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UV hyper-resistance in Prochlorococcus MED4 results from a single base pair deletion just upstream of an operon encoding nudix hydrolase and photolyase

Identifieur interne : 000525 ( Pmc/Curation ); précédent : 000524; suivant : 000526

UV hyper-resistance in Prochlorococcus MED4 results from a single base pair deletion just upstream of an operon encoding nudix hydrolase and photolyase

Auteurs : Marcia S. Osburne [États-Unis] ; Brianne M. Holmbeck [États-Unis] ; Jorge Frias-Lopez [États-Unis] ; Robert Steen [États-Unis] ; Katherine Huang [États-Unis] ; Libusha Kelly [États-Unis] ; Allison Coe [États-Unis] ; Kristin Waraska [États-Unis] ; Andrew Gagne [États-Unis] ; Sallie W. Chisholm [États-Unis]

Source :

RBID : PMC:2955971

Abstract

Exposure to solar radiation can cause mortality in natural communities of pico-phytoplankton, both at the surface and to a depth of at least 30 m. DNA damage is a significant cause of death, mainly due to cyclobutane pyrimidine dimer formation, which can be lethal if not repaired. While developing a UV mutagenesis protocol for the marine cyanobacterium Prochlorococcus, we isolated a UV-hyper-resistant variant of high light-adapted strain MED4. The hyper-resistant strain was constitutively upregulated for expression of the mutT-phrB operon, encoding nudix hydrolase and photolyase, both of which are involved in repair of DNA damage that can be caused by UV light. Photolyase (PhrB) breaks pyrimidine dimers typically caused by UV exposure, using energy from visible light in the process known as photoreactivation. Nudix hydrolase (MutT) hydrolyses 8-oxo-dGTP, an aberrant form of GTP that results from oxidizing conditions, including UV radiation, thus impeding mispairing and mutagenesis by preventing incorporation of the aberrant form into DNA. These processes are error-free, in contrast to error-prone SOS dark repair systems that are widespread in bacteria. The UV-hyper-resistant strain contained only a single mutation: a 1 bp deletion in the intergenic region directly upstream of the mutT-phrB operon. Two subsequent enrichments for MED4 UV-hyper-resistant strains from MED4 wild-type cultures gave rise to strains containing this same 1 bp deletion, affirming its connection to the hyper-resistant phenotype. These results have implications for Prochlorococcus DNA repair mechanisms, genome stability and possibly lysogeny.


Url:
DOI: 10.1111/j.1462-2920.2010.02203.x
PubMed: 20345942
PubMed Central: 2955971

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PMC:2955971

Le document en format XML

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<p>Exposure to solar radiation can cause mortality in natural communities of pico-phytoplankton, both at the surface and to a depth of at least 30 m. DNA damage is a significant cause of death, mainly due to cyclobutane pyrimidine dimer formation, which can be lethal if not repaired. While developing a UV mutagenesis protocol for the marine cyanobacterium
<italic>Prochlorococcus</italic>
, we isolated a UV-hyper-resistant variant of high light-adapted strain MED4. The hyper-resistant strain was constitutively upregulated for expression of the
<italic>mutT</italic>
-
<italic>phrB</italic>
operon, encoding nudix hydrolase and photolyase, both of which are involved in repair of DNA damage that can be caused by UV light. Photolyase (PhrB) breaks pyrimidine dimers typically caused by UV exposure, using energy from visible light in the process known as photoreactivation. Nudix hydrolase (MutT) hydrolyses 8-oxo-dGTP, an aberrant form of GTP that results from oxidizing conditions, including UV radiation, thus impeding mispairing and mutagenesis by preventing incorporation of the aberrant form into DNA. These processes are error-free, in contrast to error-prone SOS dark repair systems that are widespread in bacteria. The UV-hyper-resistant strain contained only a single mutation: a 1 bp deletion in the intergenic region directly upstream of the
<italic>mutT</italic>
-
<italic>phrB</italic>
operon. Two subsequent enrichments for MED4 UV-hyper-resistant strains from MED4 wild-type cultures gave rise to strains containing this same 1 bp deletion, affirming its connection to the hyper-resistant phenotype. These results have implications for
<italic>Prochlorococcus</italic>
DNA repair mechanisms, genome stability and possibly lysogeny.</p>
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</TEI>
<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Environ Microbiol</journal-id>
<journal-id journal-id-type="publisher-id">emi</journal-id>
<journal-title-group>
<journal-title>Environmental Microbiology</journal-title>
</journal-title-group>
<issn pub-type="ppub">1462-2912</issn>
<issn pub-type="epub">1462-2920</issn>
<publisher>
<publisher-name>Blackwell Publishing Ltd</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">20345942</article-id>
<article-id pub-id-type="pmc">2955971</article-id>
<article-id pub-id-type="doi">10.1111/j.1462-2920.2010.02203.x</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Research Articles</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>UV hyper-resistance in
<italic>Prochlorococcus</italic>
MED4 results from a single base pair deletion just upstream of an operon encoding nudix hydrolase and photolyase</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Osburne</surname>
<given-names>Marcia S</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
<xref ref-type="corresp" rid="cor1">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Holmbeck</surname>
<given-names>Brianne M</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Frias-Lopez</surname>
<given-names>Jorge</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
<xref ref-type="author-notes" rid="fn1"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Steen</surname>
<given-names>Robert</given-names>
</name>
<xref ref-type="aff" rid="au2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Huang</surname>
<given-names>Katherine</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Kelly</surname>
<given-names>Libusha</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Coe</surname>
<given-names>Allison</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Waraska</surname>
<given-names>Kristin</given-names>
</name>
<xref ref-type="aff" rid="au2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Gagne</surname>
<given-names>Andrew</given-names>
</name>
<xref ref-type="aff" rid="au2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Chisholm</surname>
<given-names>Sallie W</given-names>
</name>
<xref ref-type="aff" rid="au1">1</xref>
</contrib>
<aff id="au1">
<label>1</label>
<institution>Department of Civil and Environmental Engineering, Massachusetts Institute of Technology</institution>
<addr-line>Cambridge, MA 02139, USA</addr-line>
</aff>
<aff id="au2">
<label>2</label>
<institution>Biopolymers Facility, Harvard Medical School</institution>
<addr-line>Boston, MA 02115, USA</addr-line>
</aff>
</contrib-group>
<author-notes>
<corresp id="cor1">*For correspondence. E-mail
<email>mosburne@mit.edu</email>
; Tel. (+1) 617 253 3310; Fax (+1) 617 258 7009.</corresp>
<fn fn-type="present-address" id="fn1">
<label></label>
<p>Present address: The Forsyth Institute, 140 The Fenway, Boston, MA 02115, USA.</p>
</fn>
<fn>
<p>Re-use of this article is permitted in accordance with the Terms and Conditions set out at
<ext-link ext-link-type="uri" xlink:href="http://www3.interscience.wiley.com/authorresources/onlineopen.html">http://www3.interscience.wiley.com/authorresources/onlineopen.html</ext-link>
</p>
</fn>
</author-notes>
<pub-date pub-type="ppub">
<month>7</month>
<year>2010</year>
</pub-date>
<volume>12</volume>
<issue>7</issue>
<fpage>1978</fpage>
<lpage>1988</lpage>
<history>
<date date-type="received">
<day>14</day>
<month>8</month>
<year>2009</year>
</date>
<date date-type="accepted">
<day>28</day>
<month>1</month>
<year>2010</year>
</date>
</history>
<permissions>
<copyright-statement>© 2010 Society for Applied Microbiology and Blackwell Publishing Ltd</copyright-statement>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/2.5/">
<license-p>Re-use of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation.</license-p>
</license>
</permissions>
<abstract>
<p>Exposure to solar radiation can cause mortality in natural communities of pico-phytoplankton, both at the surface and to a depth of at least 30 m. DNA damage is a significant cause of death, mainly due to cyclobutane pyrimidine dimer formation, which can be lethal if not repaired. While developing a UV mutagenesis protocol for the marine cyanobacterium
<italic>Prochlorococcus</italic>
, we isolated a UV-hyper-resistant variant of high light-adapted strain MED4. The hyper-resistant strain was constitutively upregulated for expression of the
<italic>mutT</italic>
-
<italic>phrB</italic>
operon, encoding nudix hydrolase and photolyase, both of which are involved in repair of DNA damage that can be caused by UV light. Photolyase (PhrB) breaks pyrimidine dimers typically caused by UV exposure, using energy from visible light in the process known as photoreactivation. Nudix hydrolase (MutT) hydrolyses 8-oxo-dGTP, an aberrant form of GTP that results from oxidizing conditions, including UV radiation, thus impeding mispairing and mutagenesis by preventing incorporation of the aberrant form into DNA. These processes are error-free, in contrast to error-prone SOS dark repair systems that are widespread in bacteria. The UV-hyper-resistant strain contained only a single mutation: a 1 bp deletion in the intergenic region directly upstream of the
<italic>mutT</italic>
-
<italic>phrB</italic>
operon. Two subsequent enrichments for MED4 UV-hyper-resistant strains from MED4 wild-type cultures gave rise to strains containing this same 1 bp deletion, affirming its connection to the hyper-resistant phenotype. These results have implications for
<italic>Prochlorococcus</italic>
DNA repair mechanisms, genome stability and possibly lysogeny.</p>
</abstract>
</article-meta>
</front>
</pmc>
</record>

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