Wolbachia infections in natural Anopheles populations affect egg laying and negatively correlate with Plasmodium development

Shaw, W. Robert; Marcenac, Perrine; Childs, Lauren M.; Buckee, Caroline O.; Baldini, Francesco; Sawadogo, Simon P.; Dabiré, Roch K.; Diabaté, Abdoulaye; Catteruccia, Flaminia

doi:10.1038/ncomms11772

Cited by 138 publications

(226 citation statements)

References 53 publications

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“…gambiae in additional villages in Burkina Faso 71 and Anopheles species collected in Illinois, USA 72 . Our study describing resident Wolbachia strains in numerous species of Anopheles malaria vectors also highlights the potential for Wolbachia to be influencing malaria transmission, as postulated by previous studies 39, 40, 73 . Although no significant correlation was present for malaria and Wolbachia prevalence in the 128 An.…”

Section: Discussionsupporting

confidence: 77%

“…gambiae s.s. individuals from DRC, we only detected co-infections in two individuals compared to 13 and 15 individuals infected only with Wolbachia or P. falciparum , respectively. As the majority (77%) of samples had neither detectable Wolbachia resident strains or P. falciparum, a larger sample size would be needed to determine if there is a correlation, as shown previously in both Burkina Faso 73 and Mali 40 . The infection prevalence of resident Wolbachia strains in An.…”

Section: Discussionmentioning

confidence: 99%

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Novel Wolbachia strains in Anopheles malaria vectors from Sub-Saharan Africa

Jeffries¹,

Lawrence²,

Golovko³

et al. 2018

Wellcome Open Res

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Background: Wolbachia, a common insect endosymbiotic bacterium that can influence pathogen transmission and manipulate host reproduction, has historically been considered absent from the Anopheles (An.) genera, but has recently been found in An. gambiae s.l. populations. As there are numerous Anopheles species that have the capacity to transmit malaria, we analysed a range of species to determine Wolbachia prevalence rates, characterise novel Wolbachia strains and determine any correlation between the presence of Plasmodium, Wolbachia and the competing endosymbiotic bacterium Asaia. Methods: Anopheles adult mosquitoes were collected from five malaria-endemic countries: Guinea, Democratic Republic of the Congo (DRC), Ghana, Uganda and Madagascar, between 2013 and 2017. Molecular analysis of samples was undertaken using quantitative PCR, Sanger sequencing, Wolbachia multilocus sequence typing (MLST) and high-throughput amplicon sequencing of the bacterial 16S rRNA gene. Results: Novel Wolbachia strains were discovered in five species: An. coluzzii, An. gambiae s.s., An. arabiensis, An. moucheti and An. species ‘A’, increasing the number of Anopheles species known to be naturally infected. Variable prevalence rates in different locations were observed and novel strains were phylogenetically diverse, clustering with Wolbachia supergroup B strains. We also provide evidence for resident strain variants within An. species ‘A’. Wolbachia is the dominant member of the microbiome in An. moucheti and An. species ‘A’, but present at lower densities in An. coluzzii. Interestingly, no evidence of Wolbachia/Asaia co-infections was seen and Asaia infection densities were also shown to be variable and location dependent. Conclusions: The important discovery of novel Wolbachia strains in Anopheles provides greater insight into the prevalence of resident Wolbachia strains in diverse malaria vectors. Novel Wolbachia strains (particularly high-density strains) are ideal candidate strains for transinfection to create stable infections in other Anopheles mosquito species, which could be used for population replacement or suppression control strategies.

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Section: Discussionsupporting

confidence: 77%

Section: Discussionmentioning

confidence: 99%

Novel Wolbachia strains in Anopheles malaria vectors from Sub-Saharan Africa

Jeffries¹,

Lawrence²,

Golovko³

et al. 2018

Wellcome Open Res

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“…arabiensis that is absent in Gabon (Table 1) . By PCR amplification of a 16S rRNA fragment (Shaw et al, 2016), we found 70 Wolbachia-positive specimens that belonged to 16 different Anopheles species, distributed throughout the country (Figure 1, Table S1). When considering only species with more than 10 screened individuals, we observed that Wolbachia infection was commonly lower than 15% (11/13), as observed in other arthropods (Duron et al, 2008;Zug & Hammerstein, 2012).…”

Section: Wolbachia Naturally Infects a Large Number Of Anopheles Spmentioning

confidence: 99%

Natural Wolbachia infections are common in the major malaria vectors in Central Africa

Ayala

Akone‐Ella

Rahola

et al. 2019

Evolutionary Applications

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During the last decade, the endosymbiont bacterium Wolbachia has emerged as a biological tool for vector disease control. However, for long time, it was believed that Wolbachia was absent in natural populations of Anopheles . The recent discovery that species within the Anopheles gambiae complex host Wolbachia in natural conditions has opened new opportunities for malaria control research in Africa. Here, we investigated the prevalence and diversity of Wolbachia infection in 25 African Anopheles species in Gabon (Central Africa). Our results revealed the presence of Wolbachia in 16 of these species, including the major malaria vectors in this area. The infection prevalence varied greatly among species, confirming that sample size is a key factor to detect the infection. Moreover, our sequencing and phylogenetic analyses showed the important diversity of Wolbachia strains that infect Anopheles . Co‐evolutionary analysis unveiled patterns of Wolbachia transmission within some Anopheles species, suggesting that past independent acquisition events were followed by co‐cladogenesis. The large diversity of Wolbachia strains that infect natural populations of Anopheles offers a promising opportunity to select suitable phenotypes for suppressing Plasmodium transmission and/or manipulating Anopheles reproduction, which in turn could be used to reduce the malaria burden in Africa.

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“…Reshuffling these modules could create proteins with altered subcellular localization patterns or novel target specificities (Gerth & Bleidorn, ). Wolbachia have attracted enormous interest from a public health point of view (Servick, ; Waltz, ), because they have a strong impact on the propagation of infectious diseases of humans by affecting the viral amplification and reproduction of disease vector insects (Burt, ; Caragata, Dutra, & Moreira, ; Shaw et al., ). Considering the fact that Wolbachia are not currently amenable to genetic modifications, manipulations of host physiology with molecular resources derived from Wolbachia would be a feasible approach for the control of vector insects.…”

Section: Discussionmentioning

confidence: 99%

Enhancing Nanos expression via the bacterial TomO protein is a conserved strategy used by the symbiont Wolbachia to fuel germ stem cell maintenance in infected Drosophila females

Oté

Yamamoto²

2018

Arch Insect Biochem Physiol

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The toxic manipulator of oogenesis (TomO) protein has been identified in the wMel strain of Wolbachia that symbioses with the vinegar fly Drosophila melanogaster, as a protein that affects host reproduction. TomO protects germ stem cells (GSCs) from degeneration, which otherwise occurs in ovaries of host females that are mutant for the gene Sex-lethal (Sxl). We isolated the TomO homologs from wPip, a Wolbachia strain from the mosquito Culex quinquefasciatus. One of the homologs, TomO 1, exerted the GSC rescue activity in fly Sxl mutants when lacking its hydrophobic stretches. The GSC-rescuing action of the TomO 1 variant was ascribable to its abilities to associate with Nanos (nos) mRNA and to enhance Nos protein expression. The analysis of structure-activity relationships with TomO homologs and TomO deletion variants revealed distinct modules in the protein that are each dedicated to different functions, i.e., subcellular localization, nos mRNA binding or Nos expression enhancement. We propose that modular reshuffling is the basis for structural and functional diversification of TomO protein members.

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Wolbachia infections in natural Anopheles populations affect egg laying and negatively correlate with Plasmodium development

Cited by 138 publications

References 53 publications

Novel Wolbachia strains in Anopheles malaria vectors from Sub-Saharan Africa

Novel Wolbachia strains in Anopheles malaria vectors from Sub-Saharan Africa

Natural Wolbachia infections are common in the major malaria vectors in Central Africa

Enhancing Nanos expression via the bacterial TomO protein is a conserved strategy used by the symbiont Wolbachia to fuel germ stem cell maintenance in infected Drosophila females

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