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.
中科院分区:
文献类型:
--
作者:
Bechade,Benoit;Cabuslay,Christian S.;Russell,Jacob A.
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.