Viral pathogens hitchhike with insect sperm for paternal transmission

Mao, Qianzhuo; Wu, Wei; Liao, Zhenfeng; Li, Jiajia; Jia, Dongsheng; Zhang, Xiaofeng; Chen, Qian; Chen, Hongyan; Wei, Jing; Wèi, Tàiyún

doi:10.1038/s41467-019-08860-4

Cited by 47 publications

(55 citation statements)

References 31 publications

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“…The copyright holder for this preprint (which this version posted June 2, 2020. ; https://doi.org/10.1101/2020.06.01.128819 doi: bioRxiv preprint leafhopper vector (89). The best precedent is probably Drosophila-infecting sigma viruses, which can be transmitted biparentally, allowing for sweeps through fly populations (63,90).…”

Section: Discussionmentioning

confidence: 99%

Partitiviruses infectingDrosophila melanogasterandAedes aegyptiexhibit efficient biparental vertical transmission

Cross

Maertens

Dunham

et al. 2020

Preprint

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13Partitiviruses are segmented, multipartite dsRNA viruses that until recently were only known to 14 infect fungi, plants, and protozoans. Metagenomic surveys have revealed that partitivirus-like 15 sequences are also commonly associated with arthropods. One arthropod-associated partitivirus, 16 galbut virus, is extraordinarily common in wild populations of Drosophila melanogaster fruit 17 flies. To begin to understand the processes that underlie this virus's high global prevalence, we 18 established colonies of wild-caught infected flies. Infection remained at stably high levels over 19 three years, with between 63-100% of individual flies infected. Galbut virus infects fly cells and 20 replicates in tissues throughout infected adults, including reproductive tissues and the gut 21 epithelium. We detected no evidence of horizontal transmission via ingestion but vertical 22 transmission from either infected females or infected males was ~100% efficient. Vertical 23 transmission of a related partitivirus, verdadero virus, that we discovered in a laboratory colony 24 of Aedes aegypti mosquitoes was similarly efficient. This suggests that efficient biparental 25 vertical transmission may be a feature of at least a subset of insect-infecting partitiviruses. To 26 study the impact of galbut virus infection free from the confounding effect of other viruses, we 27 generated an inbred line of flies with galbut virus as the only detectable virus infection. We were 28 able to transmit infection experimentally via microinjection of homogenate from these galbut-29 only flies. This sets the stage for experiments to understand the biological impact and possible 30 utility of partitiviruses infecting important model organisms and disease vectors.31 32 Keywords: 33 Drosophila melanogaster, Aedes aegypti, galbut virus, verdadero virus, partitivirus, arthropod, 34 vertical transmission, metagenomics, virus discovery, virome. 35 36 Importance 37 38Galbut virus is a recently discovered partitivirus that is extraordinarly common in wild 39 populations of the model organism Drosophila melanogaster. Like most viruses discovered 40 through metagenomics, most of the basic biological questions about this virus remain 41 unanswered. We found that galbut virus, along with a closely related partitivirus found in Aedes 42 aegypti mosquitoes, is transmitted from infected females or males to offspring with ~100% 43 efficiency and can be maintained in laboratory colonies over years. This represents one of the 44 most efficient means of virus transmission described, and likely underlies the successful spread 45 of these viruses through insect populations. We created Drosophila lines that contained galbut 46 virus as the only virus infection and showed that these flies can be used as a source for 47 experimental infections. This provides insight into how arthropod-infecting partitiviruses may be 48 maintained in nature and sets the stage for exploration of their biology and potential utility. 49 50 51 52Metagenomic surveys of wild organisms have...

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Section: Discussionmentioning

confidence: 99%

Partitiviruses infectingDrosophila melanogasterandAedes aegyptiexhibit efficient biparental vertical transmission

Cross

Maertens

Dunham

et al. 2020

Preprint

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“…Such considerations raise the possibility that spermatozoa could act as potential vectors of this highly infectious disease. This happens in insects 5 —why not us?…”

Section: Figurementioning

confidence: 98%

COVID‐19 and human spermatozoa—Potential risks for infertility and sexual transmission?

Aitken

2020

Andrology

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The COVID‐19 (SARS‐CoV‐2) virus has created a global pandemic responsible for over 500,000 deaths and untold human and economic suffering. Attention has rightly focused on the respiratory system, because this is where a life‐and‐death battle is waged between the viral horde and the host’s immune system. However, other tissues are also susceptible to viral attack including the kidney, heart and brain. The purpose of this communication is to highlight the evidence that the male reproductive system, particularly spermatozoa, constitute another vulnerable target, raising the possibility that COVID‐19 might ultimately induce male infertility and/or facilitate the sexual transmission of this virus, depending on the level of infection.

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“…It was unclear whether the association of P10 with sperm was physical binding or a specific protein-protein interaction, but it may represent a unique means for DcRV to utilize nonstructural proteins in male insects for vertical and horizontal transmission. Other viruses which are able to exploit the sperm for viral transmission are usually limited to the infection of sperm (41, 43, 44). The sperm-associated spread of DcRV via tubules might be less stable, because the exterior binding of tubules has a potential risk of loss and damage during mating.…”

Section: Discussionmentioning

confidence: 99%

A Nonstructural Protein Responsible for Viral Spread of a Novel Insect Reovirus Provides a Safe Channel for Biparental Virus Transmission to Progeny

Chen

Godfrey

Liu

et al. 2019

J Virol

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Diaphorina citri reovirus (DcRV) was previously identified based on metagenomics surveys for virus discovery. Here, we demonstrated that DcRV induces persistent infection in its psyllid host, Diaphorina citri. DcRV was efficiently vertically passed to offspring in a biparental manner. Transmission electron microscopic and immunological analyses showed that the DcRV-encoded nonstructural protein P10 assembled into a virion-packaging tubular structure which is associated with the spread of DcRV throughout the bodies of D. citri insects. P10 tubules containing virions were associated with oocytes of female and sperm of male D. citri insects, suggesting a role in the highly efficient biparental transmission of DcRV. Knocking down P10 by RNA interference for males reduced the percentage of DcRV-infected progeny and for females reduced the viral accumulation in progeny. These results, for the first time, show that a nonstructural protein of a novel insect reovirus provides a safe and pivotal channel for virus spread and biparental transmission to progeny. IMPORTANCE The Asian citrus psyllid, Diaphorina citri Kuwayama, is an important pest in the worldwide citrus industry. It is the vector of “Candidatus Liberibacter asiaticus,” the bacterial pathogen of Huanglongbing, which is currently considered the most destructive disease of citrus worldwide. DcRV was previously identified based on metagenomics surveys for virus discovery. Here, we found that this novel and persistent insect reovirus took advantage of a virus-encoded nonstructural protein, P10, for efficient vertical transmission from parents to progeny. P10 assembled into a virion-packaging tubular structure and was associated with oocytes of female D. citri and sperm of males. Consistent with this, knockdown of P10 for either male or female D. citri insects inhibited DcRV transmission to offspring. This tubular strategy for viral spread and biparental transmission might serve as a target for controlling viral vertical transmission and population expansion.

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Viral pathogens hitchhike with insect sperm for paternal transmission

Cited by 47 publications

References 31 publications

Partitiviruses infectingDrosophila melanogasterandAedes aegyptiexhibit efficient biparental vertical transmission

Partitiviruses infectingDrosophila melanogasterandAedes aegyptiexhibit efficient biparental vertical transmission

COVID‐19 and human spermatozoa—Potential risks for infertility and sexual transmission?

A Nonstructural Protein Responsible for Viral Spread of a Novel Insect Reovirus Provides a Safe Channel for Biparental Virus Transmission to Progeny

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