Mirror-imaged doublets of Tetmemena pustulata: Implications for the development of left–right asymmetry

Abstract

Ciliated protozoa possess cellular axes reflected in the arrangement of their ciliature. Upon transverse fission, daughter cells develop an identical ciliary pattern, ensuring perpetuation of the cellular phenotype. Experimentally manipulated cells can be induced to form atypical phenotypes, capable of intraclonal propagation and regeneration after encystment. One such phenotype in the ciliate Tetmemena pustulata (formerly Stylonychia pustulata) is the mirror-imaged doublet. These cells possess two distinct sets of ciliature, juxtaposed on the surfaces in mirror image symmetry, with a common anterior–posterior axis. We have examined whether individual ciliary components of Tetmemena mirror-image doublets are mirror imaged. Ultrastructural analysis indicates that despite global mirror imaging of the ciliature, detailed organization of the membranelles is reversed in the mirror-image oral apparatus (OA), such that the ciliary effective stroke propels food away from the OA. Assembly of compound ciliary structures of both OAs starts out identically, but as the structures associated with the mirror-image OA continue to form, the new set of membranelles undergoes a 180° planar rotation on the ventral surface relative to the same structures in the typical OA. The overall symmetry of the OA thus appears to be separable from the more localized assembly of individual basal bodies. True mirror imagery of the membranelles would require new enantiomorphic forms of the individual ciliary components, particularly the basal bodies, which is never observed. These observations suggest a mechanistic hypothesis with implications for the development of left–right asymmetry not only in ciliates, but perhaps also in development of left–right asymmetry in general.