Highly Reduced Genomes of Protist Endosymbionts Show Evolutionary Convergence.
Identifieur interne : 000029 ( Main/Exploration ); précédent : 000028; suivant : 000030Highly Reduced Genomes of Protist Endosymbionts Show Evolutionary Convergence.
Auteurs : Emma E. George [Canada] ; Filip Husnik [Canada] ; Daria Tashyreva [République tchèque] ; Galina Prokopchuk [République tchèque] ; Aleš Horák [République tchèque] ; Waldan K. Kwong [Canada] ; Julius Lukeš [République tchèque] ; Patrick J. Keeling [Canada]Source :
- Current biology : CB [ 1879-0445 ] ; 2020.
Abstract
Genome evolution in bacterial endosymbionts is notoriously extreme: the combined effects of strong genetic drift and unique selective pressures result in highly reduced genomes with distinctive adaptations to hosts [1-4]. These processes are mostly known from animal endosymbionts, where nutritional endosymbioses represent the best-studied systems. However, eukaryotic microbes, or protists, also harbor diverse bacterial endosymbionts, but their genome reduction and functional relationships with their hosts are largely unexplored [5-7]. We sequenced the genomes of four bacterial endosymbionts from three species of diplonemids, poorly studied but abundant and diverse heterotrophic protists [8-12]. The endosymbionts come from two bacterial families, Rickettsiaceae and Holosporaceae, that have invaded two families of diplonemids, and their genomes have converged on an extremely small size (605-632 kilobase pairs [kbp]), similar gene content (e.g., metabolite transporters and secretion systems), and reduced metabolic potential (e.g., loss of energy metabolism). These characteristics are generally found in both families, but the diplonemid endosymbionts have evolved greater extremes in parallel. They possess modified type VI secretion systems that could function in manipulating host metabolism or other intracellular interactions. Finally, modified cellular machinery like the ATP synthase without oxidative phosphorylation, and the reduced flagellar apparatus present in some diplonemid endosymbionts and nutritional animal endosymbionts, indicates that intracellular mechanisms have converged in bacterial endosymbionts with various functions and from different eukaryotic hosts across the tree of life.
DOI: 10.1016/j.cub.2019.12.070
PubMed: 31978335
Affiliations:
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George</name><affiliation wicri:level="4"><nlm:affiliation>University of British Columbia, Department of Botany, Vancouver, BC V6T 1Z4, Canada. Electronic address: 3mma6eorg3@gmail.com.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>University of British Columbia, Department of Botany, Vancouver, BC V6T 1Z4</wicri:regionArea><orgName type="university">Université de la Colombie-Britannique</orgName><placeName><settlement type="city">Vancouver</settlement><region type="state">Colombie-Britannique </region></placeName></affiliation></author><author><name sortKey="Husnik, Filip" sort="Husnik, Filip" uniqKey="Husnik F" first="Filip" last="Husnik">Filip Husnik</name><affiliation wicri:level="4"><nlm:affiliation>University of British Columbia, Department of Botany, Vancouver, BC V6T 1Z4, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>University of British Columbia, Department of Botany, Vancouver, BC V6T 1Z4</wicri:regionArea><orgName type="university">Université de la Colombie-Britannique</orgName><placeName><settlement type="city">Vancouver</settlement><region type="state">Colombie-Britannique </region></placeName></affiliation></author><author><name sortKey="Tashyreva, Daria" sort="Tashyreva, Daria" uniqKey="Tashyreva D" first="Daria" last="Tashyreva">Daria Tashyreva</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic.</nlm:affiliation><country xml:lang="fr">République tchèque</country><wicri:regionArea>Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice</wicri:regionArea><wicri:noRegion>370 05 České Budějovice</wicri:noRegion></affiliation></author><author><name sortKey="Prokopchuk, Galina" sort="Prokopchuk, Galina" uniqKey="Prokopchuk G" first="Galina" last="Prokopchuk">Galina Prokopchuk</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic.</nlm:affiliation><country xml:lang="fr">République tchèque</country><wicri:regionArea>Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice</wicri:regionArea><wicri:noRegion>370 05 České Budějovice</wicri:noRegion></affiliation></author><author><name sortKey="Horak, Ales" sort="Horak, Ales" uniqKey="Horak A" first="Aleš" last="Horák">Aleš Horák</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic; University of South Bohemia, Faculty of Science, 370 05 České Budějovice, Czech Republic.</nlm:affiliation><country xml:lang="fr">République tchèque</country><wicri:regionArea>Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic; University of South Bohemia, Faculty of Science, 370 05 České Budějovice</wicri:regionArea><wicri:noRegion>370 05 České Budějovice</wicri:noRegion></affiliation></author><author><name sortKey="Kwong, Waldan K" sort="Kwong, Waldan K" uniqKey="Kwong W" first="Waldan K" last="Kwong">Waldan K. Kwong</name><affiliation wicri:level="4"><nlm:affiliation>University of British Columbia, Department of Botany, Vancouver, BC V6T 1Z4, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>University of British Columbia, Department of Botany, Vancouver, BC V6T 1Z4</wicri:regionArea><orgName type="university">Université de la Colombie-Britannique</orgName><placeName><settlement type="city">Vancouver</settlement><region type="state">Colombie-Britannique </region></placeName></affiliation></author><author><name sortKey="Lukes, Julius" sort="Lukes, Julius" uniqKey="Lukes J" first="Julius" last="Lukeš">Julius Lukeš</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic; University of South Bohemia, Faculty of Science, 370 05 České Budějovice, Czech Republic.</nlm:affiliation><country xml:lang="fr">République tchèque</country><wicri:regionArea>Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic; University of South Bohemia, Faculty of Science, 370 05 České Budějovice</wicri:regionArea><wicri:noRegion>370 05 České Budějovice</wicri:noRegion></affiliation></author><author><name sortKey="Keeling, Patrick J" sort="Keeling, Patrick J" uniqKey="Keeling P" first="Patrick J" last="Keeling">Patrick J. Keeling</name><affiliation wicri:level="4"><nlm:affiliation>University of British Columbia, Department of Botany, Vancouver, BC V6T 1Z4, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>University of British Columbia, Department of Botany, Vancouver, BC V6T 1Z4</wicri:regionArea><orgName type="university">Université de la Colombie-Britannique</orgName><placeName><settlement type="city">Vancouver</settlement><region type="state">Colombie-Britannique </region></placeName></affiliation></author></analytic><series><title level="j">Current biology : CB</title><idno type="eISSN">1879-0445</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Genome evolution in bacterial endosymbionts is notoriously extreme: the combined effects of strong genetic drift and unique selective pressures result in highly reduced genomes with distinctive adaptations to hosts [1-4]. These processes are mostly known from animal endosymbionts, where nutritional endosymbioses represent the best-studied systems. However, eukaryotic microbes, or protists, also harbor diverse bacterial endosymbionts, but their genome reduction and functional relationships with their hosts are largely unexplored [5-7]. We sequenced the genomes of four bacterial endosymbionts from three species of diplonemids, poorly studied but abundant and diverse heterotrophic protists [8-12]. The endosymbionts come from two bacterial families, Rickettsiaceae and Holosporaceae, that have invaded two families of diplonemids, and their genomes have converged on an extremely small size (605-632 kilobase pairs [kbp]), similar gene content (e.g., metabolite transporters and secretion systems), and reduced metabolic potential (e.g., loss of energy metabolism). These characteristics are generally found in both families, but the diplonemid endosymbionts have evolved greater extremes in parallel. They possess modified type VI secretion systems that could function in manipulating host metabolism or other intracellular interactions. Finally, modified cellular machinery like the ATP synthase without oxidative phosphorylation, and the reduced flagellar apparatus present in some diplonemid endosymbionts and nutritional animal endosymbionts, indicates that intracellular mechanisms have converged in bacterial endosymbionts with various functions and from different eukaryotic hosts across the tree of life.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">31978335</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>02</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1879-0445</ISSN><JournalIssue CitedMedium="Internet"><Volume>30</Volume><Issue>5</Issue><PubDate><Year>2020</Year><Month>03</Month><Day>09</Day></PubDate></JournalIssue><Title>Current biology : CB</Title><ISOAbbreviation>Curr Biol</ISOAbbreviation></Journal><ArticleTitle>Highly Reduced Genomes of Protist Endosymbionts Show Evolutionary Convergence.</ArticleTitle><Pagination><MedlinePgn>925-933.e3</MedlinePgn></Pagination><ELocationID EIdType="pii" ValidYN="Y">S0960-9822(19)31703-8</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1016/j.cub.2019.12.070</ELocationID><Abstract><AbstractText>Genome evolution in bacterial endosymbionts is notoriously extreme: the combined effects of strong genetic drift and unique selective pressures result in highly reduced genomes with distinctive adaptations to hosts [1-4]. These processes are mostly known from animal endosymbionts, where nutritional endosymbioses represent the best-studied systems. However, eukaryotic microbes, or protists, also harbor diverse bacterial endosymbionts, but their genome reduction and functional relationships with their hosts are largely unexplored [5-7]. We sequenced the genomes of four bacterial endosymbionts from three species of diplonemids, poorly studied but abundant and diverse heterotrophic protists [8-12]. The endosymbionts come from two bacterial families, Rickettsiaceae and Holosporaceae, that have invaded two families of diplonemids, and their genomes have converged on an extremely small size (605-632 kilobase pairs [kbp]), similar gene content (e.g., metabolite transporters and secretion systems), and reduced metabolic potential (e.g., loss of energy metabolism). These characteristics are generally found in both families, but the diplonemid endosymbionts have evolved greater extremes in parallel. They possess modified type VI secretion systems that could function in manipulating host metabolism or other intracellular interactions. Finally, modified cellular machinery like the ATP synthase without oxidative phosphorylation, and the reduced flagellar apparatus present in some diplonemid endosymbionts and nutritional animal endosymbionts, indicates that intracellular mechanisms have converged in bacterial endosymbionts with various functions and from different eukaryotic hosts across the tree of life.</AbstractText><CopyrightInformation>Copyright © 2020 Elsevier Ltd. All rights reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>George</LastName><ForeName>Emma E</ForeName><Initials>EE</Initials><AffiliationInfo><Affiliation>University of British Columbia, Department of Botany, Vancouver, BC V6T 1Z4, Canada. Electronic address: 3mma6eorg3@gmail.com.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Husnik</LastName><ForeName>Filip</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>University of British Columbia, Department of Botany, Vancouver, BC V6T 1Z4, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tashyreva</LastName><ForeName>Daria</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Prokopchuk</LastName><ForeName>Galina</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Horák</LastName><ForeName>Aleš</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic; University of South Bohemia, Faculty of Science, 370 05 České Budějovice, Czech Republic.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kwong</LastName><ForeName>Waldan K</ForeName><Initials>WK</Initials><AffiliationInfo><Affiliation>University of British Columbia, Department of Botany, Vancouver, BC V6T 1Z4, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lukeš</LastName><ForeName>Julius</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Institute of Parasitology, Biology Centre, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic; University of South Bohemia, Faculty of Science, 370 05 České Budějovice, Czech Republic.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Keeling</LastName><ForeName>Patrick J</ForeName><Initials>PJ</Initials><AffiliationInfo><Affiliation>University of British Columbia, Department of Botany, Vancouver, BC V6T 1Z4, Canada.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>01</Month><Day>23</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Curr Biol</MedlineTA><NlmUniqueID>9107782</NlmUniqueID><ISSNLinking>0960-9822</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Holosporaceae</Keyword><Keyword MajorTopicYN="Y">Muller’s ratchet</Keyword><Keyword MajorTopicYN="Y">Rickettsiaceae</Keyword><Keyword MajorTopicYN="Y">T6SS</Keyword><Keyword MajorTopicYN="Y">convergent evolution</Keyword><Keyword MajorTopicYN="Y">diplonemid</Keyword><Keyword MajorTopicYN="Y">endosymbiosis</Keyword><Keyword MajorTopicYN="Y">genome reduction</Keyword><Keyword MajorTopicYN="Y">protist</Keyword><Keyword MajorTopicYN="Y">secretion systems</Keyword></KeywordList><CoiStatement>Declaration of Interests The authors declare no competing interests.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>07</Month><Day>24</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2019</Year><Month>09</Month><Day>24</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>12</Month><Day>23</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>1</Month><Day>25</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>1</Month><Day>25</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>1</Month><Day>25</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">31978335</ArticleId><ArticleId IdType="pii">S0960-9822(19)31703-8</ArticleId><ArticleId IdType="doi">10.1016/j.cub.2019.12.070</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Canada</li><li>République tchèque</li></country><region><li>Colombie-Britannique </li></region><settlement><li>Vancouver</li></settlement><orgName><li>Université de la Colombie-Britannique</li></orgName></list><tree><country name="Canada"><region name="Colombie-Britannique "><name sortKey="George, Emma E" sort="George, Emma E" uniqKey="George E" first="Emma E" last="George">Emma E. George</name></region><name sortKey="Husnik, Filip" sort="Husnik, Filip" uniqKey="Husnik F" first="Filip" last="Husnik">Filip Husnik</name><name sortKey="Keeling, Patrick J" sort="Keeling, Patrick J" uniqKey="Keeling P" first="Patrick J" last="Keeling">Patrick J. Keeling</name><name sortKey="Kwong, Waldan K" sort="Kwong, Waldan K" uniqKey="Kwong W" first="Waldan K" last="Kwong">Waldan K. Kwong</name></country><country name="République tchèque"><noRegion><name sortKey="Tashyreva, Daria" sort="Tashyreva, Daria" uniqKey="Tashyreva D" first="Daria" last="Tashyreva">Daria Tashyreva</name></noRegion><name sortKey="Horak, Ales" sort="Horak, Ales" uniqKey="Horak A" first="Aleš" last="Horák">Aleš Horák</name><name sortKey="Lukes, Julius" sort="Lukes, Julius" uniqKey="Lukes J" first="Julius" last="Lukeš">Julius Lukeš</name><name sortKey="Prokopchuk, Galina" sort="Prokopchuk, Galina" uniqKey="Prokopchuk G" first="Galina" last="Prokopchuk">Galina Prokopchuk</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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