A novel strain of Leishmania braziliensis harbors not a toti- but a bunyavirus
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
39729426
PubMed Central
PMC11717295
DOI
10.1371/journal.pntd.0012767
PII: PNTD-D-24-01390
Knihovny.cz E-zdroje
- MeSH
- Bunyaviridae klasifikace genetika izolace a purifikace MeSH
- fylogeneze MeSH
- Leishmania braziliensis * genetika izolace a purifikace MeSH
- lidé MeSH
- Orthobunyavirus genetika klasifikace izolace a purifikace fyziologie MeSH
- RNA-viry genetika klasifikace izolace a purifikace MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
Leishmania is a genus of the family Trypanosomatidae that unites obligatory parasitic flagellates causing a variety of vector-borne diseases collectively called leishmaniasis. The symptoms range from relatively innocuous skin lesions to complete failures of visceral organs. The disease is exacerbated if a parasite harbors Leishmania RNA viruses (LRVs) of the family Pseudototiviridae. Screening a novel isolate of L. braziliensis, we revealed that it possesses not a toti-, but a bunyavirus of the family Leishbuviridae. To the best of our knowledge, this is a very first discovery of a bunyavirus infecting a representative of the Leishmania subgenus Viannia. We suggest that these viruses may serve as potential factors of virulence in American leishmaniasis and encourage researchers to test leishmanial strains for the presence of not only LRVs, but also other RNA viruses.
Central European Institute of Technology Masaryk University Brno Czechia
Department of Biomedical Sciences Institute of Tropical Medicine Antwerp Belgium
Department of Biomedical Sciences University of Antwerp Antwerp Belgium
Department of Infectious Diseases Regional Hospital Liberec Liberec Czechia
Department of Parasitology Faculty of Science Charles University Prague Czechia
Faculty of Biology Lomonosov Moscow State University Moscow Russia
Life Science Research Centre Faculty of Science University of Ostrava Ostrava Czechia
Zoological Institute of the Russian Academy of Sciences St Petersburg Russia
Zobrazit více v PubMed
Kostygov AY, Karnkowska A, Votýpka J, Tashyreva D, Maciszewski K, Yurchenko V, Lukeš J Euglenozoa: taxonomy, diversity and ecology, symbioses and viruses. Open Biol. 2021;11: 200407. doi: 10.1098/rsob.200407 PubMed DOI PMC
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: 466–480. doi: 10.1016/j.pt.2018.03.002 PubMed DOI
Frolov AO, Kostygov AY, Yurchenko V Development of monoxenous trypanosomatids and phytomonads in insects. Trends Parasitol. 2021;37: 538–551. doi: 10.1016/j.pt.2021.02.004 PubMed DOI
McGhee RB, Cosgrove WB Biology and physiology of the lower Trypanosomatidae. Microbiol Rev. 1980;44: 140–173. doi: 10.1128/mr.44.1.140-173.1980 PubMed DOI PMC
Kostygov AY, Albanaz ATS, Butenko A, Gerasimov ES, Lukeš J, Yurchenko V Phylogenetic framework to explore trait evolution in Trypanosomatidae. Trends Parasitol. 2024;40: 96–99. doi: 10.1016/j.pt.2023.11.009 PubMed DOI
Kostygov AY, Yurchenko V Revised classification of the subfamily Leishmaniinae (Trypanosomatidae). Folia Parasitol 2017;64: 020. doi: 10.14411/fp.2017.020 PubMed DOI
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: 430–442. PubMed
WHO (2024) Leishmaniasis. https://www.who.int/en/news-room/fact-sheets/detail/leishmaniasis.
Bruschi F, Gradoni L (2018) The leishmaniases: old neglected tropical diseases. Cham, Switzerland: Springer. 245 pp. p.
Zakharova A, Albanaz ATS, Opperdoes FR, Škodová-Sveráková I, Zagirova D, Saura 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: e0010510. PubMed 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. PubMed PMC
Peacock CS, Seeger K, Harris D, Murphy L, Ruiz JC, Quail MA, et al.. Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat Genet. 2007;39: 839–847. PubMed PMC
Imamura H, Monsieurs P, Jara M, Sanders M, Maes I, Vanaerschot M, et al.. Evaluation of whole genome amplification and bioinformatic methods for the characterization of Leishmania genomes at a single cell level. Sci Rep. 2020;10: 15043. PubMed PMC
Fiebig M, Kelly S, Gluenz E Comparative life cycle transcriptomics revises Leishmania mexicana genome annotation and links a chromosome duplication with parasitism of vertebrates. PLoS Pathog. 2015;11: e1005186. PubMed 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: e170487. doi: 10.1590/0074-02760170487 PubMed DOI PMC
Grybchuk D, Akopyants NS, Kostygov AY, Konovalovas A, Lye LF, Dobson DE, 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: E506–E515. PubMed PMC
Molyneux DH Virus-like particles in Leishmania parasites. Nature. 1974;249: 588–589. PubMed
Lefkowitz EJ, Dempsey DM, Hendrickson RC, Orton RJ, Siddell SG, Smith DB Virus taxonomy: the database of the International Committee on Taxonomy of Viruses (ICTV). Nucleic Acids Res. 2018;46: D708–D717. doi: 10.1093/nar/gkx932 PubMed DOI PMC
Widmer G, Comeau AM, Furlong DB, Wirth DF, Patterson JL Characterization of a RNA virus from the parasite Leishmania. Proc Natl Acad Sci U S A. 1989;86: 5979–5982. PubMed PMC
Weeks R, Aline RF Jr., Myler PJ, Stuart K LRV1 viral particles in Leishmania guyanensis contain double-stranded or single-stranded RNA. J Virol. 1992;66: 1389–1393. PubMed 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: 84–90. PubMed
Ives A, Ronet C, Prevel F, Ruzzante G, Fuertes-Marraco S, Schutz F, et al.. Leishmania RNA virus controls the severity of mucocutaneous leishmaniasis. Science. 2011;331: 775–778. PubMed PMC
Brettmann EA, Shaik JS, Zangger H, Lye LF, Kuhlmann FM, Akopyants NS, et al.. Tilting the balance between RNA interference and replication eradicates Leishmania RNA virus 1 and mitigates the inflammatory response. Proc Natl Acad Sci U S A. 2016;113: 11998–12005. PubMed PMC
Rossi M, Castiglioni P, Hartley MA, Eren RO, Prevel F, Desponds C, et al.. Type I interferons induced by endogenous or exogenous viral infections promote metastasis and relapse of leishmaniasis. Proc Natl Acad Sci U S A. 2017;114: 4987–4992. doi: 10.1073/pnas.1621447114 PubMed DOI PMC
Adaui V, Lye LF, Akopyants NS, Zimic M, Llanos-Cuentas A, Garcia L, et al.. Association of the endobiont double-stranded RNA virus LRV1 with treatment failure for human leishmaniasis caused by Leishmania braziliensis in Peru and Bolivia. J Infect Dis. 2016;213: 112–121. PubMed PMC
Bourreau E, Ginouves M, Prevot G, Hartley MA, Gangneux JP, Robert-Gangneux F, et al.. Presence of Leishmania RNA Virus 1 in Leishmania guyanensis increases the risk of first-line treatment failure and symptomatic relapse. J Infect Dis. 2016;213: 105–111. PubMed
Jha B, Reverte M, Ronet C, Prevel F, Morgenthaler FD, Desponds C, et al.. In and out: Leishmania metastasis by hijacking lymphatic system and migrating immune cells. Front Cell Infect Microbiol. 2022;12: 941860. PubMed PMC
Kostygov AY, Grybchuk D, Kleschenko Y, Chistyakov DS, Lukashev AN, Gerasimov ES, Yurchenko V Analyses of Leishmania-LRV co-phylogenetic patterns and evolutionary variability of viral proteins. Viruses. 2021;13: 2305. PubMed PMC
Rêgo FD, da Silva ES, Lopes VV, Teixeira-Neto RG, Belo VS, Fonseca Júnior AA, et al.. First report of putative Leishmania RNA virus 2 (LRV2) in Leishmania infantum strains from canine and human visceral leishmaniasis cases in the southeast of Brazil. Mem Inst Oswaldo Cruz. 2023;118: e230071. PubMed PMC
Kleschenko Y, Grybchuk D, Matveeva NS, Macedo DH, Ponirovsky EN, Lukashev AN, Yurchenko V Molecular characterization of Leishmania RNA virus 2 in Leishmania major from Uzbekistan. Genes. 2019;10: e830. PubMed PMC
Saberi R, Fakhar M, Hajjaran H, Ataei-Pirkooh A, Mohebali M, Taghipour N, 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. PubMed
Klocek D, Grybchuk D, Tichá L, Votýpka J, Volf P, Kostygov AY, Yurchenko V Evolution of RNA viruses in trypanosomatids: new insights from the analysis of Sauroleishmania. Parasitol Res. 2023;122: 2279–2286. PubMed PMC
Saura A, Zakharova A, Klocek D, Gerasimov ES, Butenko A, Macedo DH, et al.. Elimination of LRVs elicits different responses in Leishmania spp. mSphere. 2022;7: e0033522. PubMed PMC
Saberi R, Fakhar M, Hajjaran H, Abbaszadeh Afshar MJ, Mohebali M, Hezarjaribi HZ, et al.. Leishmania RNA virus 2 (LRV2) exacerbates dermal lesions caused by Leishmania major and comparatively unresponsive to meglumine antimoniate treatment. Exp Parasitol. 2022;241: 108340. PubMed
Mirabedini Z, Mirjalali H, Kazemirad E, Khamesipour A, Samimirad K, Koosha M, et al.. The effects of Leishmania RNA virus 2 (LRV2) on the virulence factors of L. major and pro-inflammatory biomarkers: an in vitro study on human monocyte cell line (THP-1). BMC Microbiol. 2023;23: 398. PubMed PMC
Grybchuk D, Macedo DH, Kleschenko Y, Kraeva N, Lukashev AN, Bates PA, et al.. The first non-LRV RNA virus in Leishmania. Viruses. 2020;12: 168. PubMed PMC
Kuhn JH, Brown K, Adkins S, de la Torre JC, Digiaro M, Ergunay K, et al.. Promotion of order Bunyavirales to class Bunyaviricetes to accommodate a rapidly increasing number of related polyploviricotine viruses. J Virol. 2024: e0106924. PubMed PMC
Macedo DH, Grybchuk D, Režnarová J, Votýpka J, Klocek D, Yurchenko T, et al.. Diversity of RNA viruses in the cosmopolitan monoxenous trypanosomatid Leptomonas pyrrhocoris. BMC Biol. 2023;21: 191. PubMed PMC
Akopyants NS, Lye LF, Dobson DE, Lukeš J, Beverley SM A novel bunyavirus-like virus of trypanosomatid protist parasites. Genome Announc. 2016;4: e00715–00716. doi: 10.1128/genomeA.00715-16 PubMed DOI PMC
Klocek D, Grybchuk D, Macedo DH, Galan A, Votýpka J, Schmid-Hempel R, et al.. RNA viruses of Crithidia bombi, a parasite of bumblebees. J Invertebr Pathol. 2023;201: 107991. PubMed
Grybchuk D, Kostygov AY, Macedo DH, Votýpka J, Lukeš J, Yurchenko V RNA viruses in Blechomonas (Trypanosomatidae) and evolution of Leishmaniavirus. mBio. 2018;9: e01932–01918. PubMed PMC
Kuhn JH, Abe J, Adkins S, Alkhovsky SV, Avšič-Županc T, Ayllón MA, et al.. Annual (2023) taxonomic update of RNA-directed RNA polymerase-encoding negative-sense RNA viruses (realm Riboviria: kingdom Orthornavirae: phylum Negarnaviricota). J Gen Virol. 2023;104: 001864. PubMed PMC
Malet H, Williams HM, Cusack S, Rosenthal M The mechanism of genome replication and transcription in bunyaviruses. PLoS Pathog. 2023;19: e1011060. doi: 10.1371/journal.ppat.1011060 PubMed DOI PMC
Wichgers Schreur PJ, Kormelink R, Kortekaas J Genome packaging of the Bunyavirales. Curr Opin Virol. 2018;33: 151–155. PubMed
Elliott RM Molecular biology of the Bunyaviridae. J Gen Virol. 1990;71: 501–522. PubMed
Barker J, daSilva LLP, Crump CM Mechanisms of bunyavirus morphogenesis and egress. J Gen Virol. 2023;104: 001845. doi: 10.1099/jgv.0.001845 PubMed DOI
Lopez L, Robayo M, Vargas M, Velez ID Thermotherapy. An alternative for the treatment of American cutaneous leishmaniasis. Trials. 2012;13: 58. doi: 10.1186/1745-6215-13-58 PubMed DOI PMC
Ishemgulova A, Kraeva N, Hlaváčová J, Zimmer SL, Butenko A, Podešvová L, et al.. A putative ATP/GTP binding protein affects Leishmania mexicana growth in insect vectors and vertebrate hosts. PLoS Negl Trop Dis. 2017;11: e0005782. PubMed PMC
Yurchenko V, Lukeš J, Tesařová M, Jirků M, Maslov DA Morphological discordance of the new trypanosomatid species phylogenetically associated with the genus Crithidia. Protist. 2008;159: 99–114. PubMed
Grybchuk D, Galan A, Klocek D, Macedo DH, Wolf YI, Votýpka J, et al.. Identification of diverse RNA viruses in Obscuromonas flagellates (Euglenozoa: Trypanosomatidae: Blastocrithidiinae). Virus Evol. 2024;10: veae037. PubMed PMC
Albanaz ATS, Carrington M, Frolov AO, Ganyukova AI, Gerasimov ES, Kostygov AY, et al.. Shining the spotlight on the neglected: new high-quality genome assemblies as a gateway to understanding the evolution of Trypanosomatidae. BMC Genomics. 2023;24: 471. doi: 10.1186/s12864-023-09591-z PubMed DOI PMC
Andrews S (2019) FastQC: a quality control tool for high throughput sequence data.
Chen S, Zhou Y, Chen Y, Gu J Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34: i884–i890. doi: 10.1093/bioinformatics/bty560 PubMed DOI PMC
Shanmugasundram A, Starns D, Böhme U, Amos B, Wilkinson PA, Harb OS, et al.. TriTrypDB: An integrated functional genomics resource for kinetoplastida. PLoS Negl Trop Dis. 2023;17: e0011058. doi: 10.1371/journal.pntd.0011058 PubMed DOI PMC
Ponsting H, Ning Z (2010) SMALT—A new mapper for DNA sequencing reads. Intelligent Systems for Molecular Biology. Boston, USA.
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al.. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20: 1297–1303. doi: 10.1101/gr.107524.110 PubMed DOI PMC
Bolger AM, Lohse M, Usadel B Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30: 2114–2120. PubMed PMC
Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al.. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013;8: 1494–1512. PubMed PMC
Langmead B, Salzberg SL Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9: 357–359. doi: 10.1038/nmeth.1923 PubMed DOI PMC
Ramirez-Gonzalez RH, Bonnal R, Caccamo M, Maclean D Bio-SAMtools: Ruby bindings for SAMtools, a library for accessing BAM files containing high-throughput sequence alignments. Source Code Biol Med. 2012;7: 6. doi: 10.1186/1751-0473-7-6 PubMed DOI PMC
Quinlan AR BEDTools: the swiss-army tool for genome feature analysis. Curr Protoc Bioinformatics. 2014;47: 11.12.11–11.12.34. doi: 10.1002/0471250953.bi1112s47 PubMed DOI PMC
Huson DH, Bryant D Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006;23: 254–267. doi: 10.1093/molbev/msj030 PubMed DOI
Gerasimov ES, Novozhilova TS, Zimmer SL, Yurchenko V Kinetoplast genome of Leishmania spp. is under strong purifying selection. Trop Med Infect Dis. 2023;8: 384. PubMed PMC
Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, Lanfear R IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020;37: 1530–1534. doi: 10.1093/molbev/msaa015 PubMed DOI PMC
Brisbin A, Bryc K, Byrnes J, Zakharia F, Omberg L, Degenhardt J, et al.. PCAdmix: principal components-based assignment of ancestry along each chromosome in individuals with admixed ancestry from two or more populations. Hum Biol. 2012;84: 343–364. doi: 10.3378/027.084.0401 PubMed DOI PMC
Browning BL, Tian X, Zhou Y, Browning SR Fast two-stage phasing of large-scale sequence data. Am J Hum Genet. 2021;108: 1880–1890. doi: 10.1016/j.ajhg.2021.08.005 PubMed DOI PMC
Heeren S, Maes I, Sanders M, Lye LF, Adaui V, Arevalo J, et al.. Diversity and dissemination of viruses in pathogenic protozoa. Nat Commun. 2023;14: 8343. doi: 10.1038/s41467-023-44085-2 PubMed DOI PMC
Buchfink B, Reuter K, Drost HG Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat Methods. 2021;18: 366–368. doi: 10.1038/s41592-021-01101-x 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: D170–D176. doi: 10.1093/nar/gkw1081 PubMed DOI PMC
Mendes Junior AAV, Filgueira CPB, Miranda LFC, de Almeida AB, Cantanhede LM, Fagundes A, et al.. First report of Leishmania (Mundinia) martiniquensis in South American territory and confirmation of Leishbunyavirus infecting this parasite in a mare. Mem Inst Oswaldo Cruz. 2023;118: e220220. PubMed PMC
Wheeler DL, Church DM, Federhen S, Lash AE, Madden TL, Pontius JU, et al.. Database resources of the National Center for Biotechnology. Nucleic Acids Res. 2003;31: 28–33. doi: 10.1093/nar/gkg033 PubMed DOI PMC
Sato K, Kato Y, Hamada M, Akutsu T, Asai K IPknot: fast and accurate prediction of RNA secondary structures with pseudoknots using integer programming. Bioinformatics. 2011;27: i85–93. doi: 10.1093/bioinformatics/btr215 PubMed DOI PMC
Reguera J, Weber F, Cusack S Bunyaviridae RNA polymerases (L-protein) have an N-terminal, influenza-like endonuclease domain, essential for viral cap-dependent transcription. PLOS Pathog. 2010;6: e1001101. PubMed PMC
Katoh K, Standley DM MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30: 772–780. PubMed PMC
Capella-Gutiérrez S, Silla-Martinez JM, Gabaldon T trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25: 1972–1973. PubMed PMC
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, et al.. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61: 539–542. doi: 10.1093/sysbio/sys029 PubMed DOI PMC
Hamilton PT, Votýpka J, Dostálová A, Yurchenko V, Bird NH, Lukeš J, et al.. Infection dynamics and immune response in a newly described Drosophila-trypanosomatid association. mBio. 2015;6: e01356–01315. PubMed PMC
Ishemgulova A, Kraeva N, Faktorová D, Podešvová L, Lukeš J, Yurchenko V T7 polymerase-driven transcription is downregulated in metacyclic promastigotes and amastigotes of Leishmania mexicana. Folia Parasitol. 2016;63: 016. PubMed
Yurchenko V, Kostygov A, Havlová J, Grybchuk-Ieremenko A, Ševčíková T, Lukeš J, et al.. Diversity of trypanosomatids in cockroaches and the description of Herpetomonas tarakana sp. n. J Eukaryot Microbiol. 2016;63 198–209. PubMed
Ishemgulova A, Hlaváčová J, Majerová K, Butenko A, Lukeš J, Votýpka J, et al.. CRISPR/Cas9 in Leishmania mexicana: a case study of LmxBTN1. PLoS One. 2018;13: e0192723. PubMed PMC
Volf P, Volfová V Establishment and maintenance of sand fly colonies. J Vector Ecol. 2011;36 Suppl 1: S1–S9. doi: 10.1111/j.1948-7134.2011.00106.x PubMed DOI
Dostálová A, Volf P Leishmania development in sand flies: parasite-vector interactions overview. Parasit Vectors. 2012;5: 276. PubMed PMC
Alexandre J, Sádlová J, Leštinová T, Vojtková B, Jančářová M, Podešvová L, et al.. Experimental infections and co-infections with Leishmania braziliensis and Leishmania infantum in two sand fly species, Lutzomyia migonei and Lutzomyia longipalpis. Sci Rep. 2020;10: 3566. PubMed PMC
Myšková J, Votýpka J, Volf P Leishmania in sand flies: comparison of quantitative polymerase chain reaction with other techniques to determine the intensity of infection. J Med Entomol. 2008;45: 133–138. PubMed
Campbell I Chi-squared and Fisher-Irwin tests of two-by-two tables with small sample recommendations. Stat Med. 2007;26: 3661–3675. doi: 10.1002/sim.2832 PubMed DOI
Tabbabi A, Caceres AG, Bustamante Chauca TP, Seki C, Choochartpong Y, Mizushima D, et al.. Nuclear and kinetoplast DNA analyses reveal genetically complex Leishmania strains with hybrid and mito-nuclear discordance in Peru. PLoS Negl Trop Dis. 2020;14: e0008797. PubMed PMC
Kato H, Caceres AG, Hashiguchi Y First evidence of a hybrid of Leishmania (Viannia) braziliensis/L. (V.) peruviana DNA detected from the phlebotomine sand fly Lutzomyia tejadai in Peru. PLoS Negl Trop Dis. 2016;10: e0004336. PubMed PMC
Odiwuor S, Veland N, Maes I, Arevalo J, Dujardin JC, Van der Auwera G Evolution of the Leishmania braziliensis species complex from amplified fragment length polymorphisms, and clinical implications. Infect Genet Evol. 2012;12: 1994–2002. PubMed
Van den Broeck F, Heeren S, Maes I, Sanders M, Cotton JA, Cupolillo E, et al.. Genome Analysis of triploid hybrid Leishmania parasite from the Neotropics. Emerg Infect Dis. 2023;29: 1076–1078. doi: 10.3201/eid2905.221456 PubMed DOI PMC
Patiño LH, Muñoz M, Cruz-Saavedra L, Muskus C, Ramírez JD Genomic diversification, structural plasticity, and hybridization in Leishmania (Viannia) braziliensis. Front Cell Infect Microbiol. 2020;10: 582192. PubMed PMC
Nolder D, Roncal N, Davies CR, Llanos-Cuentas A, Miles MA Multiple hybrid genotypes of Leishmania (viannia) in a focus of mucocutaneous Leishmaniasis. Am J Trop Med Hyg. 2007;76: 573–578. PubMed
Ren F, Zhou M, Deng F, Wang H, Ning YJ Combinatorial minigenome systems for emerging banyangviruses reveal viral reassortment potential and importance of a protruding nucleotide in genome "panhandle" for promoter activity and reassortment. Front Microbiol. 2020;11: 599. doi: 10.3389/fmicb.2020.00599 PubMed DOI PMC
Van den Broeck F, Savill NJ, Imamura H, Sanders M, Maes I, Cooper S, et al.. Ecological divergence and hybridization of Neotropical Leishmania parasites. Proc Natl Acad Sci U S A. 2020;117: 25159–25168. PubMed PMC
Romano A, Inbar E, Debrabant A, Charmoy M, Lawyer P, Ribeiro-Gomes F, et al.. Cross-species genetic exchange between visceral and cutaneous strains of Leishmania in the sand fly vector. Proc Natl Acad Sci U S A. 2014;111: 16808–16813. PubMed PMC
Akopyants NS, Kimblin N, Secundino N, Patrick R, Peters N, Lawyer P, et al.. Demonstration of genetic exchange during cyclical development of Leishmania in the sand fly vector. Science. 2009;324: 265–268. PubMed PMC
Sádlová J, Yeo M, Seblová V, Lewis MD, Mauricio I, Volf P, Miles MA Visualisation of Leishmania donovani fluorescent hybrids during early stage development in the sand fly vector. PLoS One. 2011;6: e19851. PubMed PMC
Lypaczewski P, Matlashewski G Leishmania donovani hybridisation and introgression in nature: a comparative genomic investigation. Lancet Microbe. 2021;2: e250–e258. PubMed
Volf P, Benková I, Myšková J, Sádlová J, Campino L, Ravel C Increased transmission potential of Leishmania major/Leishmania infantum hybrids. Int J Parasitol. 2007;37: 589–593. PubMed PMC
Rogers MB, Downing T, Smith BA, Imamura H, Sanders M, Svobodova M, et al.. Genomic confirmation of hybridisation and recent inbreeding in a vector-isolated Leishmania population. PLoS Genet. 2014;10: e1004092. PubMed PMC
Songumpai N, Promrangsee C, Noopetch P, Siriyasatien P, Preativatanyou K First evidence of co-circulation of emerging Leishmania martiniquensis, Leishmania orientalis, and Crithidia sp. in culicoides biting midges (Diptera: Ceratopogonidae), the putative vectors for autochthonous transmission in southern Thailand. Trop Med Infect Dis. 2022;7: 379. PubMed PMC
Bhattarai NR, Das ML, Rijal S, van der Auwera G, Picado A, Khanal B, et al.. Natural infection of Phlebotomus argentipes with Leishmania and other trypanosomatids in a visceral leishmaniasis endemic region of Nepal. Trans R Soc Trop Med Hyg. 2009;103: 1087–1092. PubMed
Ferreira TdS Minuzzi-Souza TT, Andrade AJ Coelho TO, Rocha Dde A Obara MT, et al.. Molecular detection of Trypanosoma sp. and Blastocrithidia sp. (Trypanosomatidae) in phlebotomine sand flies (Psychodidae) in the Federal District of Brazil. Rev Soc Bras Med Trop. 2015;48: 776–779. PubMed
Akhoundi M, Kuhls K, Cannet A, Votýpka J, Marty P, Delaunay P, Sereno D A historical overview of the classification, evolution, and dispersion of Leishmania parasites and sandflies. PLoS Negl Trop Dis. 2016;10: e0004349. PubMed PMC
Vasconcelos CI, Cronemberger-Andrade A, Souza-Melo N, Maricato JT, Xander P, Batista WL, et al.. Stress induces release of extracellular vesicles by Trypanosoma cruzi trypomastigotes. J Immunol Res. 2021;2021: 2939693. PubMed PMC
Dong G, Filho AL, Olivier M Modulation of host-pathogen communication by extracellular vesicles (EVs) of the protozoan parasite Leishmania. Front Cell Infect Microbiol. 2019;9: 100. PubMed PMC
Eliaz D, Kannan S, Shaked H, Arvatz G, Tkacz ID, Binder L, et al.. Exosome secretion affects social motility in Trypanosoma brucei. PLoS Pathog. 2017;13: e1006245. PubMed PMC
Grimaldi G Jr., Tesh RB Leishmaniases of the New World: current concepts and implications for future research. Clin Microbiol Rev. 1993;6: 230–250. doi: 10.1128/CMR.6.3.230 PubMed DOI PMC
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. PubMed
Cantanhêde LM, da Silva Junior CF, Ito MM, Felipin KP, Nicolete R, Salcedo JM, et al.. Further evidence of an association between the presence of Leishmania RNA Virus 1 and the mucosal manifestations in tegumentary leishmaniasis patients. PLoS Negl Trop Dis. 2015;9: e0004079. PubMed PMC
Bonilla AA, Pineda V, Calzada JE, Saldaña A, Laurenti MD, Goya S, et al.. Epidemiology and genetic characterization of Leishmania RNA virus in Leishmania (Viannia) spp. isolates from cutaneous leishmaniasis endemic areas in Panama. Microorganisms. 2024;12: 1317. PubMed PMC
Zabala-Peñafiel A, Fantinatti M, Dias-Lopes G, da Silva JL, Miranda LFC, Lyra MR, et al.. First report of Leishmania RNA virus 1 in Leishmania (Viannia) braziliensis clinical isolates from Rio de Janeiro State—Brazil. Mem Inst Oswaldo Cruz. 2022;117: e210107. PubMed PMC
Parra-Muñoz M, Aponte S, Ovalle-Bracho C, Saavedra CH, Echeverry MC Detection of Leishmania RNA Virus in clinical samples from cutaneous leishmaniasis patients varies according to the type of sample. Am J Trop Med Hyg. 2021;104: 233–239. PubMed PMC