Factors influencing infection and transmission of<i>Anopheles gambiae</i>densovirus (AgDNV) in mosquitoes

Barik, Tapan Kumar; Suzuki, Yasutsugu; Rasgon, Jason L.

doi:10.7717/peerj.2691

Cited by 12 publications

(30 citation statements)

References 17 publications

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“…In general, prevalent members of the natural virome should evolve towards lower pathogenicity in their habitual host lineages. Consistent with that expectation, a symbiotic Anopheles densovirus (studied for its potential use as a paratransgenesis tool) elicited low transcriptional response upon infection, and neither mosquito age at infection nor feeding regime affected viral titers [ 30 , 31 ]. However, maintenance of bacterial microbiome commensals in the non-pathogenic commensal state requires active policing by basal host immunity [ 32 ].…”

Section: Discussionmentioning

confidence: 89%

Highly focused transcriptional response of Anopheles coluzzii to O’nyong nyong arbovirus during the primary midgut infection

2018

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BackgroundAnopheles mosquitoes are efficient vectors of human malaria, but it is unknown why they do not transmit viruses as well as Aedes and Culex mosquitoes. The only arbovirus known to be consistently transmitted by Anopheles mosquitoes is O’nyong nyong virus (ONNV, genus Alphavirus, family Togaviridae). The interaction of Anopheles mosquitoes with RNA viruses has been relatively unexamined.ResultsWe transcriptionally profiled the African malaria vector, Anopheles coluzzii, infected with ONNV. Mosquitoes were fed on an infectious bloodmeal and were analyzed by Illumina RNAseq at 3 days post-bloodmeal during the primary virus infection of the midgut epithelium, before systemic dissemination. Virus infection triggers transcriptional regulation of just 30 host candidate genes. Most of the regulated candidate genes are novel, without known function. Of the known genes, a significant cluster includes candidates with predicted involvement in carbohydrate metabolism. Two candidate genes encoding leucine-rich repeat immune (LRIM) factors point to possible involvement of immune protein complexes in the mosquito antiviral response. The primary ONNV infection by bloodmeal shares little transcriptional response in common with ONNV infection by intrathoracic injection, nor with midgut infection by the malaria parasites, Plasmodium falciparum or P. berghei. Profiling of A. coluzzii microRNA (miRNA) identified 118 known miRNAs and 182 potential novel miRNA candidates, with just one miRNA regulated by ONNV infection. This miRNA was not regulated by other previously reported treatments, and may be virus specific. Coexpression analysis of miRNA abundance and messenger RNA expression revealed discrete clusters of genes regulated by Imd and JAK/STAT, immune signaling pathways that are protective against ONNV in the primary infection.ConclusionsONNV infection of the A. coluzzii midgut triggers a remarkably limited gene regulation program of mostly novel candidate genes, which likely includes host genes deployed for antiviral defense, as well as genes manipulated by the virus to facilitate infection. Functional dissection of the ONNV-response candidate genes is expected to generate novel insight into the mechanisms of virus-vector interaction.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4918-0) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 89%

Highly focused transcriptional response of Anopheles coluzzii to O’nyong nyong arbovirus during the primary midgut infection

2018

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“…Previous studies reported that AgDNV is venereally transmitted from infected males to the spermatheca of mated females (6). To test whether sexually-transmitted AgDNV can also lead to disseminated infection in mated females, we again allowed uninfected, virgin females to mate with either AgDNV- or PBS-injected males.…”

Section: Resultsmentioning

confidence: 99%

“…In its natural An. gambiae host, AgDNV can infect both sexes and all developmental stages, replicating particularly well in adults post-emergence (6, 7). Notably though, AgDNV is a benign virus that does not cause mortality or even a marked transcriptional response in its mosquito host (8).…”

Section: Introductionmentioning

confidence: 99%

“…Previously, it was found that AgDNV can be venereally transmitted from infected males to the spermatheca of females post-mating (6), yet it is not known if venereally transmitted AgDNV remains contained to the spermatheca or if it can also lead to disseminated infection in females. This information is important for determining whether infected male releases could be a viable method for introducing AgDNV-based tools into field populations of female An.…”

Section: Introductionmentioning

confidence: 99%

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Sexual transmission of Anopheles gambiae densovirus (AgDNV) leads to disseminated infection in mated females

Werling

Johnson

Metz

et al. 2022

Preprint

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Background: Anopheles gambiae densovirus (AgDNV) is an insect-specific, single-stranded DNA virus that infects An. gambiae, the major mosquito species responsible for transmitting malaria parasites throughout Sub-Saharan Africa. AgDNV is a benign virus that is very specific to its mosquito host and therefore has potential to serve as a vector control tool via paratransgenesis (genetic modification of mosquito symbionts) to limit transmission of human pathogens. Prior to being engineered into a control tool, the natural transmission dynamics of AgDNV between An. gambiae mosquitoes needs to be fully understood. Additionally, improved knowledge of AgDNV infection in male mosquitoes is needed. In this study, we examine the tissue tropism of AgDNV in the male reproductive tract and investigate both venereal and vertical transmission dynamics of the virus. Methods: An. gambiae adult males were infected with AgDNV via micro-injection and reproductive tissues collected and assayed for AgDNV using qPCR. Next, uninfected females were introduced to AgDNV-infected or control males and, after several nights of mating, both the spermatheca and female carcass were assessed for venereally transmitted AgDNV. Finally, F1s from this cross were collected and assayed to quantify vertical transmission of the virus. Results: AgDNV infected the reproductive tract of male mosquitoes, including the testes and male accessory glands (MAGs), without affecting mating rates. AgDNV-infected males venereally transmitted virus to females, and these venereally-infected females developed disseminated infection throughout the body. However, AgDNV was not vertically transmitted to F1s resulting from this cross. Conclusions: Infected male releases could be an effective strategy to introduce AgDNV-based paratransgenic tools into naive populations of An. gambiae females.

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“…Densoviruses (DNVs) persist as chronic infections in mosquito origin cells, and metagenomic techniques also confirm their presence in wild‐caught mosquitoes (O'Neill et al, ; Shi et al, ). In addition to this, DNVs also infect all developmental stages of mosquitoes which leads to larval death (Barik, Suzuki, & Rasgon, ; Barreau, Jousset, & Bergoin, ). Mosquito densoviruses (MDVs) have been identified in multiple mosquito species, such as Ae.…”

Section: Resultsmentioning

confidence: 99%

A viral metagenomic analysis reveals rich viral abundance and diversity in mosquitoes from pig farms

Hameed

Liu

Anwar

et al. 2019

Transbound Emerg Dis

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Mosquitoes harbour a diversity of viruses and are responsible for several mosquito‐borne viral diseases of humans and animals, thereby leading to major public health concerns, and significant economic losses across the globe. Viral metagenomics offers a great opportunity for bulk analysis of viral genomes retrieved directly from environmental samples. In this study, we performed a viral metagenomic analysis of five pools of mosquitoes belonging to Aedes, Anopheles and Culex species, collected from different pig farms in the vicinity of Shanghai, China, to explore the viral community carried by mosquitoes. The resulting metagenomic data revealed that viral community in the mosquitoes was highly diverse and varied in abundance among pig farms, which comprised of more than 48 viral taxonomic families, specific to vertebrates, invertebrates, plants, fungi, bacteria and protozoa. In addition, a considerable number of viral reads were related to viruses that are not classified by host. The read sequences related to animal viruses included parvoviruses, anelloviruses, circoviruses, flavivirus, rhabdovirus and seadornaviruses, which might be taken up by mosquitoes from viremic animal hosts during blood feeding. Notably, sample G1 contained the most abundant sequence related to Banna virus, which is of public health interest because it causes encephalitis in humans. Furthermore, non‐classified viruses also shared considerable virus sequences in all the samples, presumably belonging to unexplored virus category. Overall, the present study provides a comprehensive knowledge of diverse viral populations carried by mosquitoes at pig farms, which is a potential source of diseases for mammals including humans and animals. These viral metagenomic data are valuable for assessment of emerging and re‐emerging viral epidemics.

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Factors influencing infection and transmission ofAnopheles gambiaedensovirus (AgDNV) in mosquitoes

Cited by 12 publications

References 17 publications

Highly focused transcriptional response of Anopheles coluzzii to O’nyong nyong arbovirus during the primary midgut infection

Highly focused transcriptional response of Anopheles coluzzii to O’nyong nyong arbovirus during the primary midgut infection

Sexual transmission of Anopheles gambiae densovirus (AgDNV) leads to disseminated infection in mated females

A viral metagenomic analysis reveals rich viral abundance and diversity in mosquitoes from pig farms

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