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Divergent and conserved elements comprise the chemoreceptive repertoire of the nonblood-feeding mosquito Toxorhynchites amboinensis.

ABSTRACT: Many mosquito species serve as vectors of diseases such as malaria and yellow fever, wherein pathogen transmission is tightly associated with the reproductive requirement of taking vertebrate blood meals. Toxorhynchites is one of only three known mosquito genera that does not host-seek and initiates egg development in the absence of a blood-derived protein bolus. These remarkable differences make Toxorhynchites an attractive comparative reference for understanding mosquito chemosensation as it pertains to host-seeking. We performed deep transcriptome profiling of adult female Toxorhynchites amboinensis bodies, antennae and maxillary palps, and identified 25,084 protein-coding "genes" in the de novo assembly. Phylogenomic analysis of 4,266 single-copy "genes" from T. amboinensis, Aedes aegypti, Anopheles gambiae, and Culex quinquefasciatus robustly supported Ae. aegypti as the closest relative of T. amboinensis, with the two species diverged approximately 40 Ma. We identified a large number of T. amboinensis chemosensory "genes," the majority of which have orthologs in other mosquitoes. Finally, cross-species expression analyses indicated that patterns of chemoreceptor transcript abundance were very similar for chemoreceptors that are conserved between T. amboinensis and Ae. aegypti, whereas T. amboinensis appeared deficient in the variety of expressed, lineage-specific chemoreceptors. Our transcriptome assembly of T. amboinensis represents the first comprehensive genomic resource for a nonblood-feeding mosquito and establishes a foundation for future comparative studies of blood-feeding and nonblood-feeding mosquitoes. We hypothesize that chemosensory genes that display discrete patterns of evolution and abundance between T. amboinensis and blood-feeding mosquitoes are likely to play critical roles in host-seeking and hence the vectorial capacity.

SUBMITTER: Zhou X

PROVIDER: S-EPMC4224357 | biostudies-literature | 2014 Oct

REPOSITORIES: biostudies-literature

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Divergent and conserved elements comprise the chemoreceptive repertoire of the nonblood-feeding mosquito Toxorhynchites amboinensis.

Zhou Xiaofan X Rinker David C DC Pitts Ronald Jason RJ Rokas Antonis A Zwiebel Laurence J LJ

Genome biology and evolution 20141016 10

Many mosquito species serve as vectors of diseases such as malaria and yellow fever, wherein pathogen transmission is tightly associated with the reproductive requirement of taking vertebrate blood meals. Toxorhynchites is one of only three known mosquito genera that does not host-seek and initiates egg development in the absence of a blood-derived protein bolus. These remarkable differences make Toxorhynchites an attractive comparative reference for understanding mosquito chemosensation as it p ...[more]

PMID: 25326137

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Project description:Endogenous viral elements derived from nonretroviral RNA viruses have been described in various animal genomes. Whether they have a biological function, such as host immune protection against related viruses, is a field of intense study. Here, we investigated the repertoire of endogenous flaviviral elements (EFVEs) in Aedes mosquitoes, the vectors of arboviruses such as dengue and chikungunya viruses. Previous studies identified three EFVEs from Aedes albopictus cell lines and one from Aedes aegypti cell lines. However, an in-depth characterization of EFVEs in wild-type mosquito populations and individual mosquitoes in vivo has not been performed. We detected the full-length DNA sequence of the previously described EFVEs and their respective transcripts in several A. albopictus and A. aegypti populations from geographically distinct areas. However, EFVE-derived proteins were not detected by mass spectrometry. Using deep sequencing, we detected the production of PIWI-interacting RNA-like small RNAs, in an antisense orientation, targeting the EFVEs and their flanking regions in vivo The EFVEs were integrated in repetitive regions of the mosquito genomes, and their flanking sequences varied among mosquito populations. We bioinformatically predicted several new EFVEs from a Vietnamese A. albopictus population and observed variation in the occurrence of those elements among mosquitoes. Phylogenetic analysis of an A. aegypti EFVE suggested that it integrated prior to the global expansion of the species and subsequently diverged among and within populations. The findings of this study together reveal the substantial structural and nucleotide diversity of flaviviral integrations in Aedes genomes. Unraveling this diversity will help to elucidate the potential biological function of these EFVEs.IMPORTANCE Endogenous viral elements (EVEs) are whole or partial viral sequences integrated in host genomes. Interestingly, some EVEs have important functions for host fitness and antiviral defense. Because mosquitoes also have EVEs in their genomes, characterizing these EVEs is a prerequisite for their potential use to manipulate the mosquito antiviral response. In the study described here, we focused on EVEs related to the Flavivirus genus, to which dengue and Zika viruses belong, in individual Aedes mosquitoes from geographically distinct areas. We show the existence in vivo of flaviviral EVEs previously identified in mosquito cell lines, and we detected new ones. We show that EVEs have evolved differently in each mosquito population. They produce transcripts and small RNAs but not proteins, suggesting a function at the RNA level. Our study uncovers the diverse repertoire of flaviviral EVEs in Aedes mosquito populations and contributes to an understanding of their role in the host antiviral system.

Project description:BackgroundThe majority of DNA contained within vertebrate genomes is non-coding, with a certain proportion of this thought to play regulatory roles during development. Conserved Non-coding Elements (CNEs) are an abundant group of putative regulatory sequences that are highly conserved across divergent groups and thus assumed to be under strong selective constraint. Many CNEs may contain regulatory factor binding sites, and their frequent spatial association with key developmental genes - such as those regulating sensory system development - suggests crucial roles in regulating gene expression and cellular patterning. Yet surprisingly little is known about the molecular evolution of CNEs across diverse mammalian taxa or their role in specific phenotypic adaptations. We examined 3,110 vertebrate-specific and ~82,000 mammalian-specific CNEs across 19 and 9 mammalian orders respectively, and tested for changes in the rate of evolution of CNEs located in the proximity of genes underlying the development or functioning of auditory systems. As we focused on CNEs putatively associated with genes underlying the development/functioning of auditory systems, we incorporated echolocating taxa in our dataset because of their highly specialised and derived auditory systems.ResultsPhylogenetic reconstructions of concatenated CNEs broadly recovered accepted mammal relationships despite high levels of sequence conservation. We found that CNE substitution rates were highest in rodents and lowest in primates, consistent with previous findings. Comparisons of CNE substitution rates from several genomic regions containing genes linked to auditory system development and hearing revealed differences between echolocating and non-echolocating taxa. Wider taxonomic sampling of four CNEs associated with the homeobox genes Hmx2 and Hmx3 - which are required for inner ear development - revealed family-wise variation across diverse bat species. Specifically within one family of echolocating bats that utilise frequency-modulated echolocation calls varying widely in frequency and intensity high levels of sequence divergence were found.ConclusionsLevels of selective constraint acting on CNEs differed both across genomic locations and taxa, with observed variation in substitution rates of CNEs among bat species. More work is needed to determine whether this variation can be linked to echolocation, and wider taxonomic sampling is necessary to fully document levels of conservation in CNEs across diverse taxa.

Dataset Information

Divergent and conserved elements comprise the chemoreceptive repertoire of the nonblood-feeding mosquito Toxorhynchites amboinensis.

Publications

Divergent and conserved elements comprise the chemoreceptive repertoire of the nonblood-feeding mosquito Toxorhynchites amboinensis.

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