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Male-killing toxin in a bacterial symbiont of Drosophila.
Nature 2018; 557(7704):252-255Nat

Abstract

Several lineages of symbiotic bacteria in insects selfishly manipulate host reproduction to spread in a population 1 , often by distorting host sex ratios. Spiroplasma poulsonii2,3 is a helical and motile, Gram-positive symbiotic bacterium that resides in a wide range of Drosophila species 4 . A notable feature of S. poulsonii is male killing, whereby the sons of infected female hosts are selectively killed during development1,2. Although male killing caused by S. poulsonii has been studied since the 1950s, its underlying mechanism is unknown. Here we identify an S. poulsonii protein, designated Spaid, whose expression induces male killing. Overexpression of Spaid in D. melanogaster kills males but not females, and induces massive apoptosis and neural defects, recapitulating the pathology observed in S. poulsonii-infected male embryos5-11. Our data suggest that Spaid targets the dosage compensation machinery on the male X chromosome to mediate its effects. Spaid contains ankyrin repeats and a deubiquitinase domain, which are required for its subcellular localization and activity. Moreover, we found a laboratory mutant strain of S. poulsonii with reduced male-killing ability and a large deletion in the spaid locus. Our study has uncovered a bacterial protein that affects host cellular machinery in a sex-specific way, which is likely to be the long-searched-for factor responsible for S. poulsonii-induced male killing.

Authors+Show Affiliations

Global Health Institute, School of Life Sciences, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland. toshiyuki.harumoto@epfl.ch.Global Health Institute, School of Life Sciences, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland. bruno.lemaitre@epfl.ch.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

29720654

Citation

Harumoto, Toshiyuki, and Bruno Lemaitre. "Male-killing Toxin in a Bacterial Symbiont of Drosophila." Nature, vol. 557, no. 7704, 2018, pp. 252-255.
Harumoto T, Lemaitre B. Male-killing toxin in a bacterial symbiont of Drosophila. Nature. 2018;557(7704):252-255.
Harumoto, T., & Lemaitre, B. (2018). Male-killing toxin in a bacterial symbiont of Drosophila. Nature, 557(7704), pp. 252-255. doi:10.1038/s41586-018-0086-2.
Harumoto T, Lemaitre B. Male-killing Toxin in a Bacterial Symbiont of Drosophila. Nature. 2018;557(7704):252-255. PubMed PMID: 29720654.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Male-killing toxin in a bacterial symbiont of Drosophila. AU - Harumoto,Toshiyuki, AU - Lemaitre,Bruno, Y1 - 2018/05/02/ PY - 2017/11/09/received PY - 2018/03/21/accepted PY - 2018/5/4/pubmed PY - 2018/11/6/medline PY - 2018/5/4/entrez SP - 252 EP - 255 JF - Nature JO - Nature VL - 557 IS - 7704 N2 - Several lineages of symbiotic bacteria in insects selfishly manipulate host reproduction to spread in a population 1 , often by distorting host sex ratios. Spiroplasma poulsonii2,3 is a helical and motile, Gram-positive symbiotic bacterium that resides in a wide range of Drosophila species 4 . A notable feature of S. poulsonii is male killing, whereby the sons of infected female hosts are selectively killed during development1,2. Although male killing caused by S. poulsonii has been studied since the 1950s, its underlying mechanism is unknown. Here we identify an S. poulsonii protein, designated Spaid, whose expression induces male killing. Overexpression of Spaid in D. melanogaster kills males but not females, and induces massive apoptosis and neural defects, recapitulating the pathology observed in S. poulsonii-infected male embryos5-11. Our data suggest that Spaid targets the dosage compensation machinery on the male X chromosome to mediate its effects. Spaid contains ankyrin repeats and a deubiquitinase domain, which are required for its subcellular localization and activity. Moreover, we found a laboratory mutant strain of S. poulsonii with reduced male-killing ability and a large deletion in the spaid locus. Our study has uncovered a bacterial protein that affects host cellular machinery in a sex-specific way, which is likely to be the long-searched-for factor responsible for S. poulsonii-induced male killing. SN - 1476-4687 UR - https://www.unboundmedicine.com/medline/citation/29720654/Male_killing_toxin_in_a_bacterial_symbiont_of_Drosophila_ L2 - https://doi.org/10.1038/s41586-018-0086-2 DB - PRIME DP - Unbound Medicine ER -