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Functional analysis of Wolbachia Cid effectors unravels cooperative interactions to target host chromatin during replication

Wolbachia are common bacteria among terrestrial arthropods. These endosymbionts transmitted through the female germline manipulate their host reproduction through several mechanisms whose most prevalent form called Cytoplasmic Incompatibility -CI- is a conditional sterility syndrome eventually favor...

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Autores principales: Terretaz, Kévin, Horard, Béatrice, Weill, Mylène, Loppin, Benjamin, Landmann, Frédéric
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10047532/
https://www.ncbi.nlm.nih.gov/pubmed/36928089
http://dx.doi.org/10.1371/journal.ppat.1011211
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author Terretaz, Kévin
Horard, Béatrice
Weill, Mylène
Loppin, Benjamin
Landmann, Frédéric
author_facet Terretaz, Kévin
Horard, Béatrice
Weill, Mylène
Loppin, Benjamin
Landmann, Frédéric
author_sort Terretaz, Kévin
collection PubMed
description Wolbachia are common bacteria among terrestrial arthropods. These endosymbionts transmitted through the female germline manipulate their host reproduction through several mechanisms whose most prevalent form called Cytoplasmic Incompatibility -CI- is a conditional sterility syndrome eventually favoring the infected progeny. Upon fertilization, the sperm derived from an infected male is only compatible with an egg harboring a compatible Wolbachia strain, this sperm leading otherwise to embryonic death. The Wolbachia Cif factors CidA and CidB responsible for CI and its neutralization function as a Toxin-Antitoxin system in the mosquito host Culex pipiens. However, the mechanism of CidB toxicity and its neutralization by the CidA antitoxin remain unexplored. Using transfected insect cell lines to perform a structure-function analysis of these effectors, we show that both CidA and CidB are chromatin interactors and CidA anchors CidB to the chromatin in a cell-cycle dependent-manner. In absence of CidA, the CidB toxin localizes to its own chromatin microenvironment and acts by preventing S-phase completion, independently of its deubiquitylase -DUB- domain. Experiments with transgenic Drosophila show that CidB DUB domain is required together with CidA during spermatogenesis to stabilize the CidA-CidB complex. Our study defines CidB functional regions and paves the way to elucidate the mechanism of its toxicity.
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spelling pubmed-100475322023-03-29 Functional analysis of Wolbachia Cid effectors unravels cooperative interactions to target host chromatin during replication Terretaz, Kévin Horard, Béatrice Weill, Mylène Loppin, Benjamin Landmann, Frédéric PLoS Pathog Research Article Wolbachia are common bacteria among terrestrial arthropods. These endosymbionts transmitted through the female germline manipulate their host reproduction through several mechanisms whose most prevalent form called Cytoplasmic Incompatibility -CI- is a conditional sterility syndrome eventually favoring the infected progeny. Upon fertilization, the sperm derived from an infected male is only compatible with an egg harboring a compatible Wolbachia strain, this sperm leading otherwise to embryonic death. The Wolbachia Cif factors CidA and CidB responsible for CI and its neutralization function as a Toxin-Antitoxin system in the mosquito host Culex pipiens. However, the mechanism of CidB toxicity and its neutralization by the CidA antitoxin remain unexplored. Using transfected insect cell lines to perform a structure-function analysis of these effectors, we show that both CidA and CidB are chromatin interactors and CidA anchors CidB to the chromatin in a cell-cycle dependent-manner. In absence of CidA, the CidB toxin localizes to its own chromatin microenvironment and acts by preventing S-phase completion, independently of its deubiquitylase -DUB- domain. Experiments with transgenic Drosophila show that CidB DUB domain is required together with CidA during spermatogenesis to stabilize the CidA-CidB complex. Our study defines CidB functional regions and paves the way to elucidate the mechanism of its toxicity. Public Library of Science 2023-03-16 /pmc/articles/PMC10047532/ /pubmed/36928089 http://dx.doi.org/10.1371/journal.ppat.1011211 Text en © 2023 Terretaz et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Terretaz, Kévin
Horard, Béatrice
Weill, Mylène
Loppin, Benjamin
Landmann, Frédéric
Functional analysis of Wolbachia Cid effectors unravels cooperative interactions to target host chromatin during replication
title Functional analysis of Wolbachia Cid effectors unravels cooperative interactions to target host chromatin during replication
title_full Functional analysis of Wolbachia Cid effectors unravels cooperative interactions to target host chromatin during replication
title_fullStr Functional analysis of Wolbachia Cid effectors unravels cooperative interactions to target host chromatin during replication
title_full_unstemmed Functional analysis of Wolbachia Cid effectors unravels cooperative interactions to target host chromatin during replication
title_short Functional analysis of Wolbachia Cid effectors unravels cooperative interactions to target host chromatin during replication
title_sort functional analysis of wolbachia cid effectors unravels cooperative interactions to target host chromatin during replication
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10047532/
https://www.ncbi.nlm.nih.gov/pubmed/36928089
http://dx.doi.org/10.1371/journal.ppat.1011211
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