Dynamics of Wolbachia pipientis gene expression across the Drosophila melanogaster life cycle
Autor(a) principal: | |
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Data de Publicação: | 2015 |
Outros Autores: | , , , , , , |
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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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 instacron:RCAAP |
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Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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RCAAP |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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