Frequent Recombination Events in Leishmania donovani: Mining Population Data
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
CZ.02.1.01/16_019/0000759
European Regional Development Fund
19-15-00054
Russian Science Foundation
PubMed
32679679
PubMed Central
PMC7400496
DOI
10.3390/pathogens9070572
PII: pathogens9070572
Knihovny.cz E-zdroje
- Klíčová slova
- Leishmania donovani species complex, concerted evolution, gene conversion, whole-genome sequencing,
- Publikační typ
- časopisecké články MeSH
The Leishmania donovani species complex consists of all L. donovani and L. infantum strains mainly responsible for visceral leishmaniasis (VL). It was suggested that genome rearrangements in Leishmania spp. occur very often, thus enabling parasites to adapt to the different environmental conditions. Some of these rearrangements may be directly linked to the virulence or explain the reduced efficacy of antimonial drugs in some isolates. In the current study, we focused on a large-scale analysis of putative gene conversion events using publicly available datasets. Previous population study of L. donovani suggested that population variability of L. donovani is relatively low, however the authors used masking procedures and strict read selection criteria. We decided to re-analyze DNA-seq data without masking sequences, because we were interested in the most dynamic fraction of the genome. The majority of samples have an excess of putative gene conversion/recombination events in the noncoding regions, however we found an overall excess of putative intrachromosomal gene conversion/recombination in the protein coding genes, compared to putative interchromosomal gene conversion/recombination events.
Institute of Cytology and Genetics 630090 Novosibirsk Russia
Life Science Research Centre Faculty of Science University of Ostrava 710 00 Ostrava Czech Republic
Zobrazit více v PubMed
Bruschi F., Gradoni L. The Leishmaniases: Old Neglected Tropical Diseases. Springer; Cham, Switzerland: 2018. p. 245.
Burza S., Croft S.L., Boelaert M. Leishmaniasis. Lancet. 2018;392:951–970. doi: 10.1016/S0140-6736(18)31204-2. PubMed DOI
Guerbouj S., Guizani I., Speybroeck N., Le Ray D., Dujardin J.C. Genomic polymorphism of Leishmania infantum: A relationship with clinical pleomorphism? Infect. Genet. Evol. 2001;1:49–59. doi: 10.1016/S1567-1348(01)00008-9. PubMed DOI
Thakur L., Singh K.K., Shanker V., Negi A., Jain A., Matlashewski G., Jain M. Atypical leishmaniasis: A global perspective with emphasis on the Indian subcontinent. PLoS Negl. Trop. Dis. 2018;12:e0006659. doi: 10.1371/journal.pntd.0006659. PubMed DOI PMC
Quinnell R.J., Courtenay O. Transmission, reservoir hosts and control of zoonotic visceral leishmaniasis. Parasitology. 2009;136:1915–1934. doi: 10.1017/S0031182009991156. PubMed DOI
Ready P.D. Epidemiology of visceral leishmaniasis. Clin. Epidemiol. 2014;6:147–154. doi: 10.2147/CLEP.S44267. PubMed DOI PMC
Lukeš J., Mauricio I.L., Schonian G., Dujardin J.C., Soteriadou K., Dedet J.P., Kuhls K., Tintaya K.W., Jirků M., Chocholova E., et al. Evolutionary and geographical history of the Leishmania donovani complex with a revision of current taxonomy. Proc. Natl. Acad. Sci. USA. 2007;104:9375–9380. doi: 10.1073/pnas.0703678104. PubMed DOI PMC
Leblois R., Kuhls K., Francois O., Schonian G., Wirth T. Guns, germs and dogs: On the origin of Leishmania chagasi. Infect. Genet. Evol. 2011;11:1091–1095. doi: 10.1016/j.meegid.2011.04.004. PubMed DOI
Zhang W.W., Ramasamy G., McCall L.I., Haydock A., Ranasinghe S., Abeygunasekara P., Sirimanna G., Wickremasinghe R., Myler P., Matlashewski G. Genetic analysis of Leishmania donovani tropism using a naturally attenuated cutaneous strain. PLoS Pathog. 2014;10:e1004244. doi: 10.1371/journal.ppat.1004244. PubMed DOI PMC
Laffitte M.N., Leprohon P., Papadopoulou B., Ouellette M. Plasticity of the Leishmania genome leading to gene copy number variations and drug resistance. F1000Research. 2016;5:2350. doi: 10.12688/f1000research.9218.1. PubMed DOI PMC
Sádlová J., Svobodová M., Volf P. Leishmania major: Effect of repeated passages through sandfly vectors or murine hosts. Ann. Trop. Med. Parasitol. 1999;93:599–611. doi: 10.1080/00034983.1999.11813463. PubMed DOI
Lypaczewski P., Hoshizaki J., Zhang W.W., McCall L.I., Torcivia-Rodriguez J., Simonyan V., Kaur A., Dewar K., Matlashewski G. A complete Leishmania donovani reference genome identifies novel genetic variations associated with virulence. Sci. Rep. 2018;8:1–14. doi: 10.1038/s41598-018-34812-x. PubMed DOI 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. doi: 10.1371/journal.ppat.1005186. PubMed DOI PMC
Rastrojo A., Garcia-Hernandez R., Vargas P., Camacho E., Corvo L., Imamura H., Dujardin J.C., Castanys S., Aguado B., Gamarro F., et al. Genomic and transcriptomic alterations in Leishmania donovani lines experimentally resistant to antileishmanial drugs. Int. J. Parasitol. Drugs Drug. Resist. 2018;8:246–264. doi: 10.1016/j.ijpddr.2018.04.002. PubMed DOI PMC
Dostálová A., Volf P. Leishmania development in sand flies: Parasite-vector interactions overview. Parasit. Vectors. 2012;5:1–12. doi: 10.1186/1756-3305-5-276. PubMed DOI PMC
Forestier C.L., Gao Q., Boons G.J. Leishmania lipophosphoglycan: How to establish structure-activity relationships for this highly complex and multifunctional glycoconjugate? Front. Cell. Infect. Microbiol. 2014;4:193. doi: 10.3389/fcimb.2014.00193. PubMed DOI PMC
Turco S.J., Spath G.F., Beverley S.M. Is lipophosphoglycan a virulence factor? A surprising diversity between Leishmania species. Trends Parasitol. 2001;17:223–226. doi: 10.1016/S1471-4922(01)01895-5. PubMed DOI
Dobson D.E., Scholtes L.D., Valdez K.E., Sullivan D.R., Mengeling B.J., Cilmi S., Turco S.J., Beverley S.M. Functional identification of galactosyltransferases (SCGs) required for species-specific modifications of the lipophosphoglycan adhesin controlling Leishmania major-sand fly interactions. J. Biol. Chem. 2003;278:15523–15531. doi: 10.1074/jbc.M301568200. PubMed DOI
Dobson D.E., Mengeling B.J., Cilmi S., Hickerson S., Turco S.J., Beverley S.M. Identification of genes encoding arabinosyltransferases (SCA) mediating developmental modifications of lipophosphoglycan required for sand fly transmission of Leishmania major. J. Biol. Chem. 2003;278:28840–28848. doi: 10.1074/jbc.M302728200. PubMed DOI
Maslov D.A., Opperdoes F.R., Kostygov A.Y., Hashimi H., Lukeš J., Yurchenko V. Recent advances in trypanosomatid research: Genome organization, expression, metabolism, taxonomy and evolution. Parasitology. 2019;146:1–27. doi: 10.1017/S0031182018000951. PubMed DOI
Lukeš J., Butenko A., Hashimi H., Maslov D.A., 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
Butenko A., Vieira T.D.S., Frolov A.O., Opperdoes F.R., Soares R.P., Kostygov A.Y., Lukeš J., Yurchenko V. Leptomonas pyrrhocoris: Genomic insight into parasite’s physiology. Curr. Genom. 2018;19:150–156. doi: 10.2174/1389202918666170815143331. PubMed DOI PMC
Manna P.T., Boehm C., Leung K.F., Natesan S.K., Field M.C. Life and times: Synthesis, trafficking, and evolution of VSG. Trends Parasitol. 2014;30:251–258. doi: 10.1016/j.pt.2014.03.004. PubMed DOI PMC
McCulloch R., Rudenko G., Borst P. Gene conversions mediating antigenic variation in Trypanosoma brucei can occur in variant surface glycoprotein expression sites lacking 70-base-pair repeat sequences. Mol. Cell. Biol. 1997;17:833–843. doi: 10.1128/MCB.17.2.833. PubMed DOI PMC
Robinson N.P., Burman N., Melville S.E., Barry J.D. Predominance of duplicative VSG gene conversion in antigenic variation in African trypanosomes. Mol. Cell. Biol. 1999;19:5839–5846. doi: 10.1128/MCB.19.9.5839. PubMed DOI PMC
Castro Neto A.L., Brito A., Rezende A.M., Magalhaes F.B., de Melo Neto O.P. In silico characterization of multiple genes encoding the GP63 virulence protein from Leishmania braziliensis: Identification of sources of variation and putative roles in immune evasion. BMC Genom. 2019;20:1–17. doi: 10.1186/s12864-019-5465-z. PubMed DOI PMC
Mauricio I.L., Gaunt M.W., Stothard J.R., Miles M.A. Glycoprotein 63 (gp63) genes show gene conversion and reveal the evolution of Old World Leishmania. Int. J. Parasitol. 2007;37:565–576. doi: 10.1016/j.ijpara.2006.11.020. PubMed DOI
Mottram J.C., Frame M.J., Brooks D.R., Tetley L., Hutchison J.E., Souza A.E., Coombs G.H. The multiple cpb cysteine proteinase genes of Leishmania mexicana encode isoenzymes that differ in their stage regulation and substrate preferences. J. Biol. Chem. 1997;272:14285–14293. doi: 10.1074/jbc.272.22.14285. PubMed DOI
Folgueira C., Cañavate C., Chicharro C., Requena J.M. Genomic organization and expression of the hsp70 locus in New and Old World Leishmania species. Parasitology. 2007;134:369–377. doi: 10.1017/S0031182006001570. PubMed DOI
Jackson A.P. The evolution of amastin surface glycoproteins in trypanosomatid parasites. Mol. Biol. Evol. 2010;27:33–45. doi: 10.1093/molbev/msp214. PubMed DOI PMC
Zhang W.W., Matlashewski G. Characterization of the A2-A2rel gene cluster in Leishmania donovani: Involvement of A2 in visceralization during infection. Mol. MicroBiol. 2001;39:935–948. doi: 10.1046/j.1365-2958.2001.02286.x. PubMed DOI
Franssen S.U., Durrant C., Stark O., Moser B., Downing T., Imamura H., Dujardin J.C., Sanders M.J., Mauricio I., Miles M.A., et al. Global genome diversity of the Leishmania donovani complex. eLife. 2020;9:e51243. doi: 10.7554/eLife.51243. PubMed DOI PMC
Malone R.E., Bullard S., Lundquist S., Kim S., Tarkowski T. A meiotic gene conversion gradient opposite to the direction of transcription. Nature. 1992;359:154–155. doi: 10.1038/359154a0. PubMed DOI
Detloff P., White M.A., Petes T.D. Analysis of a gene conversion gradient at the his4 locus in Saccharomyces cerevisiae. Genetics. 1992;132:113–123. PubMed PMC
Nicolas A., Petes T.D. Polarity of meiotic gene conversion in fungi: Contrasting views. Experientia. 1994;50:242–252. doi: 10.1007/BF01924007. PubMed DOI
Kostygov A.Y., Yurchenko V. Revised classification of the subfamily Leishmaniinae (Trypanosomatidae) Folia Parasitol. 2017;64:20. doi: 10.14411/fp.2017.020. PubMed DOI
Ohta T. On the evolution of multigene families. Theor. Popul. Biol. 1983;23:216–240. doi: 10.1016/0040-5809(83)90015-1. PubMed DOI
Koop B.F., Miyamoto M.M., Embury J.E., Goodman M., Czelusniak J., Slightom J.L. Nucleotide sequence and evolution of the orangutan epsilon globin gene region and surrounding Alu repeats. J. Mol. Evol. 1986;24:94–102. doi: 10.1007/BF02099956. PubMed DOI
Nei M., Rogozin I.B., Piontkivska H. Purifying selection and birth-and-death evolution in the ubiquitin gene family. Proc. Natl. Acad. Sci. USA. 2000;97:10866–10871. doi: 10.1073/pnas.97.20.10866. PubMed DOI PMC
Imamura H., Downing T., Van den Broeck F., Sanders M.J., Rijal S., Sundar S., Mannaert A., Vanaerschot M., Berg M., De Muylder G., et al. Evolutionary genomics of epidemic visceral leishmaniasis in the Indian subcontinent. eLife. 2016;5:e12613. doi: 10.7554/eLife.12613. PubMed DOI PMC
Eickbush T.H., Burke W.D. The silkmoth late chorion locus. II. Gradients of gene conversion in two paired multigene families. J. Mol. Biol. 1986;190:357–366. doi: 10.1016/0022-2836(86)90007-0. PubMed DOI
Alani E., Reenan R.A., Kolodner R.D. Interaction between mismatch repair and genetic recombination in Saccharomyces cerevisiae. Genetics. 1994;137:19–39. PubMed PMC
Dooner H.K., He L. Polarized gene conversion at the bz locus of maize. Proc. Natl. Acad. Sci. USA. 2014;111:13918–13923. doi: 10.1073/pnas.1415482111. PubMed DOI PMC
Palmer S., Schildkraut E., Lazarin R., Nguyen J., Nickoloff J.A. Gene conversion tracts in Saccharomyces cerevisiae can be extremely short and highly directional. Nucleic. Acids. Res. 2003;31:1164–1173. doi: 10.1093/nar/gkg219. PubMed DOI PMC
Wang S., Chen Y. Phylogenomic analysis demonstrates a pattern of rare and long-lasting concerted evolution in prokaryotes. Commun. Biol. 2018;1:1–11. doi: 10.1038/s42003-018-0014-x. PubMed DOI PMC
Perelygin A.A., Kondrashov F.A., Rogozin I.B., Brinton M.A. Evolution of the mouse polyubiquitin-C gene. J. Mol. Evol. 2002;55:202–210. doi: 10.1007/s00239-002-2318-0. PubMed DOI
Dover G. Molecular drive: A cohesive mode of species evolution. Nature. 1982;299:111–117. doi: 10.1038/299111a0. PubMed DOI
Makin L., Gluenz E. cAMP signalling in trypanosomatids: Role in pathogenesis and as a drug target. Trends Parasitol. 2015;31:373–379. doi: 10.1016/j.pt.2015.04.014. PubMed DOI PMC
Mony B.M., MacGregor P., Ivens A., Rojas F., Cowton A., Young J., Horn D., Matthews K. Genome-wide dissection of the quorum sensing signalling pathway in Trypanosoma brucei. Nature. 2014;505:681–685. doi: 10.1038/nature12864. PubMed DOI PMC
Imhof S., Knusel S., Gunasekera K., Vu X.L., Roditi I. Social motility of African trypanosomes is a property of a distinct life-cycle stage that occurs early in tsetse fly transmission. PLoS Pathog. 2014;10:e1004493. doi: 10.1371/journal.ppat.1004493. PubMed DOI PMC
Sanchez M.A., Zeoli D., Klamo E.M., Kavanaugh M.P., Landfear S.M. A family of putative receptor-adenylate cyclases from Leishmania donovani. J. Biol. Chem. 1995;270:17551–17558. doi: 10.1074/jbc.270.29.17551. PubMed DOI
Downing T., Imamura H., Decuypere S., Clark T.G., Coombs G.H., Cotton J.A., Hilley J.D., de Doncker S., Maes I., Mottram J.C., et al. Whole genome sequencing of multiple Leishmania donovani clinical isolates provides insights into population structure and mechanisms of drug resistance. Genome Res. 2011;21:2143–2156. doi: 10.1101/gr.123430.111. PubMed DOI PMC
Downing T., Stark O., Vanaerschot M., Imamura H., Sanders M., Decuypere S., de Doncker S., Maes I., Rijal S., Sundar S., et al. Genome-wide SNP and microsatellite variation illuminate population-level epidemiology in the Leishmania donovani species complex. Infect. Genet. Evol. 2012;12:149–159. doi: 10.1016/j.meegid.2011.11.005. PubMed DOI PMC
Khromov-Borisov N.N., Rogozin I.B., Pegas Henriques J.A., de Serres F.J. Similarity pattern analysis in mutational distributions. Mutat. Res. 1999;430:55–74. doi: 10.1016/S0027-5107(99)00148-7. PubMed DOI
Kumar S., Stecher G., Li M., Knyaz C., Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol. Biol. Evol. 2018;35:1547–1549. doi: 10.1093/molbev/msy096. PubMed DOI PMC
Kostygov A.Y., Grybchuk-Ieremenko A., Malysheva M.N., Frolov A.O., Yurchenko V. Molecular revision of the genus Wallaceina. Protist. 2014;165:594–604. doi: 10.1016/j.protis.2014.07.001. PubMed DOI
Genomic analysis of Leishmania turanica strains from different regions of Central Asia