The development and evolution of actin-containing organelles during spermiogenesis of a primitive nematode

Spermatogenesis in the primitive marine nematode Sphaerolaimus hirsutus (Chromadoria, Sphaerolaimidae) was investigated by examining the ultrastructure and cytochemistry. Spermatozoa are lenticular cells of about 15 microns in diameter and are devoid of flagellum and acrosome as in other nematodes. In spermatocytes, dictyosomes produced transient structures, the fibrous body-membranous organelle complexes (FB-MO). In spermatids, the FBs were arranged as cartwheel spokes, with the FBs in the centre and the MOs at the periphery. The FBs were first made up of parallel fibres and surrounded by a membrane, then, in a later stage, showed a dense central structure with a surrounding vermiculate region and were devoid of membrane. The FBs contain actin as shown by immunofluorescence using a monoclonal anti-actin antibody and by affinity cytochemistry using fluorescent phalloidin. MOs contained mainly F-actin as shown by their labelling by phalloidin. In spermatozoa, the MOs were no longer peripheral but arranged on a ring in the central region of the cell and the FBs disappeared to form the cytoskeleton of the cell outer region. It was assumed, by analogy with the ultrastructure of other nematodes, that this cytoskeleton was made up of major-sperm-protein (MSP). Labelling of spermatids of Caenorhabditis elegans also revealed the presence of actin, but cells and actin spots were very small. This demonstrates the interest of Sphaerolaimus as a giant sperm model in which fibrous bodies and membranous organelles can be distinguished. In the few species in which it has been studied (C elegans and Ascaris suum), MSP is thought to constitute in spermatozoa a motile cytoskeleton excluding the presence of actin. However, the present study of Sphaerolaimus shows that the actin cytoskeleton is present during nematode spermiogenesis.