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Evidence of natural Wolbachia infections in field populations of Anopheles gambiae.

ABSTRACT: Wolbachia are maternally transmitted intracellular bacteria that invade insect populations by manipulating their reproduction and immunity and thus limiting the spread of numerous human pathogens. Experimental Wolbachia infections can reduce Plasmodium numbers in Anopheles mosquitoes in the laboratory, however, natural Wolbachia infections in field anophelines have never been reported. Here we show evidence of Wolbachia infections in Anopheles gambiae in Burkina Faso, West Africa. Sequencing of the 16S rRNA gene identified Wolbachia sequences in both female and male germlines across two seasons, and determined that these sequences are vertically transmitted from mother to offspring. Whole-genome sequencing of positive samples suggests that the genetic material identified in An. gambiae belongs to a novel Wolbachia strain, related to but distinct from strains infecting other arthropods. The evidence of Wolbachia infections in natural Anopheles populations promotes further investigations on the possible use of natural Wolbachia-Anopheles associations to limit malaria transmission.

SUBMITTER: Baldini F

PROVIDER: S-EPMC4059924 | biostudies-literature | 2014 Jun

REPOSITORIES: biostudies-literature

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Evidence of natural Wolbachia infections in field populations of Anopheles gambiae.

Baldini Francesco F Segata Nicola N Pompon Julien J Marcenac Perrine P Shaw W Robert WR Dabiré Roch K RK Diabaté Abdoulaye A Levashina Elena A EA Catteruccia Flaminia F

Nature communications 20140606

Wolbachia are maternally transmitted intracellular bacteria that invade insect populations by manipulating their reproduction and immunity and thus limiting the spread of numerous human pathogens. Experimental Wolbachia infections can reduce Plasmodium numbers in Anopheles mosquitoes in the laboratory, however, natural Wolbachia infections in field anophelines have never been reported. Here we show evidence of Wolbachia infections in Anopheles gambiae in Burkina Faso, West Africa. Sequencing of ...[more]

PMID: 24905191

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Project description:Wolbachia (Alphaproteobacteria, Rickettsiales) is an intraovarially transmitted symbiont of insects able to exert striking phenotypes, including reproductive manipulations and pathogen blocking. These phenotypes make Wolbachia a promising tool to combat mosquito-borne diseases. Although Wolbachia is present in the majority of terrestrial arthropods, including many disease vectors, it was considered absent from Anopheles gambiae mosquitos, the main vectors of malaria in sub-Saharan Africa. In 2014, Wolbachia sequences were detected in A. gambiae samples collected in Burkina Faso. Subsequently, similar evidence came from collections all over Africa, revealing a high Wolbachia 16S rRNA sequence diversity, low abundance, and a lack of congruence between host and symbiont phylogenies. Here, we reanalyze and discuss recent evidence on the presence of Wolbachia sequences in A. gambiae. We find that although detected at increasing frequencies, the unusual properties of these Wolbachia sequences render them insufficient to diagnose natural infections in A. gambiae Future studies should focus on uncovering the origin of Wolbachia sequence variants in Anopheles and seeking sequence-independent evidence for this new symbiosis. Understanding the ecology of Anopheles mosquitos and their interactions with Wolbachia will be key in designing successful, integrative approaches to limit malaria spread. Although the prospect of using Wolbachia to fight malaria is intriguing, the newly discovered strains do not bring it closer to realization.IMPORTANCE Anopheles gambiae mosquitos are the main vectors of malaria, threatening around half of the world's population. The bacterial symbiont Wolbachia can interfere with disease transmission by other important insect vectors, but until recently, it was thought to be absent from natural A. gambiae populations. Here, we critically analyze the genomic, metagenomic, PCR, imaging, and phenotypic data presented in support of the presence of natural Wolbachia infections in A. gambiae We find that they are insufficient to diagnose Wolbachia infections and argue for the need of obtaining robust data confirming basic Wolbachia characteristics in this system. Determining the Wolbachia infection status of Anopheles is critical due to its potential to influence Anopheles population structure and Plasmodium transmission.

Project description:The endosymbiotic bacterium Wolbachia is being investigated as a potential control agent in several important vector insect species. Recent studies have shown that Wolbachia can protect the insect host against a wide variety of pathogens, resulting in reduced transmission of parasites and viruses. It has been proposed that compromised vector competence of Wolbachia-infected insects is due to up-regulation of the host innate immune system or metabolic competition. Anopheles mosquitoes, which transmit human malaria parasites, have never been found to harbor Wolbachia in nature. While transient somatic infections can be established in Anopheles, no stable artificially-transinfected Anopheles line has been developed despite numerous attempts. However, cultured Anopheles cells can be stably infected with multiple Wolbachia strains such as wAlbB from Aedes albopictus, wRi from Drosophila simulans and wMelPop from Drosophila melanogaster. Infected cell lines provide an amenable system to investigate Wolbachia-Anopheles interactions in the absence of an infected mosquito strain. We used Affymetrix GeneChip microarrays to investigate the effect of wAlbB and wRi infection on the transcriptome of cultured Anopheles Sua5B cells, and for a subset of genes used quantitative PCR to validate results in somatically-infected Anopheles mosquitoes. Wolbachia infection had a dramatic strain-specific effect on gene expression in this cell line, with almost 700 genes in total regulated representing a diverse array of functional classes. Very strikingly, infection resulted in a significant down-regulation of many immune, stress and detoxification-related transcripts. This is in stark contrast to the induction of immune genes observed in other insect hosts. We also identified genes that may be potentially involved in Wolbachia-induced reproductive and pathogenic phenotypes. Somatically-infected mosquitoes had similar responses to cultured cells. The data show that Wolbachia has a profound and unique effect on Anopheles gene expression in cultured cells, and has important implications for mechanistic understanding of Wolbachia-induced phenotypes and potential novel strategies to control malaria.

Project description:BackgroundThe endosymbiont bacterium Wolbachia is maternally inherited and naturally infects some filarial nematodes and a diverse range of arthropods, including mosquito vectors responsible for disease transmission in humans. Previously, it has been found infecting most mosquito species but absent in Anopheles and Aedes aegypti. However, recently these two mosquito species were found to be naturally infected with Wolbachia. We report here the extent of Wolbachia infections in field-collected mosquitoes from Malaysia based on PCR amplification of the Wolbachia wsp and 16S rRNA genes.MethodsThe prevalence of Wolbachia in Culicinae mosquitoes was assessed via PCR with wsp primers. For some of the mosquitoes, in which the wsp primers failed to amplify a product, Wolbachia screening was performed using nested PCR targeting the 16S rRNA gene. Wolbachia sequences were aligned using Geneious 9.1.6 software, analyzed with BLAST, and the most similar sequences were downloaded. Phylogenetic analyses were carried out with MEGA 7.0 software. Graphs were drawn with GraphPad Prism 8.0 software.ResultsA total of 217 adult mosquitoes representing 26 mosquito species were screened. Of these, infections with Wolbachia were detected in 4 and 15 mosquito species using wsp and 16S rRNA primers, respectively. To our knowledge, this is the first time Wolbachia was detected using 16S rRNA gene amplification, in some Anopheles species (some infected with Plasmodium), Culex sinensis, Culex vishnui, Culex pseudovishnui, Mansonia bonneae and Mansonia annulifera. Phylogenetic analysis based on wsp revealed Wolbachia from most of the mosquitoes belonged to Wolbachia Supergroup B. Based on 16S rRNA phylogenetic analysis, the Wolbachia strain from Anopheles mosquitoes were more closely related to Wolbachia infecting Anopheles from Africa than from Myanmar.ConclusionsWolbachia was found infecting Anopheles and other important disease vectors such as Mansonia. Since Wolbachia can affect its host by reducing the life span and provide resistance to pathogen infection, several studies have suggested it as a potential innovative tool for vector/vector-borne disease control. Therefore, it is important to carry out further studies on natural Wolbachia infection in vector mosquitoes' populations as well as their long-term effects in new hosts and pathogen suppression.

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Evidence of natural Wolbachia infections in field populations of Anopheles gambiae.

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Evidence of natural Wolbachia infections in field populations of Anopheles gambiae.

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