Egg-laying by female Aedes aegypti shapes the bacterial communities of breeding sites

Autores
Mosquera, Katherine D.; Martínez Villegas, Luis Eduardo; Rocha Fernandes, Gabriel; Rocha David, Mariana; Maciel de Freitas, Rafael; Moreira, Luciano A; Lorenzo, Marcelo Gustavo
Año de publicación
2023
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Background: Aedes aegypti, the main arboviral mosquito vector, is attracted to human dwellings and makes use of human-generated breeding sites. Past research has shown that bacterial communities associated with such sites undergo compositional shifts as larvae develop and that exposure to different bacteria during larval stages can have an impact on mosquito development and life-history traits. Based on these facts, we hypothesized that female Ae. aegypti shape the bacteria communities of breeding sites during oviposition as a form of niche construction to favor offspring fitness. Results: To test this hypothesis, we first verified that gravid females can act as mechanical vectors of bacteria. We then elaborated an experimental scheme to test the impact of oviposition on breeding site microbiota. Five different groups of experimental breeding sites were set up with a sterile aqueous solution of larval food, and subsequently exposed to (1) the environment alone, (2) surface-sterilized eggs, (3) unsterilized eggs, (4) a non-egg laying female, or (5) oviposition by a gravid female. The microbiota of these differently treated sites was assessed by amplicon-oriented DNA sequencing once the larvae from the sites with eggs had completed development and formed pupae. Microbial ecology analyses revealed significant differences between the five treatments in terms of diversity. In particular, between-treatment shifts in abundance profiles were detected, showing that females induce a significant decrease in microbial alpha diversity through oviposition. In addition, indicator species analysis pinpointed bacterial taxa with significant predicting values and fidelity coefficients for the samples in which single females laid eggs. Furthermore, we provide evidence regarding how one of these indicator taxa, Elizabethkingia, exerts a positive effect on the development and fitness of mosquito larvae. Conclusions: Ovipositing females impact the composition of the microbial community associated with a breeding site, promoting certain bacterial taxa over those prevailing in the environment. Among these bacteria, we found known mosquito symbionts and showed that they can improve offspring fitness if present in the water where eggs are laid. We deem this oviposition-mediated bacterial community shaping as a form of niche construction initiated by the gravid female.
Fil: Mosquera, Katherine D.. Fundación Oswaldo Cruz; Brasil
Fil: Martínez Villegas, Luis Eduardo. Ohio State University; Estados Unidos. Fundación Oswaldo Cruz; Brasil
Fil: Rocha Fernandes, Gabriel. Fundación Oswaldo Cruz; Brasil
Fil: Rocha David, Mariana. Fundación Oswaldo Cruz; Brasil
Fil: Maciel de Freitas, Rafael. Fundación Oswaldo Cruz; Brasil
Fil: Moreira, Luciano A. Fundación Oswaldo Cruz; Brasil
Fil: Lorenzo, Marcelo Gustavo. Fundación Oswaldo Cruz; Brasil. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mar del Plata. Instituto de Investigaciones en Biodiversidad y Biotecnología; Argentina
Materia
AEDES AEGYPTI
BREEDING SITES
MICROBIOTA
NICHE CONSTRUCTION
OVIPOSITION
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/250243

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network_name_str CONICET Digital (CONICET)
spelling Egg-laying by female Aedes aegypti shapes the bacterial communities of breeding sitesMosquera, Katherine D.Martínez Villegas, Luis EduardoRocha Fernandes, GabrielRocha David, MarianaMaciel de Freitas, RafaelMoreira, Luciano ALorenzo, Marcelo GustavoAEDES AEGYPTIBREEDING SITESMICROBIOTANICHE CONSTRUCTIONOVIPOSITIONhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Background: Aedes aegypti, the main arboviral mosquito vector, is attracted to human dwellings and makes use of human-generated breeding sites. Past research has shown that bacterial communities associated with such sites undergo compositional shifts as larvae develop and that exposure to different bacteria during larval stages can have an impact on mosquito development and life-history traits. Based on these facts, we hypothesized that female Ae. aegypti shape the bacteria communities of breeding sites during oviposition as a form of niche construction to favor offspring fitness. Results: To test this hypothesis, we first verified that gravid females can act as mechanical vectors of bacteria. We then elaborated an experimental scheme to test the impact of oviposition on breeding site microbiota. Five different groups of experimental breeding sites were set up with a sterile aqueous solution of larval food, and subsequently exposed to (1) the environment alone, (2) surface-sterilized eggs, (3) unsterilized eggs, (4) a non-egg laying female, or (5) oviposition by a gravid female. The microbiota of these differently treated sites was assessed by amplicon-oriented DNA sequencing once the larvae from the sites with eggs had completed development and formed pupae. Microbial ecology analyses revealed significant differences between the five treatments in terms of diversity. In particular, between-treatment shifts in abundance profiles were detected, showing that females induce a significant decrease in microbial alpha diversity through oviposition. In addition, indicator species analysis pinpointed bacterial taxa with significant predicting values and fidelity coefficients for the samples in which single females laid eggs. Furthermore, we provide evidence regarding how one of these indicator taxa, Elizabethkingia, exerts a positive effect on the development and fitness of mosquito larvae. Conclusions: Ovipositing females impact the composition of the microbial community associated with a breeding site, promoting certain bacterial taxa over those prevailing in the environment. Among these bacteria, we found known mosquito symbionts and showed that they can improve offspring fitness if present in the water where eggs are laid. We deem this oviposition-mediated bacterial community shaping as a form of niche construction initiated by the gravid female.Fil: Mosquera, Katherine D.. Fundación Oswaldo Cruz; BrasilFil: Martínez Villegas, Luis Eduardo. Ohio State University; Estados Unidos. Fundación Oswaldo Cruz; BrasilFil: Rocha Fernandes, Gabriel. Fundación Oswaldo Cruz; BrasilFil: Rocha David, Mariana. Fundación Oswaldo Cruz; BrasilFil: Maciel de Freitas, Rafael. Fundación Oswaldo Cruz; BrasilFil: Moreira, Luciano A. Fundación Oswaldo Cruz; BrasilFil: Lorenzo, Marcelo Gustavo. Fundación Oswaldo Cruz; Brasil. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mar del Plata. Instituto de Investigaciones en Biodiversidad y Biotecnología; ArgentinaBioMed Central2023-12info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/250243Mosquera, Katherine D.; Martínez Villegas, Luis Eduardo; Rocha Fernandes, Gabriel; Rocha David, Mariana; Maciel de Freitas, Rafael; et al.; Egg-laying by female Aedes aegypti shapes the bacterial communities of breeding sites; BioMed Central; Bmc Biology; 21; 1; 12-20231741-7007CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1186/s12915-023-01605-2info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-15T14:23:38Zoai:ri.conicet.gov.ar:11336/250243instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-10-15 14:23:39.056CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Egg-laying by female Aedes aegypti shapes the bacterial communities of breeding sites
title Egg-laying by female Aedes aegypti shapes the bacterial communities of breeding sites
spellingShingle Egg-laying by female Aedes aegypti shapes the bacterial communities of breeding sites
Mosquera, Katherine D.
AEDES AEGYPTI
BREEDING SITES
MICROBIOTA
NICHE CONSTRUCTION
OVIPOSITION
title_short Egg-laying by female Aedes aegypti shapes the bacterial communities of breeding sites
title_full Egg-laying by female Aedes aegypti shapes the bacterial communities of breeding sites
title_fullStr Egg-laying by female Aedes aegypti shapes the bacterial communities of breeding sites
title_full_unstemmed Egg-laying by female Aedes aegypti shapes the bacterial communities of breeding sites
title_sort Egg-laying by female Aedes aegypti shapes the bacterial communities of breeding sites
dc.creator.none.fl_str_mv Mosquera, Katherine D.
Martínez Villegas, Luis Eduardo
Rocha Fernandes, Gabriel
Rocha David, Mariana
Maciel de Freitas, Rafael
Moreira, Luciano A
Lorenzo, Marcelo Gustavo
author Mosquera, Katherine D.
author_facet Mosquera, Katherine D.
Martínez Villegas, Luis Eduardo
Rocha Fernandes, Gabriel
Rocha David, Mariana
Maciel de Freitas, Rafael
Moreira, Luciano A
Lorenzo, Marcelo Gustavo
author_role author
author2 Martínez Villegas, Luis Eduardo
Rocha Fernandes, Gabriel
Rocha David, Mariana
Maciel de Freitas, Rafael
Moreira, Luciano A
Lorenzo, Marcelo Gustavo
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv AEDES AEGYPTI
BREEDING SITES
MICROBIOTA
NICHE CONSTRUCTION
OVIPOSITION
topic AEDES AEGYPTI
BREEDING SITES
MICROBIOTA
NICHE CONSTRUCTION
OVIPOSITION
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Background: Aedes aegypti, the main arboviral mosquito vector, is attracted to human dwellings and makes use of human-generated breeding sites. Past research has shown that bacterial communities associated with such sites undergo compositional shifts as larvae develop and that exposure to different bacteria during larval stages can have an impact on mosquito development and life-history traits. Based on these facts, we hypothesized that female Ae. aegypti shape the bacteria communities of breeding sites during oviposition as a form of niche construction to favor offspring fitness. Results: To test this hypothesis, we first verified that gravid females can act as mechanical vectors of bacteria. We then elaborated an experimental scheme to test the impact of oviposition on breeding site microbiota. Five different groups of experimental breeding sites were set up with a sterile aqueous solution of larval food, and subsequently exposed to (1) the environment alone, (2) surface-sterilized eggs, (3) unsterilized eggs, (4) a non-egg laying female, or (5) oviposition by a gravid female. The microbiota of these differently treated sites was assessed by amplicon-oriented DNA sequencing once the larvae from the sites with eggs had completed development and formed pupae. Microbial ecology analyses revealed significant differences between the five treatments in terms of diversity. In particular, between-treatment shifts in abundance profiles were detected, showing that females induce a significant decrease in microbial alpha diversity through oviposition. In addition, indicator species analysis pinpointed bacterial taxa with significant predicting values and fidelity coefficients for the samples in which single females laid eggs. Furthermore, we provide evidence regarding how one of these indicator taxa, Elizabethkingia, exerts a positive effect on the development and fitness of mosquito larvae. Conclusions: Ovipositing females impact the composition of the microbial community associated with a breeding site, promoting certain bacterial taxa over those prevailing in the environment. Among these bacteria, we found known mosquito symbionts and showed that they can improve offspring fitness if present in the water where eggs are laid. We deem this oviposition-mediated bacterial community shaping as a form of niche construction initiated by the gravid female.
Fil: Mosquera, Katherine D.. Fundación Oswaldo Cruz; Brasil
Fil: Martínez Villegas, Luis Eduardo. Ohio State University; Estados Unidos. Fundación Oswaldo Cruz; Brasil
Fil: Rocha Fernandes, Gabriel. Fundación Oswaldo Cruz; Brasil
Fil: Rocha David, Mariana. Fundación Oswaldo Cruz; Brasil
Fil: Maciel de Freitas, Rafael. Fundación Oswaldo Cruz; Brasil
Fil: Moreira, Luciano A. Fundación Oswaldo Cruz; Brasil
Fil: Lorenzo, Marcelo Gustavo. Fundación Oswaldo Cruz; Brasil. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mar del Plata. Instituto de Investigaciones en Biodiversidad y Biotecnología; Argentina
description Background: Aedes aegypti, the main arboviral mosquito vector, is attracted to human dwellings and makes use of human-generated breeding sites. Past research has shown that bacterial communities associated with such sites undergo compositional shifts as larvae develop and that exposure to different bacteria during larval stages can have an impact on mosquito development and life-history traits. Based on these facts, we hypothesized that female Ae. aegypti shape the bacteria communities of breeding sites during oviposition as a form of niche construction to favor offspring fitness. Results: To test this hypothesis, we first verified that gravid females can act as mechanical vectors of bacteria. We then elaborated an experimental scheme to test the impact of oviposition on breeding site microbiota. Five different groups of experimental breeding sites were set up with a sterile aqueous solution of larval food, and subsequently exposed to (1) the environment alone, (2) surface-sterilized eggs, (3) unsterilized eggs, (4) a non-egg laying female, or (5) oviposition by a gravid female. The microbiota of these differently treated sites was assessed by amplicon-oriented DNA sequencing once the larvae from the sites with eggs had completed development and formed pupae. Microbial ecology analyses revealed significant differences between the five treatments in terms of diversity. In particular, between-treatment shifts in abundance profiles were detected, showing that females induce a significant decrease in microbial alpha diversity through oviposition. In addition, indicator species analysis pinpointed bacterial taxa with significant predicting values and fidelity coefficients for the samples in which single females laid eggs. Furthermore, we provide evidence regarding how one of these indicator taxa, Elizabethkingia, exerts a positive effect on the development and fitness of mosquito larvae. Conclusions: Ovipositing females impact the composition of the microbial community associated with a breeding site, promoting certain bacterial taxa over those prevailing in the environment. Among these bacteria, we found known mosquito symbionts and showed that they can improve offspring fitness if present in the water where eggs are laid. We deem this oviposition-mediated bacterial community shaping as a form of niche construction initiated by the gravid female.
publishDate 2023
dc.date.none.fl_str_mv 2023-12
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/250243
Mosquera, Katherine D.; Martínez Villegas, Luis Eduardo; Rocha Fernandes, Gabriel; Rocha David, Mariana; Maciel de Freitas, Rafael; et al.; Egg-laying by female Aedes aegypti shapes the bacterial communities of breeding sites; BioMed Central; Bmc Biology; 21; 1; 12-2023
1741-7007
CONICET Digital
CONICET
url http://hdl.handle.net/11336/250243
identifier_str_mv Mosquera, Katherine D.; Martínez Villegas, Luis Eduardo; Rocha Fernandes, Gabriel; Rocha David, Mariana; Maciel de Freitas, Rafael; et al.; Egg-laying by female Aedes aegypti shapes the bacterial communities of breeding sites; BioMed Central; Bmc Biology; 21; 1; 12-2023
1741-7007
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1186/s12915-023-01605-2
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv BioMed Central
publisher.none.fl_str_mv BioMed Central
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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