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Comprehensive characterization of internal and cuticle surface microbiota of laboratory-reared F(1)Anopheles albimanus originating from different sites

BACKGROUND: Research on mosquito-microbe interactions may lead to new tools for mosquito and mosquito-borne disease control. To date, such research has largely utilized laboratory-reared mosquitoes that typically lack the microbial diversity of wild populations. A logical progression in this area in...

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Autores principales: Dada, Nsa, Benedict, Ana Cristina, López, Francisco, Lol, Juan C., Sheth, Mili, Dzuris, Nicole, Padilla, Norma, Lenhart, Audrey
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8542342/
https://www.ncbi.nlm.nih.gov/pubmed/34688298
http://dx.doi.org/10.1186/s12936-021-03934-5
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author Dada, Nsa
Benedict, Ana Cristina
López, Francisco
Lol, Juan C.
Sheth, Mili
Dzuris, Nicole
Padilla, Norma
Lenhart, Audrey
author_facet Dada, Nsa
Benedict, Ana Cristina
López, Francisco
Lol, Juan C.
Sheth, Mili
Dzuris, Nicole
Padilla, Norma
Lenhart, Audrey
author_sort Dada, Nsa
collection PubMed
description BACKGROUND: Research on mosquito-microbe interactions may lead to new tools for mosquito and mosquito-borne disease control. To date, such research has largely utilized laboratory-reared mosquitoes that typically lack the microbial diversity of wild populations. A logical progression in this area involves working under controlled settings using field-collected mosquitoes or, in most cases, their progeny. Thus, an understanding of how laboratory colonization affects the assemblage of mosquito microbiota would aid in advancing mosquito microbiome studies and their applications beyond laboratory settings. METHODS: Using high throughput 16S rRNA amplicon sequencing, the internal and cuticle surface microbiota of F(1) progeny of wild-caught adult Anopheles albimanus from four locations in Guatemala were characterized. A total of 132 late instar larvae and 135 2–5 day-old, non-blood-fed virgin adult females that were reared under identical laboratory conditions, were pooled (3 individuals/pool) and analysed. RESULTS: Results showed location-associated heterogeneity in both F(1) larval internal (p = 0.001; pseudo-F = 9.53) and cuticle surface (p = 0.001; pseudo-F = 8.51) microbiota, and only F(1) adult cuticle surface (p = 0.001; pseudo-F = 4.5) microbiota, with a more homogenous adult internal microbiota (p = 0.12; pseudo-F = 1.6) across collection sites. Overall, ASVs assigned to Leucobacter, Thorsellia, Chryseobacterium and uncharacterized Enterobacteriaceae, dominated F(1) larval internal microbiota, while Acidovorax, Paucibacter, and uncharacterized Comamonadaceae, dominated the larval cuticle surface. F(1) adults comprised a less diverse microbiota compared to larvae, with ASVs assigned to the genus Asaia dominating both internal and cuticle surface microbiota, and constituting at least 70% of taxa in each microbial niche. CONCLUSIONS: These results suggest that location-specific heterogeneity in filed mosquito microbiota can be transferred to F(1) progeny under normal laboratory conditions, but this may not last beyond the F(1) larval stage without adjustments to maintain field-derived microbiota. These findings provide the first comprehensive characterization of laboratory-colonized F(1) An. albimanus progeny from field-derived mothers. This provides a background for studying how parentage and environmental conditions differentially or concomitantly affect mosquito microbiome composition, and how this can be exploited in advancing mosquito microbiome studies and their applications beyond laboratory settings. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12936-021-03934-5.
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spelling pubmed-85423422021-10-25 Comprehensive characterization of internal and cuticle surface microbiota of laboratory-reared F(1)Anopheles albimanus originating from different sites Dada, Nsa Benedict, Ana Cristina López, Francisco Lol, Juan C. Sheth, Mili Dzuris, Nicole Padilla, Norma Lenhart, Audrey Malar J Research BACKGROUND: Research on mosquito-microbe interactions may lead to new tools for mosquito and mosquito-borne disease control. To date, such research has largely utilized laboratory-reared mosquitoes that typically lack the microbial diversity of wild populations. A logical progression in this area involves working under controlled settings using field-collected mosquitoes or, in most cases, their progeny. Thus, an understanding of how laboratory colonization affects the assemblage of mosquito microbiota would aid in advancing mosquito microbiome studies and their applications beyond laboratory settings. METHODS: Using high throughput 16S rRNA amplicon sequencing, the internal and cuticle surface microbiota of F(1) progeny of wild-caught adult Anopheles albimanus from four locations in Guatemala were characterized. A total of 132 late instar larvae and 135 2–5 day-old, non-blood-fed virgin adult females that were reared under identical laboratory conditions, were pooled (3 individuals/pool) and analysed. RESULTS: Results showed location-associated heterogeneity in both F(1) larval internal (p = 0.001; pseudo-F = 9.53) and cuticle surface (p = 0.001; pseudo-F = 8.51) microbiota, and only F(1) adult cuticle surface (p = 0.001; pseudo-F = 4.5) microbiota, with a more homogenous adult internal microbiota (p = 0.12; pseudo-F = 1.6) across collection sites. Overall, ASVs assigned to Leucobacter, Thorsellia, Chryseobacterium and uncharacterized Enterobacteriaceae, dominated F(1) larval internal microbiota, while Acidovorax, Paucibacter, and uncharacterized Comamonadaceae, dominated the larval cuticle surface. F(1) adults comprised a less diverse microbiota compared to larvae, with ASVs assigned to the genus Asaia dominating both internal and cuticle surface microbiota, and constituting at least 70% of taxa in each microbial niche. CONCLUSIONS: These results suggest that location-specific heterogeneity in filed mosquito microbiota can be transferred to F(1) progeny under normal laboratory conditions, but this may not last beyond the F(1) larval stage without adjustments to maintain field-derived microbiota. These findings provide the first comprehensive characterization of laboratory-colonized F(1) An. albimanus progeny from field-derived mothers. This provides a background for studying how parentage and environmental conditions differentially or concomitantly affect mosquito microbiome composition, and how this can be exploited in advancing mosquito microbiome studies and their applications beyond laboratory settings. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12936-021-03934-5. BioMed Central 2021-10-23 /pmc/articles/PMC8542342/ /pubmed/34688298 http://dx.doi.org/10.1186/s12936-021-03934-5 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Dada, Nsa
Benedict, Ana Cristina
López, Francisco
Lol, Juan C.
Sheth, Mili
Dzuris, Nicole
Padilla, Norma
Lenhart, Audrey
Comprehensive characterization of internal and cuticle surface microbiota of laboratory-reared F(1)Anopheles albimanus originating from different sites
title Comprehensive characterization of internal and cuticle surface microbiota of laboratory-reared F(1)Anopheles albimanus originating from different sites
title_full Comprehensive characterization of internal and cuticle surface microbiota of laboratory-reared F(1)Anopheles albimanus originating from different sites
title_fullStr Comprehensive characterization of internal and cuticle surface microbiota of laboratory-reared F(1)Anopheles albimanus originating from different sites
title_full_unstemmed Comprehensive characterization of internal and cuticle surface microbiota of laboratory-reared F(1)Anopheles albimanus originating from different sites
title_short Comprehensive characterization of internal and cuticle surface microbiota of laboratory-reared F(1)Anopheles albimanus originating from different sites
title_sort comprehensive characterization of internal and cuticle surface microbiota of laboratory-reared f(1)anopheles albimanus originating from different sites
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8542342/
https://www.ncbi.nlm.nih.gov/pubmed/34688298
http://dx.doi.org/10.1186/s12936-021-03934-5
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