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Kinetid structure of choanoflagellates and choanocytes of sponges does not support their close relationship Igor Pozdnyakov, Agniya Sokolova, Alexander Ereskovsky, Sergey Karpov To cite this version: Igor Pozdnyakov, Agniya Sokolova, Alexander Ereskovsky, Sergey Karpov. Kinetid structure of choanoflagellates and choanocytes of sponges does not support their close relationship. Protistology, 2017, 11 (4), pp.248-264. 10.21685/1680-0826-2017-11-4-6. hal-01764702 HAL Id: hal-01764702 https://hal.archives-ouvertes.fr/hal-01764702 Submitted on 12 Apr 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Protistology 11 (4), 248–264 (2017) Protistology Kinetid structure of choanoflagellates and choano- cytes of sponges does not support their close relationship Igor R. Pozdnyakov1, Agniya M. Sokolova2,3, Alexander V. Ereskovsky4,5 and Sergey A. Karpov1,6 1 Department of Invertebrate Zoology, Biological Faculty, St. Petersburg State University, St. Petersburg, Russia 2 A.N. Severtzov Institute of Ecology and Evolution, Moscow, Russia 3 N.K. Koltzov Institute of Developmental Biology, Moscow, Russia 4 Mediterranean Institute of Marine and Terrestrial Biodiversity and Ecology (IMBE), Aix Marseille University, CNRS, IRD, Avignon Université, Marseille France 5 Department of Embryology, Biological Faculty, St. Petersburg State University, St. Petersburg, Russia 6 Zoological Institute of Russian Academy of Science, St. Petersburg, Russia | Submitted November 19, 2017 | Accepted December 5, 2017 | Summary Any discussion of the origin of Metazoa during the last 150 years and particularly in the recent years when the sister relationship of choanoflagellates and Metazoa was unambiguously shown by molecular phylogeny refers to the similarity of sponge choanocytes to choanoflagellates. These two types of collared radially symmetric cells are superficially similar with respect to the presence of microvilli around a single flagellum and flat mitochondrial cristae which are common for many eukaryotes. But a comparison of the most informative structure having a stable phylogenetic signal, the flagellar apparatus or kinetid, has been neglected. The kinetid is well studied in choanoflagellates and is rather uniform, but in choanocytes this structure has been investigated in the last five years and is represented by several types of kinetids. Here we review the kinetid structure in choanocytes of Porifera to establish the most conservative type of kinetid in this phylum. The detailed comparison of this kinetid with the flagellar apparatus of choanoflagellates demonstrates their fundamental difference in many respects. The choanocyte kinetid contains more features which can be considered plesiomorphic for the opisthokonts than the kinetid of the choanoflagellates. Therefore, the hypothesis about the origin of Porifera, and consequently of all Metazoa directly from choanoflagellate-like unicellular organism is not confirmed by their kinetid structure. Key words: origin of Metazoa, kinetid, ultrastructure, choanoflagellate, choanocyte, Porifera doi:10.21685/1680-0826-2017-11-4-6 © 2017 The Author(s) Protistology © 2017 Protozoological Society Affiliated with RAS Protistology · 249 Introduction the choanoflagellates and the Metazoa has now been confirmed on many occasions (Cavalier-Smith, Choanocytes, flagellated cells of adult sponges, 1996; Borchiellini et al., 1998, 2001; Leadbeater having a flagellum surrounded by the collar were and Kelly, 2001; Medina et al., 2003; King et al., first described by James-Clark (1867). They line 2008; Philippe et al., 2009; Shalchian-Tabrizi, 2008; the so called choanocyte chambers and serve as Taylor et al., 2007; Wörheide et al. 2012; Pisani et feeding cells in sponges. In his description, James- al., 2015; Torruella et al., 2015; Simion et al., 2017). Clark noted their close morphological similarity to choanoflagellates, or collar flagellates, a group of heterotrophic flagellates with a single flagellum also Do choanoflagellates represent the image of surrounded by a collar (James-Clark, 1866). They a metazoan ancestor? are sedentary single or colonial and live in freshwater and marine habitats. The choanoflagellates are In 2003 the genes responsible for cell adhesion the only protozoa with a collar and are similar to and cellular signaling that allow cells of multicellular choanocytes in morphology and mode of nutrition. animals to interact with the extracellular matrix and As a result, James-Clark (1867) proposed that with each other, were found in choanoflagellates sponges should be considered as colonial protozoa. (King, 2003). It became clear that metazoan His assumption did not persist for long. By the multicellularity arose by modification of genes middle of the 19th century, sponges were considered controlling cytological mechanisms already pre- to be the multicellular animals (Leuckart,1854, sent in unicellular organisms (Ruiz-Trillo et al., cit. ex Leadbeater, 2015; Haeckel, 1866; Sollas, 2007; King et al., 2008). Further the genes encoding 1886; Delage, 1892), but the similarity between neuropeptides (Fairclough et al., 2013), sphingo- choanocytes and choanoflagellates determined the glycolipid metabolism regulators (Burkhardt, 2015), views on the origin and evolution of Porifera and cadherins (Nichols, 2012), and signaling ability with multicellular animals in general. In the middle of the participation of Ca2+ ions (Cai, 2008) have been the 19th century two views on the origin of sponges found in choanoflagellates. These findings further were proposed: Haeckel accepted one ancestor supported the hypothesis that the metazoan ancestor for the Metazoa including sponges (Haeckel, was similar to choanoflagellates. The phylogeny 1874) whilst Sollas suggested their independent of multicellular animals with an origin from a origin (Sollas, 1886). All subsequent views on the choanoflagellate-like ancestor has been elaborated position of sponges in the animal kingdom until in the recent reviews (Nielsen, 2012; Cavalier- the end of the 20th century were based on one Smith, 2016; Brunet and King, 2017). or other of these views (Tuzet, 1963; Bergquist, However, homologues of these specific meta- 1978; Salvini-Plawen, 1978; Seravin, 1986). The zoan genes proved to be the feature not only of majority of authors agreed with the evolutionary choanoflagellates. Gene sets encoding some of the origin and deriving of sponges and all Metazoa from cellular systems and processes of Metazoa have colonial choanoflagellates (Ivanov, 1968; Tuzet, been found in other unicellular representatives 1963; Bergquist, 1978; Salvini-Plawen, 1978). of both opisthokont subdivisions, the Holozoa The morphological similarity of choanocytes and (includes Metazoa and several protistan lineages) choanoflagellates at the level of light and partly and the Holomycota (includes Fungi and two electron microscopy, based predominantly on their protistan lineages) (Sebe-Pedros et al., 2010, radial symmetry and apical collar around a single 2013). The homologues of proteins involved in flagellum, was confirmed and highlighted many the nervous activity of Metazoa were known for times (Tuzet, 1963; Salvini-Plawen, 1978; Simpson, fungi earlier (Schulze et al., 1994). Moreover, 1984; Maldonado, 2004; Leadbeater, 2015). individual components of their gene sets have also Since the time when comparative molecular been found in Amoebozoa, the supergroup sister to methods became available for the phylogeny of Opisthokonta, and in one of the deepest lineages of Metazoa (Wainright et al., 1993), the choano- the latter supercluster, the Apusozoa (Sebe-Pedros flagellates were found to be a sister group to the et al., 2010). Metazoa which led to the suggestion that both The choanoflagellates also do not occupy the groups had evolved from a common ancestor. Since first place in terms of the quantity of metazoan genes this first publication, the sister relationship between possessed. Some genes of multicellular animals 250 · Igor R. Pozdnyakov, Agniya M. Sokolova, et al. found in the lower representatives of Opisthokonta The choanoflagellates are well studied in this are absent in choanoflagellates (Sebe-Pedros et al., respect and it has been shown in many papers 2010, 2013, 2016). Thus, the choanoflagellates look that the single celled and colonial, sedentary more like simplified organisms that have apparently and swimming, marine and freshwater, naked lost some of the genes present in a metazoan ances- and thecate or loricate – all of them have very tor (O’Malley et al., 2016). Such an idea has already conservative internal cell structure and flagellar been expressed by Maldonado (2004) from the apparatus (Laval, 1971; Leadbeater, 1972, 1977, morphological and common biological points of 1983, 1991, 2015; Leadbeater and Morton, 1974; view. Hibberd, 1975; Karpov, 1981, 1982, 1985; 2016; Thus, the latest molecular data are not in Zhukov and Karpov, 1985; Karpov and Leadbeater, agreement with the hypothesis of the origin of 1998; Karpov and Zhukov, 2000; Leadbeater Metazoa from
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  • General Introduction and Objectives 3

    General Introduction and Objectives 3

    General introduction and objectives 3 General introduction: General body organization: The phylum Porifera is commonly referred to as sponges. The phylum, that comprises more than 6,000 species, is divided into three classes: Calcarea, Hexactinellida and Demospongiae. The latter class contains more than 85% of the living species. They are predominantly marine, with the notable exception of the family Spongillidae, an extant group of freshwater demosponges whose fossil record begins in the Cretaceous. Sponges are ubiquitous benthic creatures, found at all latitudes beneath the world's oceans, and from the intertidal to the deep-sea. Sponges are considered as the most basal phylum of metazoans, since most of their features appear to be primitive, and it is widely accepted that multicellular animals consist of a monophyletic group (Zrzavy et al. 1998). Poriferans appear to be diploblastic (Leys 2004; Maldonado 2004), although the two cellular sheets are difficult to homologise with those of the rest of metazoans. They are sessile animals, though it has been shown that some are able to move slowly (up to 4 mm per day) within aquaria (e.g., Bond and Harris 1988; Maldonado and Uriz 1999). They lack organs, possessing cells that develop great number of functions. The sponge body is lined by a pseudoepithelial layer of flat cells (exopinacocytes). Anatomically and physiologically, tissues of most sponges (but carnivorous sponges) are organized around an aquiferous system of excurrent and incurrent canals (Rupert and Barnes 1995). These canals are lined by a pseudoepithelial layer of flat cells (endopinacocytes).Water flows into the sponge body through multiple apertures (ostia) General introduction and objectives 4 to the incurrent canals which end in the choanocyte chambers (Fig.