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1. The midgut epithelium of mosquitoes adjusts cell proliferation and endoreplication to respond to physiological challenges

   https://doi.org/10.1186/s12915-023-01769-x  

   Taracena-Agarwal, M. L. ; Hixson, B. ; Nandakumar, S. ; Girard-Mejia, A. P. ; Chen, R. Y. ; Huot, L. ; Padilla, N. ; Buchon, N. ( January 2024 , BMC Biology)

   Hematophagous mosquitoes transmit many pathogens that cause human diseases. Pathogen acquisition and transmission occur when female mosquitoes blood feed to acquire nutrients for reproduction. The midgut epithelium of mosquitoes serves as the point of entry for transmissible viruses and parasites.

   We studied midgut epithelial dynamics in five major mosquito vector species by quantifying PH3-positive cells (indicative of mitotic proliferation), the incorporation of nucleotide analogs (indicative of DNA synthesis accompanying proliferation and/or endoreplication), and the ploidy (by flow cytometry) of cell populations in the posterior midgut epithelium of adult females. Our results show that the epithelial dynamics of post-emergence maturation and of mature sugar-fed guts were similar in members of theAedes,Culex, andAnophelesgenera. In the first three days post-emergence, ~ 20% of cells in the posterior midgut region of interest incorporated nucleotide analogs, concurrent with both proliferative activity and a broad shift toward higher ploidy. In mature mosquitoes maintained on sugar, an average of 3.5% of cells in the posterior midgut region of interest incorporated nucleotide analogs from five to eight days post-emergence, with a consistent presence of mitotic cells indicating constant cell turnover. Oral bacterial infection triggered a sharp increase in mitosis and nucleotide analog incorporation, suggesting that the mosquito midgut undergoes accelerated cellular turnover in response to damage. Finally, blood feeding resulted in an increase in cell proliferation, but the nature and intensity of the response varied by mosquito species and by blood source (human, bovine, avian or artificial). InAn. gambiae, enterocytes appeared to reenter the cell cycle to increase ploidy after consuming blood from all sources except avian.

   We saw that epithelial proliferation, differentiation, and endoreplication reshape the blood-fed gut to increase ploidy, possibly to facilitate increased metabolic activity. Our results highlight the plasticity of the midgut epithelium in mosquitoes’ physiological responses to distinct challenges.

    

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2. Redox state affects fecundity and insecticide susceptibility in Anopheles gambiae

   https://doi.org/10.1038/s41598-018-31360-2  

   Champion, Cody J. ; Xu, Jiannong ( August 2018 , Scientific Reports)

   Redox reactions play a central role in the metabolism of an organism. It is vital to maintain redox homeostasis in response to the fluctuation of redox shift in various biological contexts. NADPH-dependent reducing capacity is one of the key factors contributing to the redox homeostasis. To understand the redox capacity and its impact on mosquito fecundity and susceptibility to insecticides inAnopheles gambiae, we examined the dynamics of elevated oxidative state via induction by paraquat (PQ) and the inhibition of NADPH regeneration by 6-aminonicotinamide (6AN). In naïve conditions, inherent oxidative capacity varies between individuals, as measured by GSSG/GSH ratio. The high GSSG/GSH ratio was negatively correlated with fecundity. Both PQ and 6AN feeding increased GSSG/GSH ratio and elevated protein carbonylation, a marker of oxidative damage. Both pro-oxidants lowered egg production. Co-feeding the pro-oxidants with antioxidant lycopene attenuated the adverse effects on fecundity, implying that oxidative stress was the cause of this phenotype. Pre-feeding with 6AN increased insecticide susceptibility in DDT resistant mosquitoes. These results indicate that oxidative state is delicate in mosquitoes, manipulation of NADPH pool may adversely affect fecundity and insecticide detoxification capacity. This knowledge can be exploited to develop novel vector control strategies targeting fecundity and insecticide resistance.

    

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3. Assessing temperature‐dependent competition between two invasive mosquito species

   https://doi.org/10.1002/eap.2334  

   Evans, Michelle V. ; Drake, John M. ; Jones, Lindsey ; Murdock, Courtney C. ( April 2021 , Ecological Applications)

   Invasive mosquitoes are expanding their ranges into new geographic areas and interacting with resident mosquito species. Understanding how novel interactions can affect mosquito population dynamics is necessary to predict transmission risk at invasion fronts. Mosquito life‐history traits are extremely sensitive to temperature, and this can lead to temperature‐dependent competition between competing invasive mosquito species. We explored temperature‐dependent competition betweenAedes aegyptiandAnopheles stephensi, two invasive mosquito species whose distributions overlap in India, the Middle East, and North Africa, whereAn. stephensiis currently expanding into the endemic range ofAe. aegypti. We followed mosquito cohorts raised at different intraspecific and interspecific densities across five temperatures (16–32°C) to measure traits relevant for population growth and to estimate species’ per capita growth rates. We then used these growth rates to derive each species’ competitive ability at each temperature. We find strong evidence for asymmetric competition at all temperatures, withAe. aegyptiemerging as the dominant competitor. This was primarily because of differences in larval survival and development times across all temperatures that resulted in a higher estimated intrinsic growth rate and competitive tolerance estimate forAe. aegypticompared toAn. stephensi. The spread ofAn. stephensiinto the African continent could lead to urban transmission of malaria, an otherwise rural disease, increasing the human population at risk and complicating malaria elimination efforts. Competition has resulted in habitat segregation of other invasive mosquito species, and our results suggest that it may play a role in determining the distribution ofAn. stephensiacross its invasive range.

    

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4. Analysis of blood-induced Anopheles gambiae midgut proteins and sexual stage Plasmodium falciparum interaction reveals mosquito genes important for malaria transmission

   https://doi.org/10.1038/s41598-020-71186-5  

   Cui, Yingjun ; Niu, Guodong ; Li, Vincent L. ; Wang, Xiaohong ; Li, Jun ( August 2020 , Scientific Reports)

   Plasmodiuminvasion of mosquito midguts is a mandatory step for malaria transmission. The roles of mosquito midgut proteins and parasite interaction during malaria transmission are not clear. This study aims to identify mosquito midgut proteins that interact with and affectP. falciparuminvasion. Based on gene expression profiles and protein sequences, 76 mosquito secretory proteins that are highly expressed in midguts and up-regulated by blood meals were chosen for analysis. About 61 candidate genes were successfully cloned fromAnopheles gambiaeand expressed in insect cells. ELISA analysis showed that 25 of the insect cell-expressed recombinant mosquito proteins interacted with theP. falciparum-infected cell lysates. Indirect immunofluorescence assays confirmed 17 of them interacted with sexual stage parasites significantly stronger than asexual stage parasites. Knockdown assays found that seven candidate genes significantly changed mosquitoes' susceptibility toP. falciparum. Four of them (AGAP006268, AGAP002848, AGAP006972, and AGAP002851) played a protective function against parasite invasion, and the other three (AGAP008138, FREP1, and HPX15) facilitatedP. falciparumtransmission to mosquitoes. Notably, AGAP008138 is a unique gene that only exists inAnophelinemosquitoes. These gene products are ideal targets to block malaria transmission.

    

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5. Interspecies microbiome transplantation recapitulates microbial acquisition in mosquitoes

   https://doi.org/10.1186/s40168-022-01256-5  

   Coon, Kerri L. ; Hegde, Shivanand ; Hughes, Grant L. ( April 2022 , Microbiome)

   Mosquitoes harbor microbial communities that play important roles in their growth, survival, reproduction, and ability to transmit human pathogens. Microbiome transplantation approaches are often used to study host-microbe interactions and identify microbial taxa and assemblages associated with health or disease. However, no such approaches have been developed to manipulate the microbiota of mosquitoes.

   Here, we developed an approach to transfer entire microbial communities between mosquito cohorts. We undertook transfers between (Culex quinquefasciatustoAedes aegypti) and within (Ae. aegyptitoAe. aegypti) species to validate the approach and determine the number of mosquitoes required to prepare donor microbiota. After the transfer, we monitored mosquito development and microbiota dynamics throughout the life cycle. Typical holometabolous lifestyle-related microbiota structures were observed, with higher dynamics of microbial structures in larval stages, including the larval water, and less diversity in adults. Microbiota diversity in recipient adults was also more similar to the microbiota diversity in donor adults.

   This study provides the first evidence for successful microbiome transplantation in mosquitoes. Our results highlight the value of such methods for studying mosquito-microbe interactions and lay the foundation for future studies to elucidate the factors underlying microbiota acquisition, assembly, and function in mosquitoes under controlled conditions.

    

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