Shape-shifting trypanosomes: Flagellar shortening followed by asymmetric division in Trypanosoma congolense from the tsetse proventriculus

Abstract

Trypanosomatids such as Leishmania and Trypanosoma are digenetic, single-celled, parasitic flagellates that undergo complex life cycles involving morphological and metabolic changes to fit them for survival in different environments within their mammalian and insect hosts. According to current consensus, asymmetric division enables trypanosomatids to achieve the major morphological rearrangements associated with transition between developmental stages. Contrary to this view, here we show that the African trypanosome Trypanosoma congolense, an important livestock pathogen, undergoes extensive cell remodelling, involving shortening of the cell body and flagellum, during its transition from free-swimming proventricular forms to attached epimastigotes in vitro. Shortening of the flagellum was associated with accumulation of PFR1, a major constituent of the paraflagellar rod, in the mid-region of the flagellum where it was attached to the substrate. However, the PFR1 depot was not essential for attachment, as it accumulated several hours after initial attachment of proventricular trypanosomes. Detergent and CaCl2 treatment failed to dislodge attached parasites, demonstrating the robust nature of flagellar attachment to the substrate; the PFR1 depot was also unaffected by these treatments. Division of the remodelled proventricular trypanosome was asymmetric, producing a small daughter cell. Each mother cell went on to produce at least one more daughter cell, while the daughter trypanosomes also proliferated, eventually resulting in a dense culture of epimastigotes. Here, by observing the synchronous development of the homogeneous population of trypanosomes in the tsetse proventriculus, we have been able to examine the transition from proventricular forms to attached epimastigotes in detail in T. congolense. This transition is difficult to observe in vivo as it happens inside the mouthparts of the tsetse fly. In T. brucei, this transition is achieved by asymmetric division of long trypomastigotes in the proventriculus, yielding short epimastigotes, which go on to colonise the salivary glands. Thus, despite their close evolutionary relationship and shared developmental route within the vector, T. brucei and T. congolense have evolved different ways of accomplishing the same developmental transition from proventricular form to attached epimastigote.

Non‐equivalence in old‐ and new‐flagellum daughter cells of a proliferative division in Trypanosoma brucei

“…Due to these modes of structure and organelle inheritance in T. brucei and related parasites, such as Trypanosoma cruzi and Trypanosoma vivax, dramatic changes to cell morphology, such as reduction of cell and flagellar length (Sharma et al, 2008;Kurup and Tarleton, 2014) and repositioning of cellular organelles during differentiation divisions (Rotureau et al, 2012;Ooi et al, 2016), are typically achieved by differential construction of the portion of the cell body that ultimately becomes the new-flagellum daughter cell. This was also observed for Trypanosoma congolense; moreover, in this parasite re-modelling of existing structures was recently also shown to be part of differentiation processes (Peacock et al, 2018).…”

Who Needs a Contractile Actomyosin Ring? The Plethora of Alternative Ways to Divide a Protozoan Parasite

“…T. brucei, T. congolense , and T. vivax have complex life cycles split between mammalian and tsetse fly hosts, comprising a series of morphologically and metabolically distinct stages. These may be replicative (bloodstream trypomastigotes in the mammal, and procyclic and epimastigote forms in the fly) or cell cycle arrested (Van Den Abbeele et al, 1999; Matthews, 2005; Gluenz et al, 2008; Rotureau et al, 2012; Capewell et al, 2016; Trindade et al, 2016; Peacock et al, 2018). Cell division has been best studied in T. brucei in the procyclic form; more limited studies in bloodstream and epimastigote forms have highlighted similarities alongside key structural/molecular differences.…”

Cell Cycle-Dependent Flagellar Disassembly in a Firebug Trypanosomatid Leptomonas pyrrhocoris

“…Flagellum disassembly/absorption is well documented in green algae and mammalian cells, where complete disassembly occurs prior to cell division (12, 13). In trypanosomatids, flagellar disassembly has been observed during the differentiation (14, 15), but not during the cell cycle (16).…”