Physiological and evolutionary contexts of a new symbiotic species from the nitrogen-recycling gut community of turtle ants

Physiological and evolutionary contexts of a new symbiotic species from the nitrogen-recycling gut community of turtle ants
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DOI:
10.1038/s41396-023-01490-1
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发表时间:
2023-08-09
期刊:
影响因子:
11
通讯作者:
Russell,Jacob A.
Russell,Jacob A.
中科院分区:
环境科学与生态学1区
文献类型:
--
作者:
Bechade,Benoit;Cabuslay,Christian S.;Russell,Jacob A.

文献摘要

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虽然基因组测序扩大了我们对共生的认识,但由于基因组冗余和体内影响的不确定性,多物种微生物组内的角色分配仍然具有挑战性。我们解决这样的问题,在这里,一个专门的氮(N)回收微生物组的龟蚁,描述了一个新的属和种的肠道共生体-Ischyrobacter davidsoniae(Betaproteobacteria:Burkholderiales:Alcaligenaceae)-及其在体内的生理背景。对扩增子测序数据的重新分析,精确分配Ischyroplasty读数,揭示了龟蚁属中似乎无处不在的分布,表明驯化时间≥ 5000万年。通过新的基因组测序,我们还表明,分歧。Davidsoniaelineages在其尿酸分解和尿素生成能力方面是保守的。通过对Ischyrophilus和单独驯化的Burkholderialessymbions的遗传学精确定义,我们的FISH显微镜显示了I. davidsoniae,在回肠前部有密集的种群。体内元转录组学和代谢组学被定位在宿主N-废物递送的位点,进一步暗示I。davidsoniae在一个共生体自主的N-循环途径。在编码这条通路的大部分过程中,我。davidsoniae仅表达成熟成虫必需步骤的一个子集,包括从尿囊酸衍生尿素的倒数第二步。其余步骤由其他专门的肠道共生体表达。总的来说,这种组合将中肠共生体产生的肌苷转化为后肠中的尿素和氨。尿素支持宿主氨基酸预算和角质层合成,并与其他活跃的N-循环的古老性质在这里发现,我。davidsoniae在保守和有影响力的多方共生中成为核心角色。
While genome sequencing has expanded our knowledge of symbiosis, role assignment within multi-species microbiomes remains challenging due to genomic redundancy and the uncertainties of in vivo impacts. We address such questions, here, for a specialized nitrogen (N) recycling microbiome of turtle ants, describing a new genus and species of gut symbiont—Ischyrobacter davidsoniae(Betaproteobacteria:Burkholderiales:Alcaligenaceae)—and its in vivo physiological context. A re-analysis of amplicon sequencing data, with precisely assignedIschyrobacterreads, revealed a seemingly ubiquitous distribution across the turtle ant genusCephalotes, suggesting ≥50 million years since domestication. Through new genome sequencing, we also show that divergentI. davidsoniaelineages are conserved in their uricolytic and urea-generating capacities. With phylogenetically refined definitions ofIschyrobacterand separately domesticatedBurkholderialessymbionts, our FISH microscopy revealed a distinct niche forI. davidsoniae, with dense populations at the anterior ileum. Being positioned at the site of host N-waste delivery, in vivo metatranscriptomics and metabolomics further implicateI. davidsoniaewithin a symbiont-autonomous N-recycling pathway. While encoding much of this pathway,I. davidsoniaeexpressed only a subset of the requisite steps in mature adult workers, including the penultimate step deriving urea from allantoate. The remaining steps were expressed by other specialized gut symbionts. Collectively, this assemblage converts inosine, made from midgut symbionts, into urea and ammonia in the hindgut. With urea supporting host amino acid budgets and cuticle synthesis, and with the ancient nature of other active N-recyclers discovered here,I. davidsoniaeemerges as a central player in a conserved and impactful, multipartite symbiosis.