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• W4386444034 abstract "A wide variety of maternally transmitted endosymbionts in insects are associated with reproductive parasitism, whereby they interfere with host reproduction to increase the ratio of infected females and spread within populations. 1 Werren J.H. Baldo L. Clark M.E. Wolbachia: master manipulators of invertebrate biology. Nat. Rev. Microbiol. 2008; 6: 741-751https://doi.org/10.1038/nrmicro1969 Crossref PubMed Scopus (1904) Google Scholar ,2 Hurst G.D.D. Frost C.L. Reproductive parasitism: maternally inherited symbionts in a biparental world. Cold Spring Harb. Perspect. Biol. 2015; 7a017699https://doi.org/10.1101/cshperspect.a017699 Crossref Scopus (82) Google Scholar Recent successes in identifying bacterial factors responsible for reproductive parasitism 3 Beckmann J.F. Fallon A.M. Detection of the Wolbachia protein WPIP0282 in mosquito spermathecae: implications for cytoplasmic incompatibility. Insect Biochem. Mol. Biol. 2013; 43: 867-878https://doi.org/10.1016/j.ibmb.2013.07.002 Crossref PubMed Scopus (75) Google Scholar ,4 Beckmann J.F. Ronau J.A. Hochstrasser M. A Wolbachia deubiquitylating enzyme induces cytoplasmic incompatibility. Nat. Microbiol. 2017; 217007https://doi.org/10.1038/nmicrobiol.2017.7 Crossref Scopus (219) Google Scholar ,5 LePage D.P. Metcalf J.A. Bordenstein S.R. On J. Perlmutter J.I. Shropshire J.D. Layton E.M. Funkhouser-Jones L.J. Beckmann J.F. Bordenstein S.R. Prophage WO genes recapitulate and enhance Wolbachia-induced cytoplasmic incompatibility. Nature. 2017; 543: 243-247https://doi.org/10.1038/nature21391 Crossref PubMed Scopus (263) Google Scholar ,6 Harumoto T. Lemaitre B. Male-killing toxin in a bacterial symbiont of Drosophila. Nature. 2018; 557: 252-255https://doi.org/10.1038/s41586-018-0086-2 Crossref PubMed Scopus (75) Google Scholar ,7 Katsuma S. Hirota K. Matsuda-Imai N. Fukui T. Muro T. Nishino K. Kosako H. Shoji K. Takanashi H. Fujii T. et al. A Wolbachia factor for male killing in lepidopteran insects. Nat. Commun. 2022; 136764https://doi.org/10.1038/s41467-022-34488-y Crossref Scopus (11) Google Scholar as well as further omics approaches 8 Bordenstein S.R. Bordenstein S.R. Eukaryotic association module in phage WO genomes from Wolbachia. Nat. Commun. 2016; 713155https://doi.org/10.1038/ncomms13155 Crossref Scopus (101) Google Scholar ,9 Gillespie J.J. Driscoll T.P. Verhoeve V.I. Rahman M.S. Macaluso K.R. Azad A.F. A tangled web: origins of reproductive parasitism. Genome Biol. Evol. 2018; 10: 2292-2309https://doi.org/10.1093/gbe/evy159 Crossref PubMed Scopus (30) Google Scholar ,10 Schubert A.F. Nguyen J.V. Franklin T.G. Geurink P.P. Roberts C.G. Sanderson D.J. Miller L.N. Ovaa H. Hofmann K. Pruneda J.N. et al. Identification and characterization of diverse OTU deubiquitinases in bacteria. EMBO J. 2020; 39e105127https://doi.org/10.15252/embj.2020105127 Crossref Scopus (29) Google Scholar ,11 Gerth M. Martinez-Montoya H. Ramirez P. Masson F. Griffin J.S. Aramayo R. Siozios S. Lemaitre B. Mateos M. Hurst G.D.D. Rapid molecular evolution of Spiroplasma symbionts of Drosophila. Microb. Genom. 2021; 7000503https://doi.org/10.1099/mgen.0.000503 Crossref Google Scholar ,12 Massey J.H. Newton I.L.G. Diversity and function of arthropod endosymbiont toxins. Trends Microbiol. 2022; 30: 185-198https://doi.org/10.1016/j.tim.2021.06.008 Abstract Full Text Full Text PDF Scopus (14) Google Scholar have highlighted the common appearance of deubiquitinase domains, although their biological roles—in particular, how they link to distinct manipulative phenotypes—remain poorly defined. Spiroplasma poulsonii is a helical and motile bacterial endosymbiont of Drosophila, 13 Malogolowkin C. Poulson D.F. Infective transfer of maternally inherited abnormal sex-ratio in Drosophila willistoni. Science. 1957; 12632 Crossref Scopus (18) Google Scholar ,14 Poulson D.F. Cytoplasmic inheritance and hereditary infections in Drosophila. in: Burdette W.J. Methodology in Basic Genetics. Holden-Day, 1963: 404-424 Google Scholar which selectively kills male progeny with a male-killing toxin Spaid (S. poulsonii androcidin), which encodes an ovarian tumor (OTU) deubiquitinase domain. 6 Harumoto T. Lemaitre B. Male-killing toxin in a bacterial symbiont of Drosophila. Nature. 2018; 557: 252-255https://doi.org/10.1038/s41586-018-0086-2 Crossref PubMed Scopus (75) Google Scholar Artificial expression of Spaid in flies reproduces male-killing-associated pathologies that include abnormal apoptosis and neural defects during embryogenesis 6 Harumoto T. Lemaitre B. Male-killing toxin in a bacterial symbiont of Drosophila. Nature. 2018; 557: 252-255https://doi.org/10.1038/s41586-018-0086-2 Crossref PubMed Scopus (75) Google Scholar ,15 Counce S.J. Poulson D.F. Developmental effects of the sex-ratio agent in embryos of Drosophila willistoni. J. Exp. Zool. 1962; 151: 17-31https://doi.org/10.1002/jez.1401510103 Crossref PubMed Scopus (34) Google Scholar ,16 Tsuchiyama-Omura S. Sakaguchi B. Koga K. Poulson D.F. Morphological features of embryogenesis in Drosophila melanogaster infected with a male-killing Spiroplasma. Zool. Sci. 1988; 5: 375-383 Google Scholar ,17 Bentley J.K. Veneti Z. Heraty J. Hurst G.D.D. The pathology of embryo death caused by the male-killing Spiroplasma bacterium in Drosophila nebulosa. BMC Biol. 2007; 59https://doi.org/10.1186/1741-7007-5-9 Crossref Scopus (32) Google Scholar ,18 Martin J. Chong T. Ferree P.M. Male killing Spiroplasma preferentially disrupts neural development in the Drosophila melanogaster embryo. PLoS One. 2013; 8e79368https://doi.org/10.1371/journal.pone.0079368 Crossref Scopus (20) Google Scholar ,19 Harumoto T. Anbutsu H. Fukatsu T. Male-killing Spiroplasma induces sex-specific cell death via host apoptotic pathway. PLoS Pathog. 2014; 10e1003956https://doi.org/10.1371/journal.ppat.1003956 Crossref Scopus (24) Google Scholar ; moreover, it highly accumulates on the dosage-compensated male X chromosome, 20 Lucchesi J.C. Kuroda M.I. Dosage compensation in Drosophila. Cold Spring Harb. Perspect. Biol. 2015; 7a019398https://doi.org/10.1101/cshperspect.a019398 Crossref PubMed Scopus (123) Google Scholar congruent with cellular defects such as the DNA damage/chromatin bridge breakage specifically induced upon that chromosome. 6 Harumoto T. Lemaitre B. Male-killing toxin in a bacterial symbiont of Drosophila. Nature. 2018; 557: 252-255https://doi.org/10.1038/s41586-018-0086-2 Crossref PubMed Scopus (75) Google Scholar ,21 Veneti Z. Bentley J.K. Koana T. Braig H.R. Hurst G.D.D. A functional dosage compensation complex required for male killing in Drosophila. Science. 2005; 307: 1461-1463https://doi.org/10.1126/science.1107182 Crossref PubMed Scopus (80) Google Scholar ,22 Cheng B. Kuppanda N. Aldrich J.C. Akbari O.S. Ferree P.M. Male-killing Spiroplasma alters behavior of the dosage compensation complex during Drosophila melanogaster embryogenesis. Curr. Biol. 2016; 26: 1339-1345https://doi.org/10.1016/j.cub.2016.03.050 Abstract Full Text Full Text PDF PubMed Scopus (18) Google Scholar ,23 Harumoto T. Anbutsu H. Lemaitre B. Fukatsu T. Male-killing symbiont damages host’s dosage-compensated sex chromosome to induce embryonic apoptosis. Nat. Commun. 2016; 712781https://doi.org/10.1038/ncomms12781 Crossref Scopus (30) Google Scholar Here, I show that without the function of OTU, Spaid is polyubiquitinated and degraded through the host ubiquitin-proteasome pathway, leading to the attenuation of male-killing activity as shown previously. 6 Harumoto T. Lemaitre B. Male-killing toxin in a bacterial symbiont of Drosophila. Nature. 2018; 557: 252-255https://doi.org/10.1038/s41586-018-0086-2 Crossref PubMed Scopus (75) Google Scholar Furthermore, I find that Spaid utilizes its OTU domain to deubiquitinate itself in an intermolecular manner. Collectively, the deubiquitinase domain of Spaid serves as a self-stabilization mechanism to facilitate male killing in flies, optimizing a molecular strategy of endosymbionts that enables the efficient manipulation of the host at a low energetic cost." @default.
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• W4386444034 title "Self-stabilization mechanism encoded by a bacterial toxin facilitates reproductive parasitism" @default.
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