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Review
. 2019 Aug:37:26-36.
doi: 10.1016/j.coviro.2019.05.005. Epub 2019 Jun 5.

Curious entanglements: interactions between mosquitoes, their microbiota, and arboviruses

Eric P Caragata  1 , Chinmay V Tikhe  1 , George Dimopoulos  2
Affiliations
Review

Curious entanglements: interactions between mosquitoes, their microbiota, and arboviruses

Eric P Caragata et al. Curr Opin Virol. 2019 Aug.

Abstract

Mosquitoes naturally harbor a diverse community of microorganisms that play a crucial role in their biology. Mosquito-microbiota interactions are abundant and complex. They can dramatically alter the mosquito immune response, and impede or enhance a mosquito's ability to transmit medically important arboviral pathogens. Yet critically, given the massive public health impact of arboviral disease, few such interactions have been well characterized. In this review, we describe the current state of knowledge of the role of microorganisms in mosquito biology, how microbial-induced changes to mosquito immunity moderate infection with arboviruses, cases of mosquito-microbial-virus interactions with a defined mechanism, and the molecular interactions that underlie the endosymbiotic bacterium Wolbachia's ability to block virus infection in mosquitoes.

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Figures

Figure 1:
Figure 1:. Key types of interactions between mosquitoes, their microbiota, and arboviruses.
(A) The larval microbiota can influence adult vector competence. Rearing Ae. aegypti larvae gnotobiotically with an Enterobacteraceae isolate or a Salmonella sp. differentially affects susceptibility to DENV infection in adults. (B) The presence of the gut microbiota can influence viral infection. An. gambiae where the microbiota has been cleared by antibiotic treatment (+AB) are less effective hosts for ONNV than those with their natural microbiota (-AB). (C) The microbiota stimulates the mosquito immune system and moderates arboviral infection. The gut microbiota induces Toll and IMD pathway activity, the latter hinders SINV infection, and prevents excess microbial proliferation. The fungus B. bassiana activates the Toll and JAK-STAT pathways thereby restricting DENV infection. (D) Infection with an arbovirus, including ZIKV and WNV, can alter the composition of the microbiota. Abbreviations: -AB: without antibiotics, +AB: with antibiotics, DENV: Dengue virus, MEC: midgut epithelial cells, MG: midgut, ONNV: O’Nyong-nyong virus, SINV: Sindbis virus, WNV: West Nile virus, ZIKV: Zika virus.
Figure 2:
Figure 2:. Mosquito-microbiota-virus interactions have diverse mechanisms.
There are few instances where the mechanisms used by microbiota to alter viral infection in mosquitoes have been identified. (A) In Ae. aegypti, the fungus Talaromyces sp. decreases host production of trypsin and other digestive proteins, which enhances DENV infection. (B) In Ae. aegypti, the bacterium Chromobacterium sp. Panama (Csp_P) restricts DENV infection by producing an aminopeptidase that digests the DENV envelope protein. (C) In Ae. aegypti, the bacterium Serratia odorifera produces the P40 polypeptide, which associates with the protein Prohibitin and enhances infection with DENV and CHIKV. (D). In Ae. aegypti, the bacterium Serratia marcescens produces the protein smEnhancin, which digests the mucin layer in the mosquito midgut, making invasion of the midgut epithelial cells easier for DENV. Abbreviations: CHIKV: Chikungunya virus, Cyt: Cytoplasm, DENV: Dengue virus, MEC: midgut epithelial cells, MG: midgut, Mt: Mitochondria. P40: Polvnentide P40. PM: Plasma membrane. Pr: Prohibitin.
Figure 3:
Figure 3:. Interactions putatively linked to Wolbachia-mediated arbovirus blocking.
Wolbachia are intracellular bacteria that dwell within membrane-bound vacuoles that associate with the ER and Golgi. Multiple Wolbachia-mosquito interactions have been implicated in Wolbachia’s ability to block arboviral infection: (A) Wolbachia interact with the miRNA pathway gene AG01, altering the mosquito miRNA profile, which leads to the expression of antiviral genes. (B) Wolbachia stimulate different mosquito immune pathways, leading to the production of AMPs that target the virus. (C) Wolbachia cause the excess production of ROS, which stimulate the Toll pathway, and/or target the virus directly. (D) Viruses enter Wolbcahia-infected cells as normal via receptor mediated endocytosis, but Wolbachia restricts viral replication by promoting mosquito XRNl-mediated degradation of viral RNA. (E) Wolbachia preferentially uses mosquito resources, particularly lipids, that are required by the virus to infect the mosquito. Some or all of these processes, or other as-yet-unidentified processes may contribute to virus blocking. Abbreviations/Key: ‘?’: It is unclear how or whether this interaction occurs, AMPs: Antimicrobial peptides, ER: Endoplasmic reticulum, EV: Endocytotic vesicle, G: Golgi apparatus, Nu: Nucleus, PM: Plasma membrane, R: Receptor mediating viral entry into cell, ROS: Reactive oxygen species, W: Wolbachia.
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