TY - JOUR
T1 - The dynamics of the midgut microbiome in Aedes aegypti during digestion reveal putative symbionts
AU - Salgado, João Felipe M.
AU - Premkrishnan, Balakrishnan N.V.
AU - Oliveira, Elaine L.
AU - Vettath, Vineeth Kodengil
AU - Goh, Feng Guang
AU - Hou, Xinjun
AU - Drautz-Moses, Daniela I.
AU - Cai, Yu
AU - Schuster, Stephan C.
AU - Junqueira, Ana Carolina M.
N1 - Publisher Copyright:
© The Author(s) 2024.
PY - 2024/8/1
Y1 - 2024/8/1
N2 - 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.
AB - 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.
KW - digestion
KW - Elizabethkingia anophelis
KW - Enterobacterales
KW - hematophagy
KW - whole-genome sequencing metagenomics
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UR - http://www.scopus.com/inward/citedby.url?scp=85201775785&partnerID=8YFLogxK
U2 - 10.1093/pnasnexus/pgae317
DO - 10.1093/pnasnexus/pgae317
M3 - Article
AN - SCOPUS:85201775785
SN - 2752-6542
VL - 3
JO - PNAS Nexus
JF - PNAS Nexus
IS - 8
M1 - pgae317
ER -