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Proboscis infection route of Beauveria bassiana triggers early death of Anopheles mosquito.

ABSTRACT: Entomopathogenic fungi are known to control vector mosquito populations. Thus, understanding the infection dynamics of entomopathogenic fungi is crucial for the effective control of insect pests such as mosquitoes. We investigated the dynamics of Beauveria bassiana s.l. 60-2 infection of Anopheles stephensi by exposing the mosquito to fungus-impregnated filter paper through two infection routes and then comparing the mortality and extent of infection. Fungal development was observed after using this inoculation method with both the tarsus route and the proboscis route, but early mosquito death occurred only after infection through the proboscis route. Fungal hyphae invaded almost all the tissues and organs before or after the death of the host, and fungal invasion of the brain was highly correlated with mortality. Moreover, although all mosquitoes that were alive at various time points after inoculation showed no fungal infection in the brain, fungal infection was detected in the brain in all dead mosquitoes. Our results suggest that fungal invasion of the brain represents one of the factors affecting mortality, and that the proboscis route of infection is critical for the early death of vector mosquitoes.

SUBMITTER: Ishii M

PROVIDER: S-EPMC5471193 | biostudies-literature | 2017 Jun

REPOSITORIES: biostudies-literature

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Proboscis infection route of Beauveria bassiana triggers early death of Anopheles mosquito.

Ishii Minehiro M Kanuka Hirotaka H Badolo Athanase A Sagnon N'Falé N Guelbeogo Wamdaogo M WM Koike Masanori M Aiuchi Daigo D

Scientific reports 20170614 1

Entomopathogenic fungi are known to control vector mosquito populations. Thus, understanding the infection dynamics of entomopathogenic fungi is crucial for the effective control of insect pests such as mosquitoes. We investigated the dynamics of Beauveria bassiana s.l. 60-2 infection of Anopheles stephensi by exposing the mosquito to fungus-impregnated filter paper through two infection routes and then comparing the mortality and extent of infection. Fungal development was observed after using ...[more]

PMID: 28615623

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Project description:The Aedes aegypti mosquito transmits devastating flaviviruses, such as Zika, dengue, and yellow fever viruses. For more effective control of the vector, the pathogenicity of Beauveria bassiana, a fungus commonly used for biological control of pest insects, may be enhanced based on in-depth knowledge of molecular interactions between the pathogen and its host. Here, we identified a mechanism employed by B. bassiana, which efficiently blocks the Ae. aegypti antifungal immune response by a protease that contains an ovarian tumor (OTU) domain. RNA-sequencing analysis showed that the depletion of OTU7B significantly upregulates the mRNA level of immunity-related genes after a challenge of the fungus. CRISPR-Cas9 knockout of OTU7B conferred a higher resistance of mosquitoes to the fungus B. bassiana. OTU7B suppressed activation of the immune response by preventing nuclear translocation of the NF-κB transcription factor Rel1, a mosquito orthologue of Drosophila Dorsal. Further studies identified tumor necrosis factor receptor-associated factor 4 (TRAF4) as an interacting protein of OTU7B. TRAF4-deficient mosquitoes were more sensitive to fungal infection, indicating TRAF4 to be the adaptor protein that activates the Toll pathway. TRAF4 is K63-link polyubiquitinated at K338 residue upon immune challenge. However, OTU7B inhibited the immune signaling by enzymatically removing the polyubiquitin chains of mosquito TRAF4. Thus, this study has uncovered a novel mechanism of fungal action against the host innate immunity, providing a platform for further improvement of fungal pathogen effectiveness. IMPORTANCE Insects use innate immunity to defend against microbial infection. The Toll pathway is a major immune signaling pathway that is associated with the antifungal immune response in mosquitoes. Our study identified a fungal-induced deubiquitinase, OTU7B, which, when knocked out, promotes the translocation of the NF-κB factor Rel1 into the nucleus and confers enhanced resistance to fungal infection. We further found the counterpart of OTU7B, TRAF4, which is a component of the Toll pathway and acts as an adaptor protein. OTU7B enzymatically removes K63-linked polyubiquitin chains from TRAF4. The immune response is suppressed, and mosquitoes become much more sensitive to the Beauveria bassiana infection. Our findings reveal a novel mechanism of fungal action against the host innate immunity.

Project description:Mosquito immunity studies have focused mainly on characterizing immune effector mechanisms elicited against parasites, bacteria and more recently, viruses. However, those elicited against entomopathogenic fungi remain poorly understood, despite the ubiquitous nature of these microorganisms and their unique invasion route that bypasses the midgut epithelium, an important immune tissue and physical barrier. Here, we used the malaria vector Anopheles gambiae as a model to investigate the role of melanization, a potent immune effector mechanism of arthropods, in mosquito defense against the entomopathogenic fungus Beauveria bassiana, using in vivo functional genetic analysis and confocal microscopy. The temporal monitoring of fungal growth in mosquitoes injected with B. bassiana conidia showed that melanin eventually formed on all stages, including conidia, germ tubes and hyphae, except the single cell hyphal bodies. Nevertheless, melanin rarely aborted the growth of any of these stages and the mycelium continued growing despite being melanized. Silencing TEP1 and CLIPA8, key positive regulators of Plasmodium and bacterial melanization in A. gambiae, abolished completely melanin formation on hyphae but not on germinating conidia or germ tubes. The detection of a layer of hemocytes surrounding germinating conidia but not hyphae suggested that melanization of early fungal stages is cell-mediated while that of late stages is a humoral response dependent on TEP1 and CLIPA8. Microscopic analysis revealed specific association of TEP1 with surfaces of hyphae and the requirement of both, TEP1 and CLIPA8, for recruiting phenoloxidase to these surfaces. Finally, fungal proliferation was more rapid in TEP1 and CLIPA8 knockdown mosquitoes which exhibited increased sensitivity to natural B. bassiana infections than controls. In sum, the mosquito melanization response retards significantly B. bassiana growth and dissemination, a finding that may be exploited to design transgenic fungi with more potent bio-control activities against mosquitoes.

Project description:Vector-borne diseases resulted into several cases of human morbidity and mortality over the years and among them is filariasis, caused by the mosquito Culex quinquefasciatus. Developing novel strategies for mosquito control without jeopardizing the environmental conditions has always been a topic of discussion and research. Integrated Vector Management (IVM) emphasizes a comprehensive approach and use of a range of strategies for vector control. Recent research evaluated the use of two entomopathogenic fungi; Beauveria bassiana and Lecanicillium lecanii in IVM, which can serve as potential organic insecticide for mosquito population control. However, their combined efficacy has not yet been evaluated against mosquito control in prior research and a gap of knowledge is still existing. So, this research was an attempt to bridge up the knowledge gap by (1) Assessing the combined efficacy of Beauveria bassiana and Lecanicillium lecanii on Culex quinquefasciatus (2) To investigate the sub-lethal concentration (LC50) of the combined fungal concentration and (3) To examine the post-mortem effects caused by the combined fungal concentration under Scanning Electron Microscope (SEM). The larval pathogenicity assay was performed on 4th instar C. quinquefasciatus larvae. Individual processed fungal solution of B. bassiana and L. lecanii were procured and to test the combined efficacy, the two solutions were mixed in equal proportions. To evaluate the sub-lethal concentration (LC50), different concentrations of the combined fungal solution were prepared by serial dilations. The mortality was recorded after 24 hours for each concentration. Upon treatment and evaluation, The LC50 values of B. bassiana and L. lecanii were 0.25 x 104 spores/ml and 0.12 x 104 spores/ml respectively and the combined fungal concentration was 0.06 x 103 spores/ml. This clearly indicated that the combined efficacy of the fungi is more significant. Further, SEM analysis revealed morphological deformities and extensive body perforations upon combined fungal treatment. These findings suggested that combining the two fungi can be a more effective way in controlling the population of Culex quinquefasciatus.

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Proboscis infection route of Beauveria bassiana triggers early death of Anopheles mosquito.

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Proboscis infection route of Beauveria bassiana triggers early death of Anopheles mosquito.

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