Gut bacteriome analysis of Anastrepha fraterculus sp. 1 during the early steps of laboratory colonization

Autores
Salgueiro, Julieta; Pimper, Lidia Elena; Segura, Diego Fernando; Milla, Fabian Horacio; Russo, Romina Maria; Asimakis, Elias D.; Stathopoulou, Panagiota; Bourtzis, Kostas; Cladera, Jorge Luis; Tsiamis, George; Lanzavecchia, Silvia Beatriz
Año de publicación
2020
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Microbial communities associated to insect species are involved in essential biological functions such as host nutrition, reproduction and survivability. Main factors have been described as modulators of gut bacterial community, such as diet, habit, developmental stage and taxonomy of the host. The present work focuses on the complex changes that gut microbial communities go through when wild insects are introduced to artificial rearing conditions. Specifically, we analyzed the effect of the laboratory colonization on the richness and diversity of the gut bacteriome hosted by the fruit fly pest Anastrepha fraterculus sp. 1. Bacterial profiles were studied by amplicon sequencing of the 16S rRNA V3–V4 hypervariable region in gut samples of males and females, in teneral (1-day-old, unfed) and post-teneral (15-day-old, fed) flies. A total of 3,147,665 sequence reads were obtained and 32 bacterial operational taxonomic units (OTUs) were identified. Proteobacteria was the most abundant phylum (93.3% of the total reads) and, Wolbachia and Enterobacter were the most represented taxa at the genus level (29.9% and 27.7%, respectively, of the total read counts). Wild and laboratory flies showed highly significant differences in the relative abundances of bacteria. The analysis of the core bacteriome showed the presence of five OTUs in all samples grouped by origin, while nine and five OTUs were exclusively detected in laboratory and wild flies, respectively. Irrespective of fly origin or sex, a dominant presence of Wolbachia was observed in teneral flies, whereas Enterobacter was highly abundant in post-teneral individuals. We evidenced significant differences in bacterial richness and diversity among generations under laboratory colonization (F0, F1, F3 and F6) and compared to laboratory and wild flies, displaying also differential patterns between teneral and post-teneral flies. Laboratory and wild A. fraterculus sp. 1 harbor different gut bacterial communities. Laboratory colonization has an important effect on the microbiota, most likely associated to the combined effects of insect physiology and environmental conditions (e.g., diet and colony management).
Instituto de Genética
Fil: Salgueiro, Julieta. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética. Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Pimper, Lidia Elena. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética. Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Segura, Diego Fernando. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética. Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Milla, Fabian Horacio. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética. Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Russo, Romina María. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética. Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Asimakis, Elias D. University of Patras. Department of Environmental Engineering; Grecia
Fil: Stathopoulou, Panagiota. University of Patras. Department of Environmental Engineering; Grecia
Fil: Bourtzis, Kostas. Vienna International Centre. Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture. Insect Pest Control Laboratory; Austria
Fil: Cladera, Jorge Luis. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética. Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Tsiamis, George. University of Patras. Department of Environmental Engineering; Grecia
Fil: Lanzavecchia, Silvia Beatriz. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética "Ewald A. Favret". Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fuente
Frontiers in Microbiology 11 : 570960 (Octubre 2020)
Materia
Taxonomy
Enterobacter
Taxonomía
Anastrepha fraterculus
Sterile Insect Technique
Bacterial Diversity
Bacterial Richness
Técnica del Insecto Estéril
Diversidad Bacteriana
Riqueza Bacteriana
Nivel de accesibilidad
acceso abierto
Condiciones de uso
http://creativecommons.org/licenses/by-nc-sa/4.0/
Repositorio
INTA Digital (INTA)
Institución
Instituto Nacional de Tecnología Agropecuaria
OAI Identificador
oai:localhost:20.500.12123/8706

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spelling Gut bacteriome analysis of Anastrepha fraterculus sp. 1 during the early steps of laboratory colonizationSalgueiro, JulietaPimper, Lidia ElenaSegura, Diego FernandoMilla, Fabian HoracioRusso, Romina MariaAsimakis, Elias D.Stathopoulou, PanagiotaBourtzis, KostasCladera, Jorge LuisTsiamis, GeorgeLanzavecchia, Silvia BeatrizTaxonomyEnterobacterTaxonomíaAnastrepha fraterculusSterile Insect TechniqueBacterial DiversityBacterial RichnessTécnica del Insecto EstérilDiversidad BacterianaRiqueza BacterianaMicrobial communities associated to insect species are involved in essential biological functions such as host nutrition, reproduction and survivability. Main factors have been described as modulators of gut bacterial community, such as diet, habit, developmental stage and taxonomy of the host. The present work focuses on the complex changes that gut microbial communities go through when wild insects are introduced to artificial rearing conditions. Specifically, we analyzed the effect of the laboratory colonization on the richness and diversity of the gut bacteriome hosted by the fruit fly pest Anastrepha fraterculus sp. 1. Bacterial profiles were studied by amplicon sequencing of the 16S rRNA V3–V4 hypervariable region in gut samples of males and females, in teneral (1-day-old, unfed) and post-teneral (15-day-old, fed) flies. A total of 3,147,665 sequence reads were obtained and 32 bacterial operational taxonomic units (OTUs) were identified. Proteobacteria was the most abundant phylum (93.3% of the total reads) and, Wolbachia and Enterobacter were the most represented taxa at the genus level (29.9% and 27.7%, respectively, of the total read counts). Wild and laboratory flies showed highly significant differences in the relative abundances of bacteria. The analysis of the core bacteriome showed the presence of five OTUs in all samples grouped by origin, while nine and five OTUs were exclusively detected in laboratory and wild flies, respectively. Irrespective of fly origin or sex, a dominant presence of Wolbachia was observed in teneral flies, whereas Enterobacter was highly abundant in post-teneral individuals. We evidenced significant differences in bacterial richness and diversity among generations under laboratory colonization (F0, F1, F3 and F6) and compared to laboratory and wild flies, displaying also differential patterns between teneral and post-teneral flies. Laboratory and wild A. fraterculus sp. 1 harbor different gut bacterial communities. Laboratory colonization has an important effect on the microbiota, most likely associated to the combined effects of insect physiology and environmental conditions (e.g., diet and colony management).Instituto de GenéticaFil: Salgueiro, Julieta. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética. Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Pimper, Lidia Elena. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética. Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Segura, Diego Fernando. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética. Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Milla, Fabian Horacio. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética. Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Russo, Romina María. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética. Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Asimakis, Elias D. University of Patras. Department of Environmental Engineering; GreciaFil: Stathopoulou, Panagiota. University of Patras. Department of Environmental Engineering; GreciaFil: Bourtzis, Kostas. Vienna International Centre. Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture. Insect Pest Control Laboratory; AustriaFil: Cladera, Jorge Luis. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética. Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Tsiamis, George. University of Patras. Department of Environmental Engineering; GreciaFil: Lanzavecchia, Silvia Beatriz. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética "Ewald A. Favret". Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFrontiers Media2021-02-22T11:35:37Z2021-02-22T11:35:37Z2020-10info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfhttp://hdl.handle.net/20.500.12123/8706https://www.frontiersin.org/articles/10.3389/fmicb.2020.570960/full1664-302Xhttps://doi.org/10.3389/fmicb.2020.570960Frontiers in Microbiology 11 : 570960 (Octubre 2020)reponame:INTA Digital (INTA)instname:Instituto Nacional de Tecnología Agropecuariaenginfo:eu-repograntAgreement/INTA/AEBIO-242411/AR./Epidemiología molecular agropecuaria de patógenos y plagas de importancia económicainfo:eu-repo/semantics/openAccesshttp://creativecommons.org/licenses/by-nc-sa/4.0/Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)2025-09-04T09:48:46Zoai:localhost:20.500.12123/8706instacron:INTAInstitucionalhttp://repositorio.inta.gob.ar/Organismo científico-tecnológicoNo correspondehttp://repositorio.inta.gob.ar/oai/requesttripaldi.nicolas@inta.gob.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:l2025-09-04 09:48:46.826INTA Digital (INTA) - Instituto Nacional de Tecnología Agropecuariafalse
dc.title.none.fl_str_mv Gut bacteriome analysis of Anastrepha fraterculus sp. 1 during the early steps of laboratory colonization
title Gut bacteriome analysis of Anastrepha fraterculus sp. 1 during the early steps of laboratory colonization
spellingShingle Gut bacteriome analysis of Anastrepha fraterculus sp. 1 during the early steps of laboratory colonization
Salgueiro, Julieta
Taxonomy
Enterobacter
Taxonomía
Anastrepha fraterculus
Sterile Insect Technique
Bacterial Diversity
Bacterial Richness
Técnica del Insecto Estéril
Diversidad Bacteriana
Riqueza Bacteriana
title_short Gut bacteriome analysis of Anastrepha fraterculus sp. 1 during the early steps of laboratory colonization
title_full Gut bacteriome analysis of Anastrepha fraterculus sp. 1 during the early steps of laboratory colonization
title_fullStr Gut bacteriome analysis of Anastrepha fraterculus sp. 1 during the early steps of laboratory colonization
title_full_unstemmed Gut bacteriome analysis of Anastrepha fraterculus sp. 1 during the early steps of laboratory colonization
title_sort Gut bacteriome analysis of Anastrepha fraterculus sp. 1 during the early steps of laboratory colonization
dc.creator.none.fl_str_mv Salgueiro, Julieta
Pimper, Lidia Elena
Segura, Diego Fernando
Milla, Fabian Horacio
Russo, Romina Maria
Asimakis, Elias D.
Stathopoulou, Panagiota
Bourtzis, Kostas
Cladera, Jorge Luis
Tsiamis, George
Lanzavecchia, Silvia Beatriz
author Salgueiro, Julieta
author_facet Salgueiro, Julieta
Pimper, Lidia Elena
Segura, Diego Fernando
Milla, Fabian Horacio
Russo, Romina Maria
Asimakis, Elias D.
Stathopoulou, Panagiota
Bourtzis, Kostas
Cladera, Jorge Luis
Tsiamis, George
Lanzavecchia, Silvia Beatriz
author_role author
author2 Pimper, Lidia Elena
Segura, Diego Fernando
Milla, Fabian Horacio
Russo, Romina Maria
Asimakis, Elias D.
Stathopoulou, Panagiota
Bourtzis, Kostas
Cladera, Jorge Luis
Tsiamis, George
Lanzavecchia, Silvia Beatriz
author2_role author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Taxonomy
Enterobacter
Taxonomía
Anastrepha fraterculus
Sterile Insect Technique
Bacterial Diversity
Bacterial Richness
Técnica del Insecto Estéril
Diversidad Bacteriana
Riqueza Bacteriana
topic Taxonomy
Enterobacter
Taxonomía
Anastrepha fraterculus
Sterile Insect Technique
Bacterial Diversity
Bacterial Richness
Técnica del Insecto Estéril
Diversidad Bacteriana
Riqueza Bacteriana
dc.description.none.fl_txt_mv Microbial communities associated to insect species are involved in essential biological functions such as host nutrition, reproduction and survivability. Main factors have been described as modulators of gut bacterial community, such as diet, habit, developmental stage and taxonomy of the host. The present work focuses on the complex changes that gut microbial communities go through when wild insects are introduced to artificial rearing conditions. Specifically, we analyzed the effect of the laboratory colonization on the richness and diversity of the gut bacteriome hosted by the fruit fly pest Anastrepha fraterculus sp. 1. Bacterial profiles were studied by amplicon sequencing of the 16S rRNA V3–V4 hypervariable region in gut samples of males and females, in teneral (1-day-old, unfed) and post-teneral (15-day-old, fed) flies. A total of 3,147,665 sequence reads were obtained and 32 bacterial operational taxonomic units (OTUs) were identified. Proteobacteria was the most abundant phylum (93.3% of the total reads) and, Wolbachia and Enterobacter were the most represented taxa at the genus level (29.9% and 27.7%, respectively, of the total read counts). Wild and laboratory flies showed highly significant differences in the relative abundances of bacteria. The analysis of the core bacteriome showed the presence of five OTUs in all samples grouped by origin, while nine and five OTUs were exclusively detected in laboratory and wild flies, respectively. Irrespective of fly origin or sex, a dominant presence of Wolbachia was observed in teneral flies, whereas Enterobacter was highly abundant in post-teneral individuals. We evidenced significant differences in bacterial richness and diversity among generations under laboratory colonization (F0, F1, F3 and F6) and compared to laboratory and wild flies, displaying also differential patterns between teneral and post-teneral flies. Laboratory and wild A. fraterculus sp. 1 harbor different gut bacterial communities. Laboratory colonization has an important effect on the microbiota, most likely associated to the combined effects of insect physiology and environmental conditions (e.g., diet and colony management).
Instituto de Genética
Fil: Salgueiro, Julieta. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética. Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Pimper, Lidia Elena. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética. Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Segura, Diego Fernando. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética. Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Milla, Fabian Horacio. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética. Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Russo, Romina María. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética. Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Asimakis, Elias D. University of Patras. Department of Environmental Engineering; Grecia
Fil: Stathopoulou, Panagiota. University of Patras. Department of Environmental Engineering; Grecia
Fil: Bourtzis, Kostas. Vienna International Centre. Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture. Insect Pest Control Laboratory; Austria
Fil: Cladera, Jorge Luis. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética. Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Tsiamis, George. University of Patras. Department of Environmental Engineering; Grecia
Fil: Lanzavecchia, Silvia Beatriz. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética "Ewald A. Favret". Laboratorio de Genética de Insectos de Importancia Económica; Argentina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
description Microbial communities associated to insect species are involved in essential biological functions such as host nutrition, reproduction and survivability. Main factors have been described as modulators of gut bacterial community, such as diet, habit, developmental stage and taxonomy of the host. The present work focuses on the complex changes that gut microbial communities go through when wild insects are introduced to artificial rearing conditions. Specifically, we analyzed the effect of the laboratory colonization on the richness and diversity of the gut bacteriome hosted by the fruit fly pest Anastrepha fraterculus sp. 1. Bacterial profiles were studied by amplicon sequencing of the 16S rRNA V3–V4 hypervariable region in gut samples of males and females, in teneral (1-day-old, unfed) and post-teneral (15-day-old, fed) flies. A total of 3,147,665 sequence reads were obtained and 32 bacterial operational taxonomic units (OTUs) were identified. Proteobacteria was the most abundant phylum (93.3% of the total reads) and, Wolbachia and Enterobacter were the most represented taxa at the genus level (29.9% and 27.7%, respectively, of the total read counts). Wild and laboratory flies showed highly significant differences in the relative abundances of bacteria. The analysis of the core bacteriome showed the presence of five OTUs in all samples grouped by origin, while nine and five OTUs were exclusively detected in laboratory and wild flies, respectively. Irrespective of fly origin or sex, a dominant presence of Wolbachia was observed in teneral flies, whereas Enterobacter was highly abundant in post-teneral individuals. We evidenced significant differences in bacterial richness and diversity among generations under laboratory colonization (F0, F1, F3 and F6) and compared to laboratory and wild flies, displaying also differential patterns between teneral and post-teneral flies. Laboratory and wild A. fraterculus sp. 1 harbor different gut bacterial communities. Laboratory colonization has an important effect on the microbiota, most likely associated to the combined effects of insect physiology and environmental conditions (e.g., diet and colony management).
publishDate 2020
dc.date.none.fl_str_mv 2020-10
2021-02-22T11:35:37Z
2021-02-22T11:35:37Z
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
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info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/20.500.12123/8706
https://www.frontiersin.org/articles/10.3389/fmicb.2020.570960/full
1664-302X
https://doi.org/10.3389/fmicb.2020.570960
url http://hdl.handle.net/20.500.12123/8706
https://www.frontiersin.org/articles/10.3389/fmicb.2020.570960/full
https://doi.org/10.3389/fmicb.2020.570960
identifier_str_mv 1664-302X
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repograntAgreement/INTA/AEBIO-242411/AR./Epidemiología molecular agropecuaria de patógenos y plagas de importancia económica
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
http://creativecommons.org/licenses/by-nc-sa/4.0/
Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)
eu_rights_str_mv openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by-nc-sa/4.0/
Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv Frontiers in Microbiology 11 : 570960 (Octubre 2020)
reponame:INTA Digital (INTA)
instname:Instituto Nacional de Tecnología Agropecuaria
reponame_str INTA Digital (INTA)
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