Structural signatures of thermal adaptation of bacterial ribosomal RNA, transfer RNA, and messenger RNA
Identifieur interne : 002847 ( Pmc/Curation ); précédent : 002846; suivant : 002848Structural signatures of thermal adaptation of bacterial ribosomal RNA, transfer RNA, and messenger RNA
Auteurs : Clara Jegousse [France, Australie] ; Yuedong Yang [Australie] ; Jian Zhan [Australie] ; Jihua Wang [République populaire de Chine] ; Yaoqi Zhou [Australie, République populaire de Chine]Source :
- PLoS ONE [ 1932-6203 ] ; 2017.
Abstract
Temperature adaptation of bacterial RNAs is a subject of both fundamental and practical interest because it will allow a better understanding of molecular mechanism of RNA folding with potential industrial application of functional thermophilic or psychrophilic RNAs. Here, we performed a comprehensive study of rRNA, tRNA, and mRNA of more than 200 bacterial species with optimal growth temperatures (OGT) ranging from 4°C to 95°C. We investigated temperature adaptation at primary, secondary and tertiary structure levels. We showed that unlike mRNA, tRNA and rRNA were optimized for their structures at compositional levels with significant tertiary structural features even for their corresponding randomly permutated sequences. tRNA and rRNA are more exposed to solvent but remain structured for hyperthermophiles with nearly OGT-independent fluctuation of solvent accessible surface area within a single RNA chain. mRNA in hyperthermophiles is essentially the same as random sequences without tertiary structures although many mRNA in mesophiles and psychrophiles have well-defined tertiary structures based on their low overall solvent exposure with clear separation of deeply buried from partly exposed bases as in tRNA and rRNA. These results provide new insight into temperature adaptation of different RNAs.
Url:
DOI: 10.1371/journal.pone.0184722
PubMed: 28910383
PubMed Central: 5598986
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wicri:level="1"><nlm:aff id="aff002"><addr-line>Institute for Glycomics and School of Information and Communication Technology, Griffith University, Gold Coast, QLD, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Institute for Glycomics and School of Information and Communication Technology, Griffith University, Gold Coast, QLD</wicri:regionArea></affiliation></author><author><name sortKey="Yang, Yuedong" sort="Yang, Yuedong" uniqKey="Yang Y" first="Yuedong" last="Yang">Yuedong Yang</name><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Institute for Glycomics and School of Information and Communication Technology, Griffith University, Gold Coast, QLD, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Institute for Glycomics and School of Information and Communication Technology, Griffith University, Gold Coast, QLD</wicri:regionArea></affiliation></author><author><name sortKey="Zhan, Jian" sort="Zhan, Jian" uniqKey="Zhan J" first="Jian" last="Zhan">Jian Zhan</name><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Institute for Glycomics and School of Information and Communication Technology, Griffith University, Gold Coast, QLD, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Institute for Glycomics and School of Information and Communication Technology, Griffith University, Gold Coast, QLD</wicri:regionArea></affiliation></author><author><name sortKey="Wang, Jihua" sort="Wang, Jihua" uniqKey="Wang J" first="Jihua" last="Wang">Jihua Wang</name><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>Shandong Provincial Key Laboratory of Biophysics, Institute of Biophysics, Dezhou University, Dezhou, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shandong Provincial Key Laboratory of Biophysics, Institute of Biophysics, Dezhou University, 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">28910383</article-id><article-id pub-id-type="pmc">5598986</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0184722</article-id><article-id pub-id-type="publisher-id">PONE-D-17-23880</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Nucleic acids</subject><subj-group><subject>RNA</subject><subj-group><subject>Non-coding RNA</subject><subj-group><subject>Ribosomal RNA</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Ribosomes</subject><subj-group><subject>Ribosomal RNA</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Cell biology</subject><subj-group><subject>Cellular structures and organelles</subject><subj-group><subject>Ribosomes</subject><subj-group><subject>Ribosomal RNA</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Nucleic acids</subject><subj-group><subject>RNA</subject><subj-group><subject>Non-coding RNA</subject><subj-group><subject>Transfer RNA</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Molecular biology</subject><subj-group><subject>Macromolecular structure analysis</subject><subj-group><subject>RNA structure</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Nucleic acids</subject><subj-group><subject>RNA</subject><subj-group><subject>RNA structure</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Molecular biology</subject><subj-group><subject>Macromolecular structure analysis</subject><subj-group><subject>RNA structure</subject><subj-group><subject>RNA folding</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Nucleic acids</subject><subj-group><subject>RNA</subject><subj-group><subject>RNA structure</subject><subj-group><subject>RNA folding</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Ecology and Environmental Sciences</subject><subj-group><subject>Extremophiles</subject></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Nucleic acids</subject><subj-group><subject>RNA</subject><subj-group><subject>Messenger RNA</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Nucleic acids</subject><subj-group><subject>RNA</subject><subj-group><subject>RNA sequences</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject><subj-group><subject>Database and Informatics Methods</subject><subj-group><subject>Biological Databases</subject><subj-group><subject>Sequence Databases</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject><subj-group><subject>Database and Informatics Methods</subject><subj-group><subject>Bioinformatics</subject><subj-group><subject>Sequence Analysis</subject><subj-group><subject>Sequence Databases</subject></subj-group></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Structural signatures of thermal adaptation of bacterial ribosomal RNA, transfer RNA, and messenger RNA</article-title><alt-title alt-title-type="running-head">Thermal adaptation of bacterial RNAs</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Jegousse</surname><given-names>Clara</given-names></name><role content-type="http://credit.casrai.org/">Data curation</role><role content-type="http://credit.casrai.org/">Formal analysis</role><role content-type="http://credit.casrai.org/">Investigation</role><role content-type="http://credit.casrai.org/">Methodology</role><role content-type="http://credit.casrai.org/">Validation</role><role content-type="http://credit.casrai.org/">Writing – original draft</role><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Yang</surname><given-names>Yuedong</given-names></name><role content-type="http://credit.casrai.org/">Data curation</role><role content-type="http://credit.casrai.org/">Formal analysis</role><role content-type="http://credit.casrai.org/">Investigation</role><role content-type="http://credit.casrai.org/">Methodology</role><role content-type="http://credit.casrai.org/">Software</role><role content-type="http://credit.casrai.org/">Supervision</role><role content-type="http://credit.casrai.org/">Validation</role><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff002"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Zhan</surname><given-names>Jian</given-names></name><role content-type="http://credit.casrai.org/">Conceptualization</role><role content-type="http://credit.casrai.org/">Formal analysis</role><role content-type="http://credit.casrai.org/">Validation</role><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff002"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Wang</surname><given-names>Jihua</given-names></name><role content-type="http://credit.casrai.org/">Conceptualization</role><role content-type="http://credit.casrai.org/">Methodology</role><role content-type="http://credit.casrai.org/">Project administration</role><role content-type="http://credit.casrai.org/">Resources</role><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-9958-5699</contrib-id><name><surname>Zhou</surname><given-names>Yaoqi</given-names></name><role content-type="http://credit.casrai.org/">Conceptualization</role><role content-type="http://credit.casrai.org/">Funding acquisition</role><role content-type="http://credit.casrai.org/">Investigation</role><role content-type="http://credit.casrai.org/">Methodology</role><role content-type="http://credit.casrai.org/">Project administration</role><role content-type="http://credit.casrai.org/">Resources</role><role content-type="http://credit.casrai.org/">Software</role><role content-type="http://credit.casrai.org/">Supervision</role><role content-type="http://credit.casrai.org/">Validation</role><role content-type="http://credit.casrai.org/">Writing – original draft</role><role content-type="http://credit.casrai.org/">Writing – review & editing</role><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="aff" rid="aff003"><sup>3</sup></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib></contrib-group><aff id="aff001"><label>1</label><addr-line>UFR Sciences et Techniques, Université de Nantes, 2 rue de la Houssinière, Nantes, France</addr-line></aff><aff id="aff002"><label>2</label><addr-line>Institute for Glycomics and School of Information and Communication Technology, Griffith University, Gold Coast, QLD, Australia</addr-line></aff><aff id="aff003"><label>3</label><addr-line>Shandong Provincial Key Laboratory of Biophysics, Institute of Biophysics, Dezhou University, Dezhou, China</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Randau</surname><given-names>Lennart</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Max-Planck-Institut fur terrestrische Mikrobiologie, GERMANY</addr-line></aff><author-notes><fn fn-type="COI-statement" id="coi001"><p><bold>Competing Interests: </bold>The authors have declared that no competing interests exist.</p></fn><corresp id="cor001">* E-mail: <email>yaoqi.zhou@griffith.edu.au</email></corresp></author-notes><pub-date pub-type="epub"><day>14</day><month>9</month><year>2017</year></pub-date><pub-date pub-type="collection"><year>2017</year></pub-date><volume>12</volume><issue>9</issue><elocation-id>e0184722</elocation-id><history><date date-type="received"><day>23</day><month>6</month><year>2017</year></date><date date-type="accepted"><day>29</day><month>8</month><year>2017</year></date></history><permissions><copyright-statement>© 2017 Jegousse et al</copyright-statement><copyright-year>2017</copyright-year><copyright-holder>Jegousse et al</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="pone.0184722.pdf"></self-uri><abstract><p>Temperature adaptation of bacterial RNAs is a subject of both fundamental and practical interest because it will allow a better understanding of molecular mechanism of RNA folding with potential industrial application of functional thermophilic or psychrophilic RNAs. Here, we performed a comprehensive study of rRNA, tRNA, and mRNA of more than 200 bacterial species with optimal growth temperatures (OGT) ranging from 4°C to 95°C. We investigated temperature adaptation at primary, secondary and tertiary structure levels. We showed that unlike mRNA, tRNA and rRNA were optimized for their structures at compositional levels with significant tertiary structural features even for their corresponding randomly permutated sequences. tRNA and rRNA are more exposed to solvent but remain structured for hyperthermophiles with nearly OGT-independent fluctuation of solvent accessible surface area within a single RNA chain. mRNA in hyperthermophiles is essentially the same as random sequences without tertiary structures although many mRNA in mesophiles and psychrophiles have well-defined tertiary structures based on their low overall solvent exposure with clear separation of deeply buried from partly exposed bases as in tRNA and rRNA. These results provide new insight into temperature adaptation of different RNAs.</p></abstract><funding-group><award-group id="award001"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100000925</institution-id><institution>National Health and Medical Research Council</institution></institution-wrap></funding-source><award-id>1059775 and 1083450</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-9958-5699</contrib-id><name><surname>Zhou</surname><given-names>Yaoqi</given-names></name></principal-award-recipient></award-group><award-group id="award002"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100001809</institution-id><institution>National Natural Science Foundation of China</institution></institution-wrap></funding-source><award-id>61671107</award-id><principal-award-recipient><name><surname>Wang</surname><given-names>Jihua</given-names></name></principal-award-recipient></award-group><award-group id="award003"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100001809</institution-id><institution>National Natural Science Foundation of China</institution></institution-wrap></funding-source><award-id>61540025</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-9958-5699</contrib-id><name><surname>Zhou</surname><given-names>Yaoqi</given-names></name></principal-award-recipient></award-group><funding-statement>This work was supported in part by National Natural Science Foundation of China (61671107) to YY and JW, by the Taishan Scholars Program of Shandong province of China, National Natural Science Foundation of China (61540025), and National Health and Medical Research Council (1059775 and 1083450) of Australia to YZ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement></funding-group><counts><fig-count count="7"></fig-count><table-count count="0"></table-count><page-count count="14"></page-count></counts><custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>Data are available within Harvard Dataverse (doi:<ext-link ext-link-type="uri" xlink:href="https://doi.org/10.7910/DVN/9DDRNU">10.7910/DVN/9DDRNU</ext-link>).</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>Data are available within Harvard Dataverse (doi:<ext-link ext-link-type="uri" xlink:href="https://doi.org/10.7910/DVN/9DDRNU">10.7910/DVN/9DDRNU</ext-link>).</p></notes></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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