The dynamics of the midgut microbiome in Aedes aegypti during digestion reveal putative symbionts
Blood-feeding is crucial for the reproductive cycle of the mosquito Aedes aegypti, as well as for the transmission of arboviruses to hosts. It is postulated that blood meals may influence the mosquito microbiome but shifts in microbial diversity and function during digestion remain elusive. We used...
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sg-ntu-dr.10356-1815612024-12-12T15:30:26Z The dynamics of the midgut microbiome in Aedes aegypti during digestion reveal putative symbionts Salgado, João Felipe M. Premkrishnan, Balakrishnan N. V. Oliveira, Elaine Lopes Vettath, Vineeth Kodengil Goh, Feng Guang Hou, Xinjun Drautz-Moses, Daniela I. Cai, Yu Schuster, Stephan Christoph Junqueira, Ana Carolina M. Singapore Center for Environmental Life Sciences Engineering Medicine, Health and Life Sciences Digestion Elizabethkingia anophelis Blood-feeding is crucial for the reproductive cycle of the mosquito Aedes aegypti, as well as for the transmission of arboviruses to hosts. It is postulated that blood meals may influence the mosquito microbiome but shifts in microbial diversity and function during digestion remain elusive. We used whole-genome shotgun metagenomics to monitor the midgut microbiome in 60 individual females of A. aegypti throughout digestion, after 12, 24, and 48 h following blood or sugar meals. Additionally, ten individual larvae were sequenced, showing microbiomes dominated by Microbacterium sp. The high metagenomic coverage allowed for microbial assignments at the species taxonomic level, also providing functional profiling. Females in the post-digestive period and larvae displayed low microbiome diversities. A striking proliferation of Enterobacterales was observed during digestion in blood-fed mosquitoes. The compositional shift was concomitant with enrichment in genes associated with carbohydrate and protein metabolism, as well as virulence factors for antimicrobial resistance and scavenging. The bacterium Elizabethkingia anophelis (Flavobacteriales), a known human pathogen, was the dominant species at the end of blood digestion. Phylogenomics suggests that its association with hematophagous mosquitoes occurred several times. We consider evidence of mutually beneficial host-microbe interactions raised from this association, potentially pivotal for the mosquito's resistance to arbovirus infection. After digestion, the observed shifts in blood-fed females' midguts shifted to a sugar-fed-like microbial profile. This study provides insights into how the microbiome of A. aegypti is modulated to fulfil digestive roles following blood meals, emphasizing proliferation of potential symbionts in response to the dynamic midgut environment. Published version This study was partially funded by Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro to A.C.M.J. (FAPERJ grant E26/211.473/2021). 2024-12-09T08:03:16Z 2024-12-09T08:03:16Z 2024 Journal Article Salgado, J. F. M., Premkrishnan, B. N. V., Oliveira, E. L., Vettath, V. K., Goh, F. G., Hou, X., Drautz-Moses, D. I., Cai, Y., Schuster, S. C. & Junqueira, A. C. M. (2024). The dynamics of the midgut microbiome in Aedes aegypti during digestion reveal putative symbionts. PNAS Nexus, 3(8), pgae317-. https://dx.doi.org/10.1093/pnasnexus/pgae317 2752-6542 https://hdl.handle.net/10356/181561 10.1093/pnasnexus/pgae317 39157462 2-s2.0-85201775785 8 3 pgae317 en PNAS nexus © The Author(s) 2024. Published by Oxford University Press on behalf of National Academy of Sciences. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (https://creativecommons.org/ licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com. application/pdf |
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Medicine, Health and Life Sciences Digestion Elizabethkingia anophelis |
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Medicine, Health and Life Sciences Digestion Elizabethkingia anophelis Salgado, João Felipe M. Premkrishnan, Balakrishnan N. V. Oliveira, Elaine Lopes Vettath, Vineeth Kodengil Goh, Feng Guang Hou, Xinjun Drautz-Moses, Daniela I. Cai, Yu Schuster, Stephan Christoph Junqueira, Ana Carolina M. The dynamics of the midgut microbiome in Aedes aegypti during digestion reveal putative symbionts |
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Blood-feeding is crucial for the reproductive cycle of the mosquito Aedes aegypti, as well as for the transmission of arboviruses to hosts. It is postulated that blood meals may influence the mosquito microbiome but shifts in microbial diversity and function during digestion remain elusive. We used whole-genome shotgun metagenomics to monitor the midgut microbiome in 60 individual females of A. aegypti throughout digestion, after 12, 24, and 48 h following blood or sugar meals. Additionally, ten individual larvae were sequenced, showing microbiomes dominated by Microbacterium sp. The high metagenomic coverage allowed for microbial assignments at the species taxonomic level, also providing functional profiling. Females in the post-digestive period and larvae displayed low microbiome diversities. A striking proliferation of Enterobacterales was observed during digestion in blood-fed mosquitoes. The compositional shift was concomitant with enrichment in genes associated with carbohydrate and protein metabolism, as well as virulence factors for antimicrobial resistance and scavenging. The bacterium Elizabethkingia anophelis (Flavobacteriales), a known human pathogen, was the dominant species at the end of blood digestion. Phylogenomics suggests that its association with hematophagous mosquitoes occurred several times. We consider evidence of mutually beneficial host-microbe interactions raised from this association, potentially pivotal for the mosquito's resistance to arbovirus infection. After digestion, the observed shifts in blood-fed females' midguts shifted to a sugar-fed-like microbial profile. This study provides insights into how the microbiome of A. aegypti is modulated to fulfil digestive roles following blood meals, emphasizing proliferation of potential symbionts in response to the dynamic midgut environment. |
author2 |
Singapore Center for Environmental Life Sciences Engineering |
author_facet |
Singapore Center for Environmental Life Sciences Engineering Salgado, João Felipe M. Premkrishnan, Balakrishnan N. V. Oliveira, Elaine Lopes Vettath, Vineeth Kodengil Goh, Feng Guang Hou, Xinjun Drautz-Moses, Daniela I. Cai, Yu Schuster, Stephan Christoph Junqueira, Ana Carolina M. |
format |
Article |
author |
Salgado, João Felipe M. Premkrishnan, Balakrishnan N. V. Oliveira, Elaine Lopes Vettath, Vineeth Kodengil Goh, Feng Guang Hou, Xinjun Drautz-Moses, Daniela I. Cai, Yu Schuster, Stephan Christoph Junqueira, Ana Carolina M. |
author_sort |
Salgado, João Felipe M. |
title |
The dynamics of the midgut microbiome in Aedes aegypti during digestion reveal putative symbionts |
title_short |
The dynamics of the midgut microbiome in Aedes aegypti during digestion reveal putative symbionts |
title_full |
The dynamics of the midgut microbiome in Aedes aegypti during digestion reveal putative symbionts |
title_fullStr |
The dynamics of the midgut microbiome in Aedes aegypti during digestion reveal putative symbionts |
title_full_unstemmed |
The dynamics of the midgut microbiome in Aedes aegypti during digestion reveal putative symbionts |
title_sort |
dynamics of the midgut microbiome in aedes aegypti during digestion reveal putative symbionts |
publishDate |
2024 |
url |
https://hdl.handle.net/10356/181561 |
_version_ |
1819113008821960704 |