Institute of Biomedical Sciences, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil.
Department of Chromatin Regulation, Max Planck Institute of Immunobiology and Epigenetics, Freiburg, Germany.
PLoS Pathog. 2021 Aug 18;17(8):e1009780. doi: 10.1371/journal.ppat.1009780. eCollection 2021 Aug.
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.
盲蝽科昆虫是克氏锥虫(恰加斯病的病原体)的血食性昆虫媒介。尽管这些物种的微生物组已经在一定程度上被研究过,但迄今为止只鉴定出一种感染 Triatoma infestans 的病毒。在这里,我们首次描述了感染 Rhodnius prolixus 的七种(+)单链 RNA 病毒(RpV1-7),它是中美洲和南美洲恰加斯病的主要传播媒介。我们表明,RpVs 属于 Iflaviridae、Permutotetraviridae 和 Solemoviridae,并通过经卵传递垂直传递给后代。与这一致的是,除了与昆虫病原性慢蜂麻痹病毒相关的 RpV2 之外,所有的 RpV 都在我们的 R. prolixus 群体中建立了持续性感染。此外,我们表明,R. prolixus 卵巢表达 22 核苷酸病毒 siRNAs(vsiRNAs),但不表达病毒 piRNAs,这些 siRNAs 源自 RpVs 复制过程中 dsRNA 中间体的加工。有趣的是,Permutotetraviruses 和 sobemoviruses 共享 vsiRNAs 池,这可能为交叉免疫系统提供基础。vsiRNAs 由母体沉积在卵子中,它们可能有助于降低病毒载量并保护发育中的胚胎。我们的研究结果首次揭示了 R. prolixus 中的复杂核心病毒组,并开始揭示三化螟中的 RNAi 抗病毒防御机制。