The Hyphosphere of Leaf-Cutting Ant Cultivars Is Enriched with Helper Bacteria

Detalhes bibliográficos
Autor(a) principal: Martiarena, Maria Jesus Sutta [UNESP]
Data de Publicação: 2023
Outros Autores: Deveau, Aurelie, Montoya, Quimi Vidaurre [UNESP], Flórez, Laura V., Rodrigues, Andre [UNESP]
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.1007/s00248-023-02187-w
http://hdl.handle.net/11449/246791
Resumo: Bacteria can live in a variety of interkingdom communities playing key ecological roles. The microbiome of leaf-cutting attine ant colonies are a remarkable example of such communities, as they support ants’ metabolic processes and the maintenance of ant-fungus gardens. Studies on this topic have explored the bacterial community of the whole fungus garden, without discerning bacterial groups associated with the nutrient storage structures (gongylidia) of ant fungal cultivars. Here we studied bacteria isolated from the surface of gongylidia in the cultivars of Atta sexdens and Acromyrmex coronatus, to assess whether the bacterial community influences the biology of the fungus. A total of 10 bacterial strains were isolated from gongylidia (Bacillus sp., Lysinibacillus sp., Niallia sp., Staphylococcus sp., Paenibacillus sp., Pantoea sp., Staphylococcus sp., and one Actinobacteria). Some bacterial isolates increased gongylidia production and fungal biomass while others had inhibitory effects. Eight bacterial strains were confirmed to form biofilm-like structures on the fungal cultivar hyphae. They also showed auxiliary metabolic functions useful for the development of the fungal garden such as phosphate solubilization, siderophore production, cellulose and chitin degradation, and antifungal activity against antagonists of the fungal cultivar. Bacteria-bacteria interaction assays revealed heterogeneous behaviors including synergism and competition, which might contribute to regulate the community structure inside the garden. Our results suggest that bacteria and the ant fungal cultivar interact directly, across a continuum of positive and negative interactions within the community. These complex relationships could ultimately contribute to the stability of the ant-fungus mutualism.
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spelling The Hyphosphere of Leaf-Cutting Ant Cultivars Is Enriched with Helper BacteriaAttine antsBacteria-fungus interactionBiofilmHelper bacteriaBacteria can live in a variety of interkingdom communities playing key ecological roles. The microbiome of leaf-cutting attine ant colonies are a remarkable example of such communities, as they support ants’ metabolic processes and the maintenance of ant-fungus gardens. Studies on this topic have explored the bacterial community of the whole fungus garden, without discerning bacterial groups associated with the nutrient storage structures (gongylidia) of ant fungal cultivars. Here we studied bacteria isolated from the surface of gongylidia in the cultivars of Atta sexdens and Acromyrmex coronatus, to assess whether the bacterial community influences the biology of the fungus. A total of 10 bacterial strains were isolated from gongylidia (Bacillus sp., Lysinibacillus sp., Niallia sp., Staphylococcus sp., Paenibacillus sp., Pantoea sp., Staphylococcus sp., and one Actinobacteria). Some bacterial isolates increased gongylidia production and fungal biomass while others had inhibitory effects. Eight bacterial strains were confirmed to form biofilm-like structures on the fungal cultivar hyphae. They also showed auxiliary metabolic functions useful for the development of the fungal garden such as phosphate solubilization, siderophore production, cellulose and chitin degradation, and antifungal activity against antagonists of the fungal cultivar. Bacteria-bacteria interaction assays revealed heterogeneous behaviors including synergism and competition, which might contribute to regulate the community structure inside the garden. Our results suggest that bacteria and the ant fungal cultivar interact directly, across a continuum of positive and negative interactions within the community. These complex relationships could ultimately contribute to the stability of the ant-fungus mutualism.Department of General and Applied Biology São Paulo State University (UNESP), Avenida 24-A, 1515, Bela Vista, SPUMR IAM Université de Lorraine INRAEDepartment of Plant and Environmental Sciences University of CopenhagenDepartment of General and Applied Biology São Paulo State University (UNESP), Avenida 24-A, 1515, Bela Vista, SPUniversidade Estadual Paulista (UNESP)INRAEUniversity of CopenhagenMartiarena, Maria Jesus Sutta [UNESP]Deveau, AurelieMontoya, Quimi Vidaurre [UNESP]Flórez, Laura V.Rodrigues, Andre [UNESP]2023-07-29T12:50:36Z2023-07-29T12:50:36Z2023-01-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.1007/s00248-023-02187-wMicrobial Ecology.1432-184X0095-3628http://hdl.handle.net/11449/24679110.1007/s00248-023-02187-w2-s2.0-85147683779Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengMicrobial Ecologyinfo:eu-repo/semantics/openAccess2023-07-29T12:50:36Zoai:repositorio.unesp.br:11449/246791Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462023-07-29T12:50:36Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv The Hyphosphere of Leaf-Cutting Ant Cultivars Is Enriched with Helper Bacteria
title The Hyphosphere of Leaf-Cutting Ant Cultivars Is Enriched with Helper Bacteria
spellingShingle The Hyphosphere of Leaf-Cutting Ant Cultivars Is Enriched with Helper Bacteria
Martiarena, Maria Jesus Sutta [UNESP]
Attine ants
Bacteria-fungus interaction
Biofilm
Helper bacteria
title_short The Hyphosphere of Leaf-Cutting Ant Cultivars Is Enriched with Helper Bacteria
title_full The Hyphosphere of Leaf-Cutting Ant Cultivars Is Enriched with Helper Bacteria
title_fullStr The Hyphosphere of Leaf-Cutting Ant Cultivars Is Enriched with Helper Bacteria
title_full_unstemmed The Hyphosphere of Leaf-Cutting Ant Cultivars Is Enriched with Helper Bacteria
title_sort The Hyphosphere of Leaf-Cutting Ant Cultivars Is Enriched with Helper Bacteria
author Martiarena, Maria Jesus Sutta [UNESP]
author_facet Martiarena, Maria Jesus Sutta [UNESP]
Deveau, Aurelie
Montoya, Quimi Vidaurre [UNESP]
Flórez, Laura V.
Rodrigues, Andre [UNESP]
author_role author
author2 Deveau, Aurelie
Montoya, Quimi Vidaurre [UNESP]
Flórez, Laura V.
Rodrigues, Andre [UNESP]
author2_role author
author
author
author
dc.contributor.none.fl_str_mv Universidade Estadual Paulista (UNESP)
INRAE
University of Copenhagen
dc.contributor.author.fl_str_mv Martiarena, Maria Jesus Sutta [UNESP]
Deveau, Aurelie
Montoya, Quimi Vidaurre [UNESP]
Flórez, Laura V.
Rodrigues, Andre [UNESP]
dc.subject.por.fl_str_mv Attine ants
Bacteria-fungus interaction
Biofilm
Helper bacteria
topic Attine ants
Bacteria-fungus interaction
Biofilm
Helper bacteria
description Bacteria can live in a variety of interkingdom communities playing key ecological roles. The microbiome of leaf-cutting attine ant colonies are a remarkable example of such communities, as they support ants’ metabolic processes and the maintenance of ant-fungus gardens. Studies on this topic have explored the bacterial community of the whole fungus garden, without discerning bacterial groups associated with the nutrient storage structures (gongylidia) of ant fungal cultivars. Here we studied bacteria isolated from the surface of gongylidia in the cultivars of Atta sexdens and Acromyrmex coronatus, to assess whether the bacterial community influences the biology of the fungus. A total of 10 bacterial strains were isolated from gongylidia (Bacillus sp., Lysinibacillus sp., Niallia sp., Staphylococcus sp., Paenibacillus sp., Pantoea sp., Staphylococcus sp., and one Actinobacteria). Some bacterial isolates increased gongylidia production and fungal biomass while others had inhibitory effects. Eight bacterial strains were confirmed to form biofilm-like structures on the fungal cultivar hyphae. They also showed auxiliary metabolic functions useful for the development of the fungal garden such as phosphate solubilization, siderophore production, cellulose and chitin degradation, and antifungal activity against antagonists of the fungal cultivar. Bacteria-bacteria interaction assays revealed heterogeneous behaviors including synergism and competition, which might contribute to regulate the community structure inside the garden. Our results suggest that bacteria and the ant fungal cultivar interact directly, across a continuum of positive and negative interactions within the community. These complex relationships could ultimately contribute to the stability of the ant-fungus mutualism.
publishDate 2023
dc.date.none.fl_str_mv 2023-07-29T12:50:36Z
2023-07-29T12:50:36Z
2023-01-01
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/10.1007/s00248-023-02187-w
Microbial Ecology.
1432-184X
0095-3628
http://hdl.handle.net/11449/246791
10.1007/s00248-023-02187-w
2-s2.0-85147683779
url http://dx.doi.org/10.1007/s00248-023-02187-w
http://hdl.handle.net/11449/246791
identifier_str_mv Microbial Ecology.
1432-184X
0095-3628
10.1007/s00248-023-02187-w
2-s2.0-85147683779
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Microbial Ecology
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
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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