Stable high-density and maternally inherited Wolbachia infections in Anopheles moucheti and Anopheles demeilloni mosquitoes

Walker, Thomas; Quek, Shannon; Jeffries, Claire L.; Bandibabone, Janvier; Dhokiya, Vishaal; Bamou, Roland; Kristan, Mojca; Messenger, Louisa A.; Gidley, Alexandra; Hornett, Emily A.; Anderson, Enyia R; Cansado-Utrilla, Cintia; Hegde, Shivanand; Chimanuka, Bantuzeko; Stevenson, Jennifer; Lobo, Neil F.; Wagstaff, Simon C.; Antonio-Nkondjio, Christophe; Irish, Seth R.; Heinz, Eva; Hughes, Grant L.

doi:10.1016/j.cub.2021.03.056

Cited by 60 publications

(75 citation statements)

References 84 publications

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“…In addition, Walker et al determined a heavy infection of Wolbachia in the ovaries of An. moucheti that could induce maternal transmission [41]. However, in this study, the mosquitoes of An.…”

Section: Discussionmentioning

confidence: 58%

Prevalence and molecular characterization of Wolbachia in field-collected Aedes albopictus, Anopheles sinensis, Armigeres subalbatus, Culex pipiens and Cx. tritaeniorhynchus in China

Yang

Zhu

et al. 2021

PLoS Negl Trop Dis

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Wolbachia are maternally transmitted intracellular bacteria that can naturally and artificially infect arthropods and nematodes. Recently, they were applied to control the spread of mosquito-borne pathogens by causing cytoplasmic incompatibility (CI) between germ cells of females and males. The ability of Wolbachia to induce CI is based on the prevalence and polymorphism of Wolbachia in natural populations of mosquitoes. In this study, we screened the natural infection level and diversity of Wolbachia in field-collected mosquitoes from 25 provinces of China based on partial sequence of Wolbachia surface protein (wsp) gene and multilocus sequence typing (MLST). Among the samples, 2489 mosquitoes were captured from 24 provinces between July and September, 2014 and the remaining 1025 mosquitoes were collected month-by-month in Yangzhou, Jiangsu province between September 2013 and August 2014. Our results showed that the presence of Wolbachia was observed in mosquitoes of Aedes albopictus (97.1%, 331/341), Armigeres subalbatus (95.8%, 481/502), Culex pipiens (87.0%, 1525/1752), Cx. tritaeniorhynchus (17.1%, 14/82), but not Anopheles sinensis (n = 88). Phylogenetic analysis indicated that high polymorphism of wsp and MLST loci was observed in Ae. albopictus mosquitoes, while no or low polymorphisms were in Ar. subalbatus and Cx. pipiens mosquitoes. A total of 12 unique mutations of deduced amino acid were identified in the wsp sequences obtained in this study, including four mutations in Wolbachia supergroup A and eight mutations in supergroup B. This study revealed the prevalence and polymorphism of Wolbachia in mosquitoes in large-scale regions of China and will provide some useful information when performing Wolbachia-based mosquito biocontrol strategies in China.

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Section: Discussionmentioning

confidence: 58%

Prevalence and molecular characterization of Wolbachia in field-collected Aedes albopictus, Anopheles sinensis, Armigeres subalbatus, Culex pipiens and Cx. tritaeniorhynchus in China

Yang

Zhu

et al. 2021

PLoS Negl Trop Dis

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“…Such a balancing act might make maintenance of CI-inducing Wolbachia strains in anopheline insects difficult and one outcome could be silencing of the toxic cifB gene by mutation. Interestingly, cifB nonsense mutations were identified by sequencing wAnM and wAnD strains recently discovered in some Anopheles species, although one cifB homologue in wAnD seems to be intact and it will be interesting to learn if this strain can induce CI 27 . Of note, cifB pseudogenization is not uncommon and is consistent with early evolutionary models that predict male incompatibility not to be selected for within a host lineage 49,50 .…”

Section: P G -C I F a ; B V A S A -C I F A ; Z P G -C I F B Z P G -C I F A ; B V A S A -C I F A ; Z P G -C I F Bmentioning

confidence: 99%

Wolbachia cifB induces cytoplasmic incompatibility in the malaria mosquito vector

et al. 2021

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Wolbachia, a maternally inherited intracellular bacterial species, can manipulate host insect reproduction by cytoplasmic incompatibility (CI), which results in embryo lethality in crosses between infected males and uninfected females. CI is encoded by two prophage genes, cifA and cifB. Wolbachia, coupled with the sterile insect technique, has been used in field trials to control populations of the dengue vector Aedes albopictus, but CI-inducing strains are not known to infect the malaria vector Anopheles gambiae. Here we show that cifA and cifB can induce conditional sterility in the malaria vector An. gambiae. We used transgenic expression of these Wolbachia-derived genes in the An. gambiae germline to show that cifB is sufficient to cause embryonic lethality and that cifB-induced sterility is rescued by cifA expression in females. When we co-expressed cifA and cifB in male mosquitoes, the CI phenotype was attenuated. In female mosquitoes, cifB impaired fertility, which was overcome by co-expression of cifA. Our findings pave the way towards using CI to control malaria mosquito vectors.

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“…This is true for Asaia and Wolbachia , which appear antagonistic to one another [ 43 , 44 ]. The recent finding of stable Wolbachia infection in Anopheles mosquitoes reinvigorates the use of this microbe for control of malaria [ 27 , 45 ]. As such, there need to be careful considerations for the type of microbial control approach to be used in a particular region given that it may impede future control strategies.…”

Section: Discussionmentioning

confidence: 99%

Molecular detection and maternal transmission of a bacterial symbiont Asaia species in field-caught Anopheles mosquitoes from Cameroon

et al. 2021

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Background Malaria control relies mainlyon insecticide-based tools. However, the effectiveness of these tools is threatened by widespread insecticide resistance in malaria vectors, highlighting the need for alternative control approaches. The endosymbiont Asaia has emerged as a promising candidate for paratransgenic control of malaria, but its biology and genetics still need to be further analyzed across Africa. Here, we investigated the prevalence of Asaia and its maternal transmission in the natural population of Anopheles mosquitoes in Cameroon. Methods Indoor-resting adult mosquitoes belonging to four species (An. coluzzii, An. arabiensis, An. funestus and An. gambiae) were collected from eight localities across Cameroon from July 2016 to February 2020. PCR was performed on the Asaia-specific 16S ribosomal RNA gene, and samples positive by PCR for Asaia were confirmed by Sanger sequencing and phylogenetic analysis. The vertical transmission of Asaia was investigated by screening F1 mosquitoes belonging to F0Asaia-positive females. Results A total of 895 mosquitoes were screened. We found 43% (384) Asaia infection prevalence in four mosquito species. Phylogenetic analysis revealed that Asaia from Cameroon clustered together with the strains of Asaia isolated from other parts of the world. In addition, seven nucleotide sequence variants were found with low genetic diversity (π = 0.00241) and nucleotide sequence variant diversity (Hd = 0.481). Asaia was vertically transmitted with high frequency (range from 42.5 to 100%). Conclusions This study provides field-based evidence of the presence of Asaia in Anopheles mosquitoes in Cameroon for exploitation as a symbiont in the control of malaria in sub-Saharan Africa. Graphical abstract

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Stable high-density and maternally inherited Wolbachia infections in Anopheles moucheti and Anopheles demeilloni mosquitoes

Cited by 60 publications

References 84 publications

Prevalence and molecular characterization of Wolbachia in field-collected Aedes albopictus, Anopheles sinensis, Armigeres subalbatus, Culex pipiens and Cx. tritaeniorhynchus in China

Prevalence and molecular characterization of Wolbachia in field-collected Aedes albopictus, Anopheles sinensis, Armigeres subalbatus, Culex pipiens and Cx. tritaeniorhynchus in China

Wolbachia cifB induces cytoplasmic incompatibility in the malaria mosquito vector

Molecular detection and maternal transmission of a bacterial symbiont Asaia species in field-caught Anopheles mosquitoes from Cameroon

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