Dynamics of Wolbachia pipientis gene expression across the Drosophila melanogaster life cycle

Detalhes bibliográficos
Autor(a) principal: Florence Gutzwiller
Data de Publicação: 2015
Outros Autores: Catarina R. Carmo, Danny E. Miller, Danny W. Rice, Irene L. Newton, R. Scott Hawley, Luis Teixeira, Casey M. Bergman
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: http://hdl.handle.net/10400.7/535
Resumo: Symbiotic interactions between microbes and their multicellular hosts have manifold impacts on molecular, cellular and organismal biology. To identify candidate bacterial genes involved in maintaining endosymbiotic associations with insect hosts, we analyzed genome-wide patterns of gene expression in the alpha-proteobacteria Wolbachia pipientis across the life cycle of Drosophila melanogaster using public data from the modENCODE project that was generated in a Wolbachia-infected version of the ISO1 reference strain. We find that the majority of Wolbachia genes are expressed at detectable levels in D. melanogaster across the entire life cycle, but that only 7.8% of 1195 Wolbachia genes exhibit robust stage- or sex-specific expression differences when studied in the "holo-organism" context. Wolbachia genes that are differentially expressed during development are typically up-regulated after D. melanogaster embryogenesis, and include many bacterial membrane, secretion system and ankyrin-repeat containing proteins. Sex-biased genes are often organised as small operons of uncharacterised genes and are mainly up-regulated in adult males D. melanogaster in an age-dependent manner suggesting a potential role in cytoplasmic incompatibility. Our results indicate that large changes in Wolbachia gene expression across the Drosophila life-cycle are relatively rare when assayed across all host tissues, but that candidate genes to understand host-microbe interaction in facultative endosymbionts can be successfully identified using holo-organism expression profiling. Our work also shows that mining public gene expression data in D. melanogaster provides a rich set of resources to probe the functional basis of the Wolbachia-Drosophila symbiosis and annotate the transcriptional outputs of the Wolbachia genome.
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spelling Dynamics of Wolbachia pipientis gene expression across the Drosophila melanogaster life cycleWolbachiaDrosophilasymbiosisdevelopmentcytoplasmic incompatibilitySymbiotic interactions between microbes and their multicellular hosts have manifold impacts on molecular, cellular and organismal biology. To identify candidate bacterial genes involved in maintaining endosymbiotic associations with insect hosts, we analyzed genome-wide patterns of gene expression in the alpha-proteobacteria Wolbachia pipientis across the life cycle of Drosophila melanogaster using public data from the modENCODE project that was generated in a Wolbachia-infected version of the ISO1 reference strain. We find that the majority of Wolbachia genes are expressed at detectable levels in D. melanogaster across the entire life cycle, but that only 7.8% of 1195 Wolbachia genes exhibit robust stage- or sex-specific expression differences when studied in the "holo-organism" context. Wolbachia genes that are differentially expressed during development are typically up-regulated after D. melanogaster embryogenesis, and include many bacterial membrane, secretion system and ankyrin-repeat containing proteins. Sex-biased genes are often organised as small operons of uncharacterised genes and are mainly up-regulated in adult males D. melanogaster in an age-dependent manner suggesting a potential role in cytoplasmic incompatibility. Our results indicate that large changes in Wolbachia gene expression across the Drosophila life-cycle are relatively rare when assayed across all host tissues, but that candidate genes to understand host-microbe interaction in facultative endosymbionts can be successfully identified using holo-organism expression profiling. Our work also shows that mining public gene expression data in D. melanogaster provides a rich set of resources to probe the functional basis of the Wolbachia-Drosophila symbiosis and annotate the transcriptional outputs of the Wolbachia genome.National Environment Research Council Ph.D. studentship (F.G.), Fundação para a Ciência e a Tecnologia postdoctoral fellowship: (SFRH/BPD/73420/2010), Stowers Institute for Medical Research award (R.S.H.), National Science Foundation grant: (NSF-IOS-1456545), Human Frontier Science Program grant: (RGY0093/ 2012), Biotechnology and Biological Sciences Research Council grant: (BB/L002817/1).Genetics Society of AmericaARCAFlorence GutzwillerCatarina R. CarmoDanny E. MillerDanny W. RiceIrene L. NewtonR. Scott HawleyLuis TeixeiraCasey M. Bergman2015-12-21T16:24:02Z2015-10-232015-10-23T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10400.7/535engDynamics of Wolbachia pipientis Gene Expression Across the Drosophila melanogaster Life Cycle Florence Gutzwiller, Catarina R. Carmo, Danny E. Miller, Danny W. Rice, Irene L. G. Newton, R. Scott Hawley, Luis Teixeira, and Casey M. Bergman G3 December 2015 5:2843-2856; Early Online October 23, 2015, doi:10.1534/g3.115.02193110.1534/g3.115.021931info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2022-11-29T14:34:54Zoai:arca.igc.gulbenkian.pt:10400.7/535Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T16:11:47.312402Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse
dc.title.none.fl_str_mv Dynamics of Wolbachia pipientis gene expression across the Drosophila melanogaster life cycle
title Dynamics of Wolbachia pipientis gene expression across the Drosophila melanogaster life cycle
spellingShingle Dynamics of Wolbachia pipientis gene expression across the Drosophila melanogaster life cycle
Florence Gutzwiller
Wolbachia
Drosophila
symbiosis
development
cytoplasmic incompatibility
title_short Dynamics of Wolbachia pipientis gene expression across the Drosophila melanogaster life cycle
title_full Dynamics of Wolbachia pipientis gene expression across the Drosophila melanogaster life cycle
title_fullStr Dynamics of Wolbachia pipientis gene expression across the Drosophila melanogaster life cycle
title_full_unstemmed Dynamics of Wolbachia pipientis gene expression across the Drosophila melanogaster life cycle
title_sort Dynamics of Wolbachia pipientis gene expression across the Drosophila melanogaster life cycle
author Florence Gutzwiller
author_facet Florence Gutzwiller
Catarina R. Carmo
Danny E. Miller
Danny W. Rice
Irene L. Newton
R. Scott Hawley
Luis Teixeira
Casey M. Bergman
author_role author
author2 Catarina R. Carmo
Danny E. Miller
Danny W. Rice
Irene L. Newton
R. Scott Hawley
Luis Teixeira
Casey M. Bergman
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv ARCA
dc.contributor.author.fl_str_mv Florence Gutzwiller
Catarina R. Carmo
Danny E. Miller
Danny W. Rice
Irene L. Newton
R. Scott Hawley
Luis Teixeira
Casey M. Bergman
dc.subject.por.fl_str_mv Wolbachia
Drosophila
symbiosis
development
cytoplasmic incompatibility
topic Wolbachia
Drosophila
symbiosis
development
cytoplasmic incompatibility
description Symbiotic interactions between microbes and their multicellular hosts have manifold impacts on molecular, cellular and organismal biology. To identify candidate bacterial genes involved in maintaining endosymbiotic associations with insect hosts, we analyzed genome-wide patterns of gene expression in the alpha-proteobacteria Wolbachia pipientis across the life cycle of Drosophila melanogaster using public data from the modENCODE project that was generated in a Wolbachia-infected version of the ISO1 reference strain. We find that the majority of Wolbachia genes are expressed at detectable levels in D. melanogaster across the entire life cycle, but that only 7.8% of 1195 Wolbachia genes exhibit robust stage- or sex-specific expression differences when studied in the "holo-organism" context. Wolbachia genes that are differentially expressed during development are typically up-regulated after D. melanogaster embryogenesis, and include many bacterial membrane, secretion system and ankyrin-repeat containing proteins. Sex-biased genes are often organised as small operons of uncharacterised genes and are mainly up-regulated in adult males D. melanogaster in an age-dependent manner suggesting a potential role in cytoplasmic incompatibility. Our results indicate that large changes in Wolbachia gene expression across the Drosophila life-cycle are relatively rare when assayed across all host tissues, but that candidate genes to understand host-microbe interaction in facultative endosymbionts can be successfully identified using holo-organism expression profiling. Our work also shows that mining public gene expression data in D. melanogaster provides a rich set of resources to probe the functional basis of the Wolbachia-Drosophila symbiosis and annotate the transcriptional outputs of the Wolbachia genome.
publishDate 2015
dc.date.none.fl_str_mv 2015-12-21T16:24:02Z
2015-10-23
2015-10-23T00:00:00Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://hdl.handle.net/10400.7/535
url http://hdl.handle.net/10400.7/535
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Dynamics of Wolbachia pipientis Gene Expression Across the Drosophila melanogaster Life Cycle Florence Gutzwiller, Catarina R. Carmo, Danny E. Miller, Danny W. Rice, Irene L. G. Newton, R. Scott Hawley, Luis Teixeira, and Casey M. Bergman G3 December 2015 5:2843-2856; Early Online October 23, 2015, doi:10.1534/g3.115.021931
10.1534/g3.115.021931
dc.rights.driver.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 Genetics Society of America
publisher.none.fl_str_mv Genetics Society of America
dc.source.none.fl_str_mv reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
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instname_str Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
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collection Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
repository.name.fl_str_mv Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
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