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 PhytomonasLeptomonas 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.

Biology Centre Institute of Parasitology Czech Academy of Sciences 370 05 České Budějovice Czech Republic

Central European Institute of Technology Masaryk University 625 00 Brno Czech Republic

Coleção de Protozoários Laboratório de Estudos Integrados em Protozoologia Instituto Oswaldo Cruz Fundação Oswaldo Cruz 21040 360 Rio de Janeiro Brazil

Department of Biochemistry and Molecular Biology Institute of Biosciences Life Sciences Center Vilnius University Vilnius 10257 Lithuania

Department of Biochemistry University of Lausanne 1066 Epalinges Switzerland

Department of Chemistry and Bioengineering Faculty of Fundamental Sciences Vilnius Gediminas Technical University Vilnius 10223 Lithuania

Department of Molecular Microbiology Washington University School of Medicine Saint Louis MO 63110

Department of Molecular Microbiology Washington University School of Medicine Saint Louis MO 63110;

Department of Parasitology Faculty of Science Charles University 128 44 Prague Czech Republic

Institute of Environmental Technologies Faculty of Science University of Ostrava 710 00 Ostrava Czech Republic

Life Science Research Centre Faculty of Science University of Ostrava 710 00 Ostrava Czech Republic

Life Science Research Centre Faculty of Science University of Ostrava 710 00 Ostrava Czech Republic;

National Center for Biotechnology Information National Library of Medicine National Institutes of Health Bethesda MD 20894

University of South Bohemia Faculty of Sciences 370 05 České Budějovice Czech Republic

Veterinary Research Institute 621 00 Brno Czech Republic

Zoological Institute of the Russian Academy of Sciences St Petersburg 199034 Russia

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