Viral discovery and diversity in trypanosomatid protozoa with a focus on relatives of the human parasite Leishmania

Abstract

Knowledge of viral diversity is expanding greatly, but many lineages remain underexplored. We surveyed RNA viruses in 52 cultured monoxenous relatives of the human parasite ( and ), as well as plant-infecting was a hotbed for viral discovery, carrying a virus (Leptomonas pyrrhocoris ostravirus 1) with a highly divergent RNA-dependent RNA polymerase missed by conventional BLAST searches, an emergent clade of tombus-like viruses, and an example of viral endogenization. A deep-branching clade of trypanosomatid narnaviruses was found, notable as bearing Narna-like virus 1 (LepseyNLV1) have been reported in cultures recovered from patients with visceral leishmaniasis. A deep-branching trypanosomatid viral lineage showing strong affinities to bunyaviruses was termed "" (LBV) and judged sufficiently distinct to warrant assignment within a proposed family termed "" Numerous relatives of trypanosomatid viruses were found in insect metatranscriptomic surveys, which likely arise from trypanosomatid microbiota. Despite extensive sampling we found no relatives of the totivirus (LRV1/2), implying that it was acquired at about the same time the became able to parasitize vertebrates. As viruses were found in over a quarter of isolates tested, many more are likely to be found in the >600 unsurveyed trypanosomatid species. Viral loss was occasionally observed in culture, providing potentially isogenic virus-free lines enabling studies probing the biological role of trypanosomatid viruses. These data shed important insights on the emergence of viruses within an important trypanosomatid clade relevant to human disease.

Origins and Evolution of the Global RNA Virome

“…Instead, branches 4 and 5 are separate and positioned deep in the tree, immediately above the split between branch 1 and the rest of the RdRps. Given the poor resolution of the RAxML tree and a strong biological argument, namely, the absence of identified ϪRNA viruses in prokaryotes or protists (with the exception of the "leishbuviruses" infecting kinetoplastids [49,50]; see also Discussion below), we believe that the tree topology presented in Fig. 1 carries more credence than that shown in Data Set S3B.…”

“…However, the pronounced similarity between the three-dimensional (3D) structures of the RdRps of ϪRNA influenza virus A and bacteriophage 6 dsRNA cystovirus (35) is compatible with our findings. Further, because virtually no ϪRNA viruses are known in prokaryotes or unicellular eukaryotes (with the single exception of the "leischbuviruses" in parasitic trypanosomatids [50], which were likely acquired from the animal hosts of these protists), their later origin from a preexisting group of ϩRNA or dsRNA viruses appears most likely.…”

“…Certainly, much caution is due in the interpretation of host range assignments from metaviromics, especially those resulting from holobiont studies. Viruses identified in holobiont samples of (for example) invertebrates could actually infect protists associated with these animals (50) or could represent contamination from fungal or plant or even prokaryotic sources. These uncertainties notwithstanding, the extensive diversity of hosts even within small branches of the RdRp tree is undeniable.…”

“…In land plants, RNA viruses, particularly those of branch 3, dramatically expanded, perhaps in part because of the exclusion of competing large DNA viruses. Finally, it seems plausible that, given the high prevalence of ϪRNA viruses in metazoa and their virtual absence in protists (with the exception of the recently discovered "leishbuviruses" that likely invaded their parasitic protist hosts via HVT from an animal host [49,50]), the viruses that comprise RdRp branch 5 evolved in animals via mixing and matching genes from reovirus-like and flavivirus-like ancestors.…”

Global status of synchronizing Leishmania RNA virus in Leishmania parasites: A systematic review with meta‐analysis

“…In addition to Leishmania species, in recent years, evidence showed that the RNAviruses are present in the genera Crithidia and Leptomonas (subfamily Leishmaniinae), as well as Phytomonas spp. (Grybchuk et al, ). According to the results of the included articles, the pooled global prevalence of LRVs in Leishmania spp.…”