Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Male-killing toxin in a bacterial symbiont of Drosophila

Abstract

Several lineages of symbiotic bacteria in insects selfishly manipulate host reproduction to spread in a population1, 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 species4. 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 embryos5,6,7,8,9,10,11. 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.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Expression of Spaid selectively eliminates male offspring.
Fig. 2: Expression of Spaid reproduces male-killing phenotypes during embryogenesis.
Fig. 3: Spaid acts through the MSL complex.
Fig. 4: Subcellular localization of Spaid.

Similar content being viewed by others

References

  1. Hurst, G. D. D. & Frost, C. L. Reproductive parasitism: maternally inherited symbionts in a biparental world. Cold Spring Harb. Perspect. Biol. 7, a017699 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  2. Williamson, D. L. & Poulson, D. F. in The Mycoplasmas, Volume III: Plant and Insect Mycoplasmas (eds Whitcomb R.F. & Tully J.G.) Ch. 6, 175–208 (Academic, New York, 1979).

  3. Williamson, D. L. et al. Spiroplasma poulsonii sp. nov., a new species associated with male-lethality in Drosophila willistoni, a neotropical species of fruit fly. Int. J. Syst. Bacteriol. 49, 611–618 (1999).

    Article  PubMed  Google Scholar 

  4. Haselkorn, T. S. The Spiroplasma heritable bacterial endosymbiont of Drosophila. Fly (Austin) 4, 80–87 (2010).

    Article  CAS  Google Scholar 

  5. 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. 5, 375–383 (1988).

    Google Scholar 

  6. 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 307, 1461–1463 (2005).

    Article  ADS  CAS  PubMed  Google Scholar 

  7. 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. 5, 9 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  8. Martin, J., Chong, T. & Ferree, P. M. Male killing Spiroplasma preferentially disrupts neural development in the Drosophila melanogaster embryo. PLoS One 8, e79368 (2013).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  9. Harumoto, T., Anbutsu, H. & Fukatsu, T. Male-killing Spiroplasma induces sex-specific cell death via host apoptotic pathway. PLoS Pathog. 10, e1003956 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  10. 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. 26, 1339–1345 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Harumoto, T., Anbutsu, H., Lemaitre, B. & Fukatsu, T. Male-killing symbiont damages host’s dosage-compensated sex chromosome to induce embryonic apoptosis. Nat. Commun. 7, 12781 (2016).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  12. Oishi, K. Spirochaete-mediated abnormal sex-ratio (SR) condition in Drosophila: a second virus associated with spirochaetes and its use in the study of the SR condition. Genet. Res. 18, 45–56 (1971).

    Article  CAS  PubMed  Google Scholar 

  13. Makarova, K. S., Aravind, L. & Koonin, E. V. A novel superfamily of predicted cysteine proteases from eukaryotes, viruses and Chlamydia pneumoniae. Trends Biochem. Sci. 25, 50–52 (2000).

    Article  CAS  PubMed  Google Scholar 

  14. Al-Khodor, S., Price, C. T., Kalia, A. & Abu Kwaik, Y. Functional diversity of ankyrin repeats in microbial proteins. Trends Microbiol. 18, 132–139 (2010).

    Article  CAS  PubMed  Google Scholar 

  15. Masson, F., Calderon Copete, S., Schüpfer, F., Garcia-Arraez, G. & Lemaitre, B. In vitro culture of the insect endosymbiont Spiroplasma poulsonii highlights bacterial genes involved in host-symbiont interaction. MBio 9, e00024-18 (2018).

    Article  CAS  PubMed  Google Scholar 

  16. Paredes, J. C. et al. Genome sequence of the Drosophila melanogaster male-killing Spiroplasma strain MSRO endosymbiont. MBio 6, e02437–14 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  17. Campos, A. R., Rosen, D. R., Robinow, S. N. & White, K. Molecular analysis of the locus elav in Drosophila melanogaster: a gene whose embryonic expression is neural specific. EMBO J. 6, 425–431 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Salz, H. K. & Erickson, J. W. Sex determination in Drosophila: The view from the top. Fly (Austin) 4, 60–70 (2010).

    Article  CAS  Google Scholar 

  19. Lucchesi, J. C. & Kuroda, M. I. Dosage compensation in Drosophila. Cold Spring Harb. Perspect. Biol. 7, a019398 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  20. Madigan, J. P., Chotkowski, H. L. & Glaser, R. L. DNA double-strand break-induced phosphorylation of Drosophila histone variant H2Av helps prevent radiation-induced apoptosis. Nucleic Acids Res. 30, 3698–3705 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Siozios, S. et al. The diversity and evolution of Wolbachia ankyrin repeat domain genes. PLoS ONE 8, e55390 (2013).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  22. Jernigan, K. K. & Bordenstein, S. R. Ankyrin domains across the Tree of Life. PeerJ 2, e264 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  23. Wu, M. et al. Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol. 2, e69 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Yamada, R., Iturbe-Ormaetxe, I., Brownlie, J. C. & O’Neill, S. L. Functional test of the influence of Wolbachia genes on cytoplasmic incompatibility expression in Drosophila melanogaster. Insect Mol. Biol. 20, 75–85 (2011).

    Article  CAS  PubMed  Google Scholar 

  25. Beckmann, J. F. & Fallon, A. M. Detection of the Wolbachia protein WPIP0282 in mosquito spermathecae: implications for cytoplasmic incompatibility. Insect Biochem. Mol. Biol. 43, 867–878 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Beckmann, J. F., Ronau, J. A. & Hochstrasser, M. A. Wolbachia deubiquitylating enzyme induces cytoplasmic incompatibility. Nat. Microbiol. 2, 17007 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  27. LePage, D. P. et al. Prophage WO genes recapitulate and enhance Wolbachia-induced cytoplasmic incompatibility. Nature 543, 243–247 (2017).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  28. Zhou, W., Rousset, F. & O’Neil, S. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc. Biol. Sci. 265, 509–515 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Fukatsu, T. & Nikoh, N. Two intracellular symbiotic bacteria from the mulberry psyllid Anomoneura mori (Insecta, Homoptera). Appl. Environ. Microbiol. 64, 3599–3606 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Fukatsu, T. & Nikoh, N. Endosymbiotic microbiota of the bamboo pseudococcid Antonina crawii (Insecta, Homoptera). Appl. Environ. Microbiol. 66, 643–650 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Kelley, R. L. et al. Expression of msl-2 causes assembly of dosage compensation regulators on the X chromosomes and female lethality in Drosophila. Cell 81, 867–877 (1995).

    Article  CAS  PubMed  Google Scholar 

  32. Brand, A. H. & Perrimon, N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415 (1993).

    CAS  PubMed  Google Scholar 

  33. Ashburner, M., Golic, K. G. & Hawley, R. S. Drosophila: a Laboratory Handbook. 2nd Edition, (Cold Spring Harbor, New York, 2005).

    Google Scholar 

  34. Rørth, P. Gal4 in the Drosophila female germline. Mech. Dev. 78, 113–118 (1998).

    Article  PubMed  Google Scholar 

  35. Pool, J. E., Wong, A. & Aquadro, C. F. Finding of male-killing Spiroplasma infecting Drosophila melanogaster in Africa implies transatlantic migration of this endosymbiont. Heredity (Edinb) 97, 27–32 (2006).

    Article  CAS  Google Scholar 

  36. Ye, F., Melcher, U., Rascoe, J. E. & Fletcher, J. Extensive chromosome aberrations in Spiroplasma citri Strain BR3. Biochem. Genet. 34, 269–286 (1996).

    Article  CAS  PubMed  Google Scholar 

  37. Ku, C., Lo, W.-S., Chen, L.-L. & Kuo, C.-H. Complete genomes of two dipteran-associated spiroplasmas provided insights into the origin, dynamics, and impacts of viral invasion in Spiroplasma. Genome Biol. Evol. 5, 1151–1164 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Anbutsu, H. & Fukatsu, T. Population dynamics of male-killing and non-male-killing spiroplasmas in Drosophila melanogaster. Appl. Environ. Microbiol. 69, 1428–1434 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Osborne, S. E., Leong, Y. S., O’Neill, S. L. & Johnson, K. N. Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathog. 5, e1000656 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  40. Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 29, e45 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Musselman, L. P. Drosophila hemolymph collection procedure. YouTube https://www.youtube.com/watch?v=im78OIBKlPA (2013).

  42. Field, D. et al. Open software for biologists: from famine to feast. Nat. Biotechnol. 24, 801–803 (2006).

    Article  CAS  PubMed  Google Scholar 

  43. Darling, A. C. E., Mau, B., Blattner, F. R. & Perna, N. T. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 14, 1394–1403 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Darling, A. E., Mau, B. & Perna, N. T. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5, e11147 (2010).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  45. Saillard, C. et al. The abundant extrachromosomal DNA content of the Spiroplasma citri GII3-3X genome. BMC Genomics 9, 195 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  46. Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014).

    Article  CAS  PubMed  Google Scholar 

  47. Carle, P. et al. Partial chromosome sequence of Spiroplasma citri reveals extensive viral invasion and important gene decay. Appl. Environ. Microbiol. 76, 3420–3426 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Alexeev, D. et al. Application of Spiroplasma melliferum proteogenomic profiling for the discovery of virulence factors and pathogenicity mechanisms in host-associated spiroplasmas. J. Proteome Res. 11, 224–236 (2012).

    Article  CAS  PubMed  Google Scholar 

  49. Lo, W.-S., Chen, L.-L., Chung, W.-C., Gasparich, G. E. & Kuo, C.-H. Comparative genome analysis of Spiroplasma melliferum IPMB4A, a honeybee-associated bacterium. BMC Genomics 14, 22 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Davis, R. E. et al. Complete genome sequence of Spiroplasma kunkelii strain CR2-3X, causal agent of corn stunt disease in Zea mays L. Genome Announc. 3, e01216–15 (2015).

    PubMed  PubMed Central  Google Scholar 

  51. Marchler-Bauer, A. et al. CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res. 39, D225–D229 (2011).

    Article  CAS  PubMed  Google Scholar 

  52. Marchler-Bauer, A. et al. CDD: NCBI’s conserved domain database. Nucleic Acids Res. 43, D222–D226 (2015).

    Article  CAS  PubMed  Google Scholar 

  53. Finn, R. D. et al. InterPro in 2017-beyond protein family and domain annotations. Nucleic Acids Res 45, D190–D199 (2017).

    Article  CAS  PubMed  Google Scholar 

  54. Liu, W. et al. IBS: an illustrator for the presentation and visualization of biological sequences. Bioinformatics 31, 3359–3361 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Su, X. Z., Wu, Y., Sifri, C. D. & Wellems, T. E. Reduced extension temperatures required for PCR amplification of extremely A+T-rich DNA. Nucleic Acids Res. 24, 1574–1575 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Hartenstein, V. Atlas of Drosophila Development. (Cold Spring Harbor, New York, 1993).

    Google Scholar 

  57. Campos-Ortega, J. A. & Hartenstein, V. The Embryonic Development of Drosophila melanogaster. (Springer, Berlin, 1997).

    Book  Google Scholar 

  58. Bopp, D., Bell, L. R., Cline, T. W. & Schedl, P. Developmental distribution of female-specific Sex-lethal proteins in Drosophila melanogaster. Genes Dev. 5, 403–415 (1991).

    Article  CAS  PubMed  Google Scholar 

  59. O’Neill, E. M., Rebay, I., Tjian, R. & Rubin, G. M. The activities of two Ets-related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway. Cell 78, 137–147 (1994).

    Article  PubMed  Google Scholar 

  60. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).

    Article  CAS  PubMed  Google Scholar 

  61. Pau, G., Fuchs, F., Sklyar, O., Boutros, M. & Huber, W. EBImage—an R package for image processing with applications to cellular phenotypes. Bioinformatics 26, 979–981 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Hollander, M., Wolfe, A. D. & Chicken, E. Nonparametric Statistical Methods, 3rd Edition, (John Wiley & Sons, New Jersey, 2013).

    MATH  Google Scholar 

Download references

Acknowledgements

We thank the Bloomington Stock Center in the USA and the Department of Drosophila Genomics and Genetic Resources at Kyoto Institute of Technology in Japan (DGGR) for fly stocks; the Developmental Studies Hybridoma Bank at the University of Iowa for monoclonal antibodies; the Drosophila Genomics Resource Center in the USA for DNA vectors; J. Jaenike, T. Murata, and M. Kuroda for providing fly strains; T. Fukatsu for the S. poulsonii-infected fly stocks that were originally established in his laboratory by T.H; J. Lucchesi for providing antibodies; the BioImaging & Optics Platform (BIOP) in EPFL for confocal microscopy; K. Harshman and the Lausanne Genomic Technologies Facility (GTF) at the University of Lausanne (UNIL) for whole-genome sequencing and draft genome assemblies; and C. Vorburger and S. Perlman for comments and suggestions on the manuscript; and the members of the laboratory for discussion and support. This work was supported by the European Research Council (ERC) Advanced Grant 339970 and the Swiss National Science Foundation (SNSF) Sinergia Grant CRSII3_154396. The purchase of the PacBio RS II system in UNIL was supported in part by the Loterie Romande through the Fondation pour la Recherche en Médecine Génétique.

Reviewer information

Nature thanks P. Ferree and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author information

Authors and Affiliations

Authors

Contributions

T.H. conceived of and designed the study, performed the experiments, analysed the data and wrote and edited the manuscript. B.L. conceived and administered the study and wrote and edited the manuscript.

Corresponding authors

Correspondence to Toshiyuki Harumoto or Bruno Lemaitre.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data figures and tables

Extended Data Fig. 1 Identification and characterization of the partial male-killing S. poulsonii strain.

a, An illustration showing the origin of the S. poulsonii strains analysed in this study. Pictures show male-killing (MK) S. poulsonii of D. melanogaster. MSRO-Ug is the original male-killing strain maintained in the Oregon-R wild-type fly. Fly stocks (Df(3L)H99 and Sxl-eGFP) artificially infected with this original strain showed complete male killing (100% MK) for the first 20 generations. Afterwards, one strain (MSRO-SE) started to show the partial male-killing phenotype, whereas the other (MSRO-H99) kept the ability to induce complete male killing. See Methods section ‘Identification and characterization of the partial male-killing S. poulsonii strain’ for more detail. b, c, Sex-ratio analysis of the adult progeny obtained from Oregon-R flies infected with MSRO-Ug, MSRO-H99, and MSRO-SE. We repeated experiments three times on the fourth, fifth and sixth generations (G4–6) after the establishment of infection. In c, the relative number of male offspring (percentage of females) obtained from Oregon-R female flies infected with MSRO-SE are plotted. Data points were excluded if the total count of flies was below 10. d, Relative titre of S. poulsonii within individual female flies. Adult females infected with three MSRO strains were kept for 0, 7 and 14 days after eclosion and analysed by qPCR. Data were normalized with respect to females from day 0 that were infected with MSRO-Ug. Different letters indicate statistically significant different groups (P < 0.01; N.S., not significant, P > 0.05; Steel–Dwass test; see Supplementary Table 2). Please note that the titres of the three strains are comparable and even the higher titre in old females (see 14 days in d) fails to induce complete male killing in MSRO-SE (c). Box and dot plots are as in Fig. 1c and sample sizes (n, number of adult flies) are shown at the bottom.

Source Data

Extended Data Fig. 2 Whole-genome sequencing studies of the male-killing S. poulsonii variants.

a, Comparison of the genomic features of three S. poulsonii strains. MSRO-H99 and MSRO-SE are newly obtained variants isolated in this study (Extended Data Fig. 1a). As a control, data from the previously reported male-killing S. poulsonii genome16 are also indicated. b, Whole-genome alignment of the three S. poulsonii strains. To start the alignment from the dnaA gene, contig 1 of MSRO-H99 was split into two fragments (contig 1.1 and 1.2). The locations of the contigs corresponding to extra chromosomes (putative plasmids; see Methods section ‘Genomic data analyses and protein domain searches’) are shown as ‘extra’. spaid (gene ID from GenBank BioProject PRJNA416288: SMH99_26490) and spaid ΔC (gene ID: SMSE_25110) are located on these extra chromosomes in MSRO-H99 (contig 4) and MSRO-SE (contig 2), respectively.

Extended Data Fig. 3 Genetic alterations of the spaid locus in the partial male-killing S. poulsonii strain.

The genome structures around the spaid loci in the male-killing (a, MSRO-Ug and MSRO-H99) and the partial male-killing (b, MSRO-SE) S. poulsonii strains. Genes encoded on opposite strands are shown in different colours (red and blue, respectively). An 828-bp deletion and nucleotide substitutions (coloured in red; corresponding amino acid sequences are presented in one-letter code) in the 3′ region of the spaid gene are indicated. These sequence alterations were confirmed using Sanger sequencing (see Methods).

Extended Data Fig. 4 Neural defects of Spaid-expressing embryos.

Representative images of stage 13–14 female (a, n = 14) and male (bn = 16) embryos maternally expressing Spaid and stained for TUNEL (green) and neural cells (Elav, magenta). Single-channel images of Elav are also shown. The outlined region in b is magnified in c with single-channel images of Elav and TUNEL. Embryos were co-stained for Elav, TUNEL, Sxl and DNA, and selected channels are shown in a–c and Fig. 2a, b, respectively.

Extended Data Fig. 5 Spaid acts through the dosage compensation machinery.

a–c, Representative images of stage 13–14 embryos ectopically expressing the MSL complex (H83M2 transgene), stained for TUNEL (green) and Sxl (magenta). GFP-expressing control female (a, n = 15), Spaid-expressing female (b, n = 20), and male (c, n = 19) embryos are shown. d, Quantification of TUNEL signals in H83M2 embryos at stages 13–14. Different characters indicate significantly different groups (P < 0.001; Steel–Dwass test; see Supplementary Table 2). The box and dot plot (females, red; males, blue) is as in Fig. 1c and sample sizes (n, number of embryos) are shown at the bottom. e, f, Representative images of epithelial cells of stage 8–10 male embryos expressing GFP (e, n = 25) and Spaid (f, n = 25), stained for DNA (green) and MSL1 (magenta) from the datasets analysed in Fig. 3. All UAS transgenes were expressed maternally.

Source Data

Extended Data Fig. 6 Expression of Spaid using a weak GAL4 driver.

The number of adult progeny (females, red; males, blue) obtained from crosses between the armadillo-GAL4 driver line (weak and ubiquitous expression) and four UAS transgenic lines (GFP, Spaid, ΔANK, and ΔOTU; n = 6 independent crosses for GFP and Spaid, n = 8 independent crosses for ΔANK and ΔOTU). The UAS-GFP line was used as a negative control. With this weak GAL4 driver, Spaid still eliminated all male progeny, while both ΔANK and ΔOTU had no impact on male viability. An asterisk indicates the statistically significant difference (P < 0.01; N.S., not significant, P > 0.05; two-tailed Mann–Whitney U test; see Supplementary Table 2). Box and dot plots are as in Fig. 1c. The total numbers of adult counts for each genotype and sex are shown at the bottom.

Source Data

Extended Data Fig. 7 A proposed model for Spaid-induced male-killing phenotypes.

Spaid utilizes the OTU domain and ankyrin repeats (ANK) to target the host nucleus and the male X chromosome. ‘MSL’ and ‘Ac’ indicate the dosage compensation complex and resultant histone acetylation, respectively. See text for other explanations.

Supplementary information

Supplementary Information

This file contains Supplementary Tables 1-2. Supplementary Table 1 contains a list of PCR primers (the names and sequences of PCR primers are indicated with the names of the target organisms) and Supplementary Table 2 contains exact P values (statistically significant pairs with an alpha level of 0.05 are indicated in red characters).

Reporting Summary

Supplementary Data

Summary of conserved domain database search results for the proteins annotated in the Spiroplasma strains MSRO-H99 (Data 1), MSRO-SE (Data 2), and in the previously published genome (Data 3; MSRO, 2015). Spaid in MSRO-H99 (SMH99_26490) and Spaid ∆C in MSRO-SE (SMSE_25110) are shown in red characters.

Source data

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Harumoto, T., Lemaitre, B. Male-killing toxin in a bacterial symbiont of Drosophila. Nature 557, 252–255 (2018). https://doi.org/10.1038/s41586-018-0086-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41586-018-0086-2

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing