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Research Article

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

Danyil Grybchuk, Natalia S. Akopyants, Alexei Y. Kostygov, Aleksandras Konovalovas, Lon-Fye Lye, Deborah E. Dobson, Haroun Zangger, Nicolas Fasel, Anzhelika Butenko, Alexander O. Frolov, Jan Votýpka, Claudia M. d’Avila-Levy, Pavel Kulich, Jana Moravcová, Pavel Plevka, Igor B. Rogozin, View ORCID ProfileSaulius Serva, Julius Lukeš, View ORCID ProfileStephen M. Beverley, and Vyacheslav Yurchenko
  1. aLife Science Research Centre, Faculty of Science, University of Ostrava, 710 00 Ostrava, Czech Republic;
  2. bDepartment of Molecular Microbiology, Washington University School of Medicine, Saint Louis, MO 63110;
  3. cZoological Institute of the Russian Academy of Sciences, St. Petersburg, 199034, Russia;
  4. dDepartment of Biochemistry and Molecular Biology, Institute of Biosciences, Life Sciences Center, Vilnius University, Vilnius 10257, Lithuania;
  5. eDepartment of Biochemistry, University of Lausanne, 1066 Epalinges, Switzerland;
  6. fDepartment of Parasitology, Faculty of Science, Charles University, 128 44 Prague, Czech Republic;
  7. gBiology Centre, Institute of Parasitology, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic;
  8. hColeção de Protozoários, Laboratório de Estudos Integrados em Protozoologia, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, 21040-360 Rio de Janeiro, Brazil;
  9. iVeterinary Research Institute, 621 00 Brno, Czech Republic;
  10. jCentral European Institute of Technology – Masaryk University, 625 00 Brno, Czech Republic;
  11. kNational Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894;
  12. lDepartment of Chemistry and Bioengineering, Faculty of Fundamental Sciences, Vilnius Gediminas Technical University, Vilnius 10223, Lithuania;
  13. mUniversity of South Bohemia, Faculty of Sciences, 370 05 České Budějovice, Czech Republic;
  14. nInstitute of Environmental Technologies, Faculty of Science, University of Ostrava, 710 00 Ostrava, Czech Republic

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PNAS January 16, 2018 115 (3) E506-E515; first published December 28, 2017; https://doi.org/10.1073/pnas.1717806115
Danyil Grybchuk
aLife Science Research Centre, Faculty of Science, University of Ostrava, 710 00 Ostrava, Czech Republic;
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Natalia S. Akopyants
bDepartment of Molecular Microbiology, Washington University School of Medicine, Saint Louis, MO 63110;
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Alexei Y. Kostygov
aLife Science Research Centre, Faculty of Science, University of Ostrava, 710 00 Ostrava, Czech Republic;
cZoological Institute of the Russian Academy of Sciences, St. Petersburg, 199034, Russia;
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Aleksandras Konovalovas
dDepartment of Biochemistry and Molecular Biology, Institute of Biosciences, Life Sciences Center, Vilnius University, Vilnius 10257, Lithuania;
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Lon-Fye Lye
bDepartment of Molecular Microbiology, Washington University School of Medicine, Saint Louis, MO 63110;
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Deborah E. Dobson
bDepartment of Molecular Microbiology, Washington University School of Medicine, Saint Louis, MO 63110;
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Haroun Zangger
eDepartment of Biochemistry, University of Lausanne, 1066 Epalinges, Switzerland;
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Nicolas Fasel
eDepartment of Biochemistry, University of Lausanne, 1066 Epalinges, Switzerland;
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Anzhelika Butenko
aLife Science Research Centre, Faculty of Science, University of Ostrava, 710 00 Ostrava, Czech Republic;
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Alexander O. Frolov
cZoological Institute of the Russian Academy of Sciences, St. Petersburg, 199034, Russia;
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Jan Votýpka
fDepartment of Parasitology, Faculty of Science, Charles University, 128 44 Prague, Czech Republic;
gBiology Centre, Institute of Parasitology, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic;
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Claudia M. d’Avila-Levy
hColeção de Protozoários, Laboratório de Estudos Integrados em Protozoologia, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, 21040-360 Rio de Janeiro, Brazil;
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Pavel Kulich
iVeterinary Research Institute, 621 00 Brno, Czech Republic;
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Jana Moravcová
jCentral European Institute of Technology – Masaryk University, 625 00 Brno, Czech Republic;
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Pavel Plevka
jCentral European Institute of Technology – Masaryk University, 625 00 Brno, Czech Republic;
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Igor B. Rogozin
kNational Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894;
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Saulius Serva
dDepartment of Biochemistry and Molecular Biology, Institute of Biosciences, Life Sciences Center, Vilnius University, Vilnius 10257, Lithuania;
lDepartment of Chemistry and Bioengineering, Faculty of Fundamental Sciences, Vilnius Gediminas Technical University, Vilnius 10223, Lithuania;
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  • ORCID record for Saulius Serva
Julius Lukeš
gBiology Centre, Institute of Parasitology, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic;
mUniversity of South Bohemia, Faculty of Sciences, 370 05 České Budějovice, Czech Republic;
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Stephen M. Beverley
bDepartment of Molecular Microbiology, Washington University School of Medicine, Saint Louis, MO 63110;
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  • For correspondence: stephen.beverley@wustl.edu vyacheslav.yurchenko@osu.cz
Vyacheslav Yurchenko
aLife Science Research Centre, Faculty of Science, University of Ostrava, 710 00 Ostrava, Czech Republic;
gBiology Centre, Institute of Parasitology, Czech Academy of Sciences, 370 05 České Budějovice, Czech Republic;
nInstitute of Environmental Technologies, Faculty of Science, University of Ostrava, 710 00 Ostrava, Czech Republic
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  • For correspondence: stephen.beverley@wustl.edu vyacheslav.yurchenko@osu.cz
  1. Contributed by Stephen M. Beverley, November 26, 2017 (sent for review October 11, 2017; reviewed by Said A. Ghabrial, Max L. Nibert, and Larry Simpson)

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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.

  • Trypanosomatidae
  • Bunyavirales
  • persistent virus infection
  • coinfection
  • coevolution

Footnotes

  • ↵1N.S.A. and A.Y.K. contributed equally to this work.

  • ↵2S.M.B. and V.Y. contributed equally to this work.

  • ↵3To whom correspondence may be addressed. Email: stephen.beverley{at}wustl.edu or vyacheslav.yurchenko{at}osu.cz.
  • Author contributions: D.G., N.S.A., A.Y.K., N.F., P.P., S.S., S.M.B., and V.Y. designed research; D.G., N.S.A., A.Y.K., A.K., L.-F.L., D.E.D., H.Z., P.K., and J.M. performed research; A.O.F., J.V., C.M.d.-L., and J.L. contributed new reagents/analytic tools; D.G., N.S.A., A.Y.K., A.B., I.B.R., S.M.B., and V.Y. analyzed data; and D.G., A.Y.K., S.M.B., and V.Y. wrote the paper.

  • Reviewers: S.A.G., University of Kentucky; M.L.N., Harvard Medical School; and L.S., University of California, Los Angeles.

  • The authors declare no conflict of interest.

  • Data deposition: The deposition and accession numbers for the sequences reported in this work are summarized in Table S3. Metatranscriptomic contigs assembled from single-read archive depositions, which cannot be deposited in GenBank because they have not been experimentally verified, are listed in Table S4.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1717806115/-/DCSupplemental.

Published under the PNAS license.

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Viral discovery in trypanosomatids
Danyil Grybchuk, Natalia S. Akopyants, Alexei Y. Kostygov, Aleksandras Konovalovas, Lon-Fye Lye, Deborah E. Dobson, Haroun Zangger, Nicolas Fasel, Anzhelika Butenko, Alexander O. Frolov, Jan Votýpka, Claudia M. d’Avila-Levy, Pavel Kulich, Jana Moravcová, Pavel Plevka, Igor B. Rogozin, Saulius Serva, Julius Lukeš, Stephen M. Beverley, Vyacheslav Yurchenko
Proceedings of the National Academy of Sciences Jan 2018, 115 (3) E506-E515; DOI: 10.1073/pnas.1717806115

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Viral discovery in trypanosomatids
Danyil Grybchuk, Natalia S. Akopyants, Alexei Y. Kostygov, Aleksandras Konovalovas, Lon-Fye Lye, Deborah E. Dobson, Haroun Zangger, Nicolas Fasel, Anzhelika Butenko, Alexander O. Frolov, Jan Votýpka, Claudia M. d’Avila-Levy, Pavel Kulich, Jana Moravcová, Pavel Plevka, Igor B. Rogozin, Saulius Serva, Julius Lukeš, Stephen M. Beverley, Vyacheslav Yurchenko
Proceedings of the National Academy of Sciences Jan 2018, 115 (3) E506-E515; DOI: 10.1073/pnas.1717806115
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