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Swimming with Protists: Perception, Motility and Flagellum Assembly

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Swimming with Protists: Perception, Motility and Flagellum Assembly REVIEWS Swimming with protists: perception, motility and flagellum assembly Michael L. Ginger*, Neil Portman‡ and Paul G. McKean* Abstract | In unicellular and multicellular eukaryotes, fast cell motility and rapid movement of material over cell surfaces are often mediated by ciliary or flagellar beating. The conserved defining structure in most motile cilia and flagella is the ‘9+2’ microtubule axoneme. Our general understanding of flagellum assembly and the regulation of flagellar motility has been led by results from seminal studies of flagellate protozoa and algae. Here we review recent work relating to various aspects of protist physiology and cell biology. In particular, we discuss energy metabolism in eukaryotic flagella, modifications to the canonical assembly pathway and flagellum function in parasite virulence. Protists The canonical ‘9+2’ microtubule axoneme is the prin- of inherited pathologies (or ciliopathies), including Eukaryotes that cannot be cipal feature of many motile cilia and flagella and is infertility, chronic respiratory disease, polycystic kid- classified as animals, fungi or one of the most iconic structures in cell biology. The ney disease and syndromes that include Bardet–Biedl, plants. The kingdom Protista origin of the eukaryotic flagellum and cilium is ancient Alstrom and Meckel syndrome6–12. Even illnesses such includes protozoa and algae. and predates the radiation, over 800 million years ago, as cancer, diabetes and obesity have been linked to cili- 1 6 Ciliates of the lineages that gave rise to extant eukaryotes . ary defects . The biological basis for some ciliopathies A ubiquitous group of protists, Therefore the absence of cilia and flagella from yeast, is undoubtedly defective sensing (an essential function members of which can be many fungi, red algae and higher plants are all examples provided by cilia), rather than defects in the assembly found in many wet of secondary loss. process or motility. Yet understanding the role that environments. Ciliates are characterized by the hair-like In animals and microorganisms that have retained defective ciliogenesis or ciliary function plays in the cell covering of the cell body the ability to assemble a cilium or flagellum, the motility biology of complex human diseases is challenging, not by hundreds of short cilia. provided by these organelles (BOX 1) often plays a crucial least because it is difficult to propagate and maintain cili- Ciliary movement contributes role in survival, development, cell feeding and repro- ated tissues and cells in culture. Many protist flagellates, to movement, cytokinesis and protists ciliates predation on other microbes. duction. Some , such as and the African by contrast, are more experimentally tractable, and for trypanosome Trypanosoma brucei, always exist in a some (for example, C. reinhardtii, trypanosomes and flagellate form, and for these protists flagellum assem- the ciliates Paramecium tetraurelia and Tetrahymena bly and motility are integral to cell morphogenesis and thermophila (FIG. 1a–f)) key biological questions can division. In other protists, such as the biflagellate green be addressed using either reverse or forward genetics. alga Chlamydomonas reinhardtii, the interchangeability In particular, stable transformation of C. reinhardtii of the flagellar basal body and the mitotic centriole is and T. brucei to produce mutant cells in which target evident2,3. The importance of flagellar biology in sexual genes are subjected to either constitutive or inducible development is nicely illustrated in apicomplexan para- RNA interference (RNAi) provides a powerful approach 4 *School of Health and sites . For some apicomplexans (such as Plasmodium to study gene function. Thus, using protists as model Medicine, Division of spp. and Toxoplasma gondii), but interestingly not for systems enables microbiologists to study aspects of flag- Biomedical and Life Sciences, others (such as Theileria spp. and Cryptosporidium hom- ellum function and assembly that are widely conserved. Lancaster University, Lancaster LA1 4YQ, UK. inis), the sexual stage of the parasite life cycle requires Such studies can be informative with regard to the study ‡Sir William Dunn School of de novo formation of flagella by male gametes. In these of human ciliopathies. Pathology, University of species, as well as in many other microorganisms, it is In this Review we consider new discoveries regarding Oxford, South Parks Road, environmental changes that provide the cue for flagellum flagellum assembly and function that pertain to various Oxford, OX1 3RE, UK. formation. aspects of protist cell biology and physiology. We first Correspondence to M.L.G. e-mail: m.ginger@lancaster. Cilium formation is essential for mouse embryonic describe the key features of a typical ‘9+2’ axoneme, and 5 ac.uk development , and defects in ciliogenesis or ciliary then briefly discuss some variations that exist in pro- doi:10.1038/nrmicro2009 function in humans are associated with a broad range tists. We will then focus on four topics: protist flagella as 838 | NOVEMBER 2008 | VOLUME 6 www.nature.com/reviews/micro REVIEWS Centriole Box 1 | Ciliary and flagellar beating A barrel-shaped organelle that contains nine triplet-microtu- For swimming microorganisms and flagellate sperm, fluid viscosity, rather than inertia, is the dominant force affecting bules and that forms the basal productive locomotion — that is, these cells swim at low Reynolds numbers149. For the purpose of this review, the body from which a flagellar differences in the definitions between flagella and cilia will not be considered. Many flagellate cells readily switch during axoneme is extended. In some swimming from using ciliary to flagellar waveforms, and vice versa124,136,150. However, the use of the term cilium perhaps eukaryotes, centrioles are helps to avoid confusion with bacterial flagella, which are structurally completely different organelles. required for mitosis. In In motile axonemes, formation of transient bridges between dynein arms on outer-doublet A-tubules with the B-tubule Chlamydomonas reinhardtii, of the adjacent outer-doublet microtubule results in microtubule sliding15. Sliding is constrained, however, due to other flagellar basal bodies are attachments, such as nexin links between adjacent outer-doublets, which convert applied force into bending. Ciliary style uncoupled from their associated axonemes to motility is characterized by asymmetric waveforms: an effective stroke provides thrust; the accompanying recovery stroke function as mitotic centrioles returns the cilium to its starting position with limited viscous resistance. For flagellates with small numbers of flagella (for during division. example, 1, 2 or 4), ciliary waveforms are typically essentially planar. For organisms such as Paramecium or in ciliated animal tissues, in which fluids move rapidly across cell surfaces (such as, across the respiratory epithelium), energetically Apicomplexa efficient151 coordination of many closely opposed cilia (metachronal patterning) uses three-dimensional waveforms. In A phylum of obligate contrast to ciliary waveforms, a flagellar waveform is propagated with a flutter-kick-style motion. The phototactic intracellular parasites that behaviour of the flagellate alga Chlamydomonas reinhardtii in response to changing light intensity provides a classic includes several important paradigm for understanding how waveform changes are signalled123,124: base-to-tip ciliary beating propels C. reinhardtii human pathogens, such as the forward, but a sudden increase in light intensity results in a brief Ca2+-signalled switch to a planar symmetrical flagellar malarial parasite Plasmodium falciparum, the opportunistic waveform, which mediates backwards swimming. By contrast, the characteristic symmetrical flagellar waveform in 136 pathogen Toxoplasma gondii trypanosomatids is occasionally punctuated by wave-reversal and by the generation of a ciliary type beat . and the water-borne parasite Cryptosporidium hominis. ‘metabolic organelles’; diverse aspects of flagellum tuzetae31 and the ‘9+0’ axonemes that are assembled by RNAi diatom A commonly used experimental assembly and maintenance; protist flagella as sensory male centric gametes. The helical motility of such tool to silence genes. In organelles; and exploiting motility perturbation as a axonemes is independent of a CP–radial spoke regula- Trypanosoma brucei, RNAi is a novel drug target against the parasite that causes African tory system and is different from the waveforms that are very tractable reverse genetic sleeping sickness. Wider comparisons with animal cell generally associated with ‘9+2’ axonemes. Interestingly, approach for studying gene biology are made when possible. recent comparative genomic analyses have revealed that function. Less robust and often unstable RNAi systems are also in the centric diatom Thalassiosira pseudonana gamete available for motility studies in Flagellum structure and composition motility occurs in the absence of known inner-dynein- Chlamydomonas reinhardtii. The first description of axoneme structure was made arm homologues, as well as in the absence of CP–radial by Manton and Clarke13, and principal features that spoke apparatuses32,33. Reynolds number A measure of the ratio of are evident in transverse sections through most ‘9+2’ The extent of architectural diversity is illustrated inertial forces to viscous forces microtubule axonemes are highlighted in FIG. 1g. Notable further with the observation
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