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Mancini, M. V.

Publications and source records attributed to Mancini, M. V..

9 recordsLinked to original sources

Microbiota-driven, strain-specific Asaia colonisation modulates mosquito vector competence

Microbiota-based mosquito control strategies are founded on the ability of bacterial symbionts to modify host biology and/or pathogen transmission. However, symbionts do not operate in isolation. Their colonisation, persistence and biological effects arise within a complex ecological network comprising the host and its resident microbiota. We hypothesized that colonisation success is not only an intrinsic property of a bacterial symbiont but emerges from interactions between bacterial strain, host background, and the native microbial community. To test this, we compared recolonisation by endogenous and exogenous Asaia strains in the invasive mosquito Aedes koreicus using wild-type and axenic mosquitoes to experimentally manipulate the microbial composition. We found that endogenous and exogenous strains followed distinct colonisation trajectories. Depletion of the resident microbiota selectively rescued colonisation by the endogenous strain, whereas both strains successfully disseminated to transmission-relevant tissues despite contrasting early gut dynamics. Furthermore, these strain-specific colonisation dynamics were associated with increased Semliki Forest virus (SFV) transmission and enhanced adult longevity, particularly following colonisation by the exogenous strain. Our findings indicate that resident microbial communities act as selective ecological filters that shape symbiont colonisation in a strain-dependent manner. More broadly, this study demonstrates that the biological effects of mosquito symbionts emerge from interactions between bacterial strains and the microbial community context, providing an ecological framework for the rational and effective development of microbiota-based vector control strategies.

microbiology↗

Thermal responses of an emerging temperate mosquito reshape arboviral transmission risk

Global warming is known to increase arboviral disease risk by enabling the expansion of tropical vectors such as Aedes aegypti and Aedes albopictus. However, whether climate-driven shifts in seasonal dynamics within temperate regions, such as warmer springs and shorter winters, create thermal settings favourable for additional vectors, which can reshape disease risk maps, is poorly understood. To answer this question, we used the invasive temperate mosquito species Aedes koreicus and tested its thermal developmental resilience, along with its vector competence for dengue and chikungunya viruses. We observed significant phenotypic variation in thermal tolerance across life stages, which translates into distinct thermal performance curves for life-history traits, ultimately shaping overall mosquito fitness. We further found that temperature effects are virus-specific, with differential impacts on infection and transmission between dengue and chikungunya viruses. These stage- and pathogen-specific responses generate carry-over effects across life stages, indicating that thermal responses may be constrained by life-history trade-offs rather than be defined by a single thermal optimum. Our results highlight the need to move beyond static, species-based risk assessments toward mechanistic frameworks that integrate thermal biology across life stages and vector-pathogen systems. As climate change increasingly reshapes seasonal structure rather than simply elevating mean temperatures, cold-adapted and temperate vectors such as Ae. koreicus, provide critical model systems to understand how transmission risk emerges outside mosquito classical thermal optima, calling for a broader paradigm shift in how global change and vector-borne disease risk are conceptualised.

ecology↗

Population-specific responses to developmental temperature in the arboviral vector : implications for climate change

The increase of environmental temperature due to current global warming is not only favoring the expansion of the distribution range of many insect species, but it is also changing their phenology. Insect phenology is tightly linked to developmental timing, which is regulated by environmental temperatures. However, the degree to which effects of developmental temperatures extend across developmental stages and their inter-stage relationships have not been thoroughly quantified in mosquitoes. Here, we used the mosquito Aedes albopictus, which is an aggressive invasive species and an arboviral vector to study how developmental temperature influences fitness across developmental stages, thermal traits, energy reserves, transcriptome, and Wolbachia prevalence in populations from either temperate or tropical regions. We show that hatchability, larval and pupal viability, and developmental speed are strongly influenced by temperature and these effects extend to wing length, body mass, longevity, content of water, protein and lipids in adults, in a population-specific manner. On the contrary, neither adult thermal preference nor heat resistance significantly change with temperature. Development at 18{degrees}C revealed to be a limiting factor for the proliferation of Wolbachia in adults and transcriptome analysis showed enrichment for functions linked to stress responses (i.e. cuticle proteins and chitin, cytochrome p450, and heat shock proteins) in mosquitoes reared at both 18{degrees}C and 32{degrees}C. Our data showed an overall reduced vector fitness performance when mosquitoes were reared at 32{degrees}C, and the absence of isomorphy in the relationship between developmental stages and temperature in the temperate population. Altogether these results have important implications for reliable model projections of the invasion potentials of Ae. albopictus and its epidemiological impact.

ecology↗

Validation of an engineered Zika virus-like particle vaccine candidate in a mosquito-mouse transmission model

The primary route of Zika virus (ZIKV) transmission is through the bite of an infected Aedes mosquito, when it probes the skin of a vertebrate host during a blood meal. Viral particles are injected into the bite site together with mosquito saliva and a complex mixture of other components. Some of them are shown to play a key role in the augmentation of the arbovirus infection in the host, with increased viremia and/or morbidity. This vector-derived contribution to the infection is not usually considered when vaccine candidates are tested in preclinical animal models. In this study, we performed a preclinical validation of a promising ZIKV vaccine candidate in a mosquito-mouse transmission model using both Asian and African ZIKV lineages. Mice were immunized with engineered ZIKV virus-like particles and subsequently infected through the bite of ZIKV-infected Ae. aegypti mosquitoes. Despite a mild increase in viremia in mosquito-infected mice compared to those infected through traditional needle injection, the vaccine protected the animals from developing the disease and strongly reduced viremia. In addition, during peak viremia, naive mosquitoes were allowed to feed on infected vaccinated and non-vaccinated mice. Our analysis of viral titers in mosquitos showed that the vaccine was able to inhibit virus transmission from the host to the vector. Author summaryZika is a mosquito-borne viral disease, causing acute debilitating symptoms and complications in infected individuals and irreversible neuronal abnormalities in newborn children. The primary vectors of ZIKV are generally considered to be mosquitoes of the genus Aedes, in particular Aedes aegypti. Despite representing a significant public health burden with a widespread transmission in many regions of the world, Zika remains a neglected disease with no effective antiviral therapies or approved vaccines to control and prevent infections. The efficacy of several promising candidate vaccines is however under investigation, mainly through artificial infections (i.e. needle-mediated injections of the virus) in animal models, while it is known that components of the mosquito bite lead to an enhancement of viral infection and spread. In this study, we have also included mosquitoes as viral vectors, demonstrating that the ability of a promising candidate vaccine to protect animals against ZIKV infections after the bite of an infected mosquito, and to also prevent its further transmission. These findings represent an additional crucial step for the development of an effective prevention tool for clinical use. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=150 SRC="FIGDIR/small/503125v1_ufig1.gif" ALT="Figure 1"> View larger version (57K): org.highwire.dtl.DTLVardef@136fd6borg.highwire.dtl.DTLVardef@137950borg.highwire.dtl.DTLVardef@1a0e01org.highwire.dtl.DTLVardef@8d90d7_HPS_FORMAT_FIGEXP M_FIG C_FIG

microbiology↗

High temperature cycles result in maternal transmission and dengue infection differences between Wolbachia strains in Aedes aegypti

Environmental factors play a crucial role in the population dynamics of arthropod endosymbionts, and therefore in the deployment of Wolbachia symbionts for the control of dengue arboviruses. The potential of Wolbachia to invade, persist and block virus transmission depends in part on its intracellular density. Several recent studies have highlighted the importance of larval rearing temperature in modulating Wolbachia densities in adults, suggesting that elevated temperatures can severely impact some strains, while having little effect on others. The effect of a replicated tropical heat cycle on Wolbachia density and levels of virus blocking was assessed using Aedes aegypti lines carrying strains wMel and wAlbB, two Wolbachia strains currently used for dengue control. Impacts on intracellular density, maternal transmission fidelity and dengue inhibition capacity were observed for wMel. In contrast wAlbB-carrying Ae. aegypti maintained a relatively constant intracellular density at high temperatures and conserved its capacity to inhibit dengue. Following larval heat treatment, wMel showed a degree of density recovery in aging adults, although this was compromised by elevated air temperatures. When choosing the Wolbachia strain to be used in a dengue control programme it is important to consider the effects of environmental temperatures on invasiveness and virus inhibition. Author summaryIn the past decades, dengue incidence has dramatically increased all over the world. An emerging dengue control strategy utilizes Ae. aegypti mosquitoes artificially transinfected with the bacterial symbiont Wolbachia, with the ultimate aim of replacing wild mosquito populations. Wolbachia is transmitted from mother to offspring and is able to interfere with virus transmission within the mosquito vector. However, the rearing temperature of mosquito larvae is known to impact on some Wolbachia strains. In this study, we compared the effects of a temperature cycle mimicking natural breeding sites in tropical climates on two Wolbachia strains, currently used for open field trials. We observed that the strain wMel was susceptible to high larval rearing temperatures, while the strain wAlbB resulted to be more stable. These results underlines the importance of understanding the impact of environmental factors on released mosquitoes, in order to ensure the most efficient strategy for dengue control.

microbiology↗

Phylogenomics reveals that Asaia symbionts from insects underwent convergent genome reduction, preserving an insecticide-degrading gene

The mosquito microbiota is composed by several lineages of microorganisms whose ecological roles and evolutionary histories have yet to be investigated in depth. Among these microorganisms, Asaia bacteria play a prominent role, given its abundance in the gut, reproductive organs and salivary glands of different mosquito species, while its presence has also been reported in several other insects. Notably, Asaia has great potential as a tool for the control of mosquito-borne diseases. Here, we present a wide phylogenomic analysis of Asaia strains isolated from different species of mosquito vectors and from different populations of the Mediterranean fruit fly (medfly) Ceratitis capitata, an insect pest of worldwide economic importance. We show that phylogenetically distant lineages of Asaia experienced independent genome reductions, despite following a common pattern, characterized by the early loss of genes involved in genome stability. This result highlights the role of specific metabolic pathways in the symbiotic relationship between Asaia and the insect host. Finally, we discovered that all but one of the Asaia strains included in the study possess the pyrethroid hydrolase gene. Phylogenetic analysis revealed that this gene is ancestral in Asaia, strongly suggesting that it played a role in the establishment of the symbiotic association between these bacteria and the mosquito hosts. We propose that this gene from the symbiont contributed to initial pyrethroid resistance in insects harboring Asaia, also considering the widespread production of pyrethrins by several plants. ImportanceWe have studied genome reduction within several strains of the insect symbiont Asaia, isolated from different species/strains of mosquito and medfly. Phylogenetically distant strains of Asaia, despite following a common pattern involving the loss of genes related to genome stability, have undergone independent genome reductions, highlighting the peculiar role of specific metabolic pathways in the symbiotic relationship between Asaia and its host. We also show that the pyrethroid hydrolase gene is present in all the Asaia strains isolated except for the South American malaria vector An. darlingi, for which resistance to pyrethroids has never been reported, suggesting a possible involvement of Asaia in determining the resistance to insecticides.

microbiology↗

Wolbachia strain wAu efficiently blocks arbovirus transmission in Aedes albopictus

The global incidence of arboviral diseases transmitted by Aedes mosquitoes, including dengue, chikungunya, yellow fever, and Zika, has increased dramatically in recent decades. The release of Aedes aegypti carrying the maternally inherited symbiont Wolbachia as an intervention to control arboviruses is being trialled in several countries. However, these efforts are compromised in many endemic regions due to the co-localization of the secondary vector Aedes albopictus, the Asian tiger mosquito. Ae. albopictus has an expanding global distribution following incursions into a number of new territories. To date, only the wMel and wPip strains of Wolbachia have been reported to be transferred into and characterized in this vector. A Wolbachia strain naturally infecting Drosophila simulans, wAu, was selected for transfer into a Malaysian Ae. albopictus line to create a novel triple-strain infection. The newly generated line showed self-compatibility, moderate fitness cost and complete resistance to Zika and dengue infections. Author summaryAedes albopictus, the invasive Asian tiger mosquito, is responsible for numerous outbreaks of important viruses such as dengue and Zika in various regions of the world. The need for alterative control interventions propelled the development of a novel approach that exploits a natural insect symbiont, Wolbachia; when transferred into non-native hosts, these maternally-inherited bacteria are able to interfere with the transmission of mosquito-borne viruses, and also provide reproductive advantages to the host, offering a promising tool for self-sustaining field applications. Currently, several field trials are ongoing for the primary vector of dengue and several other arboviruses, Aedes aegypti, providing encouraging results. In this study, Ae. albopictus has been targeted for a similar approach: this mosquito species naturally carries two strains of Wolbachia. The artificial introduction of a third, non-native strain made this line less able to transmit dengue and Zika viruses and had an impact on its fitness.

microbiology↗

A Microsporidian blocks Plasmodium falciparum transmission in Anopheles arabiensis mosquitoes

Malaria imposes an enormous burden on sub-Saharan Africa, and evidence that incidence could be starting to increase again1 suggests the limits of currently applied control strategies have now been reached. A possible novel control approach involves the dissemination in mosquitoes of inherited symbiotic microbes to block transmission. This strategy is exemplified by the use of transmission-blocking Wolbachia in Aedes aegypti against dengue virus2-7. However, in the Anopheles gambiae complex, the primary African vectors of malaria, there limited reports of inherited symbionts with transmission-blocking capacity8-10. Here we show that a newly discovered vertically transmitted species of Microsporidia symbiont in the An. gambiae complex blocks Plasmodium transmission. Microsporidia MB is present at moderate prevalence in geographically dispersed populations of An. arabienesis in Kenya, localized to the mosquito midgut and ovaries, and is not associated with significant reductions in adult host fecundity or survival. Field collected Microsporidia MB-infected An. arabiensis were never found to harbor P. falciparum gametocytes and on experimental infection with P. falciparum no sporozoites could be detected in Microsporidia MB-infected mosquitos. As a Plasmodium transmission-blocking microbe that is non-virulent and vertically transmitted, Microsporidia MB could be exploited as a novel malaria control tool.

microbiology↗

Establishment of Wolbachia strain wAlbB in Malaysian populations of Aedes aegypti for dengue control

Dengue has enormous health impacts globally. A novel approach to decrease dengue incidence involves the introduction of Wolbachia endosymbionts that block dengue virus transmission into populations of the primary vector mosquito, Aedes aegypti. The wMel Wolbachia strain has previously been trialed in open releases of Ae. aegypti; however the wAlbB strain has been shown to maintain higher density than wMel at high larval rearing temperatures. Releases of Ae. aegypti mosquitoes carrying wAlbB were carried out in 6 diverse sites in greater Kuala Lumpur, Malaysia, with high endemic dengue transmission. The strain was successfully established and maintained at very high population frequency at some sites, or persisted with additional releases following fluctuations at other sites. Based on passive case monitoring, reduced human dengue incidence was observed in the release sites when compared to control sites. The wAlbB strain of Wolbachia provides a promising option as a tool for dengue control, particularly in very hot climates.

microbiology↗