The Transfer of the Ferredoxin Gene From the Chloroplast to the Nuclear Genome Is Ancient Within the Paraphyletic Genus Thalassiosira.
Identifieur interne : 000021 ( Main/Exploration ); précédent : 000020; suivant : 000022The Transfer of the Ferredoxin Gene From the Chloroplast to the Nuclear Genome Is Ancient Within the Paraphyletic Genus Thalassiosira.
Auteurs : Alexandra-Sophie Roy [Allemagne] ; Christian Woehle [Allemagne] ; Julie Laroche [Canada]Source :
- Frontiers in microbiology [ 1664-302X ] ; 2020.
Abstract
Ferredoxins are iron-sulfur proteins essential for a wide range of organisms because they are an electron transfer mediator involved in multiple metabolic pathways. In phytoplankton, these proteins are active in the mature chloroplasts, but the petF gene, encoding for ferredoxin, has been found either to be in the chloroplast genome or transferred to the nuclear genome as observed in the green algae and higher plant lineage. We experimentally determined the location of the petF gene in 12 strains of Thalassiosira covering three species using DNA sequencing and qPCR assays. The results showed that petF gene is located in the nuclear genome of all confirmed Thalassiosira oceanica strains (CCMP0999, 1001, 1005, and 1006) tested. In contrast, all Thalassiosira pseudonana (CCMP1012, 1013, 1014, and 1335) and Thalassiosira weissflogii (CCMP1010, 1049, and 1052) strains studied retained the gene in the chloroplast genome, as generally observed for Bacillariophyceae. Our evolutionary analyses further extend the dataset on the localization of the petF gene in the Thalassiosirales. The realization that the petF gene is nuclear-encoded in the Skeletonema genus allowed us to trace the petF gene transfer back to a single event that occurred within the paraphyletic genus Thalassiosira. Phylogenetic analyses revealed the need to reassess the taxonomic assignment of the Thalassiosira strain CCMP1616, since the genes used in our study did not cluster within the T. oceanica lineage. Our results suggest that this strains' diversification occurred prior to the ferredoxin gene transfer event. The functional transfer of petF genes provides insight into the evolutionary processes leading to chloroplast genome reduction and suggests ecological adaptation as a driving force for such chloroplast to nuclear gene transfer.
DOI: 10.3389/fmicb.2020.523689
PubMed: 33123095
PubMed Central: PMC7566914
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">The Transfer of the Ferredoxin Gene From the Chloroplast to the Nuclear Genome Is Ancient Within the Paraphyletic Genus <i>Thalassiosira</i>.</title><author><name sortKey="Roy, Alexandra Sophie" sort="Roy, Alexandra Sophie" uniqKey="Roy A" first="Alexandra-Sophie" last="Roy">Alexandra-Sophie Roy</name><affiliation wicri:level="3"><nlm:affiliation>Genomic Microbiology, Institute of General Microbiology, Kiel University, Kiel, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Genomic Microbiology, Institute of General Microbiology, Kiel University, Kiel</wicri:regionArea><placeName><region type="land" nuts="2">Schleswig-Holstein</region><settlement type="city">Kiel</settlement></placeName></affiliation></author><author><name sortKey="Woehle, Christian" sort="Woehle, Christian" uniqKey="Woehle C" first="Christian" last="Woehle">Christian Woehle</name><affiliation wicri:level="1"><nlm:affiliation>Max Planck-Genome-Centre Cologne, Max Planck Institute for Plant Breeding Research, Cologne, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Max Planck-Genome-Centre Cologne, Max Planck Institute for Plant Breeding Research, Cologne</wicri:regionArea><wicri:noRegion>Cologne</wicri:noRegion><wicri:noRegion>Cologne</wicri:noRegion><wicri:noRegion>Cologne</wicri:noRegion></affiliation></author><author><name sortKey="Laroche, Julie" sort="Laroche, Julie" uniqKey="Laroche J" first="Julie" last="Laroche">Julie Laroche</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biology, Dalhousie University, Halifax, NS, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Department of Biology, Dalhousie University, Halifax, NS</wicri:regionArea><wicri:noRegion>NS</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:33123095</idno><idno type="pmid">33123095</idno><idno type="doi">10.3389/fmicb.2020.523689</idno><idno type="pmc">PMC7566914</idno><idno type="wicri:Area/Main/Corpus">000011</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000011</idno><idno type="wicri:Area/Main/Curation">000011</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000011</idno><idno type="wicri:Area/Main/Exploration">000011</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">The Transfer of the Ferredoxin Gene From the Chloroplast to the Nuclear Genome Is Ancient Within the Paraphyletic Genus <i>Thalassiosira</i>.</title><author><name sortKey="Roy, Alexandra Sophie" sort="Roy, Alexandra Sophie" uniqKey="Roy A" first="Alexandra-Sophie" last="Roy">Alexandra-Sophie Roy</name><affiliation wicri:level="3"><nlm:affiliation>Genomic Microbiology, Institute of General Microbiology, Kiel University, Kiel, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Genomic Microbiology, Institute of General Microbiology, Kiel University, Kiel</wicri:regionArea><placeName><region type="land" nuts="2">Schleswig-Holstein</region><settlement type="city">Kiel</settlement></placeName></affiliation></author><author><name sortKey="Woehle, Christian" sort="Woehle, Christian" uniqKey="Woehle C" first="Christian" last="Woehle">Christian Woehle</name><affiliation wicri:level="1"><nlm:affiliation>Max Planck-Genome-Centre Cologne, Max Planck Institute for Plant Breeding Research, Cologne, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Max Planck-Genome-Centre Cologne, Max Planck Institute for Plant Breeding Research, Cologne</wicri:regionArea><wicri:noRegion>Cologne</wicri:noRegion><wicri:noRegion>Cologne</wicri:noRegion><wicri:noRegion>Cologne</wicri:noRegion></affiliation></author><author><name sortKey="Laroche, Julie" sort="Laroche, Julie" uniqKey="Laroche J" first="Julie" last="Laroche">Julie Laroche</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biology, Dalhousie University, Halifax, NS, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Department of Biology, Dalhousie University, Halifax, NS</wicri:regionArea><wicri:noRegion>NS</wicri:noRegion></affiliation></author></analytic><series><title level="j">Frontiers in microbiology</title><idno type="ISSN">1664-302X</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">Ferredoxins are iron-sulfur proteins essential for a wide range of organisms because they are an electron transfer mediator involved in multiple metabolic pathways. In phytoplankton, these proteins are active in the mature chloroplasts, but the <i>petF</i> gene, encoding for ferredoxin, has been found either to be in the chloroplast genome or transferred to the nuclear genome as observed in the green algae and higher plant lineage. We experimentally determined the location of the <i>petF</i> gene in 12 strains of <i>Thalassiosira</i> covering three species using DNA sequencing and qPCR assays. The results showed that <i>petF</i> gene is located in the nuclear genome of all confirmed <i>Thalassiosira oceanica</i> strains (CCMP0999, 1001, 1005, and 1006) tested. In contrast, all <i>Thalassiosira pseudonana</i> (CCMP1012, 1013, 1014, and 1335) and <i>Thalassiosira weissflogii</i> (CCMP1010, 1049, and 1052) strains studied retained the gene in the chloroplast genome, as generally observed for Bacillariophyceae. Our evolutionary analyses further extend the dataset on the localization of the <i>petF</i> gene in the Thalassiosirales. The realization that the <i>petF</i> gene is nuclear-encoded in the <i>Skeletonema</i> genus allowed us to trace the <i>petF</i> gene transfer back to a single event that occurred within the paraphyletic genus <i>Thalassiosira</i>. Phylogenetic analyses revealed the need to reassess the taxonomic assignment of the <i>Thalassiosira</i> strain CCMP1616, since the genes used in our study did not cluster within the <i>T</i>. <i>oceanica</i> lineage. Our results suggest that this strains' diversification occurred prior to the ferredoxin gene transfer event. The functional transfer of <i>petF</i> genes provides insight into the evolutionary processes leading to chloroplast genome reduction and suggests ecological adaptation as a driving force for such chloroplast to nuclear gene transfer.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">33123095</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>31</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1664-302X</ISSN><JournalIssue CitedMedium="Print"><Volume>11</Volume><PubDate><Year>2020</Year></PubDate></JournalIssue><Title>Frontiers in microbiology</Title><ISOAbbreviation>Front Microbiol</ISOAbbreviation></Journal><ArticleTitle>The Transfer of the Ferredoxin Gene From the Chloroplast to the Nuclear Genome Is Ancient Within the Paraphyletic Genus <i>Thalassiosira</i>.</ArticleTitle><Pagination><MedlinePgn>523689</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fmicb.2020.523689</ELocationID><Abstract><AbstractText>Ferredoxins are iron-sulfur proteins essential for a wide range of organisms because they are an electron transfer mediator involved in multiple metabolic pathways. In phytoplankton, these proteins are active in the mature chloroplasts, but the <i>petF</i> gene, encoding for ferredoxin, has been found either to be in the chloroplast genome or transferred to the nuclear genome as observed in the green algae and higher plant lineage. We experimentally determined the location of the <i>petF</i> gene in 12 strains of <i>Thalassiosira</i> covering three species using DNA sequencing and qPCR assays. The results showed that <i>petF</i> gene is located in the nuclear genome of all confirmed <i>Thalassiosira oceanica</i> strains (CCMP0999, 1001, 1005, and 1006) tested. In contrast, all <i>Thalassiosira pseudonana</i> (CCMP1012, 1013, 1014, and 1335) and <i>Thalassiosira weissflogii</i> (CCMP1010, 1049, and 1052) strains studied retained the gene in the chloroplast genome, as generally observed for Bacillariophyceae. Our evolutionary analyses further extend the dataset on the localization of the <i>petF</i> gene in the Thalassiosirales. The realization that the <i>petF</i> gene is nuclear-encoded in the <i>Skeletonema</i> genus allowed us to trace the <i>petF</i> gene transfer back to a single event that occurred within the paraphyletic genus <i>Thalassiosira</i>. Phylogenetic analyses revealed the need to reassess the taxonomic assignment of the <i>Thalassiosira</i> strain CCMP1616, since the genes used in our study did not cluster within the <i>T</i>. <i>oceanica</i> lineage. Our results suggest that this strains' diversification occurred prior to the ferredoxin gene transfer event. The functional transfer of <i>petF</i> genes provides insight into the evolutionary processes leading to chloroplast genome reduction and suggests ecological adaptation as a driving force for such chloroplast to nuclear gene transfer.</AbstractText><CopyrightInformation>Copyright © 2020 Roy, Woehle and LaRoche.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Roy</LastName><ForeName>Alexandra-Sophie</ForeName><Initials>AS</Initials><AffiliationInfo><Affiliation>Genomic Microbiology, Institute of General Microbiology, Kiel University, Kiel, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Woehle</LastName><ForeName>Christian</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Max Planck-Genome-Centre Cologne, Max Planck Institute for Plant Breeding Research, Cologne, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>LaRoche</LastName><ForeName>Julie</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Biology, Dalhousie University, Halifax, NS, Canada.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>10</Month><Day>02</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Microbiol</MedlineTA><NlmUniqueID>101548977</NlmUniqueID><ISSNLinking>1664-302X</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">PETF</Keyword><Keyword MajorTopicYN="N">T. oceanica</Keyword><Keyword MajorTopicYN="N">T. pseudonana</Keyword><Keyword MajorTopicYN="N">T. weissflogii</Keyword><Keyword MajorTopicYN="N">Thalassiosira genus</Keyword><Keyword MajorTopicYN="N">ferredoxin</Keyword><Keyword MajorTopicYN="N">gene 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