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

Detalhes bibliográficos
Autor(a) principal: Zani, Renata de Oliveira Aquino [UNESP]
Data de Publicação: 2021
Outros Autores: Ferro, Milene [UNESP], Bacci, Maurício [UNESP]
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.1002/ece3.8213
http://hdl.handle.net/11449/230056
Resumo: 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 Three phylogenetically distinct and culturable diazotrophs are perennial symbionts of leaf-cutting antsThe 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.Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)Centro de Estudos de Insetos Sociais (CEIS) Universidade Estadual Paulista (UNESP), SPDepartamento de Biologia Geral e Aplicada Universidade Estadual Paulista (UNESP), SPCentro de Estudos de Insetos Sociais (CEIS) Universidade Estadual Paulista (UNESP), SPDepartamento de Biologia Geral e Aplicada Universidade Estadual Paulista (UNESP), SPCNPq: 155742/2018-3CAPES: 2016/18380-2CAPES: 88887.468201/2019-00Universidade Estadual Paulista (UNESP)Zani, Renata de Oliveira Aquino [UNESP]Ferro, Milene [UNESP]Bacci, Maurício [UNESP]2022-04-29T08:37:22Z2022-04-29T08:37:22Z2021-12-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/article17686-17699http://dx.doi.org/10.1002/ece3.8213Ecology and Evolution, v. 11, n. 24, p. 17686-17699, 2021.2045-7758http://hdl.handle.net/11449/23005610.1002/ece3.82132-s2.0-85121137410Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengEcology and Evolutioninfo:eu-repo/semantics/openAccess2024-04-11T14:57:20Zoai:repositorio.unesp.br:11449/230056Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T19:07:03.272872Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv 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
spellingShingle Three phylogenetically distinct and culturable diazotrophs are perennial symbionts of leaf-cutting ants
Zani, Renata de Oliveira Aquino [UNESP]
title_short 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_sort Three phylogenetically distinct and culturable diazotrophs are perennial symbionts of leaf-cutting ants
author Zani, Renata de Oliveira Aquino [UNESP]
author_facet Zani, Renata de Oliveira Aquino [UNESP]
Ferro, Milene [UNESP]
Bacci, Maurício [UNESP]
author_role author
author2 Ferro, Milene [UNESP]
Bacci, Maurício [UNESP]
author2_role author
author
dc.contributor.none.fl_str_mv Universidade Estadual Paulista (UNESP)
dc.contributor.author.fl_str_mv Zani, Renata de Oliveira Aquino [UNESP]
Ferro, Milene [UNESP]
Bacci, Maurício [UNESP]
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.
publishDate 2021
dc.date.none.fl_str_mv 2021-12-01
2022-04-29T08:37:22Z
2022-04-29T08:37:22Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.1002/ece3.8213
Ecology and Evolution, v. 11, n. 24, p. 17686-17699, 2021.
2045-7758
http://hdl.handle.net/11449/230056
10.1002/ece3.8213
2-s2.0-85121137410
url http://dx.doi.org/10.1002/ece3.8213
http://hdl.handle.net/11449/230056
identifier_str_mv Ecology and Evolution, v. 11, n. 24, p. 17686-17699, 2021.
2045-7758
10.1002/ece3.8213
2-s2.0-85121137410
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Ecology and Evolution
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 17686-17699
dc.source.none.fl_str_mv Scopus
reponame:Repositório Institucional da UNESP
instname:Universidade Estadual Paulista (UNESP)
instacron:UNESP
instname_str Universidade Estadual Paulista (UNESP)
instacron_str UNESP
institution UNESP
reponame_str Repositório Institucional da UNESP
collection Repositório Institucional da UNESP
repository.name.fl_str_mv Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)
repository.mail.fl_str_mv
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