The dynamics of the midgut microbiome in Aedes aegypti during digestion reveal putative symbionts

Author:

Salgado João Felipe M12ORCID,Premkrishnan Balakrishnan N V3,Oliveira Elaine L3ORCID,Vettath Vineeth Kodengil3,Goh Feng Guang45ORCID,Hou Xinjun45ORCID,Drautz-Moses Daniela I3,Cai Yu45ORCID,Schuster Stephan C3ORCID,Junqueira Ana Carolina M2ORCID

Affiliation:

1. RG Insect Microbiology and Symbiosis, Max Planck Institute for Terrestrial Microbiology , Karl-von-Frisch str. 10, Marburg 35043 , Germany

2. Departamento de Genética, Instituto de Biologia, Universidade Federal do Rio de Janeiro , 373 Avenida Carlos Chagas Filho, Rio de Janeiro, RJ 21941-902 , Brazil

3. Singapore Center for Environmental Life Sciences Engineering (SCELSE), Nanyang Technological University , 60 Nanyang Drive, Singapore 637551 , Singapore

4. Temasek Life Sciences Laboratory, National University of Singapore , 1 Research Link, Singapore 117604 , Singapore

5. Department of Biological Sciences, National University of Singapore , 16 Science Drive 4, Block S3, #05-01, Singapore 117558 , Singapore

Abstract

Abstract 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.

Funder

FAPERJ

Publisher

Oxford University Press (OUP)

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