Targeted diversity generation by intraterrestrial archaea and archaeal viruses
Identifieur interne : 000611 ( Ncbi/Merge ); précédent : 000610; suivant : 000612Targeted diversity generation by intraterrestrial archaea and archaeal viruses
Auteurs : Blair G. Paul [États-Unis] ; Sarah C. Bagby [États-Unis] ; Elizabeth Czornyj [États-Unis] ; Diego Arambula [États-Unis] ; Sumit Handa [États-Unis] ; Alexander Sczyrba [Allemagne, États-Unis] ; Partho Ghosh [États-Unis] ; Jeff F. Miller [États-Unis] ; David L. Valentine [États-Unis]Source :
- Nature Communications [ 2041-1723 ] ; 2015.
Abstract
In the evolutionary arms race between microbes, their parasites, and their neighbours, the capacity for rapid protein diversification is a potent weapon. Diversity-generating retroelements (DGRs) use mutagenic reverse transcription and retrohoming to generate myriad variants of a target gene. Originally discovered in pathogens, these retroelements have been identified in bacteria and their viruses, but never in archaea. Here we report the discovery of intact DGRs in two distinct intraterrestrial archaeal systems: a novel virus that appears to infect archaea in the marine subsurface, and, separately, two uncultivated nanoarchaea from the terrestrial subsurface. The viral DGR system targets putative tail fibre ligand-binding domains, potentially generating >1018 protein variants. The two single-cell nanoarchaeal genomes each possess ≥4 distinct DGRs. Against an expected background of low genome-wide mutation rates, these results demonstrate a previously unsuspected potential for rapid, targeted sequence diversification in intraterrestrial archaea and their viruses.
Url:
DOI: 10.1038/ncomms7585
PubMed: 25798780
PubMed Central: 4372165
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Paul</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>Marine Science Institute, University of California</institution>, Santa Barbara, California 93106,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Bagby, Sarah C" sort="Bagby, Sarah C" uniqKey="Bagby S" first="Sarah C." last="Bagby">Sarah C. Bagby</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>Marine Science Institute, University of California</institution>, Santa Barbara, California 93106,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Czornyj, Elizabeth" sort="Czornyj, Elizabeth" uniqKey="Czornyj E" first="Elizabeth" last="Czornyj">Elizabeth Czornyj</name><affiliation wicri:level="1"><nlm:aff id="a2"><institution>Department of Microbiology, Immunology and Molecular Genetics, University of California</institution>, Los Angeles, California 90095,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Arambula, Diego" sort="Arambula, Diego" uniqKey="Arambula D" first="Diego" last="Arambula">Diego Arambula</name><affiliation wicri:level="1"><nlm:aff id="a2"><institution>Department of Microbiology, Immunology and Molecular Genetics, University of California</institution>, Los Angeles, California 90095,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Handa, Sumit" sort="Handa, Sumit" uniqKey="Handa S" first="Sumit" last="Handa">Sumit Handa</name><affiliation wicri:level="1"><nlm:aff id="a3"><institution>Department of Chemistry and Biochemistry, University of California San Diego</institution>, La Jolla, California 92093,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Sczyrba, Alexander" sort="Sczyrba, Alexander" uniqKey="Sczyrba A" first="Alexander" last="Sczyrba">Alexander Sczyrba</name><affiliation wicri:level="1"><nlm:aff id="a4"><institution>Center for Biotechnology and Faculty of Technology, Bielefeld University</institution>, 33615 Bielefeld,<country>Germany</country></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="a5"><institution>DOE Joint Genome Institute</institution>, Walnut Creek, California 94598,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Ghosh, Partho" sort="Ghosh, Partho" uniqKey="Ghosh P" first="Partho" last="Ghosh">Partho Ghosh</name><affiliation wicri:level="1"><nlm:aff id="a3"><institution>Department of Chemistry and Biochemistry, University of California San Diego</institution>, La Jolla, California 92093,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Miller, Jeff F" sort="Miller, Jeff F" uniqKey="Miller J" first="Jeff F." last="Miller">Jeff F. Miller</name><affiliation wicri:level="1"><nlm:aff id="a2"><institution>Department of Microbiology, Immunology and Molecular Genetics, University of California</institution>, Los Angeles, California 90095,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="a6"><institution>Molecular Biology Institute, University of California</institution>, Los Angeles, California 90095,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="a7"><institution>California NanoSystems Institute, University of California</institution>, Los Angeles, California 90095,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Valentine, David L" sort="Valentine, David L" uniqKey="Valentine D" first="David L." last="Valentine">David L. Valentine</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>Marine Science Institute, University of California</institution>, Santa Barbara, California 93106,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="a8"><institution>Department of Earth Science, University of California Santa Barbara</institution>, Santa Barbara, California 93106<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></analytic><series><title level="j">Nature Communications</title><idno type="eISSN">2041-1723</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>In the evolutionary arms race between microbes, their parasites, and their neighbours, the capacity for rapid protein diversification is a potent weapon. Diversity-generating retroelements (DGRs) use mutagenic reverse transcription and retrohoming to generate myriad variants of a target gene. Originally discovered in pathogens, these retroelements have been identified in bacteria and their viruses, but never in archaea. Here we report the discovery of intact DGRs in two distinct intraterrestrial archaeal systems: a novel virus that appears to infect archaea in the marine subsurface, and, separately, two uncultivated nanoarchaea from the terrestrial subsurface. The viral DGR system targets putative tail fibre ligand-binding domains, potentially generating >10<sup>18</sup> protein variants. The two single-cell nanoarchaeal genomes each possess ≥4 distinct DGRs. Against an expected background of low genome-wide mutation rates, these results demonstrate a previously unsuspected potential for rapid, targeted sequence diversification in intraterrestrial archaea and their viruses.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Kallmeyer, J" uniqKey="Kallmeyer J">J. Kallmeyer</name></author><author><name sortKey="Pockalny, R" uniqKey="Pockalny R">R. Pockalny</name></author><author><name sortKey="Adhikari, R R" uniqKey="Adhikari R">R. R. Adhikari</name></author><author><name sortKey="Smith, D C" uniqKey="Smith D">D. C. Smith</name></author><author><name sortKey="Dhondt, S" uniqKey="Dhondt S">S. DHondt</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lipp, J" uniqKey="Lipp J">J. Lipp</name></author><author><name sortKey="Morono, Y" uniqKey="Morono Y">Y. Morono</name></author><author><name sortKey="Inagaki, F" uniqKey="Inagaki F">F. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Nat Commun</journal-id><journal-id journal-id-type="iso-abbrev">Nat Commun</journal-id><journal-title-group><journal-title>Nature Communications</journal-title></journal-title-group><issn pub-type="epub">2041-1723</issn><publisher><publisher-name>Nature Pub. Group</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">25798780</article-id><article-id pub-id-type="pmc">4372165</article-id><article-id pub-id-type="pii">ncomms7585</article-id><article-id pub-id-type="doi">10.1038/ncomms7585</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Targeted diversity generation by intraterrestrial archaea and archaeal viruses</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Paul</surname><given-names>Blair G.</given-names></name><xref ref-type="aff" rid="a1">1</xref></contrib><contrib contrib-type="author"><name><surname>Bagby</surname><given-names>Sarah C.</given-names></name><xref ref-type="aff" rid="a1">1</xref></contrib><contrib contrib-type="author"><name><surname>Czornyj</surname><given-names>Elizabeth</given-names></name><xref ref-type="aff" rid="a2">2</xref></contrib><contrib contrib-type="author"><name><surname>Arambula</surname><given-names>Diego</given-names></name><xref ref-type="aff" rid="a2">2</xref></contrib><contrib contrib-type="author"><name><surname>Handa</surname><given-names>Sumit</given-names></name><xref ref-type="aff" rid="a3">3</xref></contrib><contrib contrib-type="author"><name><surname>Sczyrba</surname><given-names>Alexander</given-names></name><xref ref-type="aff" rid="a4">4</xref><xref ref-type="aff" rid="a5">5</xref><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-4405-3847</contrib-id></contrib><contrib contrib-type="author"><name><surname>Ghosh</surname><given-names>Partho</given-names></name><xref ref-type="aff" rid="a3">3</xref></contrib><contrib contrib-type="author"><name><surname>Miller</surname><given-names>Jeff F.</given-names></name><xref ref-type="aff" rid="a2">2</xref><xref ref-type="aff" rid="a6">6</xref><xref ref-type="aff" rid="a7">7</xref></contrib><contrib contrib-type="author"><name><surname>Valentine</surname><given-names>David L.</given-names></name><xref ref-type="corresp" rid="c1">a</xref><xref ref-type="aff" rid="a1">1</xref><xref ref-type="aff" rid="a8">8</xref></contrib><aff id="a1"><label>1</label><institution>Marine Science Institute, University of California</institution>, Santa Barbara, California 93106,<country>USA</country></aff><aff id="a2"><label>2</label><institution>Department of Microbiology, Immunology and Molecular Genetics, University of California</institution>, Los Angeles, California 90095,<country>USA</country></aff><aff id="a3"><label>3</label><institution>Department of Chemistry and Biochemistry, University of California San Diego</institution>, La Jolla, California 92093,<country>USA</country></aff><aff id="a4"><label>4</label><institution>Center for Biotechnology and Faculty of Technology, Bielefeld University</institution>, 33615 Bielefeld,<country>Germany</country></aff><aff id="a5"><label>5</label><institution>DOE Joint Genome Institute</institution>, Walnut Creek, California 94598,<country>USA</country></aff><aff id="a6"><label>6</label><institution>Molecular Biology Institute, University of California</institution>, Los Angeles, California 90095,<country>USA</country></aff><aff id="a7"><label>7</label><institution>California NanoSystems Institute, University of California</institution>, Los Angeles, California 90095,<country>USA</country></aff><aff id="a8"><label>8</label><institution>Department of Earth Science, University of California Santa Barbara</institution>, Santa Barbara, California 93106<country>USA</country></aff></contrib-group><author-notes><corresp id="c1"><label>a</label><email>valentine@geol.ucsb.edu</email></corresp></author-notes><pub-date pub-type="epub"><day>23</day><month>03</month><year>2015</year></pub-date><volume>6</volume><elocation-id>6585</elocation-id><history><date date-type="received"><day>10</day><month>12</month><year>2014</year></date><date date-type="accepted"><day>09</day><month>02</month><year>2015</year></date></history><permissions><copyright-statement>Copyright © 2015, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.</copyright-statement><copyright-year>2015</copyright-year><copyright-holder>Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.</copyright-holder><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link></license-p></license></permissions><abstract><p>In the evolutionary arms race between microbes, their parasites, and their neighbours, the capacity for rapid protein diversification is a potent weapon. Diversity-generating retroelements (DGRs) use mutagenic reverse transcription and retrohoming to generate myriad variants of a target gene. Originally discovered in pathogens, these retroelements have been identified in bacteria and their viruses, but never in archaea. Here we report the discovery of intact DGRs in two distinct intraterrestrial archaeal systems: a novel virus that appears to infect archaea in the marine subsurface, and, separately, two uncultivated nanoarchaea from the terrestrial subsurface. The viral DGR system targets putative tail fibre ligand-binding domains, potentially generating >10<sup>18</sup> protein variants. The two single-cell nanoarchaeal genomes each possess ≥4 distinct DGRs. Against an expected background of low genome-wide mutation rates, these results demonstrate a previously unsuspected potential for rapid, targeted sequence diversification in intraterrestrial archaea and their viruses.</p></abstract><abstract abstract-type="web-summary"><p><inline-graphic id="i1" xlink:href="ncomms7585-i1.jpg"></inline-graphic>Diversity-generating retroelements (DGRs) are genetic elements that introduce sequence variation within target genes in bacteria and their viruses. Here, Paul <italic>et al</italic>. report the discovery of DGRs in an archaeal virus and in two archaea from marine and terrestrial subsurface environments, respectively.</p></abstract></article-meta></front><floats-group><fig id="f1"><label>Figure 1</label><caption><title>Retroelement-containing ANMV-1 genome obtained from methane seep sediment.</title><p>(<bold>a</bold>) Annotated coding sequences (CDS) designated by arrows that are coloured according to predicted function. Genes with blast similarity to ANME protein sequences are highlighted in red below each corresponding ANMV-1 locus (<xref ref-type="supplementary-material" rid="S1">Supplementary Table 1</xref>). Symbols above selected annotations indicate putative gene names: terL, terminase large subunit; tbp, TATA-box binding protein; nrdD, anaerobic ribonucleoside triphosphate reductase; AdtA, DGR TP; RT, reverse transcriptase. An open box highlights the DGR cassette with flanking putative tail fibres (tail fib.), shown below the genome. (<bold>b</bold>) Putative <italic>cis</italic>- and <italic>trans</italic>-acting features of the ANMV-1 DGR. RT, accessory variability determinant (Avd) and AdtA ORFs are shown as blue, grey and green arrows, respectively. Purple boxes indicate template and variable repeat regions (TR and VR). The IMH and cognate IMH* sites are highlighted in yellow. The expanded DGR view depicts the putative retrohoming target site. Estimated number of nucleotide sequence variants is given above VR (TR* cDNAs), based on theoretical mutagenesis of adenines in TR intermediate RNA.</p></caption><graphic xlink:href="ncomms7585-f1"></graphic></fig><fig id="f2"><label>Figure 2</label><caption><title>Grouping of DGRs from <italic>Nanoarchaeota</italic>.</title><p>(<bold>a</bold>) Positions of four DGR cassettes in each OTU, coloured by homology-based groups (note ungrouped OTU1 DGR in grey). Contigs are shown with DGRs on the forward strand (rev., reverse complement). (<bold>b</bold>) DGR groups, ordered by RT and TP homologies. A PhyML tree (left) was constructed with 100 bootstrap replicates (support indicated on branches) from concatenated alignments of TP and RT amino-acid sequences for each complete DGR cassette. Group 4 includes an incomplete DGR for OTU1 contig 26 (missing RT ORF). A schematic for nanoarchaeal DGRs shows the direction of information transfer during targeted mutagenesis. TP and RT genes are shown as green and blue arrows, respectively, while purple boxes indicate variable and template regions (VR and TR). Bar graphs show pairwise similarity between aligned OTU1 and OTU2 sequences for major DGR features, TP, VR, TR and RT. NA (not applicable) indicates that a feature is not found in the DGR.</p></caption><graphic xlink:href="ncomms7585-f2"></graphic></fig><fig id="f3"><label>Figure 3</label><caption><title>Conserved and putative regulatory features of Nanoarchaeota DGRs.</title><p>IMH sites (IMH and IMH*) are shown as yellow boxes, and the trinucleotide-loop hairpin is given in an expanded view at right. Dark grey arrows indicate ORFs between RT and TP whose amino-acid sequences have comparable isoelectric point and molecular weight to accessory variability determinant (Avd; pI=9±1; <italic>M</italic><sub>w</sub>=10±5).</p></caption><graphic xlink:href="ncomms7585-f3"></graphic></fig><fig id="f4"><label>Figure 4</label><caption><title>RT phylogeny for archaeal DGRs.</title><p>(<bold>a</bold>) Maximum-likelihood phylogenetic tree of RT representatives aligned with ANMV-1 and DUSEL4 Nanoarchaeota sequences. Green branches correspond to bacterial and bacteria-derived RTs (from chromosomes, plasmids, mitochondria, chloroplasts and bacteriophage), red branches indicate archaeal and archaeal virus RTs, and black branches represent RTs from eukaryotes and their viruses. Retroelement clades and key representatives are labelled as follows: DGRs, diversity-generating retroelements; DIRS, Dictyostelium retrotransposons; GemV, geminiviridae; G2L, group-II intron-like (G2L are numbered according to Simon and Zimmerly (<italic>24</italic>)); Hpdn, hepadnaviruses; LTR, long terminal repeat retroelements; NPV, nucleopolyhedralviruses; non-LTR, non-long terminal repeat retroelements; RtV, retroviridae; unk, unknown or unclassified. The scale shows substitutions per site. For clarity, bootstrap values are not shown for the full RT tree. (<bold>b</bold>) Expanded subtree view of DGR RT representatives. A red box highlights the archaeal DGR clade. NCBI accession codes are given for representatives in the subtree, but previously described bacterial DGRs are explicitly named. The representative for Bordetella phage BPP is labelled ‘BPP’. Coloured circles at internal nodes indicate branch support.</p></caption><graphic xlink:href="ncomms7585-f4"></graphic></fig><fig id="f5"><label>Figure 5</label><caption><title>Tetranucleotide distributions of DUSEL4 <italic>Nanoarchaeota</italic>.</title><p>(<bold>a</bold>,<bold>b</bold>) Non-metric multidimensional scaling plots of tetranucleotide distributions of (<bold>a</bold>) concatenated DUSEL4 DGRs (red) and (<bold>b</bold>) separately concatenated DUSEL4 DGR RT (blue) and TP genes (green), compared with the rest of the DUSEL4 Nanoarchaeota OTU1 and OTU2 genomes (greyscale circles). Each point on the ordination plots represents one 5-kb fragment. Dashed ellipses indicate the 95% confidence region.</p></caption><graphic xlink:href="ncomms7585-f5"></graphic></fig></floats-group></pmc><affiliations><list><country><li>Allemagne</li><li>États-Unis</li></country></list><tree><country name="États-Unis"><noRegion><name sortKey="Paul, Blair G" sort="Paul, Blair G" uniqKey="Paul B" first="Blair G." last="Paul">Blair G. Paul</name></noRegion><name sortKey="Arambula, Diego" sort="Arambula, Diego" uniqKey="Arambula D" first="Diego" last="Arambula">Diego Arambula</name><name sortKey="Bagby, Sarah C" sort="Bagby, Sarah C" uniqKey="Bagby S" first="Sarah C." last="Bagby">Sarah C. Bagby</name><name sortKey="Czornyj, Elizabeth" sort="Czornyj, Elizabeth" uniqKey="Czornyj E" first="Elizabeth" last="Czornyj">Elizabeth Czornyj</name><name sortKey="Ghosh, Partho" sort="Ghosh, Partho" uniqKey="Ghosh P" first="Partho" last="Ghosh">Partho Ghosh</name><name sortKey="Handa, Sumit" sort="Handa, Sumit" uniqKey="Handa S" first="Sumit" last="Handa">Sumit Handa</name><name sortKey="Miller, Jeff F" sort="Miller, Jeff F" uniqKey="Miller J" first="Jeff F." last="Miller">Jeff F. Miller</name><name sortKey="Miller, Jeff F" sort="Miller, Jeff F" uniqKey="Miller J" first="Jeff F." last="Miller">Jeff F. Miller</name><name sortKey="Miller, Jeff F" sort="Miller, Jeff F" uniqKey="Miller J" first="Jeff F." last="Miller">Jeff F. Miller</name><name sortKey="Sczyrba, Alexander" sort="Sczyrba, Alexander" uniqKey="Sczyrba A" first="Alexander" last="Sczyrba">Alexander Sczyrba</name><name sortKey="Valentine, David L" sort="Valentine, David L" uniqKey="Valentine D" first="David L." last="Valentine">David L. Valentine</name><name sortKey="Valentine, David L" sort="Valentine, David L" uniqKey="Valentine D" first="David L." last="Valentine">David L. Valentine</name></country><country name="Allemagne"><noRegion><name sortKey="Sczyrba, Alexander" sort="Sczyrba, Alexander" uniqKey="Sczyrba A" first="Alexander" last="Sczyrba">Alexander Sczyrba</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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