Flagellar apparatus structure of choanoflagellates
© Karpov. 2016
Received: 22 October 2015
Accepted: 18 February 2016
Published: 4 May 2016
Phylum choanoflagellata is the nearest unicellular neighbor of metazoa at the phylogenetic tree. They are single celled or form the colonies, can be presented by naked cells or live in theca or lorica, but in all cases they have a flagellum surrounded by microvilli of the collar. They have rather uniform and peculiar flagellar apparatus structure with flagellar basal body (FB) producing a flagellum, and non-flagellar basal body (NFB) lying orthogonal to the FB. Long flagellar transition zone contains a unique structure among eukaryotes, the central filament, which connects central microtubules to the transversal plate. Both basal bodies are composed of triplets and interconnected with fibrillar bridge. They also contain the internal arc-shaped connectives between the triplets. The FB has prominent transitional fibers similar to those of chytrid zoospores and choanocytes of sponges, and a radial microtubular root system. The ring-shaped microtubule organizing center (MTOC) produces radial root microtubules, but in some species a MTOC is represented by separate foci. The NFB has a narrow fibrillar root directed towards the Golgi apparatus in association with membrane-bounded sac. Prior to cell division, the basal bodies replicate and migrate to poles of elongated nucleus. The basal bodies serve as MTOCs for the spindle microtubules during nuclear division by semiopen orthomitosis.
Body of the primer
Choanoflagellates: Monosiga ovata, Codosiga botrytis, Desmarella thienemanni, Salpingoeca sp.
The representatives of Craspedida, M. ovata, C. botrytis, D. thienemanni and Salpingoeca sp., are better studied in respect of flagellar apparatus structure. They have rather uniform flagellar apparatus, composed of one flagellum and two basal bodies, as well as all the other choanoflagellates, differing from each other by the microtubular root organization.
Basal body structure
The flagellar apparatus of choanoflagellates is composed of one flagellum and two orthogonal basal bodies (flagellar and non-flagellar ones) producing the microtubular and fibrillar roots. Both basal bodies are mainly similar to each other, contain triplets of microtubules.
The long transition zone contains a transversal plate located above the cell surface. The central two microtubules within the flagellar transition zone are replaced by a single central filament of some considerable length, which connects the transversal plate with central tubules (Fig. 4). Sometimes the thickness in the center of transversal plate is present. A central filament has been described for the first time by D. Hibberd in C. botrytis  and then was found in all investigated choanoflagellates [6–8, 13, 18]. This central filament is unique for choanoflagellates as no such structure was found in the flagellar transition zone of other eukaryotes .
In M. ovata, the proximal portion of flagellar basal body is surrounded by a ring of electron dense material from which the root, containing approximately 60 radially arranged microtubules, originates (Fig. 5a). In the immediate region of the flagellar base, the microtubules are stacked in two layers and two additional rings of electron dense material fill the spaces between the microtubules (Fig. 5a). From the flagellar base, the microtubules pass outwards and laterally just beneath the plasma membrane for about one-third or half the length of the cell (Figs. 1, 5c). They are probably responsible for shaping the apical end of the cell. The organization of the root microtubules around the FB is the same in many members of the Acanthoecida and Salpingoeca . But the root organization in the naked Craspedida is more complex with the radial microtubules converging on 4–5 foci in C. botrytis  and D. thienemanni (Fig. 3b) and on two cylinders in Sphaeroeca volvox (Fig. 5b).
From the lower surface of NFB, a long, narrow, slightly striated, fibrillar root passes obliquely towards the Golgi apparatus (Figs. 1, 5c). It is associated with one surface of a membrane-bounded sac which extends from the region of the flagellar base and passes to about half way along the dictyosome. This fibrillar-membrane complex is closely associated with the dictyosome and its orientation appears to be determined by the relative position of the dictyosome with respect to the nucleus. In M. ovata, the fibrillar root can either be directed away from the end of the NFB or deflected backwards underneath the flagellar base.
The fibrillar bridge between the two basal bodies and the narrow striated fibrillar root passing in Golgi apparatus direction and closely applied to a membrane sac is probably present in all choanoflagellates .
Basal body life cycle and other functions
New basal bodies appear on the base of the old ones before cell division. Each basal body produces the nascent basal body (Fig. 5d). Then the flagellum is retracted into the cell and the axoneme is disassembled. The pairs of basal bodies each composed from the old and the new one migrate from each other to the poles of the prophases’ nucleus [10, 12]. Which basal body (the old or the new one) produces a new flagellum in the daughter cell is not clear at the moment. Both basal bodies present in the cyst of M. ovata . Thus, the FB and NFB present at all studied stages of the choanoflagellate life cycle function as a centrosome during mitosis.
Notable basal body findings
The notable finding about basal bodies of choanoflagellates is the central filament in the flagellar transition zone—a unique structure among eukaryotes. Another feature, which is also rare in protists, is a radial microtubular system. The differences in microtubular root organization reflect the peculiarities of choanoflagellates at the genus level [6, 11]. The prominent transition filaments are the characters of flagellar apparatus of chytridiomycete zoospores , and of the sponge choanocytes [23, 24], but the internal arc-shaped connectives in both the FB and NFBs have been found in the choanoflagellates only .
Future of basal body research in choanoflagellates
The flagellar apparatus structure has been studied in details in craspedid freshwater choanoflagellates [11, 13, 21]. Such information on marine representatives is rather poor at the moment [15–17, 20, 21] because of difficulties with fixation of marine cells. The central filament in the transition zone has been found in marine Stephanoeca diplocostata , but the other peculiarities are not clear. According to our general dogma, that the marine choanoflagellates are more ancient than the freshwater ones, we can propose that close attention to the flagellar apparatus of marine choanoflagellates can give new unexpected knowledge on the flagellar apparatus characters.
This work was partly supported by the FRBR Grant No. 15-04-03324.
The author declare that no competing interests.
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- Barr DJS. Chytridiomycota. In: McLaughlin DJ, McLaughlin EG, Lemke PA, editors. The mycota VII, part A: systematics and evolution. Berlin: Springer-Verlag; 2001. p. 93–112.Google Scholar
- Carr M, Leadbeater BSC, Hassan R, Nelson M, Baldauf SL. Molecular phylogeny of choanoflagellates, the sister group to Metazoa. PNAS. 2008;105:16641–6.View ArticlePubMedPubMed CentralGoogle Scholar
- Fairclough SR, Kramer E, Zeng Q, Young S, Robertson HM, Begovic E, Richter DJ, et al. Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta. Genome Biol. 2013;14:R15. doi:10.1186/gb-2013-14-2-r15.View ArticlePubMedPubMed CentralGoogle Scholar
- Hibberd DJ. Observations on the ultrastructure of the choanoflagellate Codosiga botrytis (Ehr.) Saville-Kent with special reference to the flagellar apparatus. J Cell Sci. 1975;17:191–219.PubMedGoogle Scholar
- James-Clark H. Conclusive proofs of the animality of the ciliate sponges, and of their affinities with the infusoria flagellata. Ann Mag Nat Hist Ser. 1868;3(19):13–8.Google Scholar
- Karpov SA. Ultrathin structure of choanoflagellate Sphaeroeca volvox. Tsitologia. 1981;23:991–6 (in Russian).Google Scholar
- Karpov SA. Ultrathin structure of choanoflagellate Monosiga ovata. Tsitologia. 1982;24:400–4 (in Russian).Google Scholar
- Karpov SA. Ultrathin structure of choanoflagellate Kentrosiga thienemanni. Tsitologia. 1985;27:947–9 (in Russian).Google Scholar
- Karpov SA. Flagellate phylogeny: ultrastructural approach. In: Leadbeater BSC, Green JC, editors. The flagellates systematics association special publications. London: Taylor and Francis; 2000. p. 336–60.Google Scholar
- Karpov SA, Leadbeater BSC. Cell and nuclear division in freshwater choanoflagellate Monosiga ovata. Eur J Protistol. 1997;33:323–34.View ArticleGoogle Scholar
- Karpov SA, Leadbeater BSC. The cytoskeleton structure and composition in choanoflagellates. J Euk Microbiol. 1998;45:361–7.View ArticleGoogle Scholar
- Karpov SA, Mylnikov AP. Preliminary observations on the ultrastructure of mitosis in choanoflagellates. Eur J Protistol. 1993;29:19–23.View ArticlePubMedGoogle Scholar
- Karpov SA, Zhukov BF. Phylum Choanomonada. In: Karpov SA, editor. Protista 1 handbook of zoology. St. Petersburg: Nauka; 2000. p. 321–36.Google Scholar
- King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, et al. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature. 2008;451:783–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Leadbeater BSC. Observations on the life-history and ultrastructure of the marine choanoflagellate Choanoeca perplexa Ellis. J Mar Biol Ass UK. 1977;57:285–301.View ArticleGoogle Scholar
- Leadbeater BSC. Life history and ultrastructure of a new marine species of Proterospongia (Choanoflagellida). J Mar Biol Ass UK. 1983;63:135–60.View ArticleGoogle Scholar
- Leadbeater BSC. Choanoflagellate organization with special reference to loricate taxa. In: Patterson DJ, Larsen J, editors. Free living heterotrophic flagellates. Oxford: University Press; 1991. p. 241–58.Google Scholar
- Leadbeater BSC. The choanoflagellates: evolution, biology and ecology. Cambridge: University Printing House; 2015.View ArticleGoogle Scholar
- Leadbeater BSC, Karpov S. Cyst Formation in a freshwater strain of the choanoflagellate Desmarella moniliformis kent. J Eukaryot Microbiol. 2000;47:433–9.View ArticlePubMedGoogle Scholar
- Leadbeater BSC, Morton C. A light and electron microscope study of the choanoflagellates Acanthoeca spectabilis ellis and A. brevipoda Ellis. Arch Microbiol. 1974;95:279–92.View ArticleGoogle Scholar
- Leadbeater BSC, Thomsen H. Order Choanoflagellida: an illustrated guide to the protozoa. 2nd ed. Lawrence: Society of Protozoologists; 2000. p. 14–38.Google Scholar
- Nitsche F, Carr M, Arndt H, Leadbeater BSC. Higher level taxonomy and molecular phylogenetics of the Choanoflagellatea. J Eukaryot Microbiol. 2011;58:452–62.View ArticlePubMedGoogle Scholar
- Pozdnyakov IR, Karpov SA. Flagellar apparatus structure of choanocyte in Sycon sp. and its significance for phylogeny of porifera. Zoomorphology. 2013;132:351–7.View ArticleGoogle Scholar
- Pozdnyakov IR, Karpov SA. Flagellar apparatus structure of choanocyte of sponge Haliclona sp. (Demospongiae, Haplosclerida) and its significance for taxonomy and phylogeny of Demospongiae. Zool Zhurn. 2015;94:1–8 (in Russian).Google Scholar
- Zhukov BF, Karpov SA. Freshwater choanoflagellates. Leningrad: Nauka; 1985 (in Russian).Google Scholar