Immunity and survival response of Atta cephalotes (Hymenoptera: Myrmicinae) workers to Metarhizium anisopliae infection: Potential role of their associated microbiota

Detalhes bibliográficos
Autor(a) principal: Valencia-Giraldo, Sandra Milena
Data de Publicação: 2021
Outros Autores: Niño-Castro, Andrea, López-Peña, Andrea, Trejos-Vidal, Danna, Correa-Bueno, Odair [UNESP], Montoya-Lerma, James
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.1371/journal.pone.0247545
http://hdl.handle.net/11449/207405
Resumo: Leaf-cutting ants of the genera Atta and Acromyrmex are at constant risk of epizootics due to their dense living conditions and frequent social interactions between genetically related individuals. To help mitigate the risk of epizootics, these ants display individual and collective immune responses, including associations with symbiotic bacteria that can enhance their resistance to pathogenic infections. For example, Acromyrmex spp. harbor actinobacteria that control infection by Escovopsis in their fungal gardens. Although Atta spp. do not maintain symbiosis with protective actinobacteria, the evidence suggests that these insects are colonized by bacterial microbiota that may play a role in their defense against pathogens. The potential role of the bacterial microbiome of Atta workers in enhancing host immunity remains unexplored. We evaluated multiple parameters of the individual immunity of Atta cephalotes (Linnaeus, 1758) workers, including hemocyte count, encapsulation response, and the antimicrobial activity of the hemolymph in the presence or absence of bacterial microbiota. Experiments were performed on ants reared under standard conditions as well as on ants previously exposed to the entomopathogenic fungus Metharrizium anisopliae. Furthermore, the effects of the presence/absence of bacteria on the survival of workers exposed to M. anisopliae were evaluated. The bacterial microbiota associated with A. cephalotes workers does not modulate the number of hemocytes under control conditions or under conditions of exposure to the fungal pathogen. In addition, infection by M. anisopliae, but not microbiota, increases the encapsulation response. Similarly, the exposure of workers to this fungus led to increased hemolymph antimicrobial activity. Conversely, the removal of bacterial microbiota did not have a significant impact on the survival of workers with M. anisopliae. Our results suggest that the bacterial microbiota associated with the cuticle of A. cephalotes workers does not play a role as a modulator of innate immunity, either at baseline or after exposure to the entomopathogen M. anisopliae. Further, upon infection, workers rely on mechanisms of humoral immunity to respond to this threat. Overall, our findings indicate that the bacterial microbiota associated with A. cephalotes workers does not play a defensive role.
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spelling Immunity and survival response of Atta cephalotes (Hymenoptera: Myrmicinae) workers to Metarhizium anisopliae infection: Potential role of their associated microbiotaLeaf-cutting ants of the genera Atta and Acromyrmex are at constant risk of epizootics due to their dense living conditions and frequent social interactions between genetically related individuals. To help mitigate the risk of epizootics, these ants display individual and collective immune responses, including associations with symbiotic bacteria that can enhance their resistance to pathogenic infections. For example, Acromyrmex spp. harbor actinobacteria that control infection by Escovopsis in their fungal gardens. Although Atta spp. do not maintain symbiosis with protective actinobacteria, the evidence suggests that these insects are colonized by bacterial microbiota that may play a role in their defense against pathogens. The potential role of the bacterial microbiome of Atta workers in enhancing host immunity remains unexplored. We evaluated multiple parameters of the individual immunity of Atta cephalotes (Linnaeus, 1758) workers, including hemocyte count, encapsulation response, and the antimicrobial activity of the hemolymph in the presence or absence of bacterial microbiota. Experiments were performed on ants reared under standard conditions as well as on ants previously exposed to the entomopathogenic fungus Metharrizium anisopliae. Furthermore, the effects of the presence/absence of bacteria on the survival of workers exposed to M. anisopliae were evaluated. The bacterial microbiota associated with A. cephalotes workers does not modulate the number of hemocytes under control conditions or under conditions of exposure to the fungal pathogen. In addition, infection by M. anisopliae, but not microbiota, increases the encapsulation response. Similarly, the exposure of workers to this fungus led to increased hemolymph antimicrobial activity. Conversely, the removal of bacterial microbiota did not have a significant impact on the survival of workers with M. anisopliae. Our results suggest that the bacterial microbiota associated with the cuticle of A. cephalotes workers does not play a role as a modulator of innate immunity, either at baseline or after exposure to the entomopathogen M. anisopliae. Further, upon infection, workers rely on mechanisms of humoral immunity to respond to this threat. Overall, our findings indicate that the bacterial microbiota associated with A. cephalotes workers does not play a defensive role.Akademiet for de Tekniske VidenskaberCenter for Emerging and Innovative SciencesMaryland Vegetable Growers AssociationUniversidad del ValleDepartment of Biology Universidad del ValleCenter for the Study of Social Insects (CEIS) São Paulo State University (UNESP) Campus Rio ClaroCenter for the Study of Social Insects (CEIS) São Paulo State University (UNESP) Campus Rio ClaroUniversidad del Valle: CI 71143Universidad del ValleUniversidade Estadual Paulista (Unesp)Valencia-Giraldo, Sandra MilenaNiño-Castro, AndreaLópez-Peña, AndreaTrejos-Vidal, DannaCorrea-Bueno, Odair [UNESP]Montoya-Lerma, James2021-06-25T10:54:36Z2021-06-25T10:54:36Z2021-02-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.1371/journal.pone.0247545PLoS ONE, v. 16, n. 2 February, 2021.1932-6203http://hdl.handle.net/11449/20740510.1371/journal.pone.02475452-s2.0-85102097654Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengPLoS ONEinfo:eu-repo/semantics/openAccess2024-04-11T14:57:01Zoai:repositorio.unesp.br:11449/207405Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-05-23T11:04:13.530294Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv Immunity and survival response of Atta cephalotes (Hymenoptera: Myrmicinae) workers to Metarhizium anisopliae infection: Potential role of their associated microbiota
title Immunity and survival response of Atta cephalotes (Hymenoptera: Myrmicinae) workers to Metarhizium anisopliae infection: Potential role of their associated microbiota
spellingShingle Immunity and survival response of Atta cephalotes (Hymenoptera: Myrmicinae) workers to Metarhizium anisopliae infection: Potential role of their associated microbiota
Valencia-Giraldo, Sandra Milena
title_short Immunity and survival response of Atta cephalotes (Hymenoptera: Myrmicinae) workers to Metarhizium anisopliae infection: Potential role of their associated microbiota
title_full Immunity and survival response of Atta cephalotes (Hymenoptera: Myrmicinae) workers to Metarhizium anisopliae infection: Potential role of their associated microbiota
title_fullStr Immunity and survival response of Atta cephalotes (Hymenoptera: Myrmicinae) workers to Metarhizium anisopliae infection: Potential role of their associated microbiota
title_full_unstemmed Immunity and survival response of Atta cephalotes (Hymenoptera: Myrmicinae) workers to Metarhizium anisopliae infection: Potential role of their associated microbiota
title_sort Immunity and survival response of Atta cephalotes (Hymenoptera: Myrmicinae) workers to Metarhizium anisopliae infection: Potential role of their associated microbiota
author Valencia-Giraldo, Sandra Milena
author_facet Valencia-Giraldo, Sandra Milena
Niño-Castro, Andrea
López-Peña, Andrea
Trejos-Vidal, Danna
Correa-Bueno, Odair [UNESP]
Montoya-Lerma, James
author_role author
author2 Niño-Castro, Andrea
López-Peña, Andrea
Trejos-Vidal, Danna
Correa-Bueno, Odair [UNESP]
Montoya-Lerma, James
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv Universidad del Valle
Universidade Estadual Paulista (Unesp)
dc.contributor.author.fl_str_mv Valencia-Giraldo, Sandra Milena
Niño-Castro, Andrea
López-Peña, Andrea
Trejos-Vidal, Danna
Correa-Bueno, Odair [UNESP]
Montoya-Lerma, James
description Leaf-cutting ants of the genera Atta and Acromyrmex are at constant risk of epizootics due to their dense living conditions and frequent social interactions between genetically related individuals. To help mitigate the risk of epizootics, these ants display individual and collective immune responses, including associations with symbiotic bacteria that can enhance their resistance to pathogenic infections. For example, Acromyrmex spp. harbor actinobacteria that control infection by Escovopsis in their fungal gardens. Although Atta spp. do not maintain symbiosis with protective actinobacteria, the evidence suggests that these insects are colonized by bacterial microbiota that may play a role in their defense against pathogens. The potential role of the bacterial microbiome of Atta workers in enhancing host immunity remains unexplored. We evaluated multiple parameters of the individual immunity of Atta cephalotes (Linnaeus, 1758) workers, including hemocyte count, encapsulation response, and the antimicrobial activity of the hemolymph in the presence or absence of bacterial microbiota. Experiments were performed on ants reared under standard conditions as well as on ants previously exposed to the entomopathogenic fungus Metharrizium anisopliae. Furthermore, the effects of the presence/absence of bacteria on the survival of workers exposed to M. anisopliae were evaluated. The bacterial microbiota associated with A. cephalotes workers does not modulate the number of hemocytes under control conditions or under conditions of exposure to the fungal pathogen. In addition, infection by M. anisopliae, but not microbiota, increases the encapsulation response. Similarly, the exposure of workers to this fungus led to increased hemolymph antimicrobial activity. Conversely, the removal of bacterial microbiota did not have a significant impact on the survival of workers with M. anisopliae. Our results suggest that the bacterial microbiota associated with the cuticle of A. cephalotes workers does not play a role as a modulator of innate immunity, either at baseline or after exposure to the entomopathogen M. anisopliae. Further, upon infection, workers rely on mechanisms of humoral immunity to respond to this threat. Overall, our findings indicate that the bacterial microbiota associated with A. cephalotes workers does not play a defensive role.
publishDate 2021
dc.date.none.fl_str_mv 2021-06-25T10:54:36Z
2021-06-25T10:54:36Z
2021-02-01
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/10.1371/journal.pone.0247545
PLoS ONE, v. 16, n. 2 February, 2021.
1932-6203
http://hdl.handle.net/11449/207405
10.1371/journal.pone.0247545
2-s2.0-85102097654
url http://dx.doi.org/10.1371/journal.pone.0247545
http://hdl.handle.net/11449/207405
identifier_str_mv PLoS ONE, v. 16, n. 2 February, 2021.
1932-6203
10.1371/journal.pone.0247545
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