Generality of toxins in defensive symbiosis: Ribosome-inactivating proteins and defense against parasitic wasps in Drosophila.

Generality of toxins in defensive symbiosis: Ribosome-inactivating proteins and defense against parasitic wasps in Drosophila.
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DOI:
10.1371/journal.ppat.1006431
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发表时间:
2017-07
期刊:
影响因子:
6.7
通讯作者:
Perlman SJ
Perlman SJ
中科院分区:
医学1区
文献类型:
--
作者:
Ballinger MJ;Perlman SJ

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虽然越来越清楚的是,多细胞生物通常含有微生物共生体,保护其宿主免受天敌的侵害,但大多数防御性共生体的机制基础在很大程度上是未知的。螺原体细菌是陆生节肢动物的广泛伴生物,并且包括保护各种果蝇免受寄生蜂和线虫侵害的菌株。最近的工作涉及核糖体失活蛋白(RIP)编码的螺原体,肠出血性大肠杆菌中的志贺样毒素,在防御一个有毒的寄生线虫在林地苍蝇,果蝇neotestacea。在此,我们通过研究螺原体RIP是否也在黄蜂保护中发挥作用,来检验RIP介导的保护作用的普遍性。黑腹果蝇D.新壳纲我们找到了强有力的证据,RIP的主要作用,核糖体RNA(rRNA)的幼虫内寄生蜂,Leptopilina heterotoma和Leptopilina boulardi,表现出RIP活性的标志。在含螺原体的宿主中,寄生蜂核糖体在28 S rRNA的α-八叠球菌素/蓖麻毒素环中显示出丰富的位点特异性脱嘌呤,在蜂卵在蝇幼虫内孵化后不久发生脱嘌呤。有趣的是,我们发现,蛹的体外寄生蜂,Pachycrepoideus vaccummiae,逃避保护螺原体,其核糖体不显示高水平的脱嘌呤。我们还表明,苍蝇核糖体显示由RIP靶向的证据很少。最后,我们发现D. neotestacea的防御螺原体编码不同的RIP基因,其丰度不同。这项工作表明,针对不同的天敌的防御共生体的特异性可能是由毒素库的进化驱动的,毒素的多样性可能在塑造宿主-共生体-敌人的相互作用中发挥作用。几乎所有的昆虫都有细菌伴侣。这些微生物可以是防御性共生体,保护其宿主免受寄生虫和病原体的侵害,在某些情况下,可以防御一种以上的敌人,为研究防御性相互作用的特异性进化提供了机会。哪些因素决定了辩护的特殊性和一般性?共生体编码的效应分子是否能在不伤害宿主的情况下对敌人采取一般性行动?我们在这里表明,共生体编码的核糖体失活毒素,以前牵连在保护果蝇对线虫寄生虫,也牵连在捍卫苍蝇对寄生蜂。我们量化的核糖体脱嘌呤的比例毒素的活性,重要的是,发现易感黄蜂在发展的早期受到攻击,并受到强烈影响,而主机和抗性黄蜂没有。我们还表明,不是一个,而是一个家庭的毒素维持和共生体表达。总之,我们的研究结果暗示毒素多样性作为一个因素,有助于共生体介导的防御特异性的演变。
While it has become increasingly clear that multicellular organisms often harbor microbial symbionts that protect their hosts against natural enemies, the mechanistic underpinnings underlying most defensive symbioses are largely unknown. Spiroplasma bacteria are widespread associates of terrestrial arthropods, and include strains that protect diverse Drosophila flies against parasitic wasps and nematodes. Recent work implicated a ribosome-inactivating protein (RIP) encoded by Spiroplasma, and related to Shiga-like toxins in enterohemorrhagic Escherichia coli, in defense against a virulent parasitic nematode in the woodland fly, Drosophila neotestacea. Here we test the generality of RIP-mediated protection by examining whether Spiroplasma RIPs also play a role in wasp protection, in D. melanogaster and D. neotestacea. We find strong evidence for a major role of RIPs, with ribosomal RNA (rRNA) from the larval endoparasitic wasps, Leptopilina heterotoma and Leptopilina boulardi, exhibiting the hallmarks of RIP activity. In Spiroplasma-containing hosts, parasitic wasp ribosomes show abundant site-specific depurination in the α-sarcin/ricin loop of the 28S rRNA, with depurination occurring soon after wasp eggs hatch inside fly larvae. Interestingly, we found that the pupal ectoparasitic wasp, Pachycrepoideus vindemmiae, escapes protection by Spiroplasma, and its ribosomes do not show high levels of depurination. We also show that fly ribosomes show little evidence of targeting by RIPs. Finally, we find that the genome of D. neotestacea’s defensive Spiroplasma encodes a diverse repertoire of RIP genes, which are differ in abundance. This work suggests that specificity of defensive symbionts against different natural enemies may be driven by the evolution of toxin repertoires, and that toxin diversity may play a role in shaping host-symbiont-enemy interactions. Nearly all insects harbor bacterial partners. These microbes can be defensive symbionts, protecting their hosts against parasites and pathogens, and in some cases, may defend against more than one enemy, presenting opportunity to study the evolution of specificity underlying defensive interactions. What factors determine specificity and generality of defense? Can symbiont-encoded effector molecules act generally against enemies without causing harm to the host? We show here that symbiont-encoded ribosome-inactivating toxins, previously implicated in protection of a Drosophila fruit fly against its nematode parasite, are also implicated in defending flies against parasitic wasps. We quantify activity of the toxin as the proportion of ribosomes depurinated and, importantly, find that susceptible wasps are attacked early in development and are strongly affected, while hosts and a resistant wasp are not. We also show that not one, but a family of toxins is maintained and expressed by symbionts. Together, our findings implicate toxin diversity as a factor contributing to the evolution of specificity in a symbiont-mediated defense.
DOI: 10.1038/ncomms12781
发表时间: 2016-09-21
影响因子: 16.6
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Harumoto T;Anbutsu H;Lemaitre B;Fukatsu T
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