Insect pathogenic fungus interacts with the gut microbiota to accelerate mosquito mortality.
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ABSTRACT:
SUBMITTER: Wei G
PROVIDER: S-EPMC5468619 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Adult mosquitoes inherit a bacterial community from larvae via transstadial transmission, an understudied process that may influence host-microbe interactions. Microbes contribute to important host life history traits, and analyzing transmitted microbial communities, the interrelationship between larval and adult-associated microbiota, and factors influencing host-microbe relationships provides targets for research. During its larval stage, the yellow fever mosquito (Aedes aegypti) hosts the trichomycete gut fungus Zancudomyces culisetae, and fungal colonization coincides with environmental perturbations in the digestive tract microecosystem. Natural populations are differentially exposed to fungi, thereby potentially harboring distinct microbiota and experiencing disparate host-microbe interactions. This study's objectives were to characterize larval and initial adult microbiomes, investigate variation in diversity and distribution of microbial communities across individuals, and assess whether larval fungal colonization impacted microbiomes at these developmental stages. Laboratory-based fungal infestation assays, sequencing of 16S rRNA gene amplicons, and bacterial load quantification protocols revealed that initial adult microbiomes varied in diversity and distribution. Larval fungal colonization had downstream effects on initial adult microbiomes, significantly reducing microbial community variation, shifting relative abundances of certain bacterial families, and influencing transstadial transmission outcomes of particular genera. Further, abundances of several families consistently decreased in adults relative to levels in larvae, possibly reflecting impacts of host development on specific bacterial taxa. These findings demonstrated that a prolific gut fungus impacted mosquito-associated microbiota at two developmental stages in an insect connected with global human health.IMPORTANCE Mosquitoes are widespread vectors of numerous human pathogens and harbor microbiota known to affect host phenotypic traits. However, little research has directly investigated how bacterial communities associated with larvae and adults are connected. We characterized whole-body bacterial communities in mosquito larvae preceding pupation and in newly emerged adults, and investigated whether a significant biotic factor, fungal colonization of the larval hindgut, impacted these microbiomes. Results showed that fungal colonization reduced microbial community variation across individuals and differentially impacted the outcomes of transstadial transmission for certain bacterial genera, revealing downstream effects of the fungus on initial adult microbiomes. The importance of our research is in providing a thorough comparative analysis of whole-body microbiota harbored in larvae and adults of the yellow fever mosquito (Aedes aegypti) and in demonstrating the important role a widespread gut fungus played in a host-associated microbiome.
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Project description:Metarhizium robertsii is a common soil fungus that occupies a specialized ecological niche as an endophyte and an insect pathogen. Previously, we showed that the endophytic capability and insect pathogenicity of Metarhizium are coupled to provide an active method of insect-derived nitrogen transfer to a host plant via fungal mycelia. We speculated that in exchange for this insect-derived nitrogen, the plant would provide photosynthate to the fungus. By using 13CO2, we show the incorporation of 13C into photosynthate and the subsequent translocation of 13C into fungal-specific carbohydrates (trehalose and chitin) in the root/endophyte complex. We determined the amount of 13C present in root-associated fungal biomass over a 21-day period by extracting fungal carbohydrates and analysing their composition using nuclear magnetic resonance (NMR) spectroscopy. These findings are evidence that the host plant is providing photosynthate to the fungus, likely in exchange for insect-derived nitrogen in a tripartite, and symbiotic, interaction.
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Project description:Most alphaviruses are transmitted by mosquito vectors and infect a wide range of vertebrate hosts, with a few exceptions. Eilat virus (EILV) in this genus is characterized by a host range restricted to mosquitoes. Its chimeric viruses have been developed as safe and effective vaccine candidates and diagnostic tools. Here, we investigated the interactions between these insect-specific viruses (ISVs) and mosquito cells, unveiling their potential roles in determining vector competence and arbovirus transmission. By RNA sequencing, we found that these ISVs profoundly modified host cell gene expression profiles. Two EILV-based chimeras, consisting of EILV’s nonstructural genes and the structural genes of Chikungunya virus (CHIKV) or Venezuelan equine encephalitis virus (VEEV), namely EILV/CHIKV (E/C) and EILV/VEEV (E/V), induced more intensive transcriptome regulation than parental EILV and activated different antiviral mechanisms in host cells. We demonstrated that E/C robustly promoted antimicrobial peptide production and E/V strongly upregulated the RNA interference pathway components. This also highlighted the intrinsic divergences between CHIKV and VEEV, representatives of the Old World and New World alphaviruses. In contrast, EILV triggered a limited antiviral response. We further showed that initial chimera infections efficiently inhibited subsequent pathogenic alphavirus replication, especially in the case of E/V infection, which almost prevented VEEV and Sindbis virus (SINV) superinfections. Altogether our study provided valuable information on developing ISVs as biological control agents.
2023-01-19 | GSE220562 | GEO
Project description:DNA methylation is an epigenetic process altered in cancer and ageing. Age-related methylation drift can be used to estimate lifespan and can be influenced by extrinsic factors such as diet. Here, we report that non-pathogenic microbiota accelerate age-related methylation drift in the colon when compared with germ-free mice. DNA methylation analyses showed that microbiota and IL10KO were associated with changes in 5% and 4.1% of CpG sites, while mice with both factors had 18% alterations. Microbiota, IL10KO, and their combination altered 0.4%, 0.4%, and 4% of CpG island methylation, respectively. These are comparable to what is seen in colon cancer. Ageing changes were accelerated in the IL10KO mice with microbiota, and the affected genes were more likely to be altered in colon cancer. Thus, the microbiota affect DNA methylation of the colon in patterns reminiscent of what is observed in ageing and colorectal cancer.
| S-EPMC9980687 | biostudies-literature
Project description:Species in the ascomycete fungal genus Cordyceps have been proposed to be the teleomorphs of Metarhizium species. The latter have been widely used as insect biocontrol agents. Cordyceps species are highly prized for use in traditional Chinese medicines, but the genes responsible for biosynthesis of bioactive components, insect pathogenicity and the control of sexuality and fruiting have not been determined.Here, we report the genome sequence of the type species Cordyceps militaris. Phylogenomic analysis suggests that different species in the Cordyceps/Metarhizium genera have evolved into insect pathogens independently of each other, and that their similar large secretomes and gene family expansions are due to convergent evolution. However, relative to other fungi, including Metarhizium spp., many protein families are reduced in C. militaris, which suggests a more restricted ecology. Consistent with its long track record of safe usage as a medicine, the Cordyceps genome does not contain genes for known human mycotoxins. We establish that C. militaris is sexually heterothallic but, very unusually, fruiting can occur without an opposite mating-type partner. Transcriptional profiling indicates that fruiting involves induction of the Zn2Cys6-type transcription factors and MAPK pathway; unlike other fungi, however, the PKA pathway is not activated.The data offer a better understanding of Cordyceps biology and will facilitate the exploitation of medicinal compounds produced by the fungus.
| S-EPMC3334602 | biostudies-literature
Project description:Most alphaviruses are transmitted by mosquito vectors and infect a wide range of vertebrate hosts, with a few exceptions. Eilat virus (EILV) in this genus is characterized by a host range restricted to mosquitoes. Its chimeric viruses have been developed as safe and effective vaccine candidates and diagnostic tools. Here, we investigated the interactions between these insect-specific viruses (ISVs) and mosquito cells, unveiling their potential roles in determining vector competence and arbovirus transmission. By RNA sequencing, we found that these ISVs profoundly modified host cell gene expression profiles. Two EILV-based chimeras, consisting of EILV's nonstructural genes and the structural genes of Chikungunya virus (CHIKV) or Venezuelan equine encephalitis virus (VEEV), namely, EILV/CHIKV (E/C) and EILV/VEEV (E/V), induced more intensive transcriptome regulation than parental EILV and activated different antiviral mechanisms in host cells. We demonstrated that E/C robustly promoted antimicrobial peptide production and E/V strongly upregulated the RNA interference pathway components. This also highlighted the intrinsic divergences between CHIKV and VEEV, representatives of the Old World and New World alphaviruses. In contrast, EILV triggered a limited antiviral response. We further showed that initial chimera infections efficiently inhibited subsequent pathogenic alphavirus replication, especially in the case of E/V infection, which almost prevented VEEV and Sindbis virus (SINV) superinfections. Altogether our study provided valuable information on developing ISVs as biological control agents. IMPORTANCE Mosquito-borne alphaviruses can cause emerging and reemerging infectious diseases, posing a considerable threat to human and animal health worldwide. However, no specific antivirals or commercial vaccines are currently available. Therefore, it is vital to develop biological control measures to contain virus transmission. Insect-specific EILV and its chimeras are supposed to induce superinfection exclusion owing to the close phylogenetical relationship with pathogenic alphaviruses. These viruses might also, like bacterial symbionts, modulate mosquito hosts' vector competence for arboviruses. However, little is known about the responses of mosquitoes or mosquito cells to ISV infections. Here, we found that EILV barely elicited antiviral defenses in host cells, while its chimeras, namely, E/C and E/V, potentiated the responses via different mechanisms. Furthermore, we showed that initial chimera infections could largely inhibit subsequent pathogenic alphavirus infections. Taken together, our study proposed insect-specific chimeras as a promising candidate for developing biological control measures against pathogenic alphaviruses.
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Project description:BACKGROUND:The composition and structure of microbial communities that inhabit the mosquito midguts are poorly understood despite their well-documented potential to impede pathogen transmission. METHODOLOGY/PRINCIPAL FINDINGS:We used MiSeq sequencing of the 16S rRNA gene to characterize the bacterial communities of field-collected populations of 12 mosquito species. After quality filtering and rarefaction, the remaining sequences were assigned to 181 operational taxonomic units (OTUs). Approximately 58% of these OTUs occurred in at least two mosquito species but only three OTUs: Gluconobacter (OTU 1), Propionibacterium (OTU 9), and Staphylococcus (OTU 31) occurred in all 12 mosquito species. Individuals of different mosquito species shared similar gut microbiota and it was common for individuals of the same species from the same study site and collection date to harbor different gut microbiota. On average, the microbiota of Aedes albopictus was the least diverse and significantly less even compared to Anopheles crucians, An. quadrimaculatus, Ae. triseriatus, Ae. vexans, Ae. japonicus, Culex restuans, and Culiseta inornata. The microbial community of Cx. pipiens and Ae. albopictus differed significantly from all other mosquitoes species and was primarily driven by the dominance of Wolbachia. CONCLUSION AND SIGNIFICANCE:These findings expand the range of mosquito species whose gut microbiota has been characterized and sets the foundation for further studies to determine the influence of these microbiota on vector susceptibility to pathogens.
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Project description:In the face of mosquito-borne disease outbreaks, effective mosquito control is a primary goal for public health. Insect repellents, containing active compounds such as DEET and picaridin, are a first defence against biting insects. Owing to widespread use and incomplete sewage treatment, these compounds are frequently detected in surface waters, but their effects on aquatic taxa such as mosquito larvae or their naturally occurring aquatic predators are poorly understood. We investigated the effects of environmentally realistic concentrations of commercial products containing DEET and picaridin on survivorship of mosquito larvae, and their potential indirect effects on survival of larval salamanders, a major predator of mosquito larvae. Larval mosquitos were not affected by exposure to repellents containing DEET or picaridin. We found no larval salamander mortality in control and DEET treatments, but mortality rates in picaridin treatments ranged from 45 to 65% after 25 days of exposure. Salamander larvae exposed to repellents containing picaridin began to display tail deformities and impaired development four days after the experiment began. Our findings suggest the possibility that environmentally realistic concentrations of picaridin-containing repellents in surface waters may increase the abundance of adult mosquitos owing to decreased predation pressure.
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Project description:The coffee berry borer (Hypothenemus hampei) is the most devastating insect pest of coffee worldwide with its infestations decreasing crop yield by up to 80%. Caffeine is an alkaloid that can be toxic to insects and is hypothesized to act as a defence mechanism to inhibit herbivory. Here we show that caffeine is degraded in the gut of H. hampei, and that experimental inactivation of the gut microbiota eliminates this activity. We demonstrate that gut microbiota in H. hampei specimens from seven major coffee-producing countries and laboratory-reared colonies share a core of microorganisms. Globally ubiquitous members of the gut microbiota, including prominent Pseudomonas species, subsist on caffeine as a sole source of carbon and nitrogen. Pseudomonas caffeine demethylase genes are expressed in vivo in the gut of H. hampei, and re-inoculation of antibiotic-treated insects with an isolated Pseudomonas strain reinstates caffeine-degradation ability confirming their key role.
| S-EPMC4510693 | biostudies-literature
Project description:Subtilisin-like Pr1 proteases of insect-pathogenic fungi are a large family of extracellular cuticle-degrading enzymes that presumably determine a capability of hyphal invasion into insect hemocoel through normal cuticle infection, but remain poorly understood although often considered as virulence factors for genetic improvement of fungal potential against pests. Here, we report that not all of 11 Pr1 family members necessarily function in Beauveria bassiana, an ancient wide-spectrum pathogen evolved insect pathogenicity ~200 million years ago. These Pr1 proteases are phylogenetically similar to or distinct from 11 homologues (Pr1A-K) early named in Metarhizium anisopliae complex, a young entomopathogen lineage undergoing molecular evolution toward Pr1 diversification, and hence renamed Pr1A1/A2, Pr1B1-B3, Pr1 C, Pr1F1-F4,4 and Pr1 G, respectively. Multiple analyses of all single gene-deleted and rescued mutants led to the recognition of five conserved members (Pr1C, Pr1G, Pr1A2, Pr1B1, and Pr1B2) contributing significantly to the fungal pathogenicity to insect. The conserved Pr1 proteases were proven to function only in cuticle degradation, individually contribute 19-29% to virulence, but play no role in post-infection cellular events critical for fungal killing action. Six other Pr1 proteases were not functional at all in either cuticle degradation during host infection or virulence-related cellular events post-infection. Therefore, only the five conserved proteases are collectively required for, and hence mark evolution of, insect pathogenicity in B. bassiana. These findings provide the first referable base for insight into the evolution of Pr1 family members in different lineages of fungal insect pathogens.
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