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Laboratory colonization by Dirofilaria immitis alters the microbiome of female Aedes aegypti mosquitoes

BACKGROUND: The ability of blood-feeding arthropods to successfully acquire and transmit pathogens of medical and veterinary importance has been shown to be interfered with, or enhanced by, the arthropod’s native microbiome. Mosquitoes transmit viruses, protozoan and filarial nematodes, the majority...

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Autores principales: Adegoke, Abdulsalam, Neff, Erik, Geary, Amie, Husser, Montana Ciara, Wilson, Kevin, Norris, Shawn Michael, Dharmarajan, Guha, Karim, Shahid
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7359625/
https://www.ncbi.nlm.nih.gov/pubmed/32660640
http://dx.doi.org/10.1186/s13071-020-04218-8
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author Adegoke, Abdulsalam
Neff, Erik
Geary, Amie
Husser, Montana Ciara
Wilson, Kevin
Norris, Shawn Michael
Dharmarajan, Guha
Karim, Shahid
author_facet Adegoke, Abdulsalam
Neff, Erik
Geary, Amie
Husser, Montana Ciara
Wilson, Kevin
Norris, Shawn Michael
Dharmarajan, Guha
Karim, Shahid
author_sort Adegoke, Abdulsalam
collection PubMed
description BACKGROUND: The ability of blood-feeding arthropods to successfully acquire and transmit pathogens of medical and veterinary importance has been shown to be interfered with, or enhanced by, the arthropod’s native microbiome. Mosquitoes transmit viruses, protozoan and filarial nematodes, the majority of which contribute to the 17% of infectious disease cases worldwide. Dirofilaria immitis, a mosquito-transmitted filarial nematodes of dogs and cats, is vectored by several mosquito species including Aedes aegypti. METHODS: In this study, we investigated the impact of D. immitis colonization on the microbiome of laboratory reared female Ae. aegypti. Metagenomic analysis of the V3–V4 variable region of the microbial 16S RNA gene was used for identification of the microbial differences down to species level. RESULTS: We generated a total of 1068 OTUs representing 16 phyla, 181 genera and 271 bacterial species. Overall, in order of abundance, Proteobacteria, Bacteroidetes, Actinobacteria and Firmicutes were the most represented phylum with D. immitis-infected mosquitoes having more of Proteobacteria (71%) than uninfected mosquitoes (56.9%). An interesting finding in this study is the detection of Klebsiella oxytoca in relatively similar abundance in infected and uninfected mosquitoes, suggesting a possible endosymbiotic relationship, and has been previously shown to indirectly compete for nutrients with fungi on domestic housefly eggs and larvae. While D. immitis colonization has no effect on the overall species richness, we identified significant differences in the composition of selected bacterial genera and phyla between the two groups. We also reported distinct compositional and phylogenetic differences in the individual bacterial species when commonly identified bacteria were compared. CONCLUSIONS: To the best of our knowledge, this is the first study to understand the impact of a filarial infection on the microbiome of its mosquito vector. Further studies are required to identify bacteria species that could play an important role in the mosquito biology. While the microbiome composition of Ae. aegypti mosquito have been previously reported, our study shows that in an effort to establish itself, a filarial nematode modifies and alters the overall microbial diversity within its mosquito host. [Image: see text]
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spelling pubmed-73596252020-07-17 Laboratory colonization by Dirofilaria immitis alters the microbiome of female Aedes aegypti mosquitoes Adegoke, Abdulsalam Neff, Erik Geary, Amie Husser, Montana Ciara Wilson, Kevin Norris, Shawn Michael Dharmarajan, Guha Karim, Shahid Parasit Vectors Research BACKGROUND: The ability of blood-feeding arthropods to successfully acquire and transmit pathogens of medical and veterinary importance has been shown to be interfered with, or enhanced by, the arthropod’s native microbiome. Mosquitoes transmit viruses, protozoan and filarial nematodes, the majority of which contribute to the 17% of infectious disease cases worldwide. Dirofilaria immitis, a mosquito-transmitted filarial nematodes of dogs and cats, is vectored by several mosquito species including Aedes aegypti. METHODS: In this study, we investigated the impact of D. immitis colonization on the microbiome of laboratory reared female Ae. aegypti. Metagenomic analysis of the V3–V4 variable region of the microbial 16S RNA gene was used for identification of the microbial differences down to species level. RESULTS: We generated a total of 1068 OTUs representing 16 phyla, 181 genera and 271 bacterial species. Overall, in order of abundance, Proteobacteria, Bacteroidetes, Actinobacteria and Firmicutes were the most represented phylum with D. immitis-infected mosquitoes having more of Proteobacteria (71%) than uninfected mosquitoes (56.9%). An interesting finding in this study is the detection of Klebsiella oxytoca in relatively similar abundance in infected and uninfected mosquitoes, suggesting a possible endosymbiotic relationship, and has been previously shown to indirectly compete for nutrients with fungi on domestic housefly eggs and larvae. While D. immitis colonization has no effect on the overall species richness, we identified significant differences in the composition of selected bacterial genera and phyla between the two groups. We also reported distinct compositional and phylogenetic differences in the individual bacterial species when commonly identified bacteria were compared. CONCLUSIONS: To the best of our knowledge, this is the first study to understand the impact of a filarial infection on the microbiome of its mosquito vector. Further studies are required to identify bacteria species that could play an important role in the mosquito biology. While the microbiome composition of Ae. aegypti mosquito have been previously reported, our study shows that in an effort to establish itself, a filarial nematode modifies and alters the overall microbial diversity within its mosquito host. [Image: see text] BioMed Central 2020-07-13 /pmc/articles/PMC7359625/ /pubmed/32660640 http://dx.doi.org/10.1186/s13071-020-04218-8 Text en © The Author(s) 2020 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/. The Creative Commons Public Domain Dedication waiver (http://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
Adegoke, Abdulsalam
Neff, Erik
Geary, Amie
Husser, Montana Ciara
Wilson, Kevin
Norris, Shawn Michael
Dharmarajan, Guha
Karim, Shahid
Laboratory colonization by Dirofilaria immitis alters the microbiome of female Aedes aegypti mosquitoes
title Laboratory colonization by Dirofilaria immitis alters the microbiome of female Aedes aegypti mosquitoes
title_full Laboratory colonization by Dirofilaria immitis alters the microbiome of female Aedes aegypti mosquitoes
title_fullStr Laboratory colonization by Dirofilaria immitis alters the microbiome of female Aedes aegypti mosquitoes
title_full_unstemmed Laboratory colonization by Dirofilaria immitis alters the microbiome of female Aedes aegypti mosquitoes
title_short Laboratory colonization by Dirofilaria immitis alters the microbiome of female Aedes aegypti mosquitoes
title_sort laboratory colonization by dirofilaria immitis alters the microbiome of female aedes aegypti mosquitoes
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7359625/
https://www.ncbi.nlm.nih.gov/pubmed/32660640
http://dx.doi.org/10.1186/s13071-020-04218-8
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