Male-killing symbiont damages host's dosage-compensated sex chromosome to induce embryonic apoptosis

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

マツノマダラカミキリの産卵生態に関する研究

目次 第1章 序論 / p1 第2章 マツノマダラカミキリの産卵痕の空間分布とその時間的変化 / p4 　1.野外における産卵痕の空間分布とその時間的変化 / p5 　2.室内における産卵痕の空間分布とその時間的変化 / p12 第3章 マツノマダラカミキリの産卵生態 / p20 　1.産卵痕,卵および幼虫が存在する産卵資源に対する産卵反応 / p21 　2.卵を含む産卵痕に対する産卵反応 / p25 　3.連続して形成された産卵痕の時間的･空間的間隔 / p35 第4章 マツノマダラカミキリ雌成虫が産卵資源内の子孫を認識する機構 / p45 　1.雌成虫由来の物質が産卵痕内の卵の有無の認識に果たす役割 / p45 　2.幼虫のフラスからの抽出物が産卵場所選好に及ぼす影響 / p52 　3.マツノマダラカミキリ雌成虫の小腮鬚と下骨鬚の感覚子 / p57 第5章 産卵の時間的差異と空間的距離が子の適応度成分に及ぼす影響 / p61 　1.同一の産卵痕を利用して産みつけられた2卵の位置と孵化時期がその後の生存率と成長に及ぼす影響 / p61 　2.孵化の時間的差異と孵化幼虫間の距離が幼虫初期の生存,発育および成長に及ぼす影響 / p72 第6章 総合考察 / p83 謝辞 / p89 要約 / p90 引用文献 / p98 図表広島大学(Hiroshima University)博士(学術)Sciencedoctora

Asymmetrical Interactions between Wolbachia and Spiroplasma Endosymbionts Coexisting in the Same Insect Host

We investigated the interactions between the endosymbionts Wolbachia pipientis strain wMel and Spiroplasma sp. strain NSRO coinfecting the host insect Drosophila melanogaster. By making use of antibiotic therapy, temperature stress, and hemolymph microinjection, we established the following strains in the same host genetic background: the SW strain, infected with both Spiroplasma and Wolbachia; the S strain, infected with Spiroplasma only; and the W strain, infected with Wolbachia only. The infection dynamics of the symbionts in these strains were monitored by quantitative PCR during host development. The infection densities of Spiroplasma exhibited no significant differences between the SW and S strains throughout the developmental course. In contrast, the infection densities of Wolbachia were significantly lower in the SW strain than in the W strain at the pupal and young adult stages. These results indicated that the interactions between the coinfecting symbionts were asymmetrical, i.e., Spiroplasma organisms negatively affected the population of Wolbachia organisms, while Wolbachia organisms did not influence the population of Spiroplasma organisms. In the host body, the symbionts exhibited their own tissue tropisms: among the tissues examined, Spiroplasma was the most abundant in the ovaries, while Wolbachia showed the highest density in Malpighian tubules. Strikingly, basically no Wolbachia organisms were detected in hemolymph, the principal location of Spiroplasma. These results suggest that different host tissues act as distinct microhabitats for the symbionts and that the lytic process in host metamorphosis might be involved in the asymmetrical interactions between the coinfecting symbionts

High and Low Temperatures Differently Affect Infection Density and Vertical Transmission of Male-Killing Spiroplasma Symbionts in Drosophila Hosts▿

We investigated the vertical transmission, reproductive phenotype, and infection density of a male-killing Spiroplasma symbiont in two Drosophila species under physiological high and low temperatures through successive host generations. In both the native host Drosophila nebulosa and the nonnative host Drosophila melanogaster, the symbiont infection and the male-killing phenotype were stably maintained at 25°C, rapidly lost at 18°C, and gradually lost at 28°C. In the nonnative host, both the high and low temperatures significantly suppressed the infection density of the spiroplasma. In the native host, by contrast, the low temperature suppressed the infection density of the spiroplasma whereas the high temperature had little effect on the infection density. These results suggested that the low temperature suppresses both the infection density and the vertical transmission of the spiroplasma whereas the high temperature suppresses the vertical transmission preferentially. The spiroplasma density was consistently higher in the native host than in the nonnative host, suggesting that the host genotype may affect the infection density of the symbiont. The temperature- and genotype-dependent instability of the symbiont infection highlights a complex genotype-by-genotype-by-environment interaction and may be relevant to the low infection frequencies of the male-killing spiroplasmas in natural Drosophila populations