Description of Zelonia daumondi sp. nov. (Trypanosomatidae: Leishmaniinae)

M.N. Malysheva, A.I. Ganyukova, D.O. Drachko, A.Y. Kostygov & A.O. Frolov

Abstract. Using light and electron microscopy, as well as molecular phylogenetic methods, we described a new species of monoxenous trypanosomatids, Zelonia daumondi sp. nov., based on three isolates collected in northwestern Russia: two from the predatory pentatomid bug Picromerus bidens (Linnaeus, 1758) and one from an overwintering female mosquito Culiseta annulata (Schrank, 1776). This is the first record of a member of the genus Zelonia Shaw, Camargo et Teixeira, 2018 in the Holarctic Region and the most northern one in the world. All three studied isolates had identical sequences of the 18S rRNA and gGAPDH genes, justifying their assignment to a single species. An isolate previously documented in the lygaeid bug Stalagmostethus fuscatus (Turton, 1802) from Madagascar was found to belong to the same species, as determined by the 18S rRNA gene sequence, thereby demonstrating a wide geographic range of the new species.

Key words: phylogeny, morphology, ultrastructure, Picromerus bidens, Culiseta annulata, new species

Zoosystematica Rossica, 2023, 32(2): 252–268 ▪ Published online 22 November 2023

https://doi.org/10.31610/zsr/2023.32.2.252 ▪ Open full article

Electronic supplementary material

GenBank accession numbers of sequences used in the phylogenetic analysis

References

Abramoff M.D., Magalhaes P.J. & Ram S.J. 2004. Image processing with ImageJ. Biophotonics Intern, 11(7): 36–42.

Barratt J., Kaufer A., Peters B., Craig D., Lawrence A., Roberts T., Lee R., McAuliffe G., Stark D. & Ellis J. 2017. Isolation of novel trypanosomatid, Zelonia australiensis sp. nov. (Kinetoplastida: Trypanosomatidae) provides support for a Gondwanan origin of dixenous parasitism in the Leishmaniinae. PLOS Neglected tropical Diseases, 11(1): e0005215. https://doi.org/10.1371/journal.pntd.0005215

Boucinha C., Caetano A.R., Santos H.L., Helaers R., Vikkula M., Branquinha M.H., Dos Santos A.L.S., Grellier P., Morelli K.A. & d’Avila-Levy C.M. 2020. Analysing ambiguities in trypanosomatids taxonomy by barcoding. Memorias do Instituto Oswaldo Cruz, 115: e200504. https://doi.org/10.1590/0074-02760200504

Dedet J.P., Geoffroy B. & Benichou J.C. 2007. Herpetomonas dedonderi n. sp. (Sarcomastigophora, Trypanosomatidae) from Haemagogus janthinomys Dyar, 1921 (Diptera, Culicidae). Journal of Protozoology, 33(4): 530–533. https://doi.org/10.1111/j.1550-7408.1986.tb05657.x

Espinosa O.A., Serrano M.G., Camargo E.P., Teixeira M.M.G. & Shaw J.J. 2018. An appraisal of the taxonomy and nomenclature of trypanosomatids presently classified as Leishmania and Endotrypanum. Parasitology, 145(4): 430–442. https://doi.org/10.1017/S0031182016002092

Fernandes A.C.S., Soares D.C., Neves R.F.C., Koeller C.M., Heise N., Adade C.M., Frases S., Meyer-Fernandes J.R., Saraiva E.M. & Souto-Padron T. 2020. Endocytosis and exocytosis in Leishmania amazonensis are modulated by bromoenol lactone. Frontiers in cellular and infection Microbiology, 10: 39. https://doi.org/10.3389/fcimb.2020.00039

Field M.C., Natesan S.K., Gabernet-Castello C. & Koumandou V.L. 2007. Intracellular trafficking in the trypanosomatids. Traffic, 8(6): 629–639. https://doi.org/10.1111/j.1600-0854.2007.00558.x

Frolov A.O., Kostygov A.Y. & Yurchenko V. 2021. Development of monoxenous trypanosomatids and phytomonads in insects. Trends in Parasitology, 37(6): 538–551. https://doi.org/10.1016/j.pt.2021.02.004

Ganyukova A.I., Malysheva M.N., Smirnov P.A. & Frolov A.O. 2019. Crithidia dobrovolskii sp. n. (Kinetoplastida: Trypanosomatidae) from parasitoid fly Lypha dubia (Diptera: Tachinidae): morphology and phylogenetic position. Protistology, 13(4): 206–214. https://doi.org/10.21685/1680-0826-2019-13-4-4

Gerasimov E.S., Kostygov A.Y., Yan S. & Kolesnikov A.A. 2012. From cryptogene to gene? ND8 editing domain reduction in insect trypanosomatids. European Journal of Protistology, 48(3): 185–193. https://doi.org/10.1016/j.ejop.2011.09.002

Hammer Ø., Harper D.A.T. & Ryan P.D. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia electronica, 4(1): 9.

Kalyaanamoorthy S., Minh B.Q., Wong T.K.F., von Haeseler A. & Jermiin L.S. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14(6): 587–589. https://doi.org/10.1038/nmeth.4285

Kaufer A., Ellis J., Stark D. & Barratt J. 2017. The evolution of trypanosomatid taxonomy. Parasites & Vectors, 10(1): 287. https://doi.org/10.1186/s13071-017-2204-7

Kostygov A.Y., Dobáková E., Grybchuk-Ieremenko A., Váhala D., Maslov D.A., Votýpka J., Lukeš J. & Yurchenko V. 2016. Novel trypanosomatid–bacterium association: evolution of endosymbiosis in action. mBio, 7(2): e01985–01915. https://doi.org/10.1128/mBio.01985-15

Kostygov A.Y. & Frolov A.O. 2007. Leptomonas jaculum (Leger, 1902) Woodcock 1914: a leptomonas or a blastocrithidia? Parazitologiya, 41(2): 126–136. (In Russian).

Kostygov A.Y., Karnkowska A., Votýpka J., Tashyreva D., Maciszewski K., Yurchenko V. & Lukeš J. 2021. Euglenozoa: taxonomy, diversity and ecology, symbioses and viruses. Open Biology, 11(3): 200407. https://doi.org/10.1098/rsob.200407

Kostygov A.Y. & Yurchenko V. 2017. Revised classification of the subfamily Leishmaniinae (Trypanosomatidae). Folia parasitologica, 64: 020. https://doi.org/10.14411/fp.2017.020

Králová J., Grybchuk-Ieremenko A., Votýpka J., Novotný V., Kment P., Lukeš J., Yurchenko V. & Kostygov A.Y. 2019. Insect trypanosomatids in Papua New Guinea: high endemism and diversity. International Journal for Parasitology, 49(13–14): 1075–1086. https://doi.org/10.1016/j.ijpara.2019.09.004

Kumar S., Stecher G., Li M., Knyaz C. & Tamura K. 2018. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35(6): 1547–1549. https://doi.org/10.1093/molbev/msy096

Link F., Borges A.R., Jones N.G. & Engstler M. 2021. To the surface and back: exo- and endocytic pathways in Trypanosoma brucei. Frontiers in cell and developmental Biology, 9: 720521. https://doi.org/10.3389/fcell.2021.720521

Maslov D.A., Lukeš J., Jirků M. & Simpson L. 1996. Phylogeny of trypanosomes as inferred from the small and large subunit rRNAs: implications for the evolution of parasitism in the trypanosomatid protozoa. Molecular and biochemical Parasitology, 75(2): 197–205. https://doi.org/10.1016/0166-6851(95)02526-x

Maslov D.A., Yurchenko V.Y., Jirků M. & Lukeš J. 2010. Two new species of trypanosomatid parasites isolated from Heteroptera in Costa Rica. Journal of eukaryotic Microbiology, 57(2): 177–188. https://doi.org/10.1111/j.1550-7408.2009.00464.x

Nguyen L.T., Schmidt H.A., von Haeseler A. & Minh B.Q. 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32(1): 268–274. https://doi.org/10.1093/molbev/msu300

Noyes H.A., Arana B.A., Chance M.L. & Maingon R. 1997. The Leishmania hertigi (Kinetoplastida; Trypanosomatidae) complex and the lizard Leishmania: their classification and evidence for a neotropical origin of the Leishmania – Endotrypanum clade. Journal of eukaryotic Microbiology, 44(5): 511–517. https://doi.org/10.1111/j.1550-7408.1997.tb05732.x

Overath P. & Engstler M. 2004. Endocytosis, membrane recycling and sorting of GPI-anchored proteins: Trypanosoma brucei as a model system. Molecular Microbiology, 53(3): 735–744. https://doi.org/10.1111/j.1365-2958.2004.04224.x

Podlipaev S.A. & Frolov A.O. 1987. Description and laboratory cultivation of Blastocrithidia miridarum sp. n. (Mastigophora, Trypanosomatidae). Parazitologiya, 21(4): 545–552. (In Russian).

R Core Team. 2022. The R Project for Statistical Computing [online]. Vienna: R Foundation for Statistical Computing. http://www.r-project.org/ [viewed 23 July 2022].

Reynolds E.S. 1963. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Journal of cell Biology, 17(1): 208–212. https://doi.org/10.1083/jcb.17.1.208

Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Hohna S., Larget B., Liu L., Suchard M.A. & Huelsenbeck J.P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3): 539–542. https://doi.org/10.1093/sysbio/sys029

Schaefer C.W. & Panizzi A.R. 2000. Heteroptera of economic importance. Boca Raton: CRC Press. 828 p.

Silverman J.S., Muratore K.A. & Bangs J.D. 2013. Characterization of the late endosomal ESCRT machinery in Trypanosoma brucei. Traffic, 14(10): 1078–1090. https://doi.org/10.1111/tra.12094

Votýpka J., Kment P., Yurchenko V. & Lukeš J. 2020. Endangered monoxenous trypanosomatid parasites: a lesson from island biogeography. Biodiversity and Conservation, 29(13): 3635–3667. https://doi.org/10.1007/s10531-020-02041-2

Wheeler R.J., Sunter J.D. & Gull K. 2016. Flagellar pocket restructuring through the Leishmania life cycle involves a discrete flagellum attachment zone. Journal of cell Science, 129(4): 854–867. https://doi.org/10.1242/jcs.183152

Yurchenko V., Lukeš J., Jirků M., Zeledon R. & Maslov D.A. 2006. Leptomonas costaricensis sp. n. (Kinetoplastea: Trypanosomatidae), a member of the novel phylogenetic group of insect trypanosomatids closely related to the genus Leishmania. Parasitology, 133(5): 537–546. https://doi.org/10.1017/S0031182006000746

Volume, Year: