A Wolbachia factor for male killing in lepidopteran insects

Katsuma, Susumu; Hirota, Kanako; Matsuda–Imai, Noriko; Fukui, Takahiro; Muro, Tomohiro; Nishino, Kazumi; Kosako, Hidetaka; Shoji, Keisuke; Takanashi, Hideki; Fujii, Takeshi; Arimura, Shin‐ichi; Kiuchi, Takashi

doi:10.1038/s41467-022-34488-y

Cited by 40 publications

(44 citation statements)

References 39 publications

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“…Other loci and mechanisms could be involved in MK, including Oscar in the expression of MK in 2 lepidopteran insects via inhibition of a protein that is essential for both masculinization and dosage compensation [ 47 ]. Our assemblies do not include any homologs of Oscar, which may not be surprising given that Oscar functions in a ZW system.…”

Section: Discussionmentioning

confidence: 99%

A male-killing Wolbachia endosymbiont is concealed by another endosymbiont and a nuclear suppressor

et al. 2023

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Bacteria that live inside the cells of insect hosts (endosymbionts) can alter the reproduction of their hosts, including the killing of male offspring (male killing, MK). MK has only been described in a few insects, but this may reflect challenges in detecting MK rather than its rarity. Here, we identify MK Wolbachia at a low frequency (around 4%) in natural populations of Drosophila pseudotakahashii. MK Wolbachia had a stable density and maternal transmission during laboratory culture, but the MK phenotype which manifested mainly at the larval stage was lost rapidly. MK Wolbachia occurred alongside a second Wolbachia strain expressing a different reproductive manipulation, cytoplasmic incompatibility (CI). A genomic analysis highlighted Wolbachia regions diverged between the 2 strains involving 17 genes, and homologs of the wmk and cif genes implicated in MK and CI were identified in the Wolbachia assembly. Doubly infected males induced CI with uninfected females but not females singly infected with CI-causing Wolbachia. A rapidly spreading dominant nuclear suppressor genetic element affecting MK was identified through backcrossing and subsequent analysis with ddRAD SNPs of the D. pseudotakahashii genome. These findings highlight the complexity of nuclear and microbial components affecting MK endosymbiont detection and dynamics in populations and the challenges of making connections between endosymbionts and the host phenotypes affected by them.

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Section: Discussionmentioning

confidence: 99%

A male-killing Wolbachia endosymbiont is concealed by another endosymbiont and a nuclear suppressor

et al. 2023

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Section: Discussionmentioning

confidence: 99%

“…Very recently, a novel Wolbachia protein designated Oscar was identified as a causative factor of male killing in Lepidoptera (60). The authors showed that the expression of Oscar kills males by directly targeting and degrading host Masculinizer protein required for masculinization and dosage compensation (60)(61)(62). Interestingly, Oscar contains a CifB-like domain, possibly possessing Ulp1 enzymatic activity, yet it does not seem to be essential for the male-killing function of Oscar (60).…”

Section: Discussionmentioning

confidence: 99%

“…Without the intrinsic deubiquitinase activity, its protein level in spermatids declined, whereas high-level expression is normally required for the induction of male sterility ( 59 ). Very recently, a novel Wolbachia protein designated Oscar was identified as a causative factor of male killing in Lepidoptera ( 60 ). The authors showed that the expression of Oscar kills males by directly targeting and degrading host Masculinizer protein required for masculinization and dosage compensation ( 60 – 62 ).…”

Section: Discussionmentioning

confidence: 99%

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Self-stabilization mechanism encoded by a bacterial toxin facilitates reproductive parasitism

Harumoto

2023

Preprint

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A wide variety of bacterial endosymbionts in insects are associated with reproductive parasitism, whereby they interfere with host reproductive systems to spread within populations. Recent successes in identifying bacterial factors responsible for reproductive parasitism have highlighted the common appearance of deubiquitinase domains, although their functional roles remain unknown. For example, Spiroplasma symbionts in Drosophila selectively kill male progeny with a male-killing toxin Spaid that encodes an OTU deubiquitinase domain. Here I show that without the function of OTU, the male-killing activity of Spaid is attenuated, though not eliminated, since it is polyubiquitinated and degraded through the host ubiquitin-proteasome pathway. 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 low-cost.

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“…pseudotakahashii system provides an opportunity to investigate the mechanism of both MK and suppression. In the current paper, the genome of the male-killer is inferred from a doubly infected individual versus one carrying the CI strain alone; the data ruled out MK mediated through one candidate gene for MK— Oscar [ 9 ]—but was consistent with another— wmk [ 10 ]. To progress this work, the genome of the MK Wolbachia strain would need to be resolved from a singly infected individual followed by functional testing of candidates through transgenic expression.…”

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confidence: 93%