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Eight Unique Basal Bodies in the Multi-Flagellated Diplomonad

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Eight Unique Basal Bodies in the Multi-Flagellated Diplomonad McInally and Dawson Cilia (2016) 5:21 DOI 10.1186/s13630-016-0042-4 Cilia REVIEW Open Access Eight unique basal bodies in the multi‑flagellated diplomonad Giardia lamblia Shane G. McInally and Scott C. Dawson* Abstract Giardia lamblia is an intestinal parasitic protist that causes significant acute and chronic diarrheal disease worldwide. Giardia belongs to the diplomonads, a group of protists in the supergroup Excavata. Diplomonads are characterized by eight motile flagella organized into four bilaterally symmetric pairs. Each of the eight Giardia axonemes has a long cytoplasmic region that extends from the centrally located basal body before exiting the cell body as a membrane- bound flagellum. Each basal body is thus unique in its cytological position and its association with different cytoskel- etal features, including the ventral disc, axonemes, and extra-axonemal structures. Inheritance of these unique and complex cytoskeletal elements is maintained through basal body migration, duplication, maturation, and their subse- quent association with specific spindle poles during cell division. Due to the complex composition and inheritance of specific basal bodies and their associated structures, Giardia may require novel basal body-associated proteins. Thus, protists such as Giardia may represent an undiscovered source of novel basal body-associated proteins. The develop- ment of new tools that make Giardia genetically tractable will enable the composition, structure, and function of the eight basal bodies to be more thoroughly explored. Keywords: Giardia lamblia, Basal body, Axonemes, Flagella Background comparisons of the cytoskeletal biology of Giardia to Giardia lamblia is a single-celled protistan parasite that other diverse flagellated protists [5]. causes acute and chronic diarrheal disease, primarily in A recent classification scheme categorized all known developing countries with inadequate sanitation and eukaryotes into six primary lineages or supergroups: water treatment [1, 2]. The life cycle of Giardia includes Opisthokonts (e.g., animals, fungi), Amoebozoa, Archae- two stages: the proliferative pathogenic trophozoite and plastida (e.g., plants and green algae), Rhizaria, Chromal- the dormant infective cyst. Giardia belongs to the diplo- veolata, and the Excavata [6, 7]. Excavate protists have monads, a group of protists in the supergroup Exca- been proposed to be a basal lineage of eukaryotes, clos- vata whose defining cytological characteristics include est to the common ancestor of all extant eukaryotes [8, eight motile flagella and two nuclei [3]. The discovery 9]. Yet, the evolutionary diversity within the Excavata of Giardia is attributed to Antonie van Leewenhoek, represents genetic distances greater than those between [4] who in 1681 observed teardrop-shaped flagellates plants, animals, and fungi [6]. Molecular phylogenetic in his own stool. More than 300 years later, our under- support for the monophyly of this group is controversial standing of Giardia cytoskeletal biology remains rudi- [10]. All known excavates have flagellated life cycle stages mentary. This deficit is primarily due to a lack of tools and, as a group, excavates are defined by the presence for genetic manipulation; however, improved cytologi- of posteriorly directed flagella and flagellar root struc- cal descriptions and increasing numbers of genomes of tures associated with the basal bodies [11]. However, Giardia species and other related diplomonads are aiding excavate biology is quite varied, and diversity within this group encompasses free-living, commensal, and parasitic forms of the following types of protists: Fornicata (diplo- *Correspondence: [email protected] monads, oxymonads, and retortamonads), Parabasalia, Department of Microbiology and Molecular Genetics, University of California Davis, One Shields Avenue, Davis, CA 95616, USA © 2016 McInally and Dawson. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons. org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. McInally and Dawson Cilia (2016) 5:21 Page 2 of 10 Euglenozoa (both euglenids and kinetoplastids), Heter- transition zones are restricted to small regions proxi- olobosea, Jakobida, and Preaxostyla. mal to the basal bodies rather than to the entire cyto- The swimming form of Giardia, or the “trophozoite,” plasmic axoneme [17]. The anterior basal bodies are has eight flagella that retain the canonical “9 + 2” struc- located toward the anterior ends of the two nuclei and ture of a motile flagellum [12]. Each flagellum also has oriented toward the anterior end of the cell. Basal bod- radial spokes, dynein arms, and outer doublet and central ies that nucleate the ventral, caudal, and posteriolateral pair microtubules [13, 14]. The eight flagella are organ- axonemes are positioned posteriorly below the two ante- ized into four bilaterally symmetrical pairs: the anterior, rior basal bodies and are oriented toward the posterior the caudal, the posteriolateral, and the ventral (Fig. 1). of the cell. Interphase trophozoites lack both barren and The basal bodies for all flagella are located in the anterior probasal bodies [18]. of the cell between the two nuclei. Each flagellar pair dif- Flagellar and basal body proteomics in Giardia have fers in its cytological position within the trophozoite and contributed to our overall understanding of flagellar in its association with ancillary structures. The coordi- structure and evolution; however, the selective isolation nated beating of Giardia’s eight motile flagella results in of axonemes or basal bodies from the extensive cytoskel- complex movements essential for motility and cell divi- eton in Giardia has proved to be challenging [19]. sion, and may aid in parasite attachment to the host gut Canonical basal body-associated proteins (e.g., centrin, epithelium [15, 16]; however, not all flagellar pairs have delta-tubulin and epsilon tubulin) and some compo- characteristic flagellar waveforms [15]. nents of the BBSome are present in the Giardia genome In general, eukaryotic flagella extend from a basal body (Table 1). Centrin localizes to two distinct clusters or centriole and are surrounded by a specialized flagel- adjacent to the two nuclei during interphase, colocaliz- lar membrane after they project from the cell surface. In ing with the flagellar basal bodies [20]. Consistent with contrast to other flagellated protists, each of the eight observations in other flagellated cells, gamma-tubulin Giardia axonemes has a long cytoplasmic region that also localizes to flagellar basal bodies during interphase; extends from a centrally located basal body before exiting however, gamma-tubulin localization is restricted only the cell body as a membrane-bound flagellum (Fig. 1 and to flagella that are newly produced during cell division see [16]). The ratio of the length of the cytoplasmic region [18]. to the membrane-bound portion varies between each fla- Notably, more than 1000 hypothetical proteins (e.g., gellar pair (e.g., over two-thirds of the length of the cau- those lacking significant similarity to proteins in other dal axonemes is in the cytoplasmic region, whereas only organisms) have been identified from the Giardia a third of the anterior axoneme is cytoplasmic). The ante- genome, and this genetic novelty is reflected in the analy- rior axonemes cross over the ventral disc spiral before ses of basal body [19] and cytoskeletal proteomes [21]. exiting on the right and left sides of the anterior region Proteins localizing to basal bodies may be structural com- of the cell. The distance from the exit point from the cell ponents or may merely dock at basal bodies before they body to the flagellar tip is about 12 µm. Running longi- are transported to other parts of the cell. Many known tudinally along the anterior-posterior axis of the cell, the basal body proteins are confirmed in the Giardia genome two caudal axonemes exit the cell body and extend about by homology or from localization studies (see centrin 7 µm at the posterior end. The ventral axonemes exit (GL50803_6744) and caltractin (GL50803_104685) in and extend about 14 µm on the ventral side in the “lat- Table 1 and imaged in Fig. 2). Other proteins identi- eral shield” region posterior to the disc. The posteriolat- fied as basal body proteins by comparative proteom- eral axonemes angle outward at the lower third of the cell ics lack basal body localization in Giardia (e.g., FAP52 body, extending about 8 µm from the cell body. Electron- (GL50803_15956) and PACRG1 (GL50803_15455), see dense “ciliary pockets” are found at the regions where Table 1), or localize to other cytoskeletal structures in each flagellum exits the cell body [17]. This review pre- addition to the basal bodies (e.g., GL50803_8557 and sents detailed findings concerning the structure, dupli- GL50803_29796, see Table 1, and imaged in Fig. 2). Fur- cation, and migration of the eight unique Giardia basal thermore, Giardia has proteins that localize to some or bodies during the parasite life cycle. all basal bodies, but lack homology to
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