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

Abstract

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.

Crithidia mellificae infection in different mammalian species in Brazil

“…The Kinetoplastea class (Excavata: Euglenozoa) is composed of free-living and parasitic protozoan species ( Adl et al, 2019 ). This class includes the Trypanosomatidae family, consisting of 25 genera ( d’Avila-Levy et al, 2015 ; Maslov et al, 2019 ; Kostygov et al, 2020 ; Lukeš et al, 2021 ) that include obligatory parasites of invertebrates, vertebrates, and plant hosts ( Hoare, 1966 ; Vickerman, 1976 ; Lukeš et al, 2014 ). These species are traditionally classified according to the number of hosts that they infect during their life cycle: monoxenous species—those that have only one host, usually an invertebrate host; and dixenous species—those that require an invertebrate and a vertebrate or plant host ( Hoare, 1966 ).…”

“…With the improvement of molecular biology tools and an increasing number of phylogenetic studies, seven subfamilies have been recognized for the Trypanosomatidae family: Leishmaniinae ( Jirků et al, 2012 , Kostygov and Yurchenko, 2017 ); Blechomonadinae ( Votýpka et al, 2013 ); Paratrypanosomatinae ( Flegontov et al, 2013 ); Strigomonadinae ( Votýpka et al, 2014 ); Phytomonadinae ( Yurchenko et al, 2016 ); Trypanosomatinae ( Maslov et al, 2019 ) and Blastocrithidiinae ( Lukeš et al, 2021 ). Nineteen genera are classified as monoxenous trypanosomatids ( d’Avila-Levy et al, 2015 ; Kaufer et al, 2017 ; Kostygov et al, 2020 ; Lukeš et al, 2021 ): Angomononas , Blastocrithidia , Blechomonas , Crithidia , Herpetomonas , Kentomonas , Jaenimonas, Lafontella , Leptomonas , Lotmaria , Novymonas , Obuscuromonas, Paratrypanosoma , Rhynchoidomonas , Sergeia , Strigonomonas, Vickermania, Wallacemonas and Zelonia . Usually, their hosts are invertebrates from the Diptera, Hemiptera, Hymenoptera and Siphonaptera orders ( Kozminsky et al, 2015 ).…”

The Remarkable Metabolism of Vickermania ingenoplastis: Genomic Predictions

“…Interestingly, the same genes have been lost from the genome of Phytomonas spp. [ 25 ], further supporting the evolutionary relatedness of these genera [ 12 ].…”

“…As an adaptation to these combined gene losses, Phytomonas spp. and V. ingenoplastis have drastically augmented their capacity for carbohydrate metabolism either by an increase in the copy number of glycolytic genes and/or the overall number of glycosomes in the cytosol [ 12 , 14 , 55 ]. Nevertheless, a critical difference between these two trypanosomatids is that V. ingenoplastis has increased its genome size by gene duplications, while Phytomonas spp.…”

“…Virtually all trypanosomatids are mono-flagellated (including an “amastigote” stage in some life cycles, which has an extremely short flagellum [ 7 ]) and use their flagella for attachment, movement, production of the extracellular vesicles, and environment sensing [ 8 , 9 , 10 , 11 ]. The only exception to this rule is members of the recently established genus Vickermania , V. ingenoplastis and V. spadyakhi [ 12 ]. These flagellates are adapted to the life in the fly midgut, to which they do not attach.…”