Cell Division of Giardia intestinalis : Flagellar Developmental Cycle Involves Transformation and Exchange of Flagella between Mastigonts of a Diplomonad Cell

Abstract

Giardia intestinalis is a binucleated diplomonad possessing four pairs of flagella of distinct location and function. Its pathogenic potential depends on the integrity of a complex microtubular cytoskeleton that undergoes a profound but poorly understood reorganization during cell division. We examined the cell division of G. intestinalis with the aid of light and electron microscopy and immunofluorescence methods and present here new observations on the reorganization of the flagellar apparatus in the dividing Giardia. Our results demonstrated the presence of a flagellar maturation process during which the flagella migrate, assume different position, and transform to different flagellar types in progeny until their maturation is completed. For each newly assembled flagellum it takes three cell cycles to become mature. The mature flagellum of Giardia is the caudal one that possesses a privileged basal body at which the microtubules of the adhesive disk nucleate. In contrast to generally accepted assumption that each of the two diplomonad mastigonts develops separately, we found that they are developmentally linked, exchanging their cytoskeletal components at the early phase of mitosis. The presence of the flagellar maturation process in a metamonad protist Giardia suggests that the basal body or centriole maturation is a universal phenomenon that may represent one of the core processes in a eukaryotic cell.The flagella of eukaryotic protists undergo a remarkable morphogenetic transformation called flagellar developmental cycle, whereby a flagellum passes through a maturation process before assuming its final position in the cell. In contrast to nucleus and some other organelles, which complete their development in a single cell cycle, it is now evident that in many groups of protists flagella require more than one cell cycle to mature (2,26). In this respect, the behavior of flagellar structures in unicellular eukaryotes closely resembles that of centrioles in animal cells (3,25).On division of a flagellate, each daughter cell receives one half of parent flagella and/or basal bodies, while the other half arise de novo. This semiconservative distribution has been known for a long time (reviewed in reference 14). However, until a pioneering study of Melkonian et al. (24) it was not clear how unicellular protists maintain the structural and functional heterogeneity of their flagellar apparatus during division. The observations of Melkonian et al. (24) on the biflagellate heterokont green alga Nephroselmis olivacea provided the first evidence that the heterogeneous flagellar apparatus is conserved in progeny through transformation of a flagellar type during cell division and that a newly formed flagellum requires more than one cell cycle to complete its development. The flagellar transformation has been later found in other groups of unicellular algae (reviewed in reference 2) and in representatives of other taxonomic groups of flagellated freeliving protists (reviewed in reference 26). There are, however, several m...

Three-dimensional analysis of mitosis and cytokinesis in the binucleate parasiteGiardia intestinalis

“…4B). These data confirm and extend a recent report of flagellar rearrangements during mitosis in Giardia (Nohynkova et al, 2006).…”

“…This basal body, with its associated flagellum, may play an indirect role in spindle nucleation and organization; its association with a spindle pole may ensure its proper segregation to the daughter cells. Our data support the recent description of movements of flagellar complexes during cell division (Nohynkova et al, 2006).…”

An actin cytoskeleton with evolutionarily conserved functions in the absence of canonical actin-binding proteins

“…During mitosis, the anterior, dorsal, and ventral flagella pairs (Fig. 2B) are repositioned by an unknown mechanism (21,22). Coincidentally, a cloud of actin was observed around the corresponding internal axonemes.…”

Basal body movements orchestrate membrane organelle division and cell morphogenesis inTrypanosoma brucei

“…Therefore, it is impossible to separate our understanding of the duplication and segregation of centrosomes and basal bodies from the wider implications for cell morphogenesis. In many cells, light microscopy has shown that morphogenesis involves particular centrosomal or basal body movements, and electron microscopy has allowed the definition of the arrangements of component filaments and rootlets (Brugerolle, 1992;Nohynkova et al, 2006;Wright et al, 1985). In only a few cases do we know much about the detailed coordination of centrosomal/basal body duplication in terms of the subsequent inheritance of cell pattern and polarity.…”