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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Main Authors: 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.
Other Authors: Singapore Center for Environmental Life Sciences Engineering
Format: Article
Language:English
Published: 2024
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Online Access:https://hdl.handle.net/10356/181561
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spelling 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
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic Medicine, Health and Life Sciences
Digestion
Elizabethkingia anophelis
spellingShingle 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
description 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
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