The transcriptional aftermath in two independently formed hybrids of the opportunistic pathogen Candida orthopsilosis

Interspecific hybridization can drive evolutionary adaptation to novel environments. The Saccharomycotina clade of budding yeasts includes many hybrid lineages, and hybridization has been proposed as a source for new pathogenic species. Candida orthopsilosis is an emerging opportunistic pathogen for...

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Detalles Bibliográficos
Autores: Hovhannisyan, Hrant, 1992-, Saus Martínez, Ester, Ksiezopolska, Ewa, Gabaldón Estevan, Juan Antonio, 1973-
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2020
País:España
Institución:Universitat Pompeu Fabra
Repositorio:Repositorio Digital de la UPF
OAI Identifier:oai:repositori.upf.edu:10230/46780
Acceso en línea:http://hdl.handle.net/10230/46780
http://dx.doi.org/10.1128/mSphere.00282-20
Access Level:acceso abierto
Palabra clave:Candida orthopsilosis
Hybridization
Pathogen
Transcriptomics
Yeasts
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spelling The transcriptional aftermath in two independently formed hybrids of the opportunistic pathogen Candida orthopsilosisHovhannisyan, Hrant, 1992-Saus Martínez, EsterKsiezopolska, EwaGabaldón Estevan, Juan Antonio, 1973-Candida orthopsilosisHybridizationPathogenTranscriptomicsYeastsInterspecific hybridization can drive evolutionary adaptation to novel environments. The Saccharomycotina clade of budding yeasts includes many hybrid lineages, and hybridization has been proposed as a source for new pathogenic species. Candida orthopsilosis is an emerging opportunistic pathogen for which most clinical isolates are hybrids, each derived from one of at least four independent crosses between the same two parental lineages. To gain insight into the transcriptomic aftermath of hybridization in these pathogens, we analyzed allele-specific gene expression in two independently formed hybrid strains and in a homozygous strain representative of one parental lineage. Our results show that the effect of hybridization on overall gene expression is rather limited, affecting ∼4% of the genes studied. However, we identified a larger effect in terms of imbalanced allelic expression, affecting ∼9.5% of the heterozygous genes in the hybrids. This effect was larger in the hybrid with more extensive loss of heterozygosity, which may indicate a tendency to avoid loss of heterozygosity in these genes. Consistently, the number of shared genes with allele-specific expression in the two independently formed hybrids was higher than random expectation, suggesting selective retention. Some of the imbalanced genes have functions related to pathogenicity, including zinc transport and superoxide dismutase activities. While it remains unclear whether the observed imbalanced genes play a role in virulence, our results suggest that differences in allele-specific expression may add an additional layer of phenotypic plasticity to traits related to virulence in C. orthopsilosis hybrids.IMPORTANCE How new pathogens emerge is an important question that remains largely unanswered. Some emerging yeast pathogens are hybrids originated through the crossing of two different species, but how hybridization contributes to higher virulence is unclear. Here, we show that hybrids selectively retain gene regulation plasticity inherited from the two parents and that this plasticity affects genes involved in virulence.This work received funding from the European Union’s Horizon 2020 Research and Innovation Program under the Marie Skłodowska-Curie grant agreement H2020-MSCA-ITN-2014-642095. T.G.’s research group also acknowledges support from the Spanish Ministry of Economy, Industry, and Competitiveness (MEIC) for the EMBL partnership, from grants “Centro de Excelencia Severo Ochoa 2013–2017” SEV-2012-0208, and BFU2015-67107 cofounded by European Regional Development Fund (ERDF), from the CERCA Program/Generalitat de Catalunya, from the Catalan Research Agency (AGAUR) SGR857, and grants from the European Union’s Horizon 2020 Research and Innovation Program under grant agreement ERC-2016-724173. T.G. also receives support from an INB grant (PT17/0009/0023 – ISCIII-SGEFI/ERDF).American Society for Microbiology202120212020info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/46780http://dx.doi.org/10.1128/mSphere.00282-20reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésmSphere. 2020; 5(3):e00282-20info:eu-repo/grantAgreement/EC/H2020/642095info:eu-repo/grantAgreement/ES/1PE/BFU2015-67107info:eu-repo/grantAgreement/EC/H2020/724173Copyright © 2020 Hovhannisyan et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license https://creativecommons.org/licenses/by/4.0/https://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/467802026-06-12T07:21:37Z
dc.title.none.fl_str_mv The transcriptional aftermath in two independently formed hybrids of the opportunistic pathogen Candida orthopsilosis
title The transcriptional aftermath in two independently formed hybrids of the opportunistic pathogen Candida orthopsilosis
spellingShingle The transcriptional aftermath in two independently formed hybrids of the opportunistic pathogen Candida orthopsilosis
Hovhannisyan, Hrant, 1992-
Candida orthopsilosis
Hybridization
Pathogen
Transcriptomics
Yeasts
title_short The transcriptional aftermath in two independently formed hybrids of the opportunistic pathogen Candida orthopsilosis
title_full The transcriptional aftermath in two independently formed hybrids of the opportunistic pathogen Candida orthopsilosis
title_fullStr The transcriptional aftermath in two independently formed hybrids of the opportunistic pathogen Candida orthopsilosis
title_full_unstemmed The transcriptional aftermath in two independently formed hybrids of the opportunistic pathogen Candida orthopsilosis
title_sort The transcriptional aftermath in two independently formed hybrids of the opportunistic pathogen Candida orthopsilosis
dc.creator.none.fl_str_mv Hovhannisyan, Hrant, 1992-
Saus Martínez, Ester
Ksiezopolska, Ewa
Gabaldón Estevan, Juan Antonio, 1973-
author Hovhannisyan, Hrant, 1992-
author_facet Hovhannisyan, Hrant, 1992-
Saus Martínez, Ester
Ksiezopolska, Ewa
Gabaldón Estevan, Juan Antonio, 1973-
author_role author
author2 Saus Martínez, Ester
Ksiezopolska, Ewa
Gabaldón Estevan, Juan Antonio, 1973-
author2_role author
author
author
dc.subject.none.fl_str_mv Candida orthopsilosis
Hybridization
Pathogen
Transcriptomics
Yeasts
topic Candida orthopsilosis
Hybridization
Pathogen
Transcriptomics
Yeasts
description Interspecific hybridization can drive evolutionary adaptation to novel environments. The Saccharomycotina clade of budding yeasts includes many hybrid lineages, and hybridization has been proposed as a source for new pathogenic species. Candida orthopsilosis is an emerging opportunistic pathogen for which most clinical isolates are hybrids, each derived from one of at least four independent crosses between the same two parental lineages. To gain insight into the transcriptomic aftermath of hybridization in these pathogens, we analyzed allele-specific gene expression in two independently formed hybrid strains and in a homozygous strain representative of one parental lineage. Our results show that the effect of hybridization on overall gene expression is rather limited, affecting ∼4% of the genes studied. However, we identified a larger effect in terms of imbalanced allelic expression, affecting ∼9.5% of the heterozygous genes in the hybrids. This effect was larger in the hybrid with more extensive loss of heterozygosity, which may indicate a tendency to avoid loss of heterozygosity in these genes. Consistently, the number of shared genes with allele-specific expression in the two independently formed hybrids was higher than random expectation, suggesting selective retention. Some of the imbalanced genes have functions related to pathogenicity, including zinc transport and superoxide dismutase activities. While it remains unclear whether the observed imbalanced genes play a role in virulence, our results suggest that differences in allele-specific expression may add an additional layer of phenotypic plasticity to traits related to virulence in C. orthopsilosis hybrids.IMPORTANCE How new pathogens emerge is an important question that remains largely unanswered. Some emerging yeast pathogens are hybrids originated through the crossing of two different species, but how hybridization contributes to higher virulence is unclear. Here, we show that hybrids selectively retain gene regulation plasticity inherited from the two parents and that this plasticity affects genes involved in virulence.
publishDate 2020
dc.date.none.fl_str_mv 2020
2021
2021
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/46780
http://dx.doi.org/10.1128/mSphere.00282-20
url http://hdl.handle.net/10230/46780
http://dx.doi.org/10.1128/mSphere.00282-20
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv mSphere. 2020; 5(3):e00282-20
info:eu-repo/grantAgreement/EC/H2020/642095
info:eu-repo/grantAgreement/ES/1PE/BFU2015-67107
info:eu-repo/grantAgreement/EC/H2020/724173
dc.rights.none.fl_str_mv https://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv American Society for Microbiology
publisher.none.fl_str_mv American Society for Microbiology
dc.source.none.fl_str_mv reponame:Repositorio Digital de la UPF
instname:Universitat Pompeu Fabra
instname_str Universitat Pompeu Fabra
reponame_str Repositorio Digital de la UPF
collection Repositorio Digital de la UPF
repository.name.fl_str_mv
repository.mail.fl_str_mv
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