Basal body structure in Trichonympha
© Guichard and Gönczy. 2016
Received: 27 November 2015
Accepted: 10 February 2016
Published: 1 March 2016
Trichonympha is a symbiotic flagellate of many species of termites and of the wood-feeding cockroach. Remarkably, this unicellular organism harbors up to over ten thousand flagella on its surface, which serve to propel it through the viscous environment of the host hindgut. In the 1960s, analysis of resin-embedded Trichonympha samples by electron microscopy revealed that the basal bodies that give rise to these flagella are exceptionally long, with a proximal, cartwheel-bearing, region some 50 times longer than that of regular centrioles. In recent years, this salient feature has prompted the analysis of the 3D architecture of Trichonympha basal bodies in the native state using cryo-electron tomography. The resulting ~40 Å resolution map of the basal body proximal region revealed a number of novel features that may be conserved in centrioles of other systems. These include proximal–distal polarity of the pinhead structure that links the cartwheel to centriolar microtubules, as well as of the linker between the A and the C microtubules. Moreover, this work demonstrated that the cartwheel is made of stacked ring-like structures that likely each comprise 18 molecules of SAS-6 proteins.
KeywordsTrichonympha Long centriole Cartwheel Cryo-tomography
Trichonympha sp. is an anaerobic symbiotic flagellate, which is part of the parabasalid goup, within the supergroup Excavata . Parabasalids are characterized by parabasal fibers that link their basal bodies to Golgi complexes. Trichonympha sp. cells are typically ~100 μm long and lack mitochondria . Note that, unless otherwise stated, the descriptions below pertain to several Trichonympha species that share essentially the same basic structural features. The same holds for the related Pseudotrichonympha sp., as well as the two Australian species Deltotrichonympha operculata and Koruga bonita [3–6].
Basic basal body structure and composition
Additional basal body structures or accessory structures
Basal body origins
How basal bodies form in Trichonympha is not known with certainty. In Deltotrichonympha operculata, basal bodies are thought to form from short subunits called kinetosomes that are arranged in a columnar fashion in the anterior region of the cell [3, 4]. It is not clear whether basal bodies form de novo or in the vicinity of existing ones.
Basal body life cycle and other functions
The basal body life cycle has been investigated in Trichonympha magna , where the long and short centrioles located close to the rostrum seem to act as centrosomes during mitosis, while the basal bodies remain at the cell surface during cell division.
Identification of basal body components
No proteomic or genomic screen has been performed to date. However, the genome of Trichonympha agilis is currently being assembled, which already allowed the identification of mRNAs encoding TaSAS-6 (Fig. 2b), α-tubulin, β-tubulin, δ-tubulin, ε-tubulin , as well as centrin (PaG and PiG, unpublished observations).
Notable basal body findings
Strengths and future of basal body research in Trichonympha
One obvious strength of Trichonympha as a model system is the large number of basal bodies per cell, which can be easily purified together with the flagella. In addition, the exceptionally long proximal region offers remarkable opportunities for structural analysis by cryo-tomography. However, the anaerobic life cycle and the lack of transgenesis and gene inactivation methods preclude at present functional studies in Trichonympha. In the future, Trichonympha could be used for proteomic analysis of purified basal bodies, in particular, to uncover proteins specific of the proximal region. Furthermore, the 5-μm-long centriole is a particularly suitable sample for accurate protein localization using super-resolution microscopy.
PaG and PiG generated the figures and wrote the manuscript. Both authors read and approved the final manuscript.
We are grateful to Virginie Hamel and Veronika Villimova for critical reading of the manuscript. We thank Davide Demurtas (BioEM core facility, EPFL) for the cryo-EM image of Trichonympha basal body. This work was supported by grants from the Swiss National Science Foundation (SNSF) to PaG (PP00P3_157517) and the European Research Council (ERC) to PiG (AdG 233335).
The authors declare that they have no competing interests.
Open AccessThis 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.
- Dack JB, Redfield RJ. Phylogenetic placement of Trichonympha. J Eukaryot Microbiol. 45(4):445–7.
- Biagini GA, Finlay BJ, Lloyd D. Evolution of the hydrogenosome. FEMS Microbiol Lett. 1997;155(2):133–40.View ArticlePubMedGoogle Scholar
- Tamm S, Tamm SL. Origin and development of free kinetosomes in the flagellates Deltotrichonympha and Koruga. J Cell Sci. 1980;42:189–205.PubMedGoogle Scholar
- Tamm SL. Free kinetosomes in Austrialian flagellates I. Types and spatial arrangement. J Cell Biol. 1972;54(1):39–55.View ArticlePubMedPubMed CentralGoogle Scholar
- Gibbons IR, Grimstone V. On flagellar structure in certain flagellates. J Biophys Biochem Cytol. 1960;7(4):697–716.View ArticlePubMedPubMed CentralGoogle Scholar
- Grimstone AV, Gibbons IR. The fine structure of the centriolar apparatus and associated structures in the complex flagellates Trichonympha and Pseudotrichonympha. Philos Trans R Soc B Biol Sci. 1966;250(766):215–42.View ArticleGoogle Scholar
- Kirby H. Flagellates of the genus trichonympha in termites. Univ Calif Publ Zool. 1932;37:349–476.Google Scholar
- Guichard P, Hachet V, Majubu N, Neves A, Demurtas D, Olieric N, Fluckiger I, Yamada A, Kihara K, Nishida Y, Moriya S, Steinmetz MO, Hongoh Y, Gönczy P. Native architecture of the centriole proximal region reveals features underlying its 9-fold radial symmetry. Curr Biol. 2013;23(17):1620–8.View ArticlePubMedGoogle Scholar
- Guichard P, Hamel V, Neves A, Gönczy P. Isolation, cryotomography, and three-dimensional reconstruction of centrioles. Methods Cell Biol. 2015;129:191–209.View ArticlePubMedGoogle Scholar
- Cleveland LR. The centrioles of Trichonympha from termites and their functions in reproduction. J Protozool. 1960;7(4):326–41.View ArticleGoogle Scholar
- Guichard P, Desfosses A, Maheshwari A, Hachet V, Dietrich C, Brune A, Ishikawa T, Sachse C, Gönczy P. Cartwheel architecture of Trichonympha basal body. Science. 2012;337(6094):553.View ArticlePubMedGoogle Scholar