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

Abstract 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...

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Main Authors: Abdulsalam Adegoke, Erik Neff, Amie Geary, Montana Ciara Husser, Kevin Wilson, Shawn Michael Norris, Guha Dharmarajan, Shahid Karim
Format: Article
Language:English
Published: BMC 2020-07-01
Series:Parasites & Vectors
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13071-020-04218-8
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spelling doaj-ed003936f8eb4a91a9dd833586c6b9252020-11-25T03:33:35ZengBMCParasites & Vectors1756-33052020-07-0113111310.1186/s13071-020-04218-8Laboratory colonization by Dirofilaria immitis alters the microbiome of female Aedes aegypti mosquitoesAbdulsalam Adegoke0Erik Neff1Amie Geary2Montana Ciara Husser3Kevin Wilson4Shawn Michael Norris5Guha Dharmarajan6Shahid Karim7Center for Molecular and Cellular Biosciences, School of Biological, Environmental, and Earth Sciences, The University of Southern MississippiSavannah River Ecology Laboratory, University of GeorgiaCenter for Molecular and Cellular Biosciences, School of Biological, Environmental, and Earth Sciences, The University of Southern MississippiCenter for Molecular and Cellular Biosciences, School of Biological, Environmental, and Earth Sciences, The University of Southern MississippiCenter for Molecular and Cellular Biosciences, School of Biological, Environmental, and Earth Sciences, The University of Southern MississippiCenter for Molecular and Cellular Biosciences, School of Biological, Environmental, and Earth Sciences, The University of Southern MississippiSavannah River Ecology Laboratory, University of GeorgiaCenter for Molecular and Cellular Biosciences, School of Biological, Environmental, and Earth Sciences, The University of Southern MississippiAbstract 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.http://link.springer.com/article/10.1186/s13071-020-04218-8MosquitoesAedes aegyptiMicrobiomeMetagenomeDirofilaria immitisDog heartworm
collection DOAJ
language English
format Article
sources DOAJ
author Abdulsalam Adegoke
Erik Neff
Amie Geary
Montana Ciara Husser
Kevin Wilson
Shawn Michael Norris
Guha Dharmarajan
Shahid Karim
spellingShingle Abdulsalam Adegoke
Erik Neff
Amie Geary
Montana Ciara Husser
Kevin Wilson
Shawn Michael Norris
Guha Dharmarajan
Shahid Karim
Laboratory colonization by Dirofilaria immitis alters the microbiome of female Aedes aegypti mosquitoes
Parasites & Vectors
Mosquitoes
Aedes aegypti
Microbiome
Metagenome
Dirofilaria immitis
Dog heartworm
author_facet Abdulsalam Adegoke
Erik Neff
Amie Geary
Montana Ciara Husser
Kevin Wilson
Shawn Michael Norris
Guha Dharmarajan
Shahid Karim
author_sort Abdulsalam Adegoke
title 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_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_sort laboratory colonization by dirofilaria immitis alters the microbiome of female aedes aegypti mosquitoes
publisher BMC
series Parasites & Vectors
issn 1756-3305
publishDate 2020-07-01
description Abstract 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.
topic Mosquitoes
Aedes aegypti
Microbiome
Metagenome
Dirofilaria immitis
Dog heartworm
url http://link.springer.com/article/10.1186/s13071-020-04218-8
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