Transportome remodeling of a symbiotic microalga inside a planktonic host
Metabolic exchange is one of the foundations of symbiotic associations between organisms and is a driving force in evolution. In the ocean, photosymbiosis between heterotrophic hosts and microalgae is powered by photosynthesis and relies on the transfer of organic carbon to the host (e.g. sugars). Y...
| Autores: | , , , , , , , , , |
|---|---|
| Tipo de recurso: | artículo |
| Estado: | Versión publicada |
| Fecha de publicación: | 2024 |
| País: | España |
| Institución: | Consejo Superior de Investigaciones Científicas (CSIC) |
| Repositorio: | DIGITAL.CSIC. Repositorio Institucional del CSIC |
| OAI Identifier: | oai:digital.csic.es:10261/383328 |
| Acceso en línea: | http://hdl.handle.net/10261/383328 https://api.elsevier.com/content/abstract/scopus_id/85214553157 |
| Access Level: | acceso abierto |
| Palabra clave: | Transporters Carbon exchange Metatranscriptomics Microalga Planktonic photosymbiosis Protists Single-cell transcriptomic Sugars |
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Transportome remodeling of a symbiotic microalga inside a planktonic host |
| title |
Transportome remodeling of a symbiotic microalga inside a planktonic host |
| spellingShingle |
Transportome remodeling of a symbiotic microalga inside a planktonic host Juéry, Caroline Transporters Carbon exchange Metatranscriptomics Microalga Planktonic photosymbiosis Protists Single-cell transcriptomic Sugars |
| title_short |
Transportome remodeling of a symbiotic microalga inside a planktonic host |
| title_full |
Transportome remodeling of a symbiotic microalga inside a planktonic host |
| title_fullStr |
Transportome remodeling of a symbiotic microalga inside a planktonic host |
| title_full_unstemmed |
Transportome remodeling of a symbiotic microalga inside a planktonic host |
| title_sort |
Transportome remodeling of a symbiotic microalga inside a planktonic host |
| dc.creator.none.fl_str_mv |
Juéry, Caroline Auladell, Adria Füssy, Zoltan Chevalier, Fabien Yee, Daniel P. Pelletier, Eric Corre, Erwan Allen, Andrew E. Richter, Daniel J. Decelle, Johan |
| author |
Juéry, Caroline |
| author_facet |
Juéry, Caroline Auladell, Adria Füssy, Zoltan Chevalier, Fabien Yee, Daniel P. Pelletier, Eric Corre, Erwan Allen, Andrew E. Richter, Daniel J. Decelle, Johan |
| author_role |
author |
| author2 |
Auladell, Adria Füssy, Zoltan Chevalier, Fabien Yee, Daniel P. Pelletier, Eric Corre, Erwan Allen, Andrew E. Richter, Daniel J. Decelle, Johan |
| author2_role |
author author author author author author author author author |
| dc.contributor.none.fl_str_mv |
Centre National de la Recherche Scientifique (France) European Commission European Research Council National Oceanic and Atmospheric Administration (US) National Science Foundation (US) Department of Energy (US) Generalitat de Catalunya Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72] |
| dc.subject.none.fl_str_mv |
Transporters Carbon exchange Metatranscriptomics Microalga Planktonic photosymbiosis Protists Single-cell transcriptomic Sugars |
| topic |
Transporters Carbon exchange Metatranscriptomics Microalga Planktonic photosymbiosis Protists Single-cell transcriptomic Sugars |
| description |
Metabolic exchange is one of the foundations of symbiotic associations between organisms and is a driving force in evolution. In the ocean, photosymbiosis between heterotrophic hosts and microalgae is powered by photosynthesis and relies on the transfer of organic carbon to the host (e.g. sugars). Yet, the identity of transferred carbohydrates as well as the molecular mechanisms that drive this exchange remain largely unknown, especially in unicellular photosymbioses that are widespread in the open ocean. Combining genomics, single-holobiont transcriptomics, and environmental metatranscriptomics, we revealed the transportome of the marine microalga Phaeocystis in symbiosis within acantharia, with a focus on sugar transporters. At the genomic level, the sugar transportome of Phaeocystis is comparable to non-symbiotic haptophytes. By contrast, we found significant remodeling of the expression of the transportome in symbiotic microalgae compared to the free-living stage. More particularly, 36% of sugar transporter genes were differentially expressed. Several of them, such as GLUTs, TPTs, and aquaporins, with glucose, triose-phosphate sugars, and glycerol as potential substrates, were upregulated at the holobiont and community level. We also showed that algal sugar transporter genes exhibit distinct temporal expression patterns during the day. This reprogramed transportome indicates that symbiosis has a major impact on sugar fluxes within and outside the algal cell, and highlights the complexity and the dynamics of metabolic exchanges between partners. This study improves our understanding of the molecular players of the metabolic connectivity underlying the ecological success of planktonic photosymbiosis and paves the way for more studies on transporters across photosymbiotic models. |
| publishDate |
2024 |
| dc.date.none.fl_str_mv |
2024 2025 2025 |
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info:eu-repo/semantics/article http://purl.org/coar/resource_type/c_6501 Publisher's version info:eu-repo/semantics/publishedVersion |
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article |
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publishedVersion |
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http://hdl.handle.net/10261/383328 https://api.elsevier.com/content/abstract/scopus_id/85214553157 |
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http://hdl.handle.net/10261/383328 https://api.elsevier.com/content/abstract/scopus_id/85214553157 |
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Inglés |
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Inglés |
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#PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/EC/HE/101059915 info:eu-repo/grantAgreement/EC/HE/101088661 info:eu-repo/grantAgreement/EC/H2020/824110 info:eu-repo/grantAgreement/EC/H2020/949745 The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1093/ismejo/wrae239 https://doi.org/10.1093/ismejo/wrae239 Sí |
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info:eu-repo/semantics/openAccess |
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openAccess |
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application/pdf |
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Oxford University Press |
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Oxford University Press |
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reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC instname:Consejo Superior de Investigaciones Científicas (CSIC) |
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Consejo Superior de Investigaciones Científicas (CSIC) |
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DIGITAL.CSIC. Repositorio Institucional del CSIC |
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DIGITAL.CSIC. Repositorio Institucional del CSIC |
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1869420235162910720 |
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Transportome remodeling of a symbiotic microalga inside a planktonic hostJuéry, CarolineAuladell, AdriaFüssy, ZoltanChevalier, FabienYee, Daniel P.Pelletier, EricCorre, ErwanAllen, Andrew E.Richter, Daniel J.Decelle, JohanTransportersCarbon exchangeMetatranscriptomicsMicroalgaPlanktonic photosymbiosisProtistsSingle-cell transcriptomicSugarsMetabolic exchange is one of the foundations of symbiotic associations between organisms and is a driving force in evolution. In the ocean, photosymbiosis between heterotrophic hosts and microalgae is powered by photosynthesis and relies on the transfer of organic carbon to the host (e.g. sugars). Yet, the identity of transferred carbohydrates as well as the molecular mechanisms that drive this exchange remain largely unknown, especially in unicellular photosymbioses that are widespread in the open ocean. Combining genomics, single-holobiont transcriptomics, and environmental metatranscriptomics, we revealed the transportome of the marine microalga Phaeocystis in symbiosis within acantharia, with a focus on sugar transporters. At the genomic level, the sugar transportome of Phaeocystis is comparable to non-symbiotic haptophytes. By contrast, we found significant remodeling of the expression of the transportome in symbiotic microalgae compared to the free-living stage. More particularly, 36% of sugar transporter genes were differentially expressed. Several of them, such as GLUTs, TPTs, and aquaporins, with glucose, triose-phosphate sugars, and glycerol as potential substrates, were upregulated at the holobiont and community level. We also showed that algal sugar transporter genes exhibit distinct temporal expression patterns during the day. This reprogramed transportome indicates that symbiosis has a major impact on sugar fluxes within and outside the algal cell, and highlights the complexity and the dynamics of metabolic exchanges between partners. This study improves our understanding of the molecular players of the metabolic connectivity underlying the ecological success of planktonic photosymbiosis and paves the way for more studies on transporters across photosymbiotic models.Research was supported by CNRS and ATIP-Avenir program funding, and by the European Union (BIOcean5D—GA#101059915 and ERC—SymbiOCEAN—101088661). This project has received funding from the European Union’s Horizon 2020 research and innovation program under grant agreement no. 824110 for the sequencing (EASI Genomics). This project has received funding from the European Union’s Horizon 2020 research and innovation program under grant agreement no. 824110 for the sequencing (EASI Genomics). Z.F. and A.A. were funded by National Oceanic and Atmospheric Administration grant NA19NOS4780181 (to A.E.A.), the National Science Foundation (NSF-OCE-1756884 to A.E.A.), and the Simons Collaboration on Principles of Microbial Ecosystems (PriME; grant ID: 970820 to A.E.A.). Their work (proposal: 10.46936/10.25585/60001426) conducted in the US Department of Energy Joint Genome Institute (https://ror.org/04xm1d337), a DOE Office of Science User Facility, is supported by the Office of Science of the US Department of Energy operated under contract no. DE-AC02-05CH11231. A.A. and D.J.R. received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement 949745—GROWCEAN—ERC-2020-STG) and from the Departament de Recerca i Universitats de la Generalitat de Catalunya (exp. 2021 SGR 00751).Peer reviewedOxford University PressCentre National de la Recherche Scientifique (France)European CommissionEuropean Research CouncilNational Oceanic and Atmospheric Administration (US)National Science Foundation (US)Department of Energy (US)Generalitat de CatalunyaConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202520252024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/383328https://api.elsevier.com/content/abstract/scopus_id/85214553157reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/EC/HE/101059915info:eu-repo/grantAgreement/EC/HE/101088661info:eu-repo/grantAgreement/EC/H2020/824110info:eu-repo/grantAgreement/EC/H2020/949745The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1093/ismejo/wrae239https://doi.org/10.1093/ismejo/wrae239Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3833282026-05-22T06:33:51Z |
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15,812429 |