Abstract
SummaryIn eukaryote pathogens, sex is an important driving force in spreading genes for drug resistance, pathogenicity, and virulence [1]. For the parasitic trypanosomes that cause African sleeping sickness, mating occurs during transmission by the tsetse vector [2, 3] and involves meiosis [4], but haploid gametes have not yet been identified. Here, we show that meiosis is a normal part of development in the insect salivary glands for all subspecies of Trypanosoma brucei, including the human pathogens. By observing insect-derived trypanosomes during the window of peak expression of meiosis-specific genes, we identified promastigote-like (PL) cells that interacted with each other via their flagella and underwent fusion, as visualized by the mixing of cytoplasmic red and green fluorescent proteins. PL cells had a short, wide body, a very long anterior flagellum, and either one or two kinetoplasts, but only the anterior kinetoplast was associated with the flagellum. Measurement of nuclear DNA contents showed that PL cells were haploid relative to diploid metacyclics. Trypanosomes are among the earliest diverging eukaryotes, and our results support the hypothesis that meiosis and sexual reproduction are ubiquitous in eukaryotes and likely to have been early innovations [5].
Highlights
Meiosis-specific proteins (MND1, DMC1, and HOP1) were expressed in T. b. brucei strain J10 [4], implying that meiosis might be an integral part of the trypanosome’s developmental cycle in the tsetse fly vector. To test this hypothesis and to obtain further information on the timing of meiosis, we extended the analysis to other strains and subspecies of T. brucei
Successful crosses of T. b. brucei, T. b. rhodesiense, and T. b. gambiense group 2 have been reported previously [8], this is the first indication that T. b. gambiense group 1 is capable of meiosis and, potentially, genetic exchange, despite lack of evidence of recombination in population genetics analyses [9, 10]
Sex provides the opportunity for new pathogen strains to arise by recombination, a phenomenon already suspected in T. b. rhodesiense [11], which has the capacity to become human infective by transfer of a single gene for human serum resistance (SRA) [12]
Summary
Trypanosomes expressing meiosis-specific genes were present in fly SG dissected between 14 and 38 days after infection (Figure 1C), with the highest frequency of expression around day 20. Gamete-like Cell-Cell Interactions Analysis of trypanosome crosses is facilitated by the incorporation of red fluorescent protein (RFP) or green fluorescent protein (GFP) into the parental clones, enabling hybrids to be identified by yellow fluorescence [3].
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