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Three phylogenetically distinct and culturable diazotrophs are perennial symbionts of leaf‐cutting ants

The obligate mutualistic basidiomycete fungus, Leucocoprinus gongylophorus, mediates nutrition of leaf‐cutting ants with carbons from vegetal matter. In addition, diazotrophic Enterobacteriales in the fungus garden and intestinal Rhizobiales supposedly mediate assimilation of atmospheric nitrogen, a...

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Autores principales: Zani, Renata de Oliveira Aquino, Ferro, Milene, Bacci, Maurício
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8717316/
https://www.ncbi.nlm.nih.gov/pubmed/35003632
http://dx.doi.org/10.1002/ece3.8213
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author Zani, Renata de Oliveira Aquino
Ferro, Milene
Bacci, Maurício
author_facet Zani, Renata de Oliveira Aquino
Ferro, Milene
Bacci, Maurício
author_sort Zani, Renata de Oliveira Aquino
collection PubMed
description The obligate mutualistic basidiomycete fungus, Leucocoprinus gongylophorus, mediates nutrition of leaf‐cutting ants with carbons from vegetal matter. In addition, diazotrophic Enterobacteriales in the fungus garden and intestinal Rhizobiales supposedly mediate assimilation of atmospheric nitrogen, and Entomoplasmatales in the genus Mesoplasma, as well as other yet unidentified strains, supposedly mediate ant assimilation of other compounds from vegetal matter, such as citrate, fructose, and amino acids. Together, these nutritional partners would support the production of high yields of leafcutter biomass. In the present investigation, we propose that three phylogenetically distinct and culturable diazotrophs in the genera Ralstonia, Methylobacterium, and Pseudomonas integrate this symbiotic nutrition network, facilitating ant nutrition on nitrogen. Strains in these genera were often isolated and directly sequenced in 16S rRNA libraries from the ant abdomen, together with the nondiazotrophs Acinetobacter and Brachybacterium. These five isolates were underrepresented in libraries, suggesting that none of them is dominant in vivo. Libraries have been dominated by four uncultured Rhizobiales strains in the genera Liberibacter, Terasakiella, and Bartonella and, only in Acromyrmex ants, by the Entomoplasmatales in the genus Mesoplasma. Acromyrmex also presented small amounts of two other uncultured Entomoplasmatales strains, Entomoplasma and Spiroplasma. The absence of Entomoplasmatales in Atta workers implicates that the association with these bacteria is not mandatory for ant biomass production. Most of the strains that we detected in South American ants were genetically similar with strains previously described in association with leafcutters from Central and North America, indicating wide geographic dispersion, and suggesting fixed ecological services.
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spelling pubmed-87173162022-01-06 Three phylogenetically distinct and culturable diazotrophs are perennial symbionts of leaf‐cutting ants Zani, Renata de Oliveira Aquino Ferro, Milene Bacci, Maurício Ecol Evol Research Articles The obligate mutualistic basidiomycete fungus, Leucocoprinus gongylophorus, mediates nutrition of leaf‐cutting ants with carbons from vegetal matter. In addition, diazotrophic Enterobacteriales in the fungus garden and intestinal Rhizobiales supposedly mediate assimilation of atmospheric nitrogen, and Entomoplasmatales in the genus Mesoplasma, as well as other yet unidentified strains, supposedly mediate ant assimilation of other compounds from vegetal matter, such as citrate, fructose, and amino acids. Together, these nutritional partners would support the production of high yields of leafcutter biomass. In the present investigation, we propose that three phylogenetically distinct and culturable diazotrophs in the genera Ralstonia, Methylobacterium, and Pseudomonas integrate this symbiotic nutrition network, facilitating ant nutrition on nitrogen. Strains in these genera were often isolated and directly sequenced in 16S rRNA libraries from the ant abdomen, together with the nondiazotrophs Acinetobacter and Brachybacterium. These five isolates were underrepresented in libraries, suggesting that none of them is dominant in vivo. Libraries have been dominated by four uncultured Rhizobiales strains in the genera Liberibacter, Terasakiella, and Bartonella and, only in Acromyrmex ants, by the Entomoplasmatales in the genus Mesoplasma. Acromyrmex also presented small amounts of two other uncultured Entomoplasmatales strains, Entomoplasma and Spiroplasma. The absence of Entomoplasmatales in Atta workers implicates that the association with these bacteria is not mandatory for ant biomass production. Most of the strains that we detected in South American ants were genetically similar with strains previously described in association with leafcutters from Central and North America, indicating wide geographic dispersion, and suggesting fixed ecological services. John Wiley and Sons Inc. 2021-12-14 /pmc/articles/PMC8717316/ /pubmed/35003632 http://dx.doi.org/10.1002/ece3.8213 Text en © 2021 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Zani, Renata de Oliveira Aquino
Ferro, Milene
Bacci, Maurício
Three phylogenetically distinct and culturable diazotrophs are perennial symbionts of leaf‐cutting ants
title Three phylogenetically distinct and culturable diazotrophs are perennial symbionts of leaf‐cutting ants
title_full Three phylogenetically distinct and culturable diazotrophs are perennial symbionts of leaf‐cutting ants
title_fullStr Three phylogenetically distinct and culturable diazotrophs are perennial symbionts of leaf‐cutting ants
title_full_unstemmed Three phylogenetically distinct and culturable diazotrophs are perennial symbionts of leaf‐cutting ants
title_short Three phylogenetically distinct and culturable diazotrophs are perennial symbionts of leaf‐cutting ants
title_sort three phylogenetically distinct and culturable diazotrophs are perennial symbionts of leaf‐cutting ants
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8717316/
https://www.ncbi.nlm.nih.gov/pubmed/35003632
http://dx.doi.org/10.1002/ece3.8213
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