Evolution of RNA viruses in trypanosomatids: new insights from the analysis of Sauroleishmania

. 2023 Oct ; 122 (10) : 2279-2286. [epub] 20230725

Jazyk angličtina Země Německo Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37490143
Odkazy

PubMed 37490143
PubMed Central PMC10495512
DOI 10.1007/s00436-023-07928-x
PII: 10.1007/s00436-023-07928-x
Knihovny.cz E-zdroje

RNA viruses play an important role in Leishmania biology and virulence. Their presence was documented in three (out of four) Leishmania subgenera. Sauroleishmania of reptiles remained the only underinvestigated group. In this work, we analyzed the viral occurrence in Sauroleishmania spp. and detected RNA viruses in three out of seven isolates under study. These viruses were of two families-Narnaviridae and Totiviridae. Phylogenetic inferences demonstrated that totiviruses from L. adleri and L. tarentolae group together within a larger cluster of LRV2s, while a narnavirus of L. gymnodactyli appeared as a phylogenetic relative of narnaviruses of Blechomonas spp. Taken together, our work not only expanded the range of trypanosomatids that can host RNA viruses but also shed new light on the evolution and potential routes of viral transmission in these flagellates.

Zobrazit více v PubMed

Adler S. The behaviour of a lizard Leishmania in hamsters and baby mice. Rev Inst Med Trop Sao Paulo. 1962;4:61–64. PubMed

Akhoundi M, et al. A historical overview of the classification, evolution, and dispersion of Leishmania parasites and sandflies. PLoS Negl Trop Dis. 2016;10(3):e0004349. doi: 10.1371/journal.pntd.0004349. PubMed DOI PMC

Akopyants NS, et al. Demonstration of genetic exchange during cyclical development of Leishmania in the sand fly vector. Science. 2009;324(5924):265–268. doi: 10.1126/science.1169464. PubMed DOI PMC

Atayde VD, et al. Exploitation of the Leishmania exosomal pathway by Leishmania RNA virus 1. Nat Microbiol. 2019;4:714–723. doi: 10.1038/s41564-018-0352-y. PubMed DOI

Belova EM. Reptiles and their importance in the epidemiology of leishmaniasis. Bull World Health Organ. 1971;44(4):553–560. PubMed PMC

Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC

Breitling R, et al. Non-pathogenic trypanosomatid protozoa as a platform for protein research and production. Protein Expr Purif. 2002;25(2):209–218. doi: 10.1016/S1046-5928(02)00001-3. PubMed DOI

Bruschi F, Gradoni L. The leishmaniases: old neglected tropical diseases. Cham, Switzerland: Springer; 2018.

Buchfink B, Reuter K, Drost HG. Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat Methods. 2021;18(4):366–368. doi: 10.1038/s41592-021-01101-x. PubMed DOI PMC

Camacho C, et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009;10:421. doi: 10.1186/1471-2105-10-421. PubMed DOI PMC

Cantanhêde LM, et al. The maze pathway of coevolution: a critical review over the Leishmania and its endosymbiotic history. Genes. 2021;12(5):657. doi: 10.3390/genes12050657. PubMed DOI PMC

Capella-Gutiérrez S, Silla-Martinez JM, Gabaldon T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25(15):1972–1973. doi: 10.1093/bioinformatics/btp348. PubMed DOI PMC

Coughlan S, Mulhair P, Sanders M, Schönian G, Cotton JA, Downing T. The genome of Leishmania adleri from a mammalian host highlights chromosome fission in Sauroleishmania. Sci Rep. 2017;7:43747. doi: 10.1038/srep43747. PubMed DOI PMC

Danecek P, et al. Twelve years of SAMtools and BCFtools. Gigascience. 2021;10(2):1–4. doi: 10.1093/gigascience/giab008. PubMed DOI PMC

das Chagas BD, et al. Interspecies and intrastrain interplay among Leishmania spp. parasites. Microorganisms. 2022;10(10):1883. doi: 10.3390/microorganisms10101883. PubMed DOI PMC

de Carvalho RVH, et al. Leishmania RNA virus exacerbates leishmaniasis by subverting innate immunity via TLR3-mediated NLRP3 inflammasome inhibition. Nat Commun. 2019;10(1):5273. doi: 10.1038/s41467-019-13356-2. PubMed DOI PMC

Di Muccio T, et al. Epidemiology of imported leishmaniasis in Italy: implications for a European endemic country. PLoS One. 2015;10(6):e0129418. doi: 10.1371/journal.pone.0129418. PubMed DOI PMC

Eren RO, et al. Mammalian innate immune response to a Leishmania-resident RNA virus increases macrophage survival to promote parasite persistence. Cell Host Microbe. 2016;20(3):318–328. doi: 10.1016/j.chom.2016.08.001. PubMed DOI PMC

Espinosa OA, Serrano MG, Camargo EP, Teixeira MMG, Shaw JJ. An appraisal of the taxonomy and nomenclature of trypanosomatids presently classified as Leishmania and Endotrypanum. Parasitology. 2018;145(4):430–442. doi: 10.1017/S0031182016002092. PubMed DOI

Grybchuk D, et al. Viral discovery and diversity in trypanosomatid protozoa with a focus on relatives of the human parasite Leishmania. Proc Natl Acad Sci U S A. 2018;115(3):E506–E515. doi: 10.1073/pnas.1717806115. PubMed DOI PMC

Grybchuk D, Kostygov AY, Macedo DH, d'Avila-Levy CM, Yurchenko V. RNA viruses in trypanosomatid parasites: a historical overview. Mem Inst Oswaldo Cruz. 2018;113(4):e170487. doi: 10.1590/0074-02760170487. PubMed DOI PMC

Grybchuk D, Kostygov AY, Macedo DH, Votýpka J, Lukeš J, Yurchenko V. RNA viruses in Blechomonas (Trypanosomatidae) and evolution of Leishmaniavirus. mBio. 2018;9(5):e01932–e01918. doi: 10.1128/mBio.01932-18. PubMed DOI PMC

Grybchuk D, et al. The first non-LRV RNA virus in Leishmania. Viruses. 2020;12(2):168. doi: 10.3390/v12020168. PubMed DOI PMC

Haas BJ, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013;8(8):1494–1512. doi: 10.1038/nprot.2013.084. PubMed DOI PMC

Hajjaran H, et al. Detection and molecular identification of Leishmania RNA virus (LRV) in Iranian Leishmania species. Arch Virol. 2016;161(12):3385–3390. doi: 10.1007/s00705-016-3044-z. PubMed DOI

Heisch RB. On Leishmania adleri sp. nov. from lacertid lizards (Latastia sp.) in Kenya. Ann Trop Med Parasitol. 1958;52(1):68–71. doi: 10.1080/00034983.1958.11685846. PubMed DOI

Ives A, et al. Leishmania RNA virus controls the severity of mucocutaneous leishmaniasis. Science. 2011;331(6018):775–778. doi: 10.1126/science.1199326. PubMed DOI PMC

Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC

Killick-Kendrick R. Phlebotomine vectors of the leishmaniases: a review. Med Vet Entomol. 1990;4(1):1–24. doi: 10.1111/j.1365-2915.1990.tb00255.x. PubMed DOI

Klatt S, Simpson L, Maslov DA, Konthur Z. Leishmania tarentolae: taxonomic classification and its application as a promising biotechnological expression host. PLoS Negl Trop Dis. 2019;13(7):e0007424. doi: 10.1371/journal.pntd.0007424. PubMed DOI PMC

Kleschenko Y, et al. Molecular characterization of Leishmania RNA virus 2 in Leishmania major from Uzbekistan. Genes. 2019;10:e830. doi: 10.3390/genes10100830. PubMed DOI PMC

Koonin EV, Dolja VV, Krupovic M. Origins and evolution of viruses of eukaryotes: the ultimate modularity. Virology. 2015;479-480:2–25. doi: 10.1016/j.virol.2015.02.039. PubMed DOI PMC

Kostygov AY, et al. Analyses of Leishmania-LRV co-phylogenetic patterns and evolutionary variability of viral proteins. Viruses. 2021;13:2305. doi: 10.3390/v13112305. PubMed DOI PMC

Kostygov AY, et al. Euglenozoa: taxonomy, diversity and ecology, symbioses and viruses. Open Biol. 2021;11:200407. doi: 10.1098/rsob.200407. PubMed DOI PMC

Kraeva N, et al. Leptomonas seymouri: adaptations to the dixenous life cycle analyzed by genome sequencing, transcriptome profiling and co-infection with Leishmania donovani. PLoS Pathog. 2015;11(8):e1005127. doi: 10.1371/journal.ppat.1005127. PubMed DOI PMC

Lafleur A, Olivier M. Viral endosymbiotic infection of protozoan parasites: how it influences the development of cutaneous leishmaniasis. PLoS Pathog. 2022;18(11):e1010910. doi: 10.1371/journal.ppat.1010910. PubMed DOI PMC

Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357–359. doi: 10.1038/nmeth.1923. PubMed DOI PMC

Latrofa MS, Mendoza-Roldan JA, Manoj R, Dantas-Torres F, Otranto D. A duplex real-time PCR assay for the detection and differentiation of Leishmania infantum and Leishmania tarentolae in vectors and potential reservoir hosts. Entomol Gen. 2021;41(5):543–551. doi: 10.1127/entomologia/2021/1178. DOI

Lukeš J, Butenko A, Hashimi H, Maslov DA, Votýpka J, Yurchenko V. Trypanosomatids are much more than just trypanosomes: clues from the expanded family tree. Trends Parasitol. 2018;34(6):466–480. doi: 10.1016/j.pt.2018.03.002. PubMed DOI

Lye LF, Akopyants NS, Dobson DE, Beverley SM. A Narnavirus-like element from the trypanosomatid protozoan parasite Leptomonas seymouri. Genome Announc. 2016;4(4):e00713–e00716. doi: 10.1128/genomeA.00713-16. PubMed DOI PMC

McMillan B. Leishmaniasis in the Sudan Republic. 22. Leishmania hoogstraali sp. n. in the gecko. J Parasitol. 1965;51(3):336–339. doi: 10.2307/3275947. PubMed DOI

Mendoza-Roldan JA, et al. Leishmania tarentolae: a new frontier in the epidemiology and control of the leishmaniases. Transbound Emerg Dis. 2022;69(5):e1326–e1337. doi: 10.1111/tbed.14660. PubMed DOI PMC

Mendoza-Roldan JA, et al. Leishmania (Sauroleishmania) tarentolae isolation and sympatric occurrence with Leishmania (Leishmania) infantum in geckoes, dogs and sand flies. PLoS Negl Trop Dis. 2022;16(8):e0010650. doi: 10.1371/journal.pntd.0010650. PubMed DOI PMC

Minh BQ, et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020;37(5):1530–1534. doi: 10.1093/molbev/msaa015. PubMed DOI PMC

Mirdita M, von den Driesch L, Galiez C, Martin MJ, Söding J, Steinegger M. Uniclust databases of clustered and deeply annotated protein sequences and alignments. Nucleic Acids Res. 2017;45(D1):D170–D176. doi: 10.1093/nar/gkw1081. PubMed DOI PMC

Nalçacı M, et al. Detection of Leishmania RNA virus 2 in Leishmania species from Turkey. Trans R Soc Trop Med Hyg. 2019;113(7):410–417. doi: 10.1093/trstmh/trz023. PubMed DOI

Olivier M, Zamboni DS. Leishmania (Viannia) guyanensis, LRV1 virus and extracellular vesicles: a dangerous trio influencing the faith of immune response during muco-cutaneous leishmaniasis. Curr Opin Immunol. 2020;66:108–113. doi: 10.1016/j.coi.2020.08.004. PubMed DOI

Polanská N, et al. Sergentomyia schwetzi: salivary gland transcriptome, proteome and enzymatic activities in two lineages adapted to different blood sources. PLoS One. 2020;15(3):e0230537. doi: 10.1371/journal.pone.0230537. PubMed DOI PMC

Pombi M, et al. Molecular detection of Leishmania (Sauroleishmania) tarentolae in human blood and Leishmania (Leishmania) infantum in Sergentomyia minuta: unexpected host-parasite contacts. Med Vet Entomol. 2020;34(4):470–475. doi: 10.1111/mve.12464. PubMed DOI

Pozio E, Gramiccia M, Gradoni L, Maroli M. Hemoflagellates in Cyrtodactylus kotschyi (Steindachner, 1870) (Reptilia, Gekkonidae) in Italy. Acta Trop. 1983;40(4):399–400. PubMed

Pozio E, Gramiccia M, Gradoni L, Maroli M. Hémoflagellés de Tarentola mauritanica L., 1758 (Reptilia, Gekkonidae) In: Rioux JA, editor. Leishmania Taxonomie et phylogenèse. Montpellier: IMEEE; 1986. pp. 149–155.

Procházková M, et al. Capsid structure of Leishmania RNA Virus 1. J Virol. 2021;95(3):e01957–e01920. doi: 10.1128/JVI.01957-20. PubMed DOI PMC

Quinlan AR. BEDTools: the Swiss-army tool for genome feature analysis. Curr Protoc Bioinformatics. 2014;47:11.12.1–11.12.34. doi: 10.1002/0471250953.bi1112s47. PubMed DOI PMC

Ranque P. Etude morphologique et biologique de quelques Trypanosomatides récoltés au Sénégal. Ph.D. thesis, Université de Aix-Marseilles; 1973.

Ronquist F, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61(3):539–542. doi: 10.1093/sysbio/sys029. PubMed DOI PMC

Rougeron V, De Meeûs T, Kako Ouraga S, Hide M, Bañuls AL. "Everything you always wanted to know about sex (but were afraid to ask)" in Leishmania after two decades of laboratory and field analyses. PLoS Pathog. 2010;6(8):e1001004. doi: 10.1371/journal.ppat.1001004. PubMed DOI PMC

Saberi R, et al. Presence and diversity of Leishmania RNA virus in an old zoonotic cutaneous leishmaniasis focus, northeastern Iran: haplotype and phylogenetic based approach. Int J Infect Dis. 2020;101:6–13. doi: 10.1016/j.ijid.2020.08.033. PubMed DOI

Sadiq S, Chen YM, Zhang YZ, Holmes EC. Resolving deep evolutionary relationships within the RNA virus phylum Lenarviricota. Virus Evol. 2022;8(1):veac055. doi: 10.1093/ve/veac055. PubMed DOI PMC

Sádlová J, et al. Visualisation of Leishmania donovani fluorescent hybrids during early stage development in the sand fly vector. PLoS One. 2011;6(5):e19851. doi: 10.1371/journal.pone.0019851. PubMed DOI PMC

Saf'janova VM. Serological comparison of leptomonad strains isolated from sandflies with Leishmania tropica and leptomonads of reptiles. Med Parazitol (Mosk) 1966;6:686–695.

Saf'janova VM. Phlebotominae sandflies as the key link of Leishmania parasitic systems. Parassitologia. 1991;33:505–511. PubMed

Saf'janova VM, Alekseev AN, Karapet'ian AB. The fate of the promastigotes of Leishmania tropica major and L. gymnodactyli in the body of Phlebotomus papatasi under conditions of a mixed infection. Parazitologiia. 1976;10(1):78–83. PubMed

Saura A, et al. Elimination of LRVs elicits different responses in Leishmania spp. mSphere. 2022;7(4):e0033522. doi: 10.1128/msphere.00335-22. PubMed DOI PMC

Scheffter SM, Ro YT, Chung IK, Patterson JL. The complete sequence of Leishmania RNA virus LRV2-1, a virus of an Old World parasite strain. Virology. 1995;212(1):84–90. doi: 10.1006/viro.1995.1456. PubMed DOI

Stuart KD, Weeks R, Guilbride L, Myler PJ. Molecular organization of Leishmania RNA virus 1. Proc Natl Acad Sci U S A. 1992;89(18):8596–8600. doi: 10.1073/pnas.89.18.8596. PubMed DOI PMC

Tichá L, Kykalová B, Sádlová J, Gramiccia M, Gradoni L, Volf P. Development of various Leishmania (Sauroleishmania) tarentolae strains in three Phlebotomus species. Microorganisms. 2021;9(11):2256. doi: 10.3390/microorganisms9112256. PubMed DOI PMC

Tichá L, Sádlová J, Bates P, Volf P. Experimental infections of sand flies and geckos with Leishmania (Sauroleishmania) adleri and Leishmania (S.) hoogstraali. Parasit Vectors. 2022;15(1):289. doi: 10.1186/s13071-022-05417-1. PubMed DOI PMC

Tichá L, et al. Experimental feeding of Sergentomyia minuta on reptiles and mammals: comparison with Phlebotomus papatasi. Parasit Vectors. 2023;16(1):126. doi: 10.1186/s13071-023-05758-5. PubMed DOI PMC

Wenyon CM. Observations on the intestinal protozoa of three Egyptian lizards, with a note on a cell-invading fungus. Parasitology. 1920;12(4):350–365. doi: 10.1017/S0031182000014347. DOI

WHO (2023) Leishmaniasis. https://www.who.int/en/news-room/fact-sheets/detail/leishmaniasis. Accessed 1 Jun 2023

Widmer G, Dooley S. Phylogenetic analysis of Leishmania RNA virus and Leishmania suggests ancient virus-parasite association. Nucleic Acids Res. 1995;23(12):2300–2304. doi: 10.1093/nar/23.12.2300. PubMed DOI PMC

Wilson V, Southgate B. Lizard Leishmania. In: Lumsden W, Evans DA, editors. Biology of Kinetoplastida. New York: Academic Press; 1979. pp. 242–268.

Wolf YI, et al. Origins and evolution of the global RNA virome. mBio. 2018;9(6):e02329–e02318. doi: 10.1128/mBio.02329-18. PubMed DOI PMC

Yurchenko V, Chistyakov DS, Akhmadishina LV, Lukashev AN, Sádlová J, Strelkova MV. Revisiting epidemiology of leishmaniasis in Central Asia: lessons learnt. Parasitology. 2023;150(2):129–136. doi: 10.1017/S0031182022001640. PubMed DOI PMC

Yurchenko V, Lukeš J, Xu X, Maslov DA. An integrated morphological and molecular approach to a new species description in the Trypanosomatidae: the case of Leptomonas podlipaevi n. sp., a parasite of Boisea rubrolineata (Hemiptera: Rhopalidae) J Eukaryot Microbiol. 2006;53(2):103–111. doi: 10.1111/j.1550-7408.2005.00078.x. PubMed DOI

Zakharova A, et al. Leishmania guyanensis M4147 as a new LRV1-bearing model parasite: phosphatidate phosphatase 2-like protein controls cell cycle progression and intracellular lipid content. PLoS Negl Trop Dis. 2022;16(6):e0010510. doi: 10.1371/journal.pntd.0010510. PubMed DOI PMC

Zangger H, et al. Leishmania aethiopica field isolates bearing an endosymbiontic dsRNA virus induce pro-inflammatory cytokine response. PLoS Negl Trop Dis. 2014;8(4):e2836. doi: 10.1371/journal.pntd.0002836. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...