Lipases secreted by a gut bacterium inhibit arbovirus transmission in mosquitoes

Yu, Xi; Tong, Liangqin; Zhang, Liming; Yang, Yun; Xiao, Xiaoping; Zhu, Yibin; Wang, Penghua; Cheng, Gong

doi:10.1371/journal.ppat.1010552

Cited by 9 publications

(8 citation statements)

References 42 publications

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“…Panama that is mosquitocidal ( 38 ) was identified as a strain of C. rhizoryzae along with Chromobacterium sp. Beijing, which was also isolated from a mosquito and was reported to inactivate dengue virus but was not reported to be mosquitocidal ( 44 ) ( Fig. 1B ; Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Yet, other studies report that C. aquaticum functions as a beneficial probiotic in fish ( 58 ) while Chromobacterium sp. Beijing exhibits activity that potentially confers resistance to an arbovirus in adult mosquitoes ( 44 ). Collectively, these findings suggest either Chromobacterium species or strains have variable host ranges as pathogens or can broadly cause disease but unknown factors determine infection risks and disease severity or potentially enable some Chromobacterium to benefit animal hosts.…”

Section: Discussionmentioning

confidence: 99%

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Increased environmental microbial diversity reduces the disease risk of a mosquitocidal pathogen

Kang,

Martinson,

Wang

et al. 2024

mBio

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Increased diversity in host-associated microbial communities often benefits animal health by provisioning nutrients and protecting against pathogens. In contrast, whether the diversity of environmental microbial communities can also benefit animal health is much less studied. In aquatic environments, water enables environmental microbes to more directly interact with pathogens and animals than in terrestrial environments, which also suggests the potential for community diversity to benefit animal health. In this study, we addressed this question by identifying a strain of Chromobacterium haemolyticum named Rain 0013 ( Ch_ R13) that is a virulent pathogen of mosquito larvae, which live in aquatic habitats. Comparative genomic and functional data suggested many Chromobacterium are both mosquitocidal and opportunistic pathogens of other animals due to conservation of virulence factors that include a broad-spectrum toxin (cyanide). However, we also identified a strongly negative correlation between diversity of the environmental microbiota and disease severity due to Ch_ R13 needing to achieve a threshold density to kill mosquito larvae. Experiments using defined (gnotobiotic) microbial communities further suggested certain environmental community members reduced Ch_ R13 densities more than others. Altogether, our results indicate Ch_ R13 and other Chromobacterium have the potential to broadly cause disease but the environmental communities of microbes in aquatic habitats attenuate disease risk. IMPORTANCE The host-specific microbiotas of animals can both reduce and increase disease risks from pathogens. In contrast, how environmental microbial communities affect pathogens is largely unexplored. Aquatic habitats are of interest because water enables environmental microbes to readily interact with animal pathogens. Here, we focused on mosquitoes, which are important disease vectors as terrestrial adults but are strictly aquatic as larvae. We identified a pathogen of mosquito larvae from the field as a strain of Chromobacterium haemolyticum . Comparative genomic analyses and functional assays indicate this strain and other Chromobacterium are mosquitocidal but are also opportunistic pathogens of other animals. We also identify a critical role for diversity of the environmental microbiota in disease risk. Our study characterizes both the virulence mechanisms of a pathogen and the role of the environmental microbiota in disease risk to an aquatic animal of significant importance to human health.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Increased environmental microbial diversity reduces the disease risk of a mosquitocidal pathogen

Kang,

Martinson,

Wang

et al. 2024

mBio

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“…During hematophagy, arthropods acquire various factors, including components from host blood and metabolites from commensal microbes, which might influence viral transmission [ 114 , 115 , 116 , 117 , 118 ]. A recent finding revealed that mosquitoes acquire a host-derived miRNA, known as miR-150-5p, which has been shown to downregulate the expression of the thrombospondin-related anonymous protein AaCT-1 mRNA, thereby disrupting the RNAi antiviral framework and promoting DENV infection and propagation in the mosquito [ 36 ].…”

Section: The Roles Of Noncoding Rnas In Vector-mediated Flavivirus In...mentioning

confidence: 99%

The Role of Noncoding RNA in the Transmission and Pathogenicity of Flaviviruses

Zhang,

Li,

Cao

et al. 2024

Viruses

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Noncoding RNAs (ncRNAs) constitute a class of RNA molecules that lack protein-coding capacity. ncRNAs frequently modulate gene expression through specific interactions with target proteins or messenger RNAs, thereby playing integral roles in a wide array of cellular processes. The Flavivirus genus comprises several significant members, such as dengue virus (DENV), Zika virus (ZIKV), and yellow fever virus (YFV), which have caused global outbreaks, resulting in high morbidity and mortality in human populations. The life cycle of arthropod-borne flaviviruses encompasses their transmission between hematophagous insect vectors and mammalian hosts. During this process, a complex three-way interplay occurs among the pathogen, vector, and host, with ncRNAs exerting a critical regulatory influence. ncRNAs not only constitute a crucial regulatory mechanism that has emerged from the coevolution of viruses and their hosts but also hold potential as antiviral targets for controlling flavivirus epidemics. This review introduces the biogenesis of flavivirus-derived ncRNAs and summarizes the regulatory roles of ncRNAs in viral replication, vector-mediated viral transmission, antiviral innate immunity, and viral pathogenicity. A profound comprehension of the interplay between ncRNAs and flaviviruses will help formulate efficacious prophylactic and therapeutic strategies against flavivirus-related diseases.

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“…Serratia marcescens gut bacteria secrete SmEnhancin ( Figure 2A -IV), which weakens the mucin layer and increases DENV infectivity in A. aegypti (Wu et al, 2019 ), whereas Chromobacterium spp. aminopeptidases and lipase production ( Figure 2A -V) degrade the DENV envelope (Ramirez et al, 2014 ; Yu et al, 2022 ), S. marcescens can also affects mosquito larval survival and adult microbiota composition (Heu et al, 2021 ). Midgut microorganisms limit arboviral development by activating immunological pathways and producing broad-spectrum AMPs, ROS, and opsonins (Xi et al, 2008 ).…”

Section: Mosquitoes and Arbovirusmentioning

confidence: 99%

A tangled threesome: understanding arbovirus infection in Aedes spp. and the effect of the mosquito microbiota

Mantilla-Granados,

Castellanos,

Velandia-Romero

2024

Front. Microbiol.

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Arboviral infections transmitted by Aedes spp. mosquitoes are a major threat to human health, particularly in tropical regions but are expanding to temperate regions. The ability of Aedes aegypti and Aedes albopictus to transmit multiple arboviruses involves a complex relationship between mosquitoes and the virus, with recent discoveries shedding light on it. Furthermore, this relationship is not solely between mosquitoes and arboviruses, but also involves the mosquito microbiome. Here, we aimed to construct a comprehensive review of the latest information about the arbovirus infection process in A. aegypti and A. albopictus, the source of mosquito microbiota, and its interaction with the arbovirus infection process, in terms of its implications for vectorial competence. First, we summarized studies showing a new mechanism for arbovirus infection at the cellular level, recently described innate immunological pathways, and the mechanism of adaptive response in mosquitoes. Second, we addressed the general sources of the Aedes mosquito microbiota (bacteria, fungi, and viruses) during their life cycle, and the geographical reports of the most common microbiota in adults mosquitoes. How the microbiota interacts directly or indirectly with arbovirus transmission, thereby modifying vectorial competence. We highlight the complexity of this tripartite relationship, influenced by intrinsic and extrinsic conditions at different geographical scales, with many gaps to fill and promising directions for developing strategies to control arbovirus transmission and to gain a better understanding of vectorial competence. The interactions between mosquitoes, arboviruses and their associated microbiota are yet to be investigated in depth.

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Lipases secreted by a gut bacterium inhibit arbovirus transmission in mosquitoes

Cited by 9 publications

References 42 publications

Increased environmental microbial diversity reduces the disease risk of a mosquitocidal pathogen

Increased environmental microbial diversity reduces the disease risk of a mosquitocidal pathogen

The Role of Noncoding RNA in the Transmission and Pathogenicity of Flaviviruses

A tangled threesome: understanding arbovirus infection in Aedes spp. and the effect of the mosquito microbiota

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