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

Significance

Largely overlooked, the viruses of protists have started to attract more attention. Several viruses of the family Totiviridae are currently implicated in the increased pathogenicity of parasitic protozoa such as Leishmania to vertebrate hosts. We conducted a broad survey of RNA viruses within trypanosomatids, one of the iconic groups of protists. These revealed several previously unidentified viral taxa including one designated “ Leishbunyaviridae” and a highly divergent virus termed “Leptomonas pyrrhocoris ostravirus 1.” Our studies provide important information on the origins as well as the diversity and distribution of viruses within a group of protists related to 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 Leishmania ( Crithidia and Leptomonas), as well as plant-infecting Phytomonas. Leptomonas pyrrhocoris 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 Leptomonas seymouri 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 “ Leishbunyavirus” (LBV) and judged sufficiently distinct to warrant assignment within a proposed family termed “ Leishbunyaviridae.” 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 Leishmaniavirus (LRV1/2), implying that it was acquired at about the same time the Leishmania 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.