Identification of the meiotic life cycle stage of Trypanosoma brucei in the tsetse fly

Abstract

Elucidating the mechanism of genetic exchange is fundamental for understanding how genes for such traits as virulence, disease phenotype, and drug resistance are transferred between pathogen strains. Genetic exchange occurs in the parasitic protists Trypanosoma brucei , T. cruzi , and Leishmania major , but the precise cellular mechanisms are unknown, because the process has not been observed directly. Here we exploit the identification of homologs of meiotic genes in the T. brucei genome and demonstrate that three functionally distinct, meiosis-specific proteins are expressed in the nucleus of a single specific cell type, defining a previously undescribed developmental stage occurring within the tsetse fly salivary gland. Expression occurs in clonal and mixed infections, indicating that the meiotic program is an intrinsic but hitherto cryptic part of the developmental cycle of trypanosomes. In experimental crosses, expression of meiosis-specific proteins usually occurred before cell fusion. This is evidence of conventional meiotic division in an excavate protist, and the functional conservation of the meiotic machinery in these divergent organisms underlines the ubiquity and basal evolution of meiosis in eukaryotes.

Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life

“…Numerous examples illustrate how little we know about the actual life of eukaryotic microorganisms, even those studied for a very long time. The kinetoplastid protozoan Trypanosoma brucei (Euglenozoa), a causative agent of sleeping sickness, is one of the beststudied protist species, yet meiosis and gametes were only detected very recently (10,11). Although meiosis has thus far been considered to be very rare in trypanosomes, it may actually be more frequent, as both intraclonal and interclonal mating has been documented (10).…”

“…The kinetoplastid protozoan Trypanosoma brucei (Euglenozoa), a causative agent of sleeping sickness, is one of the beststudied protist species, yet meiosis and gametes were only detected very recently (10,11). Although meiosis has thus far been considered to be very rare in trypanosomes, it may actually be more frequent, as both intraclonal and interclonal mating has been documented (10). The sexual cycle of the ascomycete fungus Aspergillus fumigatus was described only in 2009 (12), i.e., nearly 150 y after the species was originally described, despite the fact that this ubiquitous causative agent of life-threatening invasive aspergillosis and important allergen causing severe asthma and sinusitis had been extensively studied for years (13).…”

DNA Repair Pathways in Trypanosomatids: from DNA Repair to Drug Resistance

“…The localization of four meiosis genes (Spo11, Dmc1, Hop1, and Mnd1) fused to yellow fluorescent protein (YFP) was monitored in the salivary glands of the tsetse fly. The expression of YFP-MND1, YFP-DMC1, and YFP-HOP1 was restricted to a subset of trypanosome epimastigotes in the salivary glands (224). These three proteins are all involved in the meiotic recombination in prophase I: MND1 stabilizes heteroduplexes after double-strand break formation, DMC1 is a recombinase homologous to RAD51, and HOP1 is a component of the lateral elements of the synaptomenal complex.…”

The languages of parasite communication

“…To date, the actual fusion event has only been observed in culture, but there is circumstantial evidence that it might also occur in the tsetse salivary glands. When flies were co-infected with trypanosomes expressing cytoplasmic red fluorescent protein or a tagged form of the meiotic marker HOP1, double-positive parasites were observed, compatible with protein exchange occurring before the formation and fusion of gametes [58]. Might this form of cell-cell communication occur in other flagellated parasites?…”