Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians

Autores
Bartoová-Sojková, Pavla; Kyslík, Jiˇrí; Alama Bermejo, Gema; Hartigan, Ashlie; Atkinson, Stephen D.; Bartholomew, Jerri; Picard-Sánchez, Amparo; Palenzuela, Oswaldo; Faber, Marc Nicolas; Holland, Jason W.; Holzer, Astrid Sybylle
Año de publicación
2021
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The evolutionary aspects of cystatins are greatly underexplored in early-emerging metazoans. Thus, we surveyed the gene organization, protein architecture, and phylogeny of cystatin homologues mined from 110 genomes and the transcriptomes of 58 basal metazoan species, encompassing free-living and parasite taxa of Porifera, Placozoa, Cnidaria (including Myxozoa), and Ctenophora. We found that the cystatin gene repertoire significantly differs among phyla, with stefins present in most of the investigated lineages but with type 2 cystatins missing in several basal metazoan groups. Similar to liver and intestinal flukes, myxozoan parasites possess atypical stefins with chimeric structure that combine motifs of classical stefins and type 2 cystatins. Other early metazoan taxa regardless of lifestyle have only the classical representation of cystatins and lack multi-domain ones. Our comprehensive phylogenetic analyses revealed that stefins and type 2 cystatins clustered into taxonomically defined clades with multiple independent paralogous groups, which probably arose due to gene duplications. The stefin clade split between the subclades of classical stefins and the atypical stefins of myxozoans and flukes. Atypical stefins represent key evolutionary innovations of the two parasite groups for which their origin might have been linked with ancestral gene chimerization, obligate parasitism, life cycle complexity, genome reduction, and host immunity.
Fil: Bartoová-Sojková, Pavla. Academy of Sciences of the Czech Republic. Biology Centre. Institute of Parasitology; República Checa
Fil: Kyslík, Jiˇrí. Academy of Sciences of the Czech Republic. Biology Centre. Institute of Parasitology; República Checa. University of South Bohemia; República Checa
Fil: Alama Bermejo, Gema. Academy of Sciences of the Czech Republic. Biology Centre. Institute of Parasitology; República Checa
Fil: Hartigan, Ashlie. Natural History Museum; Reino Unido
Fil: Atkinson, Stephen D.. State University of Oregon; Estados Unidos
Fil: Bartholomew, Jerri. State University of Oregon; Estados Unidos
Fil: Picard-Sánchez, Amparo. Academy of Sciences of the Czech Republic. Biology Centre. Institute of Parasitology; República Checa. Instituto de Acuicultura Torre de la Sal; España
Fil: Palenzuela, Oswaldo. Instituto de Acuicultura Torre de la Sal; España
Fil: Faber, Marc Nicolas. University of Aberdeen; Reino Unido
Fil: Holland, Jason W.. University Of Aberdeeen; Reino Unido
Fil: Holzer, Astrid Sybylle. Academy of Sciences of the Czech Republic. Biology Centre. Institute of Parasitology; República Checa
Materia
CYSTEINE PROTEASE INHIBITOR
STEFIN
SIGNAL PEPTIDE
PARASITE
PHYLOGENETIC ANALYSIS
DIVERSIFICATION
PROTEIN STRUCTURE
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/162195
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/162195
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic CnidariansBartoová-Sojková, PavlaKyslík, JiˇríAlama Bermejo, GemaHartigan, AshlieAtkinson, Stephen D.Bartholomew, JerriPicard-Sánchez, AmparoPalenzuela, OswaldoFaber, Marc NicolasHolland, Jason W.Holzer, Astrid SybylleCYSTEINE PROTEASE INHIBITORSTEFINSIGNAL PEPTIDEPARASITEPHYLOGENETIC ANALYSISDIVERSIFICATIONPROTEIN STRUCTUREhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1The evolutionary aspects of cystatins are greatly underexplored in early-emerging metazoans. Thus, we surveyed the gene organization, protein architecture, and phylogeny of cystatin homologues mined from 110 genomes and the transcriptomes of 58 basal metazoan species, encompassing free-living and parasite taxa of Porifera, Placozoa, Cnidaria (including Myxozoa), and Ctenophora. We found that the cystatin gene repertoire significantly differs among phyla, with stefins present in most of the investigated lineages but with type 2 cystatins missing in several basal metazoan groups. Similar to liver and intestinal flukes, myxozoan parasites possess atypical stefins with chimeric structure that combine motifs of classical stefins and type 2 cystatins. Other early metazoan taxa regardless of lifestyle have only the classical representation of cystatins and lack multi-domain ones. Our comprehensive phylogenetic analyses revealed that stefins and type 2 cystatins clustered into taxonomically defined clades with multiple independent paralogous groups, which probably arose due to gene duplications. The stefin clade split between the subclades of classical stefins and the atypical stefins of myxozoans and flukes. Atypical stefins represent key evolutionary innovations of the two parasite groups for which their origin might have been linked with ancestral gene chimerization, obligate parasitism, life cycle complexity, genome reduction, and host immunity.Fil: Bartoová-Sojková, Pavla. Academy of Sciences of the Czech Republic. Biology Centre. Institute of Parasitology; República ChecaFil: Kyslík, Jiˇrí. Academy of Sciences of the Czech Republic. Biology Centre. Institute of Parasitology; República Checa. University of South Bohemia; República ChecaFil: Alama Bermejo, Gema. Academy of Sciences of the Czech Republic. Biology Centre. Institute of Parasitology; República ChecaFil: Hartigan, Ashlie. Natural History Museum; Reino UnidoFil: Atkinson, Stephen D.. State University of Oregon; Estados UnidosFil: Bartholomew, Jerri. State University of Oregon; Estados UnidosFil: Picard-Sánchez, Amparo. Academy of Sciences of the Czech Republic. Biology Centre. Institute of Parasitology; República Checa. Instituto de Acuicultura Torre de la Sal; EspañaFil: Palenzuela, Oswaldo. Instituto de Acuicultura Torre de la Sal; EspañaFil: Faber, Marc Nicolas. University of Aberdeen; Reino UnidoFil: Holland, Jason W.. University Of Aberdeeen; Reino UnidoFil: Holzer, Astrid Sybylle. Academy of Sciences of the Czech Republic. Biology Centre. Institute of Parasitology; República ChecaMDPI AG2021-02info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/162195Bartoová-Sojková, Pavla; Kyslík, Jiˇrí; Alama Bermejo, Gema; Hartigan, Ashlie; Atkinson, Stephen D.; et al.; Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians; MDPI AG; Biology; 10; 2; 2-2021; 1-162079-7737CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.3390/biology10020110info:eu-repo/semantics/altIdentifier/url/https://www.mdpi.com/2079-7737/10/2/110info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:59:06Zoai:ri.conicet.gov.ar:11336/162195instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 09:59:06.891CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians
title Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians
spellingShingle Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians
Bartoová-Sojková, Pavla
CYSTEINE PROTEASE INHIBITOR
STEFIN
SIGNAL PEPTIDE
PARASITE
PHYLOGENETIC ANALYSIS
DIVERSIFICATION
PROTEIN STRUCTURE
title_short Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians
title_full Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians
title_fullStr Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians
title_full_unstemmed Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians
title_sort Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians
dc.creator.none.fl_str_mv Bartoová-Sojková, Pavla
Kyslík, Jiˇrí
Alama Bermejo, Gema
Hartigan, Ashlie
Atkinson, Stephen D.
Bartholomew, Jerri
Picard-Sánchez, Amparo
Palenzuela, Oswaldo
Faber, Marc Nicolas
Holland, Jason W.
Holzer, Astrid Sybylle
author Bartoová-Sojková, Pavla
author_facet Bartoová-Sojková, Pavla
Kyslík, Jiˇrí
Alama Bermejo, Gema
Hartigan, Ashlie
Atkinson, Stephen D.
Bartholomew, Jerri
Picard-Sánchez, Amparo
Palenzuela, Oswaldo
Faber, Marc Nicolas
Holland, Jason W.
Holzer, Astrid Sybylle
author_role author
author2 Kyslík, Jiˇrí
Alama Bermejo, Gema
Hartigan, Ashlie
Atkinson, Stephen D.
Bartholomew, Jerri
Picard-Sánchez, Amparo
Palenzuela, Oswaldo
Faber, Marc Nicolas
Holland, Jason W.
Holzer, Astrid Sybylle
author2_role author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv CYSTEINE PROTEASE INHIBITOR
STEFIN
SIGNAL PEPTIDE
PARASITE
PHYLOGENETIC ANALYSIS
DIVERSIFICATION
PROTEIN STRUCTURE
topic CYSTEINE PROTEASE INHIBITOR
STEFIN
SIGNAL PEPTIDE
PARASITE
PHYLOGENETIC ANALYSIS
DIVERSIFICATION
PROTEIN STRUCTURE
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv The evolutionary aspects of cystatins are greatly underexplored in early-emerging metazoans. Thus, we surveyed the gene organization, protein architecture, and phylogeny of cystatin homologues mined from 110 genomes and the transcriptomes of 58 basal metazoan species, encompassing free-living and parasite taxa of Porifera, Placozoa, Cnidaria (including Myxozoa), and Ctenophora. We found that the cystatin gene repertoire significantly differs among phyla, with stefins present in most of the investigated lineages but with type 2 cystatins missing in several basal metazoan groups. Similar to liver and intestinal flukes, myxozoan parasites possess atypical stefins with chimeric structure that combine motifs of classical stefins and type 2 cystatins. Other early metazoan taxa regardless of lifestyle have only the classical representation of cystatins and lack multi-domain ones. Our comprehensive phylogenetic analyses revealed that stefins and type 2 cystatins clustered into taxonomically defined clades with multiple independent paralogous groups, which probably arose due to gene duplications. The stefin clade split between the subclades of classical stefins and the atypical stefins of myxozoans and flukes. Atypical stefins represent key evolutionary innovations of the two parasite groups for which their origin might have been linked with ancestral gene chimerization, obligate parasitism, life cycle complexity, genome reduction, and host immunity.
Fil: Bartoová-Sojková, Pavla. Academy of Sciences of the Czech Republic. Biology Centre. Institute of Parasitology; República Checa
Fil: Kyslík, Jiˇrí. Academy of Sciences of the Czech Republic. Biology Centre. Institute of Parasitology; República Checa. University of South Bohemia; República Checa
Fil: Alama Bermejo, Gema. Academy of Sciences of the Czech Republic. Biology Centre. Institute of Parasitology; República Checa
Fil: Hartigan, Ashlie. Natural History Museum; Reino Unido
Fil: Atkinson, Stephen D.. State University of Oregon; Estados Unidos
Fil: Bartholomew, Jerri. State University of Oregon; Estados Unidos
Fil: Picard-Sánchez, Amparo. Academy of Sciences of the Czech Republic. Biology Centre. Institute of Parasitology; República Checa. Instituto de Acuicultura Torre de la Sal; España
Fil: Palenzuela, Oswaldo. Instituto de Acuicultura Torre de la Sal; España
Fil: Faber, Marc Nicolas. University of Aberdeen; Reino Unido
Fil: Holland, Jason W.. University Of Aberdeeen; Reino Unido
Fil: Holzer, Astrid Sybylle. Academy of Sciences of the Czech Republic. Biology Centre. Institute of Parasitology; República Checa
description The evolutionary aspects of cystatins are greatly underexplored in early-emerging metazoans. Thus, we surveyed the gene organization, protein architecture, and phylogeny of cystatin homologues mined from 110 genomes and the transcriptomes of 58 basal metazoan species, encompassing free-living and parasite taxa of Porifera, Placozoa, Cnidaria (including Myxozoa), and Ctenophora. We found that the cystatin gene repertoire significantly differs among phyla, with stefins present in most of the investigated lineages but with type 2 cystatins missing in several basal metazoan groups. Similar to liver and intestinal flukes, myxozoan parasites possess atypical stefins with chimeric structure that combine motifs of classical stefins and type 2 cystatins. Other early metazoan taxa regardless of lifestyle have only the classical representation of cystatins and lack multi-domain ones. Our comprehensive phylogenetic analyses revealed that stefins and type 2 cystatins clustered into taxonomically defined clades with multiple independent paralogous groups, which probably arose due to gene duplications. The stefin clade split between the subclades of classical stefins and the atypical stefins of myxozoans and flukes. Atypical stefins represent key evolutionary innovations of the two parasite groups for which their origin might have been linked with ancestral gene chimerization, obligate parasitism, life cycle complexity, genome reduction, and host immunity.
publishDate 2021
dc.date.none.fl_str_mv 2021-02
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/162195
Bartoová-Sojková, Pavla; Kyslík, Jiˇrí; Alama Bermejo, Gema; Hartigan, Ashlie; Atkinson, Stephen D.; et al.; Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians; MDPI AG; Biology; 10; 2; 2-2021; 1-16
2079-7737
CONICET Digital
CONICET
url http://hdl.handle.net/11336/162195
identifier_str_mv Bartoová-Sojková, Pavla; Kyslík, Jiˇrí; Alama Bermejo, Gema; Hartigan, Ashlie; Atkinson, Stephen D.; et al.; Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians; MDPI AG; Biology; 10; 2; 2-2021; 1-16
2079-7737
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.3390/biology10020110
info:eu-repo/semantics/altIdentifier/url/https://www.mdpi.com/2079-7737/10/2/110
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv MDPI AG
publisher.none.fl_str_mv MDPI AG
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.070432

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