Structural and Physiological Analyses of the Alkanesulphonate-Binding Protein (SsuA) of the Citrus Pathogen Xanthomonas citri
Identifieur interne : 000979 ( Pmc/Checkpoint ); précédent : 000978; suivant : 000980Structural and Physiological Analyses of the Alkanesulphonate-Binding Protein (SsuA) of the Citrus Pathogen Xanthomonas citri
Auteurs : Fabiano T Foli De Araújo [Brésil] ; Victor M. Bolanos-Garcia [Royaume-Uni] ; Cristiane T. Pereira [Brésil] ; Mario Sanches [Canada] ; Elisa E. Oshiro [Brésil] ; Rita C. C. Ferreira [Brésil] ; Dimitri Y. Chigardze [Royaume-Uni] ; João Alexandre Gonçalves Barbosa [Brésil] ; Luís Carlos De Souza Ferreira [Brésil] ; Celso E. Benedetti [Brésil] ; Tom L. Blundell [Royaume-Uni] ; Andrea Balan [Brésil]Source :
- PLoS ONE [ 1932-6203 ] ; 2013.
Abstract
The uptake of sulphur-containing compounds plays a pivotal role in the physiology of bacteria that live in aerobic soils where organosulfur compounds such as sulphonates and sulphate esters represent more than 95% of the available sulphur. Until now, no information has been available on the uptake of sulphonates by bacterial plant pathogens, particularly those of the
A single operon-like gene cluster (
The present study unravels unique structural and functional features of the
Url:
DOI: 10.1371/journal.pone.0080083
PubMed: 24282519
PubMed Central: 3839906
Affiliations:
- Brésil, Canada, Royaume-Uni
- Angleterre, Angleterre de l'Est, État de São Paulo
- Cambridge, São Paulo
- Université de Cambridge, Université de São Paulo
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PMC:3839906Le document en format XML
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Structural and Physiological Analyses of the Alkanesulphonate-Binding Protein (SsuA) of the Citrus Pathogen <italic>Xanthomonas citri</italic>
</title>
<author><name sortKey="T Foli De Araujo, Fabiano" sort="T Foli De Araujo, Fabiano" uniqKey="T Foli De Araujo F" first="Fabiano" last="T Foli De Araújo">Fabiano T Foli De Araújo</name>
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<author><name sortKey="Bolanos Garcia, Victor M" sort="Bolanos Garcia, Victor M" uniqKey="Bolanos Garcia V" first="Victor M." last="Bolanos-Garcia">Victor M. Bolanos-Garcia</name>
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<author><name sortKey="Chigardze, Dimitri Y" sort="Chigardze, Dimitri Y" uniqKey="Chigardze D" first="Dimitri Y." last="Chigardze">Dimitri Y. Chigardze</name>
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<author><name sortKey="Barbosa, Joao Alexandre Goncalves" sort="Barbosa, Joao Alexandre Goncalves" uniqKey="Barbosa J" first="João Alexandre Gonçalves" last="Barbosa">João Alexandre Gonçalves Barbosa</name>
<affiliation wicri:level="1"><nlm:aff id="aff5"><addr-line>Departamento de Genética, Universidade Católica de Brasília, Brasilia, Districto Federal, Brazil</addr-line>
</nlm:aff>
<country xml:lang="fr">Brésil</country>
<wicri:regionArea>Departamento de Genética, Universidade Católica de Brasília, Brasilia, Districto Federal</wicri:regionArea>
<wicri:noRegion>Districto Federal</wicri:noRegion>
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<author><name sortKey="De Souza Ferreira, Luis Carlos" sort="De Souza Ferreira, Luis Carlos" uniqKey="De Souza Ferreira L" first="Luís Carlos" last="De Souza Ferreira">Luís Carlos De Souza Ferreira</name>
<affiliation wicri:level="4"><nlm:aff id="aff1"><addr-line>Departamento de Microbiologia, Universidade de São Paulo, São Paulo, São Paulo, Brazil</addr-line>
</nlm:aff>
<country xml:lang="fr">Brésil</country>
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<placeName><settlement type="city">São Paulo</settlement>
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</placeName>
<orgName type="university">Université de São Paulo</orgName>
</affiliation>
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<author><name sortKey="Benedetti, Celso E" sort="Benedetti, Celso E" uniqKey="Benedetti C" first="Celso E." last="Benedetti">Celso E. Benedetti</name>
<affiliation wicri:level="3"><nlm:aff id="aff3"><addr-line>Laboratório Nacional de Biociências, Centro de Pesquisa em Energia e Materiais, Campinas, São Paulo, Brazil</addr-line>
</nlm:aff>
<country xml:lang="fr">Brésil</country>
<wicri:regionArea>Laboratório Nacional de Biociências, Centro de Pesquisa em Energia e Materiais, Campinas, São Paulo</wicri:regionArea>
<placeName><settlement type="city">São Paulo</settlement>
<region type="state">État de São Paulo</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Blundell, Tom L" sort="Blundell, Tom L" uniqKey="Blundell T" first="Tom L." last="Blundell">Tom L. Blundell</name>
<affiliation wicri:level="4"><nlm:aff id="aff2"><addr-line>Department of Biochemistry, University of Cambridge, Cambridge, United Kingdom</addr-line>
</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>Department of Biochemistry, University of Cambridge, Cambridge</wicri:regionArea>
<orgName type="university">Université de Cambridge</orgName>
<placeName><settlement type="city">Cambridge</settlement>
<region type="country">Angleterre</region>
<region type="région" nuts="1">Angleterre de l'Est</region>
</placeName>
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<author><name sortKey="Balan, Andrea" sort="Balan, Andrea" uniqKey="Balan A" first="Andrea" last="Balan">Andrea Balan</name>
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</nlm:aff>
<country xml:lang="fr">Brésil</country>
<wicri:regionArea>Laboratório Nacional de Biociências, Centro de Pesquisa em Energia e Materiais, Campinas, São Paulo</wicri:regionArea>
<placeName><settlement type="city">São Paulo</settlement>
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</placeName>
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<series><title level="j">PLoS ONE</title>
<idno type="eISSN">1932-6203</idno>
<imprint><date when="2013">2013</date>
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<front><div type="abstract" xml:lang="en"><sec><title>Background</title>
<p>The uptake of sulphur-containing compounds plays a pivotal role in the physiology of bacteria that live in aerobic soils where organosulfur compounds such as sulphonates and sulphate esters represent more than 95% of the available sulphur. Until now, no information has been available on the uptake of sulphonates by bacterial plant pathogens, particularly those of the <italic>Xanthomonas</italic>
genus, which encompasses several pathogenic species. In the present study, we characterised the alkanesulphonate uptake system (Ssu) of <italic>Xanthomonas axonopodis</italic>
pv. <italic>citri</italic>
306 strain (<italic>X. citri</italic>
), the etiological agent of citrus canker.</p>
</sec>
<sec><title>Methodology/Principal Findings</title>
<p>A single operon-like gene cluster (<italic>ssuEDACB</italic>
) that encodes both the sulphur uptake system and enzymes involved in desulphurisation was detected in the genomes of <italic>X. citri</italic>
and of the closely related species. We characterised <italic>X. citri</italic>
SsuA protein, a periplasmic alkanesulphonate-binding protein that, together with SsuC and SsuB, defines the alkanesulphonate uptake system. The crystal structure of SsuA bound to MOPS, MES and HEPES, which is herein described for the first time, provides evidence for the importance of a conserved dipole in sulphate group coordination, identifies specific amino acids interacting with the sulphate group and shows the presence of a rather large binding pocket that explains the rather wide range of molecules recognised by the protein. Isolation of an isogenic <italic>ssuA-</italic>
knockout derivative of the <italic>X. citri</italic>
306 strain showed that disruption of alkanesulphonate uptake affects both xanthan gum production and generation of canker lesions in sweet orange leaves.</p>
</sec>
<sec><title>Conclusions/Significance</title>
<p>The present study unravels unique structural and functional features of the <italic>X. citri</italic>
SsuA protein and provides the first experimental evidence that an ABC uptake system affects the virulence of this phytopathogen.</p>
</sec>
</div>
</front>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<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, USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">24282519</article-id>
<article-id pub-id-type="pmc">3839906</article-id>
<article-id pub-id-type="publisher-id">PONE-D-13-16274</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0080083</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Structural and Physiological Analyses of the Alkanesulphonate-Binding Protein (SsuA) of the Citrus Pathogen <italic>Xanthomonas citri</italic>
</article-title>
<alt-title alt-title-type="running-head">The SsuA Protein from <italic>Xanthomonas citri</italic>
</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Tófoli de Araújo</surname>
<given-names>Fabiano</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bolanos-Garcia</surname>
<given-names>Victor M.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Pereira</surname>
<given-names>Cristiane T.</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Sanches</surname>
<given-names>Mario</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Oshiro</surname>
<given-names>Elisa E.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ferreira</surname>
<given-names>Rita C. C.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chigardze</surname>
<given-names>Dimitri Y.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Barbosa</surname>
<given-names>João Alexandre Gonçalves</given-names>
</name>
<xref ref-type="aff" rid="aff5"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>de Souza Ferreira</surname>
<given-names>Luís Carlos</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Benedetti</surname>
<given-names>Celso E.</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Blundell</surname>
<given-names>Tom L.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Balan</surname>
<given-names>Andrea</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>*</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
<addr-line>Departamento de Microbiologia, Universidade de São Paulo, São Paulo, São Paulo, Brazil</addr-line>
</aff>
<aff id="aff2"><label>2</label>
<addr-line>Department of Biochemistry, University of Cambridge, Cambridge, United Kingdom</addr-line>
</aff>
<aff id="aff3"><label>3</label>
<addr-line>Laboratório Nacional de Biociências, Centro de Pesquisa em Energia e Materiais, Campinas, São Paulo, Brazil</addr-line>
</aff>
<aff id="aff4"><label>4</label>
<addr-line>Monte Sinai Hospital, Toronto, Ontario, Canada</addr-line>
</aff>
<aff id="aff5"><label>5</label>
<addr-line>Departamento de Genética, Universidade Católica de Brasília, Brasilia, Districto Federal, Brazil</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Hofmann</surname>
<given-names>Andreas</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>Griffith University, Australia</addr-line>
</aff>
<author-notes><corresp id="cor1">* E-mail: <email>andrea.balan@lnbio.cnpem.br</email>
</corresp>
<fn fn-type="conflict"><p><bold>Competing Interests: </bold>
The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con"><p>Conceived and designed the experiments: AB LCSF CB. Performed the experiments: FA CTP MS DC AB. Analyzed the data: AB LCSF TLB VBG JB. Contributed reagents/materials/analysis tools: RF EO. Wrote the paper: AB LCSF.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2013</year>
</pub-date>
<pub-date pub-type="epub"><day>25</day>
<month>11</month>
<year>2013</year>
</pub-date>
<volume>8</volume>
<issue>11</issue>
<elocation-id>e80083</elocation-id>
<history><date date-type="received"><day>22</day>
<month>4</month>
<year>2013</year>
</date>
<date date-type="accepted"><day>9</day>
<month>10</month>
<year>2013</year>
</date>
</history>
<permissions><copyright-year>2013</copyright-year>
<copyright-holder>Tófoli de Araújo, et al</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/3.0/"><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/3.0/">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>
<abstract><sec><title>Background</title>
<p>The uptake of sulphur-containing compounds plays a pivotal role in the physiology of bacteria that live in aerobic soils where organosulfur compounds such as sulphonates and sulphate esters represent more than 95% of the available sulphur. Until now, no information has been available on the uptake of sulphonates by bacterial plant pathogens, particularly those of the <italic>Xanthomonas</italic>
genus, which encompasses several pathogenic species. In the present study, we characterised the alkanesulphonate uptake system (Ssu) of <italic>Xanthomonas axonopodis</italic>
pv. <italic>citri</italic>
306 strain (<italic>X. citri</italic>
), the etiological agent of citrus canker.</p>
</sec>
<sec><title>Methodology/Principal Findings</title>
<p>A single operon-like gene cluster (<italic>ssuEDACB</italic>
) that encodes both the sulphur uptake system and enzymes involved in desulphurisation was detected in the genomes of <italic>X. citri</italic>
and of the closely related species. We characterised <italic>X. citri</italic>
SsuA protein, a periplasmic alkanesulphonate-binding protein that, together with SsuC and SsuB, defines the alkanesulphonate uptake system. The crystal structure of SsuA bound to MOPS, MES and HEPES, which is herein described for the first time, provides evidence for the importance of a conserved dipole in sulphate group coordination, identifies specific amino acids interacting with the sulphate group and shows the presence of a rather large binding pocket that explains the rather wide range of molecules recognised by the protein. Isolation of an isogenic <italic>ssuA-</italic>
knockout derivative of the <italic>X. citri</italic>
306 strain showed that disruption of alkanesulphonate uptake affects both xanthan gum production and generation of canker lesions in sweet orange leaves.</p>
</sec>
<sec><title>Conclusions/Significance</title>
<p>The present study unravels unique structural and functional features of the <italic>X. citri</italic>
SsuA protein and provides the first experimental evidence that an ABC uptake system affects the virulence of this phytopathogen.</p>
</sec>
</abstract>
<funding-group><funding-statement>This work was supported by Fundação de Amparo àPesquisa do Estado de São Paulo and the Conselho Nacional de Pesquisas. 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><page-count count="14"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Brésil</li>
<li>Canada</li>
<li>Royaume-Uni</li>
</country>
<region><li>Angleterre</li>
<li>Angleterre de l'Est</li>
<li>État de São Paulo</li>
</region>
<settlement><li>Cambridge</li>
<li>São Paulo</li>
</settlement>
<orgName><li>Université de Cambridge</li>
<li>Université de São Paulo</li>
</orgName>
</list>
<tree><country name="Brésil"><region name="État de São Paulo"><name sortKey="T Foli De Araujo, Fabiano" sort="T Foli De Araujo, Fabiano" uniqKey="T Foli De Araujo F" first="Fabiano" last="T Foli De Araújo">Fabiano T Foli De Araújo</name>
</region>
<name sortKey="Balan, Andrea" sort="Balan, Andrea" uniqKey="Balan A" first="Andrea" last="Balan">Andrea Balan</name>
<name sortKey="Barbosa, Joao Alexandre Goncalves" sort="Barbosa, Joao Alexandre Goncalves" uniqKey="Barbosa J" first="João Alexandre Gonçalves" last="Barbosa">João Alexandre Gonçalves Barbosa</name>
<name sortKey="Benedetti, Celso E" sort="Benedetti, Celso E" uniqKey="Benedetti C" first="Celso E." last="Benedetti">Celso E. Benedetti</name>
<name sortKey="De Souza Ferreira, Luis Carlos" sort="De Souza Ferreira, Luis Carlos" uniqKey="De Souza Ferreira L" first="Luís Carlos" last="De Souza Ferreira">Luís Carlos De Souza Ferreira</name>
<name sortKey="Ferreira, Rita C C" sort="Ferreira, Rita C C" uniqKey="Ferreira R" first="Rita C. C." last="Ferreira">Rita C. C. Ferreira</name>
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