into animal mitochondrial genomes</title><title>BioEssays</title><addtitle>Bioessays</addtitle><description>In contrast to bilaterian animals, non‐bilaterian mitochondrial genomes contain atypical genes, often attributed to horizontal gene transfer (HGT) as an ad hoc explanation. Although prevalent in plants, HGT into animal mitochondrial genomes is rare, lacking suitable explanatory models for their occurrence. HGT of the mismatch DNA repair gene (mtMutS) from giant viruses to octocoral (soft corals and their kin) mitochondrial genomes provides a model for how barriers to HGT to animal mitochondria may be overcome. A review of the available literature suggests that this HGT was mediated by an alveolate endosymbiont infected with a lysogenic phycodnavirus that enabled insertion of the homing endonuclease containing mtMutS into octocoral mitochondrial genomes. We posit that homing endonuclease domains and similar selfish elements play a crucial role in such inter‐domain gene transfers. Understanding the role of selfish genetic elements in HGT has the potential to aid development of tools for manipulating animal mitochondrial DNA.
Alveolate endosymbiont infected with lysogenic phycodnavirus was able to transfer mitochondrial DNA mismatch repair gene (mtMutS) to the octocoral mitochondrial genome. This ancient and rare horizontal gene transfer (HGT) event was facilitated by a selfish genetic element. The model presented here provides novel insights into the mechanisms of HGT into animal mitochondrial genomes.</description><subject>Animals</subject><subject>Corals</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA repair</subject><subject>DNA, Mitochondrial - genetics</subject><subject>Domains</subject><subject>Endonuclease</subject><subject>endosymbiont gene transfer</subject><subject>Evolution, Molecular</subject><subject>Gene transfer</subject><subject>Gene Transfer, Horizontal - genetics</subject><subject>Genome, Mitochondrial - genetics</subject><subject>Genomes</subject><subject>giant viruses</subject><subject>Homing</subject><subject>Homing endonuclease</subject><subject>horizontal gene transfer</subject><subject>Horizontal transfer</subject><subject>Literature reviews</subject><subject>Mitochondria</subject><subject>Mitochondria - genetics</subject><subject>Mitochondrial DNA</subject><subject>mitochondrial genome</subject><subject>mtMutS</subject><subject>octocorals</subject><subject>Phycodnaviridae</subject><subject>Phylogeny</subject><subject>Repetitive Sequences, Nucleic Acid - genetics</subject><subject>Viruses</subject><issn>0265-9247</issn><issn>1521-1878</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkbtuFTEQhi0EIieBlhJZoqHZgy977N0yiZIQKRIFUK98GSeOdu3E3hN0Oh6BOo-XJ8mEk4tEQzWa8Te_5vdPyAfOlpwx8cVGqEvBhGCM9-wVWfCV4A3vdPeaLJhQq6YXrd4hu7VeMsZ6Jdq3ZEeqlgum-YLc7icXIc0Uks91M9mY03z3-88EPpoZPJ2LSXWKteIDzYEaWmEMsV7Qc0hAr0q-iR4qzqfsYaQhF5pvoLg8xXROrSklQql0ztuFv3oBCo0JRybFyYx0inN2Fzn5ErFDLk9Q35E3wYwV3j_WPfLz-OjH4dfm7NvJ6eH-WeOk6FhjZKtaudJdp2zHjOu9lkEAD15YYZVggbtgpHbWGy64k947LbS0qm17zVu5Rz5vddHL9RrqPKBdB-NoEuR1HZDtmVJSS0Q__YNe5nVJeB1SiHCleoXUcku5kmstEIargjbLZuBseEhteEhteE4NFz4-yq4tfvwz_hQTAv0W-BVH2PxHbjg4Pfr-In4PGe-nwg</recordid><startdate>202302</startdate><enddate>202302</enddate><creator>Shimpi, Gaurav G.</creator><creator>Bentlage, Bastian</creator><general>Wiley Subscription Services, Inc</general><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>7QL</scope><scope>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7T7</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-9554-3125</orcidid></search><sort><creationdate>202302</creationdate><title>Ancient endosymbiont‐mediated transmission of a selfish gene provides a model for overcoming barriers to gene transfer into animal mitochondrial genomes</title><author>Shimpi, Gaurav G. ; Bentlage, Bastian</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3280-a3464357886b80ac9d73f2e1fd2b2b620f1cfa37cbda121c3ddc7273b64497143</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Animals</topic><topic>Corals</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA repair</topic><topic>DNA, Mitochondrial - genetics</topic><topic>Domains</topic><topic>Endonuclease</topic><topic>endosymbiont gene transfer</topic><topic>Evolution, Molecular</topic><topic>Gene transfer</topic><topic>Gene Transfer, Horizontal - genetics</topic><topic>Genome, Mitochondrial - genetics</topic><topic>Genomes</topic><topic>giant viruses</topic><topic>Homing</topic><topic>Homing endonuclease</topic><topic>horizontal gene transfer</topic><topic>Horizontal transfer</topic><topic>Literature reviews</topic><topic>Mitochondria</topic><topic>Mitochondria - genetics</topic><topic>Mitochondrial DNA</topic><topic>mitochondrial genome</topic><topic>mtMutS</topic><topic>octocorals</topic><topic>Phycodnaviridae</topic><topic>Phylogeny</topic><topic>Repetitive Sequences, Nucleic Acid - genetics</topic><topic>Viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Shimpi, Gaurav G.</creatorcontrib><creatorcontrib>Bentlage, Bastian</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>BioEssays</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Shimpi, Gaurav G.</au><au>Bentlage, Bastian</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Ancient endosymbiont‐mediated transmission of a selfish gene provides a model for overcoming barriers to gene transfer into animal mitochondrial genomes</atitle><jtitle>BioEssays</jtitle><addtitle>Bioessays</addtitle><date>2023-02</date><risdate>2023</risdate><volume>45</volume><issue>2</issue><spage>e2200190</spage><epage>n/a</epage><pages>e2200190-n/a</pages><issn>0265-9247</issn><eissn>1521-1878</eissn><abstract>In contrast to bilaterian animals, non‐bilaterian mitochondrial genomes contain atypical genes, often attributed to horizontal gene transfer (HGT) as an ad hoc explanation. Although prevalent in plants, HGT into animal mitochondrial genomes is rare, lacking suitable explanatory models for their occurrence. HGT of the mismatch DNA repair gene (mtMutS) from giant viruses to octocoral (soft corals and their kin) mitochondrial genomes provides a model for how barriers to HGT to animal mitochondria may be overcome. A review of the available literature suggests that this HGT was mediated by an alveolate endosymbiont infected with a lysogenic phycodnavirus that enabled insertion of the homing endonuclease containing mtMutS into octocoral mitochondrial genomes. We posit that homing endonuclease domains and similar selfish elements play a crucial role in such inter‐domain gene transfers. Understanding the role of selfish genetic elements in HGT has the potential to aid development of tools for manipulating animal mitochondrial DNA.
Alveolate endosymbiont infected with lysogenic phycodnavirus was able to transfer mitochondrial DNA mismatch repair gene (mtMutS) to the octocoral mitochondrial genome. This ancient and rare horizontal gene transfer (HGT) event was facilitated by a selfish genetic element. The model presented here provides novel insights into the mechanisms of HGT into animal mitochondrial genomes.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>36412071</pmid><doi>10.1002/bies.202200190</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-9554-3125</orcidid></addata></record> |
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subjects | Animals Corals Deoxyribonucleic acid DNA DNA repair DNA, Mitochondrial - genetics Domains Endonuclease endosymbiont gene transfer Evolution, Molecular Gene transfer Gene Transfer, Horizontal - genetics Genome, Mitochondrial - genetics Genomes giant viruses Homing Homing endonuclease horizontal gene transfer Horizontal transfer Literature reviews Mitochondria Mitochondria - genetics Mitochondrial DNA mitochondrial genome mtMutS octocorals Phycodnaviridae Phylogeny Repetitive Sequences, Nucleic Acid - genetics Viruses |
title | Ancient endosymbiont‐mediated transmission of a selfish gene provides a model for overcoming barriers to gene transfer into animal mitochondrial genomes |
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