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Forward genetics in Wolbachia: regulation of Wolbachia proliferation by the amplification and deletion of an addictive genomic island

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dc.contributor.authorDuarte, Elves H.
dc.contributor.authorCarvalho, Ana
dc.contributor.authorLópez-Madrigal, Sergio
dc.contributor.authorCosta, João
dc.contributor.authorTeixeira, Luis
dc.date.accessioned2021-09-16T16:08:20Z
dc.date.available2021-09-16T16:08:20Z
dc.date.issued2021
dc.descriptionCopyright: © 2021 Duarte et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.pt_PT
dc.description.abstractWolbachia is one of the most prevalent bacterial endosymbionts, infecting approximately 40% of terrestrial arthropod species. Wolbachia is often a reproductive parasite but can also provide fitness benefits to its host, as, for example, protection against viral pathogens. This protective effect is currently being applied to fight arboviruses transmission by releasing Wolbachia-transinfected mosquitoes. Titre regulation is a crucial aspect of Wolbachia biology. Higher titres can lead to stronger phenotypes and fidelity of transmission but can have a higher cost to the host. Since Wolbachia is maternally transmitted, its fitness depends on host fitness, and, therefore, its cost to the host may be under selection. Understanding how Wolbachia titres are regulated and other aspects of Wolbachia biology has been hampered by the lack of genetic tools. Here we developed a forward genetic screen to identify new Wolbachia over-proliferative mutant variants. We characterized in detail two new mutants, wMelPop2 and wMelOctoless, and show that the amplification or loss of the Octomom genomic region lead to over-proliferation. These results confirm previous data and expand on the complex role of this genomic region in the control of Wolbachia proliferation. Both new mutants shorten the host lifespan and increase antiviral protection. Moreover, we show that Wolbachia proliferation rate in Drosophila melanogaster depends on the interaction between Octomom copy number, the host developmental stage, and temperature. Our analysis also suggests that the life shortening and antiviral protection phenotypes of Wolbachia are dependent on different, but related, properties of the endosymbiont; the rate of proliferation and the titres near the time of infection, respectively. We also demonstrate the feasibility of a novel and unbiased experimental approach to study Wolbachia biology, which could be further adapted to characterize other genetically intractable bacterial endosymbionts.pt_PT
dc.description.sponsorshipL.T. received funding for this project from the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation programme (grant agreement n°773260 – WOLBAKIAN, https://erc.europa.eu) and the Fundação para a Ciência e Tecnologia (grant IF/00839/2015, www.fct.pt). E.H.D. was supported by the fellowship SFRH/BD/113757/2015 from Fundação para a Ciência e Tecnologia (www.fct.pt), in the context of the Graduate Program Science for the Development. The fly work at the Fly Facility of Instituto Gulbenkian de Ciência (Oeiras, Portugal), was partially supported by the research infrastructure Congento, co-financed by Lisboa Regional Operational Programme (Lisboa2020), under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund (ERDF) and Fundação para a Ciência e Tecnologia (Portugal) under the project LISBOA-01-0145-FEDER-022170. The NGS analysis at the Genomics Unit of Instituto Gulbenkian de Ciência (Oeiras, Portugal), was partially supported by ONEIDA project (LISBOA-01-0145-FEDER-016417) co-funded by FEEI - "Fundos Europeus Estruturais e de Investimento" from "Programa Operacional Regional Lisboa 2020" and by national funds from FCT - "Fundação para a Ciência e a Tecnologia. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.pt_PT
dc.description.versioninfo:eu-repo/semantics/publishedVersionpt_PT
dc.identifier.citationPLoS Genet. 2021 Jun 18;17(6):e1009612pt_PT
dc.identifier.doi10.1371/journal.pgen.1009612pt_PT
dc.identifier.eissn1553-7404
dc.identifier.issn1553-7390
dc.identifier.urihttp://hdl.handle.net/10451/49534
dc.language.isoengpt_PT
dc.peerreviewedyespt_PT
dc.publisherPLOS Geneticspt_PT
dc.relationIF/00839/2015pt_PT
dc.relationLISBOA-01-0145-FEDER-022170pt_PT
dc.relationFunctional genetics of Wolbachia proliferation and protection to viruses
dc.relation.publisherversionhttps://journals.plos.org/plosgenetics/pt_PT
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/pt_PT
dc.subjectWolbachiapt_PT
dc.subjectInvertebrate genomicspt_PT
dc.subjectGenomicspt_PT
dc.subjectEggspt_PT
dc.subjectLarvaept_PT
dc.subjectDrosophila melanogasterpt_PT
dc.subjectGeneticspt_PT
dc.subjectSingle nucleotide polymorphismspt_PT
dc.titleForward genetics in Wolbachia: regulation of Wolbachia proliferation by the amplification and deletion of an addictive genomic islandpt_PT
dc.typejournal article
dspace.entity.typePublication
oaire.awardNumber49219
oaire.awardNumber773260
oaire.awardTitleFunctional genetics of Wolbachia proliferation and protection to viruses
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/OE/49219/PT
oaire.awardURIinfo:eu-repo/grantAgreement/EC/H2020/773260/EU
oaire.citation.issue6pt_PT
oaire.citation.titlePLOS Geneticspt_PT
oaire.citation.volume17pt_PT
oaire.fundingStreamOE
oaire.fundingStreamH2020
person.familyNameCosta
person.familyNameTeixeira
person.givenNameJoão
person.givenNameLuis
person.identifier480560
person.identifier.ciencia-idD317-CBF8-5590
person.identifier.orcid0000-0002-5831-4921
person.identifier.orcid0000-0001-8326-6645
person.identifier.ridH-6106-2013
person.identifier.scopus-author-id55499748300
person.identifier.scopus-author-id56304527800
project.funder.identifierhttp://doi.org/10.13039/501100001871
project.funder.identifierhttp://doi.org/10.13039/501100008530
project.funder.nameFundação para a Ciência e a Tecnologia
project.funder.nameEuropean Commission
rcaap.rightsopenAccesspt_PT
rcaap.typearticlept_PT
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relation.isAuthorOfPublication1c19bd76-85fd-435b-a1f3-4a27336d650c
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