Physiological and evolutionary contexts of a new symbiotic species from the nitrogen-recycling gut community of turtle ants.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
10 2023
10 2023
Historique:
received:
21
03
2023
accepted:
27
07
2023
revised:
21
07
2023
pmc-release:
01
10
2024
medline:
18
9
2023
pubmed:
10
8
2023
entrez:
9
8
2023
Statut:
ppublish
Résumé
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 assigned Ischyrobacter reads, revealed a seemingly ubiquitous distribution across the turtle ant genus Cephalotes, suggesting ≥50 million years since domestication. Through new genome sequencing, we also show that divergent I. davidsoniae lineages are conserved in their uricolytic and urea-generating capacities. With phylogenetically refined definitions of Ischyrobacter and separately domesticated Burkholderiales symbionts, our FISH microscopy revealed a distinct niche for I. davidsoniae, with dense populations at the anterior ileum. Being positioned at the site of host N-waste delivery, in vivo metatranscriptomics and metabolomics further implicate I. davidsoniae within a symbiont-autonomous N-recycling pathway. While encoding much of this pathway, I. davidsoniae expressed 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. davidsoniae emerges as a central player in a conserved and impactful, multipartite symbiosis.
Identifiants
pubmed: 37558860
doi: 10.1038/s41396-023-01490-1
pii: 10.1038/s41396-023-01490-1
pmc: PMC10504363
doi:
Substances chimiques
Nitrogen
N762921K75
Urea
8W8T17847W
Banques de données
Dryad
['10.5061/dryad.kwh70rz5d']
figshare
['10.6084/m9.figshare.21989537']
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
1751-1764Informations de copyright
© 2023. The Author(s), under exclusive licence to International Society for Microbial Ecology.
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