Vickermania gen. nov., trypanosomatids that use two joined flagella to resist midgut peristaltic flow within the fly hos

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RESEARCH ARTICLE

Open Access

Vickermania gen. nov., trypanosomatids that use two joined flagella to resist midgut peristaltic flow within the fly host Alexei Y. Kostygov1,2* , Alexander O. Frolov2, Marina N. Malysheva2, Anna I. Ganyukova2, Lyudmila V. Chistyakova2, Daria Tashyreva3, Martina Tesařová3, Viktoria V. Spodareva1,2, Jana Režnarová1, Diego H. Macedo1, Anzhelika Butenko1,3, Claudia M. d’Avila-Levy4, Julius Lukeš3,5 and Vyacheslav Yurchenko1,6

Abstract Background: The family Trypanosomatidae encompasses parasitic flagellates, some of which cause serious vectortransmitted 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. Keywords: Herpetomonas muscarum ingenoplastis, Cell cycle, Flagella connector, Trypanosoma brucei

* Correspondence: [email protected] 1 Life Science Research Centre, Faculty of Science, University of Ostrava, Chittussiho 10, 710 00 Ostrava, Czechia 2 Zoological Institute of the Russian Academy of Sciences, St. Petersburg 199034, Russia Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative