Male-killing Symbiont Damages Host's Dosage-compensated Sex Chromosome to Induce Embryonic Apoptosis

Overview

Journal Nat Commun

Specialty Biology

Date 2016 Sep 22

PMID 27650264

Citations 27

Authors

Toshiyuki Harumoto

Hisashi Anbutsu

Bruno Lemaitre

Takema Fukatsu

Affiliations

Soon will be listed here.

Abstract

Some symbiotic bacteria are capable of interfering with host reproduction in selfish ways. How such bacteria can manipulate host's sex-related mechanisms is of fundamental interest encompassing cell, developmental and evolutionary biology. Here, we uncover the molecular and cellular mechanisms underlying Spiroplasma-induced embryonic male lethality in Drosophila melanogaster. Transcriptomic analysis reveals that many genes related to DNA damage and apoptosis are up-regulated specifically in infected male embryos. Detailed genetic and cytological analyses demonstrate that male-killing Spiroplasma causes DNA damage on the male X chromosome interacting with the male-specific lethal (MSL) complex. The damaged male X chromosome exhibits a chromatin bridge during mitosis, and bridge breakage triggers sex-specific abnormal apoptosis via p53-dependent pathways. Notably, the MSL complex is not only necessary but also sufficient for this cytotoxic process. These results highlight symbiont's sophisticated strategy to target host's sex chromosome and recruit host's molecular cascades toward massive apoptosis in a sex-specific manner.

Citing Articles

Bioinformatics analysis of the Microsporidia sp. MB genome: a malaria transmission-blocking symbiont of the Anopheles arabiensis mosquito.

Angango L, Herren J, Tastan Bishop O BMC Genomics. 2024; 25(1):1132.

PMID: 39578727 PMC: 11585130. DOI: 10.1186/s12864-024-11046-y.

Geographical, Seasonal, and Growth-Related Dynamics of Gut Microbiota in a Grapevine Pest, Apolygus spinolae (Heteroptera: Miridae).

Morimura H, Ishigami K, Sato T, Sone T, Kikuchi Y Microb Ecol. 2024; 87(1):112.

PMID: 39249553 PMC: 11383845. DOI: 10.1007/s00248-024-02426-8.

Prophage proteins alter long noncoding RNA and DNA of developing sperm to induce a paternal-effect lethality.

Kaur R, McGarry A, Shropshire J, Leigh B, Bordenstein S Science. 2024; 383(6687):1111-1117.

PMID: 38452081 PMC: 11187695. DOI: 10.1126/science.adk9469.

Host plant-mediated effects on symbiont: implications for biological characteristics and nutritional metabolism of pea aphids ().

Liu H, Yang Q, Liu J, Ul Haq I, Li Y, Zhang Q Front Plant Sci. 2023; 14:1288997.

PMID: 38126022 PMC: 10731267. DOI: 10.3389/fpls.2023.1288997.

A Light in the Dark: Uncovering Wolbachia-Host Interactions Using Fluorescence Imaging.

Serbus L Methods Mol Biol. 2023; 2739:349-373.

PMID: 38006562 DOI: 10.1007/978-1-0716-3553-7_21.

References

Martin J, Chong T, Ferree P . Male killing Spiroplasma preferentially disrupts neural development in the Drosophila melanogaster embryo. PLoS One. 2013; 8(11):e79368. PMC: 3827344. DOI: 10.1371/journal.pone.0079368. View

Serbus L, Sullivan W . A cellular basis for Wolbachia recruitment to the host germline. PLoS Pathog. 2007; 3(12):e190. PMC: 2134955. DOI: 10.1371/journal.ppat.0030190. View

Landmann F, Orsi G, Loppin B, Sullivan W . Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus. PLoS Pathog. 2009; 5(3):e1000343. PMC: 2652114. DOI: 10.1371/journal.ppat.1000343. View

Robinow S, White K . Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. J Neurobiol. 1991; 22(5):443-61. DOI: 10.1002/neu.480220503. View

Anbutsu H, Fukatsu T . Evasion, suppression and tolerance of Drosophila innate immunity by a male-killing Spiroplasma endosymbiont. Insect Mol Biol. 2010; 19(4):481-8. DOI: 10.1111/j.1365-2583.2010.01008.x. View

Osman D, Buchon N, Chakrabarti S, Huang Y, Su W, Poidevin M . Autocrine and paracrine unpaired signaling regulate intestinal stem cell maintenance and division. J Cell Sci. 2012; 125(Pt 24):5944-9. DOI: 10.1242/jcs.113100. View

Hamilton P, Peng F, Boulanger M, Perlman S . A ribosome-inactivating protein in a Drosophila defensive symbiont. Proc Natl Acad Sci U S A. 2015; 113(2):350-5. PMC: 4720295. DOI: 10.1073/pnas.1518648113. View

Xie J, Vilchez I, Mateos M . Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma. PLoS One. 2010; 5(8):e12149. PMC: 2921349. DOI: 10.1371/journal.pone.0012149. View

Oliver K, Degnan P, Hunter M, Moran N . Bacteriophages encode factors required for protection in a symbiotic mutualism. Science. 2009; 325(5943):992-4. PMC: 5473335. DOI: 10.1126/science.1174463. View

10.

Tsuchiyama S, Sakaguchi B, Oishi K . Analysis of gynandromorph survivals in Drosophila melanogaster infected with the male-killing SR organisms. Genetics. 1978; 89(4):711-21. PMC: 1213863. DOI: 10.1093/genetics/89.4.711. View

11.

Frydman H, Li J, Robson D, Wieschaus E . Somatic stem cell niche tropism in Wolbachia. Nature. 2006; 441(7092):509-12. DOI: 10.1038/nature04756. View

12.

Anbutsu H, Fukatsu T . Tissue-specific infection dynamics of male-killing and nonmale-killing spiroplasmas in Drosophila melanogaster. FEMS Microbiol Ecol. 2006; 57(1):40-6. DOI: 10.1111/j.1574-6941.2006.00087.x. View

13.

Wichmann A, Jaklevic B, Su T . Ionizing radiation induces caspase-dependent but Chk2- and p53-independent cell death in Drosophila melanogaster. Proc Natl Acad Sci U S A. 2006; 103(26):9952-7. PMC: 1502560. DOI: 10.1073/pnas.0510528103. View

14.

Brodsky M, Nordstrom W, Tsang G, Kwan E, Rubin G, Abrams J . Drosophila p53 binds a damage response element at the reaper locus. Cell. 2000; 101(1):103-13. DOI: 10.1016/S0092-8674(00)80627-3. View

15.

Ollmann M, Young L, Di Como C, Karim F, Belvin M, Robertson S . Drosophila p53 is a structural and functional homolog of the tumor suppressor p53. Cell. 2000; 101(1):91-101. DOI: 10.1016/S0092-8674(00)80626-1. View

16.

Hurst G, Frost C . Reproductive parasitism: maternally inherited symbionts in a biparental world. Cold Spring Harb Perspect Biol. 2015; 7(5). PMC: 4448626. DOI: 10.1101/cshperspect.a017699. View

17.

Fast E, Toomey M, Panaram K, Desjardins D, Kolaczyk E, Frydman H . Wolbachia enhance Drosophila stem cell proliferation and target the germline stem cell niche. Science. 2011; 334(6058):990-2. PMC: 4030408. DOI: 10.1126/science.1209609. View

18.

Kinner A, Wu W, Staudt C, Iliakis G . Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res. 2008; 36(17):5678-94. PMC: 2553572. DOI: 10.1093/nar/gkn550. View

19.

Bentley J, Veneti Z, Heraty J, Hurst G . The pathology of embryo death caused by the male-killing Spiroplasma bacterium in Drosophila nebulosa. BMC Biol. 2007; 5:9. PMC: 1832177. DOI: 10.1186/1741-7007-5-9. View

20.

Harumoto T, Anbutsu H, Fukatsu T . Male-killing Spiroplasma induces sex-specific cell death via host apoptotic pathway. PLoS Pathog. 2014; 10(2):e1003956. PMC: 3923752. DOI: 10.1371/journal.ppat.1003956. View