Abstract
Schistosomes infect hundreds of millions of people in the developing world. Transmission of these parasites relies on a stem cell-driven, clonal expansion of larvae inside a molluscan intermediate host. How this novel asexual reproductive strategy relates to current models of stem cell maintenance and germline specification is unclear. Here, we demonstrate that this proliferative larval cell population (germinal cells) shares some molecular signatures with stem cells from diverse organisms, in particular neoblasts of planarians (free-living relatives of schistosomes). We identify two distinct germinal cell lineages that differ in their proliferation kinetics and expression of a nanos ortholog. We show that a vasa/PL10 homolog is required for proliferation and maintenance of both populations, whereas argonaute2 and a fibroblast growth factor receptor-encoding gene are required only for nanos-negative cells. Our results suggest that an ancient stem cell-based developmental program may have enabled the evolution of the complex life cycle of parasitic flatworms. DOI:http://dx.doi.org/10.7554/eLife.00768.001.
Highlights
Schistosoma flatworms infect 230 million people worldwide and cause ∼250,000 deaths per year
In vitro transformation of miracidia into sporocysts triggered germinal cell proliferation (Yoshino and Laursen, 1995; Ivanchenko et al, 1999; Bixler et al, 2001): we observed these cells in mitosis as early as 24 hr post-transformation (∼0.2 mitoses per animal) (Figure 1C,D), which is consistent with the behavior of these cells in vivo after miracidia penetrate a snail host (Schutte, 1974)
Sm-ago2-1, Sm-vlg-3, and Sm-nanos-2, are upregulated in sporocysts, but with different kinetics (Figure 2C and Table 1; for clarity, the prefix ‘Sm’ will be omitted from gene names for the rest of the paper): ago2-1 increases steadily in expression throughout early sporocyst development; vlg-3 expression increases sharply following transformation, plateaus; and nanos-2 mRNA expression does not increase until 4 days post-transformation. To examine whether these genes are expressed in germinal cells, we developed a method for whole-mount RNA fluorescence in situ hybridization (FISH) in sporocysts
Summary
Schistosoma flatworms infect 230 million people worldwide and cause ∼250,000 deaths per year (van der Werf et al, 2003). These trematodes are transmitted through a life cycle that alternates between asexual and sexual generations in invertebrate intermediate and vertebrate definitive hosts, respectively (Clark, 1974; Shoop, 1988). The life cycle initiates as eggs are excreted from a mammalian host into freshwater, releasing ciliated, free-swimming larvae called miracidia that seek out and penetrate a snail intermediate host. Mature cercariae emerge from the snail into freshwater, burrow through the epidermis of mammalian hosts, migrate to species-specific niches in the host vascular system, develop to adulthood, and begin to reproduce sexually, thereby completing the life cycle. Asexual amplification inside of the snail is vital for propagation of schistosomes
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