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Intracellular amorphous carbonates uncover a new biomineralization process in eukaryotes.

Identifieur interne : 000934 ( PubMed/Checkpoint ); précédent : 000933; suivant : 000935

Intracellular amorphous carbonates uncover a new biomineralization process in eukaryotes.

Auteurs : A. Martignier [Suisse] ; M. Pacton [France] ; M. Filella [Suisse] ; J-M Jaquet [Suisse] ; F. Barja [Suisse] ; K. Pollok [Allemagne] ; F. Langenhorst [Allemagne] ; S. Lavigne [Suisse] ; P. Guagliardo [Australie] ; M R Kilburn [Australie] ; C. Thomas [France] ; R. Martini [Suisse] ; D. Ariztegui [Suisse]

Source :

RBID : pubmed:27696636

Descripteurs français

English descriptors

Abstract

Until now, descriptions of intracellular biomineralization of amorphous inclusions involving alkaline-earth metal (AEM) carbonates other than calcium have been confined exclusively to cyanobacteria (Couradeau et al., 2012). Here, we report the first evidence of the presence of intracellular amorphous granules of AEM carbonates (calcium, strontium, and barium) in unicellular eukaryotes. These inclusions, which we have named micropearls, show concentric and oscillatory zoning on a nanometric scale. They are widespread in certain eukaryote phytoplankters of Lake Geneva (Switzerland) and represent a previously unknown type of non-skeletal biomineralization, revealing an unexpected pathway in the geochemical cycle of AEMs. We have identified Tetraselmis cf. cordiformis (Chlorophyta, Prasinophyceae) as being responsible for the formation of one micropearl type containing strontium ([Ca,Sr]CO3 ), which we also found in a cultured strain of Tetraselmis cordiformis. A different flagellated eukaryotic cell forms barium-rich micropearls [(Ca,Ba)CO3 ]. The strontium and barium concentrations of both micropearl types are extremely high compared with the undersaturated water of Lake Geneva (the Ba/Ca ratio of the micropearls is up to 800,000 times higher than in the water). This can only be explained by a high biological pre-concentration of these elements. The particular characteristics of the micropearls, along with the presence of organic sulfur-containing compounds-associated with and surrounding the micropearls-strongly suggest the existence of a yet-unreported intracellular biomineralization pathway in eukaryotic micro-organisms.

DOI: 10.1111/gbi.12213
PubMed: 27696636


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<div type="abstract" xml:lang="en">Until now, descriptions of intracellular biomineralization of amorphous inclusions involving alkaline-earth metal (AEM) carbonates other than calcium have been confined exclusively to cyanobacteria (Couradeau et al., 2012). Here, we report the first evidence of the presence of intracellular amorphous granules of AEM carbonates (calcium, strontium, and barium) in unicellular eukaryotes. These inclusions, which we have named micropearls, show concentric and oscillatory zoning on a nanometric scale. They are widespread in certain eukaryote phytoplankters of Lake Geneva (Switzerland) and represent a previously unknown type of non-skeletal biomineralization, revealing an unexpected pathway in the geochemical cycle of AEMs. We have identified Tetraselmis cf. cordiformis (Chlorophyta, Prasinophyceae) as being responsible for the formation of one micropearl type containing strontium ([Ca,Sr]CO3 ), which we also found in a cultured strain of Tetraselmis cordiformis. A different flagellated eukaryotic cell forms barium-rich micropearls [(Ca,Ba)CO3 ]. The strontium and barium concentrations of both micropearl types are extremely high compared with the undersaturated water of Lake Geneva (the Ba/Ca ratio of the micropearls is up to 800,000 times higher than in the water). This can only be explained by a high biological pre-concentration of these elements. The particular characteristics of the micropearls, along with the presence of organic sulfur-containing compounds-associated with and surrounding the micropearls-strongly suggest the existence of a yet-unreported intracellular biomineralization pathway in eukaryotic micro-organisms.</div>
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<ArticleTitle>Intracellular amorphous carbonates uncover a new biomineralization process in eukaryotes.</ArticleTitle>
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<MedlinePgn>240-253</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1111/gbi.12213</ELocationID>
<Abstract>
<AbstractText>Until now, descriptions of intracellular biomineralization of amorphous inclusions involving alkaline-earth metal (AEM) carbonates other than calcium have been confined exclusively to cyanobacteria (Couradeau et al., 2012). Here, we report the first evidence of the presence of intracellular amorphous granules of AEM carbonates (calcium, strontium, and barium) in unicellular eukaryotes. These inclusions, which we have named micropearls, show concentric and oscillatory zoning on a nanometric scale. They are widespread in certain eukaryote phytoplankters of Lake Geneva (Switzerland) and represent a previously unknown type of non-skeletal biomineralization, revealing an unexpected pathway in the geochemical cycle of AEMs. We have identified Tetraselmis cf. cordiformis (Chlorophyta, Prasinophyceae) as being responsible for the formation of one micropearl type containing strontium ([Ca,Sr]CO3 ), which we also found in a cultured strain of Tetraselmis cordiformis. A different flagellated eukaryotic cell forms barium-rich micropearls [(Ca,Ba)CO3 ]. The strontium and barium concentrations of both micropearl types are extremely high compared with the undersaturated water of Lake Geneva (the Ba/Ca ratio of the micropearls is up to 800,000 times higher than in the water). This can only be explained by a high biological pre-concentration of these elements. The particular characteristics of the micropearls, along with the presence of organic sulfur-containing compounds-associated with and surrounding the micropearls-strongly suggest the existence of a yet-unreported intracellular biomineralization pathway in eukaryotic micro-organisms.</AbstractText>
<CopyrightInformation>© 2016 John Wiley & Sons Ltd.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Martignier</LastName>
<ForeName>A</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>Department of Earth Sciences, University of Geneva, Geneva, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Pacton</LastName>
<ForeName>M</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Laboratoire de Géologie de Lyon, Lyon 1 University, Villeurbanne, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Filella</LastName>
<ForeName>M</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Institute F.-A. Forel, University of Geneva, Geneva, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Jaquet</LastName>
<ForeName>J-M</ForeName>
<Initials>JM</Initials>
<AffiliationInfo>
<Affiliation>Department of Earth Sciences, University of Geneva, Geneva, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Barja</LastName>
<ForeName>F</ForeName>
<Initials>F</Initials>
<AffiliationInfo>
<Affiliation>Microbiology unit, University of Geneva, Geneva, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Pollok</LastName>
<ForeName>K</ForeName>
<Initials>K</Initials>
<AffiliationInfo>
<Affiliation>Institute of Geosciences, Friedrich Schiller University Jena, Jena, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Langenhorst</LastName>
<ForeName>F</ForeName>
<Initials>F</Initials>
<AffiliationInfo>
<Affiliation>Institute of Geosciences, Friedrich Schiller University Jena, Jena, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Lavigne</LastName>
<ForeName>S</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Service de l'Ecologie de l'Eau (SECOE), Geneva, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Guagliardo</LastName>
<ForeName>P</ForeName>
<Initials>P</Initials>
<AffiliationInfo>
<Affiliation>Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, Perth, WA, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kilburn</LastName>
<ForeName>M R</ForeName>
<Initials>MR</Initials>
<AffiliationInfo>
<Affiliation>Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, Perth, WA, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Thomas</LastName>
<ForeName>C</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>CARRTEL of Thonon-les-Bains, INRA, Thonon-les-Bains, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Martini</LastName>
<ForeName>R</ForeName>
<Initials>R</Initials>
<AffiliationInfo>
<Affiliation>Department of Earth Sciences, University of Geneva, Geneva, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ariztegui</LastName>
<ForeName>D</ForeName>
<Initials>D</Initials>
<AffiliationInfo>
<Affiliation>Department of Earth Sciences, University of Geneva, Geneva, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2016</Year>
<Month>09</Month>
<Day>30</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>England</Country>
<MedlineTA>Geobiology</MedlineTA>
<NlmUniqueID>101185472</NlmUniqueID>
<ISSNLinking>1472-4669</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D002254">Carbonates</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D002254" MajorTopicYN="N">Carbonates</DescriptorName>
<QualifierName UI="Q000032" MajorTopicYN="Y">analysis</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D000460" MajorTopicYN="N">Chlorophyta</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="Y">chemistry</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D003593" MajorTopicYN="N">Cytoplasm</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="Y">chemistry</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D060106" MajorTopicYN="N">Lakes</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D053858" MajorTopicYN="Y">Metabolic Networks and Pathways</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010839" MajorTopicYN="N">Phytoplankton</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013557" MajorTopicYN="N">Switzerland</DescriptorName>
</MeshHeading>
</MeshHeadingList>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="received">
<Year>2016</Year>
<Month>04</Month>
<Day>27</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2016</Year>
<Month>08</Month>
<Day>25</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="pubmed">
<Year>2016</Year>
<Month>10</Month>
<Day>4</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline">
<Year>2017</Year>
<Month>9</Month>
<Day>7</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2016</Year>
<Month>10</Month>
<Day>4</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">27696636</ArticleId>
<ArticleId IdType="doi">10.1111/gbi.12213</ArticleId>
</ArticleIdList>
</PubmedData>
</pubmed>
<affiliations>
<list>
<country>
<li>Allemagne</li>
<li>Australie</li>
<li>France</li>
<li>Suisse</li>
</country>
<region>
<li>Auvergne-Rhône-Alpes</li>
<li>Canton de Genève</li>
<li>Rhône-Alpes</li>
</region>
<settlement>
<li>Genève</li>
<li>Lyon</li>
<li>Thonon-les-Bains</li>
<li>Villeurbanne</li>
</settlement>
<orgName>
<li>Université de Genève</li>
</orgName>
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<region name="Canton de Genève">
<name sortKey="Martignier, A" sort="Martignier, A" uniqKey="Martignier A" first="A" last="Martignier">A. Martignier</name>
</region>
<name sortKey="Ariztegui, D" sort="Ariztegui, D" uniqKey="Ariztegui D" first="D" last="Ariztegui">D. Ariztegui</name>
<name sortKey="Barja, F" sort="Barja, F" uniqKey="Barja F" first="F" last="Barja">F. Barja</name>
<name sortKey="Filella, M" sort="Filella, M" uniqKey="Filella M" first="M" last="Filella">M. Filella</name>
<name sortKey="Jaquet, J M" sort="Jaquet, J M" uniqKey="Jaquet J" first="J-M" last="Jaquet">J-M Jaquet</name>
<name sortKey="Lavigne, S" sort="Lavigne, S" uniqKey="Lavigne S" first="S" last="Lavigne">S. Lavigne</name>
<name sortKey="Martini, R" sort="Martini, R" uniqKey="Martini R" first="R" last="Martini">R. Martini</name>
</country>
<country name="France">
<region name="Auvergne-Rhône-Alpes">
<name sortKey="Pacton, M" sort="Pacton, M" uniqKey="Pacton M" first="M" last="Pacton">M. Pacton</name>
</region>
<name sortKey="Thomas, C" sort="Thomas, C" uniqKey="Thomas C" first="C" last="Thomas">C. Thomas</name>
</country>
<country name="Allemagne">
<noRegion>
<name sortKey="Pollok, K" sort="Pollok, K" uniqKey="Pollok K" first="K" last="Pollok">K. Pollok</name>
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<name sortKey="Langenhorst, F" sort="Langenhorst, F" uniqKey="Langenhorst F" first="F" last="Langenhorst">F. Langenhorst</name>
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<name sortKey="Guagliardo, P" sort="Guagliardo, P" uniqKey="Guagliardo P" first="P" last="Guagliardo">P. Guagliardo</name>
</noRegion>
<name sortKey="Kilburn, M R" sort="Kilburn, M R" uniqKey="Kilburn M" first="M R" last="Kilburn">M R Kilburn</name>
</country>
</tree>
</affiliations>
</record>

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