Gilthead seabream mucus glycosylation is complex, differs between epithelial sites and carries unusual poly N-acetylhexosamine motifs

Gilthead seabream (Sparus aurata) is a marine finfish of economic importance in aquaculture. Despite its adaptability to varying culture conditions, gilthead seabream culture can be affected by viral, bacterial or parasitic diseases. The main route of entry of pathogens is through mucosal surfaces....

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Detalhes bibliográficos
Autores: Thomsson, Kristina A., Benktander, John, Toxqui-Rodríguez, S., Piazzon de Haro, María Carla, Linden, Sara K.
Tipo de documento: artigo
Estado:Versão publicada
Data de publicação:2024
País:España
Recursos:Consejo Superior de Investigaciones Científicas (CSIC)
Repositório:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/373364
Acesso em linha:http://hdl.handle.net/10261/373364
Access Level:Acceso aberto
Palavra-chave:Epithelial surface
Mucosal defense
Mucus barrier
O-Glycans
N-Glycans
Glycomics
Microbiota
RNAseq
Mass spectrometry
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spelling Gilthead seabream mucus glycosylation is complex, differs between epithelial sites and carries unusual poly N-acetylhexosamine motifsThomsson, Kristina A.Benktander, JohnToxqui-Rodríguez, S.Piazzon de Haro, María CarlaLinden, Sara K.Epithelial surfaceMucosal defenseMucus barrierO-GlycansN-GlycansGlycomicsMicrobiotaRNAseqMass spectrometryGilthead seabream (Sparus aurata) is a marine finfish of economic importance in aquaculture. Despite its adaptability to varying culture conditions, gilthead seabream culture can be affected by viral, bacterial or parasitic diseases. The main route of entry of pathogens is through mucosal surfaces. Teleost external and internal surfaces are covered by mucus, mainly comprised of highly glycosylated proteins called mucins. The mucin glycans regulate pathogen growth, adhesion, virulence and inter and intra species communication. Here, we characterized the gilthead seabream mucus glycosylation, compared it to previously described species and investigated associations with microbiota. 214 glycans were identified. The majority of the glycans were found at more than one epithelial surface, but 27, 22 and 89 O-glycan structures were unique to skin, gill and intestinal sample groups, respectively. Six O-glycan core types were observed. The majority of the seabream skin and gill O-glycans were neutral with unusual poly HexNAc motifs. In contrast, seabream intestinal O-glycans were highly acidic and not of the ‘poly HexNAc’ type observed in skin and gill. Furthermore, gilthead seabream gill mucosa had less oligomannose and more complex N-glycans compared to skin and intestine. The concentration and diversity of bacteria was similar in skin, gill and intestine, but the bacterial species differed between epithelia and co-varied with glycan epitopes. The presence of a complex mucus glycosylation with plenty of glycan epitopes for bacterial foraging, suggest that the skin mucosal defense in seabream includes an abundant resident microbiota. This large library of structures provides a platform for further studies, for example aiming to identifying glycans to use for diagnostic purposes, to study host-microbe interactions or disease intervention therapies.The work was supported by the project MucosalFrontier (PID2020-115070RA-I00) funded by MCIN/AEI/10.13039/501100011033, the Swedish Research Council Formas (2018–01419), the Carl Tryggers (23–02971), Engkvists and Wilhelm and Martina Lundgrens Foundations.Peer reviewedElsevierMinisterio de Ciencia, Innovación y Universidades (España)Agencia Estatal de Investigación (España)Swedish Research CouncilCarl Trygger FoundationOlle Engkvist FoundationConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202420242024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/373364reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-115070RA-I00The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI http://doi.org/10.50821/GLYCOPOST-GPST000422https://doi.org/10.1016/j.fsi.2024.109864Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3733642026-05-22T06:33:51Z
dc.title.none.fl_str_mv Gilthead seabream mucus glycosylation is complex, differs between epithelial sites and carries unusual poly N-acetylhexosamine motifs
title Gilthead seabream mucus glycosylation is complex, differs between epithelial sites and carries unusual poly N-acetylhexosamine motifs
spellingShingle Gilthead seabream mucus glycosylation is complex, differs between epithelial sites and carries unusual poly N-acetylhexosamine motifs
Thomsson, Kristina A.
Epithelial surface
Mucosal defense
Mucus barrier
O-Glycans
N-Glycans
Glycomics
Microbiota
RNAseq
Mass spectrometry
title_short Gilthead seabream mucus glycosylation is complex, differs between epithelial sites and carries unusual poly N-acetylhexosamine motifs
title_full Gilthead seabream mucus glycosylation is complex, differs between epithelial sites and carries unusual poly N-acetylhexosamine motifs
title_fullStr Gilthead seabream mucus glycosylation is complex, differs between epithelial sites and carries unusual poly N-acetylhexosamine motifs
title_full_unstemmed Gilthead seabream mucus glycosylation is complex, differs between epithelial sites and carries unusual poly N-acetylhexosamine motifs
title_sort Gilthead seabream mucus glycosylation is complex, differs between epithelial sites and carries unusual poly N-acetylhexosamine motifs
dc.creator.none.fl_str_mv Thomsson, Kristina A.
Benktander, John
Toxqui-Rodríguez, S.
Piazzon de Haro, María Carla
Linden, Sara K.
author Thomsson, Kristina A.
author_facet Thomsson, Kristina A.
Benktander, John
Toxqui-Rodríguez, S.
Piazzon de Haro, María Carla
Linden, Sara K.
author_role author
author2 Benktander, John
Toxqui-Rodríguez, S.
Piazzon de Haro, María Carla
Linden, Sara K.
author2_role author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia, Innovación y Universidades (España)
Agencia Estatal de Investigación (España)
Swedish Research Council
Carl Trygger Foundation
Olle Engkvist Foundation
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Epithelial surface
Mucosal defense
Mucus barrier
O-Glycans
N-Glycans
Glycomics
Microbiota
RNAseq
Mass spectrometry
topic Epithelial surface
Mucosal defense
Mucus barrier
O-Glycans
N-Glycans
Glycomics
Microbiota
RNAseq
Mass spectrometry
description Gilthead seabream (Sparus aurata) is a marine finfish of economic importance in aquaculture. Despite its adaptability to varying culture conditions, gilthead seabream culture can be affected by viral, bacterial or parasitic diseases. The main route of entry of pathogens is through mucosal surfaces. Teleost external and internal surfaces are covered by mucus, mainly comprised of highly glycosylated proteins called mucins. The mucin glycans regulate pathogen growth, adhesion, virulence and inter and intra species communication. Here, we characterized the gilthead seabream mucus glycosylation, compared it to previously described species and investigated associations with microbiota. 214 glycans were identified. The majority of the glycans were found at more than one epithelial surface, but 27, 22 and 89 O-glycan structures were unique to skin, gill and intestinal sample groups, respectively. Six O-glycan core types were observed. The majority of the seabream skin and gill O-glycans were neutral with unusual poly HexNAc motifs. In contrast, seabream intestinal O-glycans were highly acidic and not of the ‘poly HexNAc’ type observed in skin and gill. Furthermore, gilthead seabream gill mucosa had less oligomannose and more complex N-glycans compared to skin and intestine. The concentration and diversity of bacteria was similar in skin, gill and intestine, but the bacterial species differed between epithelia and co-varied with glycan epitopes. The presence of a complex mucus glycosylation with plenty of glycan epitopes for bacterial foraging, suggest that the skin mucosal defense in seabream includes an abundant resident microbiota. This large library of structures provides a platform for further studies, for example aiming to identifying glycans to use for diagnostic purposes, to study host-microbe interactions or disease intervention therapies.
publishDate 2024
dc.date.none.fl_str_mv 2024
2024
2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/373364
url http://hdl.handle.net/10261/373364
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-115070RA-I00
The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI http://doi.org/10.50821/GLYCOPOST-GPST000422
https://doi.org/10.1016/j.fsi.2024.109864
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
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