Transovarial transmission of a core virome in the Chagas disease vector Rhodnius prolixus.

Tarcísio Fontenele De Brito,Nicola Iovino,Ingrid Alexandre De Abreu Brito,Mateus Antonio Berni,Attilio Pane,Vitor Lima Coelho,Maira Arruda Cardoso,Fides Lea Zenk,Mark D Stenglein

doi:10.1371/journal.ppat.1009780

Tarcísio Fontenele De Brito, Nicola Iovino + Show 7 more

Open Access

https://doi.org/10.1371/journal.ppat.1009780

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Abstract

Triatomine assassin bugs comprise hematophagous insect vectors of Trypanosoma cruzi, the causative agent of Chagas disease. Although the microbiome of these species has been investigated to some extent, only one virus infecting Triatoma infestans has been identified to date. Here, we describe for the first time seven (+) single-strand RNA viruses (RpV1-7) infecting Rhodnius prolixus, a primary vector of Chagas disease in Central and South America. We show that the RpVs belong to the Iflaviridae, Permutotetraviridae and Solemoviridae and are vertically transmitted from the mothers to the progeny via transovarial transmission. Consistent with this, all the RpVs, except RpV2 that is related to the entomopathogenic Slow bee paralysis virus, established persistent infections in our R. prolixus colony. Furthermore, we show that R. prolixus ovaries express 22-nucleotide viral siRNAs (vsiRNAs), but not viral piRNAs, that originate from the processing of dsRNA intermediates during viral replication of the RpVs. Interestingly, the permutotetraviruses and sobemoviruses display shared pools of vsiRNAs that might provide the basis for a cross-immunity system. The vsiRNAs are maternally deposited in the eggs, where they likely contribute to reduce the viral load and protect the developing embryos. Our results unveil for the first time a complex core virome in R. prolixus and begin to shed light on the RNAi-based antiviral defenses in triatomines.

Highlights

Triatomine insects (Hemiptera, Reduviidae, Triatominae) include hematophagous species that are responsible for the transmission of Chagas disease, an infectious illness that affects 6–7 million people worldwide [1]
We show for the first time that triatomines can support the concomitant infection of a variety of RNA viruses belonging to distantly related viral families
Alignment of the contigs in previtellogenic stages of oogenesis (PVS) with those found in Egg led us to identify 7 unique viral genomes, which we labeled Rhodnius prolixus Virus 1–7 (RpV1-7) (Fig 1)

Summary

Introduction

Triatomine insects (Hemiptera, Reduviidae, Triatominae) include hematophagous species that are responsible for the transmission of Chagas disease, an infectious illness that affects 6–7 million people worldwide [1]. The insect genera Rhodnius, Triatoma and Panstrongylus harbor well established vectors of Trypanosoma cruzi, the etiologic agent of the illness, with Rhodnius prolixus being the most important vector in Colombia, Venezuela and other areas in Central and South America.The protozoan is typically transmitted to the human host through the feces and urine of the bug. 10,000 people die of Chagas disease per year. Vectorial transmission has only been documented in Central and South America, this disease has already spread to the United States of America, Canada, many European Countries, Australia and Japan due to food-borne transmission, blood transfusions, organ transplantation, laboratory accidents and congenital transmission from mother to child [3,4,5]. There are no vaccines or cures for the illness and the most efficient methods to reduce its spreading rely on vector control strategies [1]

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