Recurrent symbiont recruitment from fungal parasites in cicadas.

Recurrent symbiont recruitment from fungal parasites in cicadas.
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DOI:
10.1073/pnas.1803245115
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发表时间:
2018-06-26
影响因子:
11.1
通讯作者:
Fukatsu T
Fukatsu T
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Matsuura Y;Moriyama M;Łukasik P;Vanderpool D;Tanahashi M;Meng XY;McCutcheon JP;Fukatsu T

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蝉依赖于基本的细菌共生体Sulcia和Hodgkinia。共生体的基因组非常精简,以提供必需氨基酸和其他营养素。在一些分枝系统中,霍奇金氏菌基因组被片段化成许多小环,这可能代表基因组侵蚀接近崩溃的关键阶段。接下来会发生什么?我们的调查显示,虽然Sulcia是保守的所有物种中,他们中的大多数已经失去了霍奇金氏,而是港口酵母样真菌协会。真菌共生体与蝉寄生的Ophiocorphic真菌在遗传学上混杂在一起,表明蝉中昆虫病原体经常性的共生体替换,并提供了对寄生-共生进化连续体、共生体基因组侵蚀补偿和宿主-共生体协会多样化的机制的见解。不同的昆虫与古老的细菌共生体有关,其基因组往往遭受急剧减少和退化。在极端情况下,这种共生体基因组似乎几乎无法维持基本的细胞功能,这构成了共生进化中的一个悬而未决的问题。在这里,我们报告了一个昆虫群,其中一个古老的共生体谱系遭受大规模的基因组侵蚀,经历了反复灭绝和更换主机相关的病原微生物。蝉与古老的细菌共生体Sulcia和Hodgkinia有关,它们的流线型基因组专门用于合成必需氨基酸,从而使宿主能够以植物汁液为生。然而,我们对24种日本对虾的检查显示,虽然所有的物种都具有沟,但只有9种保留了霍奇金病,并且它们的基因组表现出相当大的结构不稳定性。剩下的15个物种缺乏霍奇金氏菌,而是含有酵母样真菌共生体。详细的系统发育分析发现重复霍奇金真菌和真菌真菌的替代蝉。真菌共生体与蝉寄生Ophiocorphic真菌,确定昆虫病原真菌共生体的起源。大部分蝉类真菌共生体是不可培养的,而白腹玫荔的共生体是可培养的,可能是因为它处于共生体替换的早期阶段。真菌共生体的基因组测序揭示了其代谢的多功能性,大概能够合成几乎所有的氨基酸,维生素和其他代谢产物,这足以弥补霍奇金氏菌的损失。这些发现突出了寄生和共生之间直接的生态和进化联系,这可能提供了一个进化轨迹,通过病原体驯化来修复恶化的古老共生关系。
Cicadas are dependent on the essential bacterial symbionts Sulcia and Hodgkinia. The symbiont genomes are extremely streamlined for provisioning of essential amino acids and other nutrients. In some cicada lineages, Hodgkinia genomes are fragmented into numerous minicircles, which may represent a critical stage of genomic erosion close to collapse. What would happen subsequently? Our survey of the Japanese cicada diversity revealed that while Sulcia is conserved among all species, the majority of them have lost Hodgkinia and instead harbor yeast-like fungal associates. The fungal symbionts are phylogenetically intermingled with cicada-parasitizing Ophiocordyceps fungi, indicating recurrent symbiont replacements by entomopathogens in cicadas and providing insights into the mechanisms underlying the parasitism-symbiosis evolutionary continuum, compensation of symbiont genome erosion, and diversification of host-symbiont associations. Diverse insects are associated with ancient bacterial symbionts, whose genomes have often suffered drastic reduction and degeneration. In extreme cases, such symbiont genomes seem almost unable to sustain the basic cellular functioning, which comprises an open question in the evolution of symbiosis. Here, we report an insect group wherein an ancient symbiont lineage suffering massive genome erosion has experienced recurrent extinction and replacement by host-associated pathogenic microbes. Cicadas are associated with the ancient bacterial co-obligate symbionts Sulcia and Hodgkinia, whose streamlined genomes are specialized for synthesizing essential amino acids, thereby enabling the host to live on plant sap. However, our inspection of 24 Japanese cicada species revealed that while all species possessed Sulcia, only nine species retained Hodgkinia, and their genomes exhibited substantial structural instability. The remaining 15 species lacked Hodgkinia and instead harbored yeast-like fungal symbionts. Detailed phylogenetic analyses uncovered repeated Hodgkinia-fungus and fungus-fungus replacements in cicadas. The fungal symbionts were phylogenetically intermingled with cicada-parasitizing Ophiocordyceps fungi, identifying entomopathogenic origins of the fungal symbionts. Most fungal symbionts of cicadas were uncultivable, but the fungal symbiont of Meimuna opalifera was cultivable, possibly because it is at an early stage of fungal symbiont replacement. Genome sequencing of the fungal symbiont revealed its metabolic versatility, presumably capable of synthesizing almost all amino acids, vitamins, and other metabolites, which is more than sufficient to compensate for the Hodgkinia loss. These findings highlight a straightforward ecological and evolutionary connection between parasitism and symbiosis, which may provide an evolutionary trajectory to renovate deteriorated ancient symbiosis via pathogen domestication.
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影响因子: 23.8
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发表时间: 2015-08-18
影响因子: 11.1
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影响因子: 1.2
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