Vickermania gen. nov., trypanosomatids that use two joined flagella to resist midgut peristaltic flow within the fly host
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
18-14-00134
Russian Science Foundation - International
AAAA-A19-119020690109-2
State Assignment for the Zoological Institute - International
16_019/0000759
European Regional Development Fund - International
16_019/0000759
European Regional Development Fund - International
20-07186S
Grantová Agentura České Republiky - International
20-07186S
Grantová Agentura České Republiky - International
LL1601
ERC CZ - International
RRC/10/2017
Moravskoslezský Kraj Research Initiative - International
Finance Code 001
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (BR) - International
PubMed
33267865
PubMed Central
PMC7712620
DOI
10.1186/s12915-020-00916-y
PII: 10.1186/s12915-020-00916-y
Knihovny.cz E-zdroje
- Klíčová slova
- Cell cycle, Flagella connector, Herpetomonas muscarum ingenoplastis, Trypanosoma brucei,
- MeSH
- flagella fyziologie MeSH
- interakce hostitele a parazita * MeSH
- moucha tse-tse parazitologie MeSH
- peristaltika MeSH
- Trypanosomatina klasifikace cytologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
BACKGROUND: The family Trypanosomatidae encompasses parasitic flagellates, some of which cause serious vector-transmitted diseases of humans and domestic animals. However, insect-restricted parasites represent the ancestral and most diverse group within the family. They display a range of unusual features and their study can provide insights into the biology of human pathogens. Here we describe Vickermania, a new genus of fly midgut-dwelling parasites that bear two flagella in contrast to other trypanosomatids, which are unambiguously uniflagellate. RESULTS: Vickermania has an odd cell cycle, in which shortly after the division the uniflagellate cell starts growing a new flagellum attached to the old one and preserves their contact until the late cytokinesis. The flagella connect to each other throughout their whole length and carry a peculiar seizing structure with a paddle-like apex and two lateral extensions at their tip. In contrast to typical trypanosomatids, which attach to the insect host's intestinal wall, Vickermania is separated from it by a continuous peritrophic membrane and resides freely in the fly midgut lumen. CONCLUSIONS: We propose that Vickermania developed a survival strategy that relies on constant movement preventing discharge from the host gut due to intestinal peristalsis. Since these parasites cannot attach to the midgut wall, they were forced to shorten the period of impaired motility when two separate flagella in dividing cells interfere with each other. The connection between the flagella ensures their coordinate movement until the separation of the daughter cells. We propose that Trypanosoma brucei, a severe human pathogen, during its development in the tsetse fly midgut faces the same conditions and follows the same strategy as Vickermania by employing an analogous adaptation, the flagellar connector.
Faculty of Sciences University of South Bohemia 370 05 České Budějovice Czechia
Institute of Parasitology Czech Academy of Sciences 370 05 České Budějovice Czechia
Instituto Oswaldo Cruz Fundação Oswaldo Cruz Rio de Janeiro 21040 900 Brazil
Martsinovsky Institute of Medical Parasitology Sechenov University Moscow 119435 Russia
Zoological Institute of the Russian Academy of Sciences St Petersburg 199034 Russia
Zobrazit více v PubMed
Podlipaev SA. Catalogue of world fauna of Trypanosomatidae (Protozoa) Leningrad: Zoologicheskii Institut AN SSSR; 1990.
Vickerman K. The diversity of the kinetoplastid flagellates. In: Biology of the Kinetoplastida. Edited by Lumsden WHR, Evans DA, vol. 1. London: Academic Press; 1976. pp. 1–34.
Bruschi F, Gradoni L. The leishmaniases: old neglected tropical diseases. Cham: Springer; 2018.
Telleria J, Tibayrenc M. American trypanosomiasis Chagas disease : one hundred years of research. 2. Amsterdam: Elsevier; 2017.
Büscher P, Cecchi G, Jamonneau V, Priotto G. Human African trypanosomiasis. Lancet. 2017;390(10110):2397–2409. doi: 10.1016/S0140-6736(17)31510-6. PubMed DOI
Záhonová K, Kostygov AY, Ševčíková T, Yurchenko V, Eliáš M. An unprecedented non-canonical nuclear genetic code with all three termination codons reassigned as sense codons. Curr Biol. 2016;26(17):2364–2369. doi: 10.1016/j.cub.2016.06.064. PubMed DOI
Teixeira MM, Borghesan TC, Ferreira RC, Santos MA, Takata CS, Campaner M, Nunes VL, Milder RV, de Souza W, Camargo EP. Phylogenetic validation of the genera Angomonas and Strigomonas of trypanosomatids harboring bacterial endosymbionts with the description of new species of trypanosomatids and of proteobacterial symbionts. Protist. 2011;162(3):503–524. doi: 10.1016/j.protis.2011.01.001. PubMed DOI
Votýpka J, Kostygov AY, Kraeva N, Grybchuk-Ieremenko A, Tesařová M, Grybchuk D, Lukeš J, Yurchenko V. Kentomonas gen. n., a new genus of endosymbiont-containing trypanosomatids of Strigomonadinae subfam. n. Protist. 2014;165(6):825–838. doi: 10.1016/j.protis.2014.09.002. PubMed DOI
Kostygov AY, Dobáková E, Grybchuk-Ieremenko A, Váhala D, Maslov DA, Votýpka J, Lukeš J, Yurchenko V. Novel trypanosomatid-bacterium association: evolution of endosymbiosis in action. mBio. 2016;7(2):e01985–e01915. doi: 10.1128/mBio.01985-15. 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, Akopyants NS, Kostygov AY, Konovalovas A, Lye LF, Dobson DE, Zangger H, Fasel N, Butenko A, Frolov AO, 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
Hoare CA, Wallace FG. Developmental stages of trypanosomatid flagellates: a new terminology. Nature. 1966;212:1385–1386. doi: 10.1038/2121385a0. DOI
Maslov DA, Votýpka J, Yurchenko V, Lukeš J. Diversity and phylogeny of insect trypanosomatids: all that is hidden shall be revealed. Trends Parasitol. 2013;29(1):43–52. doi: 10.1016/j.pt.2012.11.001. PubMed DOI
Maslov DA, Opperdoes FR, Kostygov AY, Hashimi H, Lukeš J, Yurchenko V. Recent advances in trypanosomatid research: genome organization, expression, metabolism, taxonomy and evolution. Parasitology. 2019;146(1):1–27. doi: 10.1017/S0031182018000951. PubMed DOI
Votýpka J, d’Avila-Levy CM, Grellier P, Maslov DA, Lukeš J, Yurchenko V. New approaches to systematics of Trypanosomatidae: criteria for taxonomic (re)description. Trends Parasitol. 2015;31(10):460–469. doi: 10.1016/j.pt.2015.06.015. PubMed DOI
Leidy J. A synopsis of entozoa and some of their ecto-congeners, observed by the author. Proc Acad Natl Sci Phila. 1856;8:42–58.
Wallace FG. The trypanosomatid parasites of insects and arachnids. Exp Parasitol. 1966;18(1):124–193. doi: 10.1016/0014-4894(66)90015-4. PubMed DOI
Prowazek S. Die Entwicklung von Herpetomonas, einem mit den Trypanosomen verwandten Flagellaten. Arb Gesundh-Amte (Berl) 1904;20:440–452.
Patton WS, Strickland C. A critical review of the relation of blood-sucking invertebrates to the life cycles of the trypanosomes of vertebrates, with a note on the occurrence of a species of Crithidia, C. ctenopthalmi, in the alimentary tract of Ctenopthalmus agyrtes, Heller. Parasitology. 1908;1(4):322–346. doi: 10.1017/S0031182000003632. DOI
Patton WS. Inoculation of dogs with the parasite of kala azar (Herpetomonas [Leishmania] donovani) with some remarks on the genus Herpetomonas. Parasitology. 1908;1(4):311–313. doi: 10.1017/S0031182000003607. DOI
Porter A. The life-cycle of Herpetomonas jaculum (Léger), parasitic in the alimentary tract of Nepa cinerea. Parasitology. 1909;2(4):367–391. doi: 10.1017/S0031182000001827. DOI
Léger L. Sur la structure et le mode de multiplication des flagélles du genre Herpetomonas Kent. Comp R Séances Soc Biol. 1902;54(14):398–400.
Mackinnon DL. Herpetomonads from the alimentary tract of certain dung-flies. Parasitology. 1910;3(3):255–274. doi: 10.1017/S0031182000002080. DOI
Woodcock HM. Further remarks on the flagellate parasites of Culex. Is there a generic type, Crithidia? Zool Anz. 1914;44(1):26–33.
Wenyon CM. Observations on Herpetomonas muscae-domesticae and some allied flagellates with special reference to the structure of their nuclei. Arch Protistenkd. 1913;31(1):1–36.
Rogers WE, Wallace FG. Two new subspecies of Herpetomonas muscarum (Leidy, 1856) Kent, 1880. J Protozool. 1971;18(4):645–654. doi: 10.1111/j.1550-7408.1971.tb03390.x. PubMed DOI
Brun R. Ultrastruktur und Zyklus von Herpetomonas muscarum, “Herpetomonas mirabilis” und Сrithidia luciliae in Chrysomyia chloropyga. Acta Trop. 1974;31(3):219–290. PubMed
Wallace FG, Wagner M, Rogers WE. Varying kinetoplast ultrastructure in two subspecies of Herpetomonas muscarum (Leidy) J Protozool. 1973;20(2):218–222. doi: 10.1111/j.1550-7408.1973.tb00868.x. PubMed DOI
Borst P, Hoeijmakers JHJ, Hajduk SL. Structure, function and evolution of kinetoplast DNA. Parasitology. 1981;82(4):81–93. doi: 10.1017/S0031182000150127. PubMed DOI
Mallinson DJ, Lackie JM, Coombs GH. The oxidative response of rabbit peritoneal neutrophils to leishmanias and other trypanosomatids. Int J Parasitol. 1989;19(6):639–645. doi: 10.1016/0020-7519(89)90042-8. PubMed DOI
Redman CA, Coombs GH. The products and pathways of glucose catabolism in Herpetomonas muscarum ingenoplastis and Herpetomonas muscarum muscarum. J Eukaryot Microbiol. 1997;44(1):46–51. doi: 10.1111/j.1550-7408.1997.tb05690.x. DOI
Vickerman K, Preston TM. Comparative cell biology of the kinetoplastid flagellates. In: WHR L, Evans DA, editors. Biology of Kinetoplastida. London: Academic Press; 1976. pp. 35–130.
He CY, Singh A, Yurchenko V. Cell cycle-dependent flagellar disassembly in a firebug trypanosomatid Leptomonas pyrrhocoris. mBio. 2019;10(6):e02424–e02419. doi: 10.1128/mBio.02424-19. PubMed DOI PMC
Archibald JM. Handbook of the protists. New York: Springer Berlin Heidelberg; 2017.
Votýpka J, Klepetková H, Jirků M, Kment P, Lukeš J. Phylogenetic relationships of trypanosomatids parasitising true bugs (Insecta: Heteroptera) in sub-Saharan Africa. Int J Parasitol. 2012;42(5):489–500. doi: 10.1016/j.ijpara.2012.03.007. PubMed DOI
Chandler JA, James PM. Discovery of trypanosomatid parasites in globally distributed Drosophila species. Plos One. 2013;8(4):e61937. doi: 10.1371/journal.pone.0061937. PubMed DOI PMC
Votýpka J, Pafco B, Modrý D, Mbohli D, Tagg N, Petrželková KJ. An unexpected diversity of trypanosomatids in fecal samples of great apes. Int J Parasitol Parasites Wildl. 2018;7(3):322–325. doi: 10.1016/j.ijppaw.2018.09.003. PubMed DOI PMC
Týč J, Votýpka J, Klepetková H, Šuláková H, Jirků M, Lukeš J. Growing diversity of trypanosomatid parasites of flies (Diptera: Brachcera): frequent cosmopolitism and moderate host specificity. Mol Phylogenet Evol. 2013;69:255–264. doi: 10.1016/j.ympev.2013.05.024. PubMed DOI
Votýpka J, Kment P, Kriegová E, Vermeij MJA, Keeling PJ, Yurchenko V, Lukeš J. High prevalence and endemism of trypanosomatids on a small Caribbean island. J Eukaryot Microbiol. 2019;66(4):600–607. doi: 10.1111/jeu.12704. PubMed DOI
d'Avila-Levy CM, Boucinha C, Kostygov A, Santos HL, Morelli KA, Grybchuk-Ieremenko A, Duval L, Votýpka J, Yurchenko V, Grellier P, et al. Exploring the environmental diversity of kinetoplastid flagellates in the high-throughput DNA sequencing era. Mem Inst Oswaldo Cruz. 2015;110(8):956–965. doi: 10.1590/0074-02760150253. PubMed DOI PMC
Frolov AO, Malysheva MN, Ganyukova AI, Spodareva VV, Yurchenko V, Kostygov AY. Development of Phytomonas lipae sp. n. (Kinetoplastea: Trypanosomatidae) in the true bug Coreus marginatus (Heteroptera: Coreidae) and insights into the evolution of life cycles in the genus Phytomonas. Plos One. 2019;14(4):e0214484. doi: 10.1371/journal.pone.0214484. PubMed DOI PMC
Zídková L, Čepička I, Votýpka J, Svobodová M. Herpetomonas trimorpha sp. nov. (Trypanosomatidae, Kinetoplastida), a parasite of the biting midge Culicoides truncorum (Ceratopogonidae, Diptera) Int J Syst Evol Microbiol. 2010;60(Pt 9):2236–2246. doi: 10.1099/ijs.0.014555-0. PubMed DOI
Wilfert L, Longdon B, Ferreira AG, Bayer F, Jiggins FM. Trypanosomatids are common and diverse parasites of Drosophila. Parasitology. 2011;138(7):858–865. doi: 10.1017/S0031182011000485. PubMed DOI
d'Avila-Levy CM, Bearzatto B, Ambroise J, Helaers R, Butenko A, Yurchenko V, Morelli KA, HLC S, Brouillard P, Grellier P, et al. First draft genome of the trypanosomatid Herpetomonas muscarum ingenoplastis through MinION Oxford Nanopore Technology and Illumina Sequencing. Trop Med Infect Dis. 2020;5(1):25. doi: 10.3390/tropicalmed5010025. PubMed DOI PMC
Adl SM, Bass D, Lane CE, Lukes J, Schoch CL, Smirnov A, Agatha S, Berney C, Brown MW, Burki F, et al. Revisions to the classification, nomenclature, and diversity of eukaryotes. J Eukaryot Microbiol. 2019;66(1):4–119. doi: 10.1111/jeu.12691. PubMed DOI PMC
Bailey CH, Brooks WM. Histological observations on larvae of the eye gnat, Hippelates pusio (diptera: Chloropidae), infected with the flagellate Herpetomonas muscarum. J Invertebr Pathol. 1972;19(3):342–353. doi: 10.1016/0022-2011(72)90232-7. PubMed DOI
Langousis G, Hill KL. Motility and more: the flagellum of Trypanosoma brucei. Nat Rev Microbiol. 2014;12(7):505–518. doi: 10.1038/nrmicro3274. PubMed DOI PMC
Frolov AO, Malysheva MN, Kostygov AY. Transformations of life cycles in the evolutionary history of trypanosomatids: endotransformations and aberrations. Parazitologiia. 2016;50(2):97–113. PubMed
Frolov AO. Trypanosomatids (Kinetoplastea: Trypanosomatida) and insects (Insecta): patterns of co-evolution and diversification of the host–parasite systems. Proc Zool Inst RAS. 2016;320(S4):16–75.
Frolov AO, Skarlato SO. Fine structure and mechanisms of adaptation of lower trypanosomatids in Hemiptera. Tsitologyia. 1995;37(7):539–560.
Tieszen KL, Molyneux DH, Abdel-Hafez SK. Host-parasite relationships of Blastocrithidia familiaris in Lygaeus pandurus Scop. (Hemiptera: Lygaeidae) Parasitology. 1986;92(1):1–12. doi: 10.1017/S003118200006340X. DOI
Lauge G, Nishioka RS. Ultrastructural study of the relations between Leptomonas oncopelti (Noguchi and Tilden), Protozoa Trypanosomatidae, and the rectal wall of adults of Oncopeltus fasciatus Dallas, Hemiptera Lygaeidae. J Morphol. 1977;154(2):291–305. doi: 10.1002/jmor.1051540207. PubMed DOI
Molyneux DH, Croft SL, Lavin DR. Studies on the host-parasite relationships of Leptomonas species (Protozoa: Kinetoplastida) of Siphonaptera. J Natl Hist. 1981;15(3):395–406. doi: 10.1080/00222938100770301. DOI
Tieszen KL, Molyneux DH, Abdelhafez SK. Host-parasite relationships and cysts of Leptomonas lygaei (Trypanosomatidae) in Lygaeus pandurus (Hemiptera, Lygaeidae) Parasitology. 1989;98:395–400. doi: 10.1017/S0031182000061473. DOI
Skalický T, Dobáková E, Wheeler RJ, Tesařová M, Flegontov P, Jirsová D, Votýpka J, Yurchenko V, Ayala FJ, Lukeš J. Extensive flagellar remodeling during the complex life cycle of Paratrypanosoma, an early-branching trypanosomatid. Proc Natl Acad Sci U S A. 2017;114(44):11757–11762. doi: 10.1073/pnas.1712311114. PubMed DOI PMC
Vickerman K, Tetley L. Flagellar surfaces of parasitic protozoa and their role in attachment. In: Bloodgood RA, editor. Ciliary and Flagellar Membranes. Boston: Springer; 1990. pp. 267–304.
Frolov AO, Malysheva MN, Ganyukova AI, Yurchenko V, Kostygov AY. Life cycle of Blastocrithidia papi sp. n. (Kinetoplastea, Trypanosomatidae) in Pyrrhocoris apterus (Hemiptera, Pyrrhocoridae) Eur J Protistol. 2017;57:85–98. doi: 10.1016/j.ejop.2016.10.007. PubMed DOI
Frolov AO, Malysheva MN, Ganyukova AI, Spodareva VV, Králová J, Yurchenko V, Kostygov AY. If host is refractory, insistent parasite goes berserk: Trypanosomatid Blastocrithidia raabei in the dock bug Coreus marginatus. Plos One. 2020;15(1):e0227832. doi: 10.1371/journal.pone.0227832. PubMed DOI PMC
Terra WR. The origin and functions of the insect peritrophic membrane and peritrophic gel. Arch Insect Biochem Physiol. 2001;47(2):47–61. doi: 10.1002/arch.1036. PubMed DOI
Peters W. Peritrophic membranes. Berlin: Springer-Verlag; 1992.
Dostálová A, Volf P. Leishmania development in sand flies: parasite-vector interactions overview. Parasit Vectors. 2012;5:276. doi: 10.1186/1756-3305-5-276. PubMed DOI PMC
Sádlová J, Volf P. Peritrophic matrix of Phlebotomus duboscqi and its kinetics during Leishmania major development. Cell Tissue Res. 2009;337(2):313–325. doi: 10.1007/s00441-009-0802-1. PubMed DOI PMC
Wheeler RJ, Scheumann N, Wickstead B, Gull K, Vaughan S. Cytokinesis in Trypanosoma brucei differs between bloodstream and tsetse trypomastigote forms: implications for microtubule-based morphogenesis and mutant analysis. Mol Microbiol. 2013;90(6):1339–1355. doi: 10.1111/mmi.12436. PubMed DOI PMC
Moreira-Leite FF, Sherwin T, Kohl L, Gull K. A trypanosome structure involved in transmitting cytoplasmic information during cell division. Science. 2001;294(5542):610–612. doi: 10.1126/science.1063775. PubMed DOI
Briggs LJ, McKean PG, Baines A, Moreira-Leite F, Davidge J, Vaughan S, Gull K. The flagella connector of Trypanosoma brucei: an unusual mobile transmembrane junction. J Cell Sci. 2004;117(Pt 9):1641–1651. doi: 10.1242/jcs.00995. PubMed DOI
Frolov AO, Malysheva MN, Yurchenko V, Kostygov AY. Back to monoxeny: Phytomonas nordicus descended from dixenous plant parasites. Eur J Protistol. 2016;52:1–10. doi: 10.1016/j.ejop.2015.08.002. PubMed DOI
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9(7):676–682. doi: 10.1038/nmeth.2019. PubMed DOI PMC
Frolov AO, Malysheva MN, Ganyukova AI, Yurchenko V, Kostygov AY. Obligate development of Blastocrithidia papi (Trypanosomatidae) in the Malpighian tubules of Pyrrhocoris apterus (Hemiptera) and coordination of host-parasite life cycles. Plos One. 2018;13(9):e0204467. doi: 10.1371/journal.pone.0204467. PubMed DOI PMC
Yurchenko V, Votýpka J, Tesařová M, Klepetková H, Kraeva N, Jirků M, Lukeš J. Ultrastructure and molecular phylogeny of four new species of monoxenous trypanosomatids from flies (Diptera: Brachycera) with redefinition of the genus Wallaceina. Folia Parasitol. 2014;61(2):97–112. doi: 10.14411/fp.2014.023. PubMed DOI
Maslov DA, Lukeš J, Jirků M, Simpson L. Phylogeny of trypanosomes as inferred from the small and large subunit rRNAs: implications for the evolution of parasitism in the trypanosomatid protozoa. Mol Biochem Parasitol. 1996;75(2):197–205. doi: 10.1016/0166-6851(95)02526-X. PubMed DOI
Maslov DA, Yurchenko VY, Jirků M, Lukeš J. Two new species of trypanosomatid parasites isolated from Heteroptera in Costa Rica. J Eukaryot Microbiol. 2010;57(2):177–188. doi: 10.1111/j.1550-7408.2009.00464.x. PubMed DOI
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
Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17(4):540–552. doi: 10.1093/oxfordjournals.molbev.a026334. PubMed DOI
Chistyakova LV, Kostygov AY, Kornilova OA, Yurchenko V. Reisolation and redescription of Balantidium duodeni Stein, 1867 (Litostomatea, Trichostomatia) Parasitol Res. 2014;113(11):4207–4215. doi: 10.1007/s00436-014-4096-1. PubMed DOI
Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268–274. doi: 10.1093/molbev/msu300. PubMed DOI PMC
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14(6):587–589. doi: 10.1038/nmeth.4285. PubMed DOI PMC
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 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
Emms DM, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 2015;16:157. doi: 10.1186/s13059-015-0721-2. PubMed DOI PMC
Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–1797. doi: 10.1093/nar/gkh340. PubMed DOI PMC
Capella-Gutierrez 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
Wang HC, Minh BQ, Susko E, Roger AJ. Modeling site heterogeneity with posterior mean site frequency profiles accelerates accurate phylogenomic estimation. Syst Biol. 2018;67(2):216–235. doi: 10.1093/sysbio/syx068. PubMed DOI
Lartillot N, Rodrigue N, Stubbs D, Richer J. PhyloBayes MPI: phylogenetic reconstruction with infinite mixtures of profiles in a parallel environment. Syst Biol. 2013;62(4):611–615. doi: 10.1093/sysbio/syt022. PubMed DOI
Kostygov AY, Frolov AO, Malysheva MN, Ganyukova AI, Chistyakova LV, Tashyreva D, Tesařová M, Spodareva VV, Režnarová J, Macedo DHF et al: Cell cycle analysis dataset for Vickermania. 2020. Figshare doi: 10.6084/m9.figshare.13154483.
Kostygov AY, Frolov AO, Malysheva MN, Ganyukova AI, Chistyakova LV, Tashyreva D, Tesařová M, Spodareva VV, Režnarová J, Macedo DHF et al: Motility analysis dataset for Vickermania. 2020. Figshare doi: 10.6084/m9.figshare.13154378.
Multiple and frequent trypanosomatid co-infections of insects: the Cuban case study
Comparative Analysis of Three Trypanosomatid Catalases of Different Origin
Genomics of Trypanosomatidae: Where We Stand and What Needs to Be Done?
Diverse telomeres in trypanosomatids
Euglenozoa: taxonomy, diversity and ecology, symbioses and viruses
The Remarkable Metabolism of Vickermania ingenoplastis: Genomic Predictions