Oogenesis and lipid metabolism in the deep-sea sponge Phakellia ventilabrum (Linnaeus, 1767)

Sponges contain an astounding diversity of lipids that serve in several biological functions, including yolk formation in their oocytes and embryos. The study of lipid metabolism during reproduction can provide information on food‑web dynamics and energetic needs of the populations in their habitats...

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Autores: Koutsouveli, Vasiliki, Balgoma, David, Checa, Antonio, Hedeland, Mikael, Riesgo Gil, Ana, Cárdenas, Paco
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2022
País:España
Recursos:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/270951
Acesso em linha:http://hdl.handle.net/10261/270951
Access Level:acceso abierto
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spelling Oogenesis and lipid metabolism in the deep-sea sponge Phakellia ventilabrum (Linnaeus, 1767)Oogenesis and lipid metabolism in the deep‑sea sponge Phakellia ventilabrum (Linnaeus, 1767)Koutsouveli, VasilikiBalgoma, DavidCheca, AntonioHedeland, MikaelRiesgo Gil, AnaCárdenas, PacoSponges contain an astounding diversity of lipids that serve in several biological functions, including yolk formation in their oocytes and embryos. The study of lipid metabolism during reproduction can provide information on food‑web dynamics and energetic needs of the populations in their habitats, however, there are no studies focusing on the lipid metabolism of sponges during their seasonal reproduction. In this study, we used histology, lipidome profiling (UHPLC‑MS), and transcriptomic analysis (RNA‑seq) on the deep‑sea sponge Phakellia ventilabrum (Demospongiae, Bubarida), a key species of North‑Atlantic sponge grounds, with the goal to (i) assess the reproductive strategy and seasonality of this species, (ii) examine the relative changes in the lipidome signal and the gene expression patterns of the enzymes participating in lipid metabolism during oogenesis. Phakellia ventilabrum is an oviparous and most certainly gonochoristic species, reproducing in May and September in the different studied areas. Half of the specimens were reproducing, generating two to five oocytes per mm 2 . Oocytes accumulated lipid droplets and as oogenesis progressed, the signal of most of the unsaturated and monounsaturated triacylglycerides increased, as well as of a few other phospholipids. In parallel, we detected upregulation of genes in female tissues related to triacylglyceride biosynthesis and others related to fatty acid beta‑oxidation. Triacylglycerides are likely the main type of lipid forming the yolk in P. ventilabrum since this lipid category has the most marked changes. In parallel, other lipid categories were engaged in fatty acid beta‑oxidation to cover the energy requirements of female individuals during oogenesis. In this study, the reproductive activity of the sponge P. ventilabrum was studied for the first time uncovering their seasonality and revealing 759 lipids, including 155 triacylglycerides. Our study has ecological and evolutionary implications providing essential information for understanding the molecular basis of reproduction and the origins and formation of lipid yolk in early‑branching metazoans.Open access funding provided by Uppsala University. This work was supported by the H2020 EU Framework Programme for Research and Innovation Project SponGES (Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation) (Grant Agreement No. 679849). Funding was also provided by a grant of the Spanish Ministry of Science and Innovation (PID2019-105769GB-I00) to AR and by María Zambrano Program (Next Generation EU), Proyecto de Internacionalización de la Unidad de Excelencia IBGM (CL-EI-2021 IBGM), and Programa Estratégico IBGM (CCVC8485) to DB.Peer reviewedNature Publishing GroupUppsala UniversityEuropean CommissionMinisterio de Ciencia e Innovación (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202220222022info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/270951reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/EC/H2020/679849info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-105769GB-I00Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2709512026-05-22T06:33:51Z
dc.title.none.fl_str_mv Oogenesis and lipid metabolism in the deep-sea sponge Phakellia ventilabrum (Linnaeus, 1767)
Oogenesis and lipid metabolism in the deep‑sea sponge Phakellia ventilabrum (Linnaeus, 1767)
title Oogenesis and lipid metabolism in the deep-sea sponge Phakellia ventilabrum (Linnaeus, 1767)
spellingShingle Oogenesis and lipid metabolism in the deep-sea sponge Phakellia ventilabrum (Linnaeus, 1767)
Koutsouveli, Vasiliki
title_short Oogenesis and lipid metabolism in the deep-sea sponge Phakellia ventilabrum (Linnaeus, 1767)
title_full Oogenesis and lipid metabolism in the deep-sea sponge Phakellia ventilabrum (Linnaeus, 1767)
title_fullStr Oogenesis and lipid metabolism in the deep-sea sponge Phakellia ventilabrum (Linnaeus, 1767)
title_full_unstemmed Oogenesis and lipid metabolism in the deep-sea sponge Phakellia ventilabrum (Linnaeus, 1767)
title_sort Oogenesis and lipid metabolism in the deep-sea sponge Phakellia ventilabrum (Linnaeus, 1767)
dc.creator.none.fl_str_mv Koutsouveli, Vasiliki
Balgoma, David
Checa, Antonio
Hedeland, Mikael
Riesgo Gil, Ana
Cárdenas, Paco
author Koutsouveli, Vasiliki
author_facet Koutsouveli, Vasiliki
Balgoma, David
Checa, Antonio
Hedeland, Mikael
Riesgo Gil, Ana
Cárdenas, Paco
author_role author
author2 Balgoma, David
Checa, Antonio
Hedeland, Mikael
Riesgo Gil, Ana
Cárdenas, Paco
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv Uppsala University
European Commission
Ministerio de Ciencia e Innovación (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
description Sponges contain an astounding diversity of lipids that serve in several biological functions, including yolk formation in their oocytes and embryos. The study of lipid metabolism during reproduction can provide information on food‑web dynamics and energetic needs of the populations in their habitats, however, there are no studies focusing on the lipid metabolism of sponges during their seasonal reproduction. In this study, we used histology, lipidome profiling (UHPLC‑MS), and transcriptomic analysis (RNA‑seq) on the deep‑sea sponge Phakellia ventilabrum (Demospongiae, Bubarida), a key species of North‑Atlantic sponge grounds, with the goal to (i) assess the reproductive strategy and seasonality of this species, (ii) examine the relative changes in the lipidome signal and the gene expression patterns of the enzymes participating in lipid metabolism during oogenesis. Phakellia ventilabrum is an oviparous and most certainly gonochoristic species, reproducing in May and September in the different studied areas. Half of the specimens were reproducing, generating two to five oocytes per mm 2 . Oocytes accumulated lipid droplets and as oogenesis progressed, the signal of most of the unsaturated and monounsaturated triacylglycerides increased, as well as of a few other phospholipids. In parallel, we detected upregulation of genes in female tissues related to triacylglyceride biosynthesis and others related to fatty acid beta‑oxidation. Triacylglycerides are likely the main type of lipid forming the yolk in P. ventilabrum since this lipid category has the most marked changes. In parallel, other lipid categories were engaged in fatty acid beta‑oxidation to cover the energy requirements of female individuals during oogenesis. In this study, the reproductive activity of the sponge P. ventilabrum was studied for the first time uncovering their seasonality and revealing 759 lipids, including 155 triacylglycerides. Our study has ecological and evolutionary implications providing essential information for understanding the molecular basis of reproduction and the origins and formation of lipid yolk in early‑branching metazoans.
publishDate 2022
dc.date.none.fl_str_mv 2022
2022
2022
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
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status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/270951
url http://hdl.handle.net/10261/270951
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
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info:eu-repo/grantAgreement/EC/H2020/679849
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-105769GB-I00
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Nature Publishing Group
publisher.none.fl_str_mv Nature Publishing Group
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
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instname_str Consejo Superior de Investigaciones Científicas (CSIC)
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