Spermiogenesis in the acoel Symsagittifera roscoffensis: nucleus-plasma membrane contact sites and microtubules.

Symsagittifera roscoffensis is a small marine worm found in the intertidal zone of sandy beaches around the European shores of the Atlantic. S. roscoffensis is a member of the Acoelomorpha, a group of flatworms formerly classified with the Platyhelminthes, but now recognised as Xenacoelomorpha, a separate phylum of disputed affinity. We have used electron microscopy to examine the process of spermiogenesis (the final stage of spermatogenesis) in S. roscoffensis, by which spermatids form highly elongated spermatozoa. Their nuclei are long and thread-like, running most of the cells length and during the process a pair of flagella are fully incorporated into the cell body. Two previously undescribed inter-organelle contact sites form at different stages of spermiogenesis. Strikingly, there is an extensive nucleus-plasma membrane contact site. Golgi-derived granules containing electron-dense filaments line up along the spermatid plasma membrane, undergo a conformational change, and donate material that forms a peri-nuclear layer that cements this contact site. We also show in earlier stage spermatids that the same granules are associated with microtubules, presumably for traffic along the elongating cell. We identify a second spermiogenesis-specific contact site where sheaths engulfing each internalising flagellum contact the nuclear envelope. Finally, detailed studies of the spermatozoon axonemes show that the central keel has varying numbers of microtubules along the length of the cell, and is likely to be a centriole derivative.