Recent studies on motility of Apicomplexa concur with the so-called glideosome concept applied for apicomplexan zoites, describing a unique mechanism of substrate-dependent gliding motility facilitated by a conserved form of actomyosin motor and subpellicular microtubules. In contrast, the gregarines and blastogregarines exhibit different modes and mechanisms of motility, correlating with diverse modifications of their cortex. This study focuses on the motility and cytoskeleton of the blastogregarine Siedleckia nematoides Caullery et Mesnil, 1898 parasitising the polychaete Scoloplos cf. armiger (Müller, 1776). The blastogregarine moves independently on a solid substrate without any signs of gliding motility; the motility in a liquid environment (in both the attached and detached forms) rather resembles a sequence of pendular, twisting, undulation, and sometimes spasmodic movements. Despite the presence of key glideosome components such as pellicle consisting of the plasma membrane and the inner membrane complex, actin, myosin, subpellicular microtubules, micronemes and glycocalyx layer, the motility mechanism of S. nematoides differs from the glideosome machinery. Nevertheless, experimental assays using cytoskeletal probes proved that the polymerised forms of actin and tubulin play an essential role in the S. nematoides movement. Similar to Selenidium archigregarines, the subpellicular microtubules organised in several layers seem to be the leading motor structures in blastogregarine motility. The majority of the detected actin was stabilised in a polymerised form and appeared to be located beneath the inner membrane complex. The experimental data suggest the subpellicular microtubules to be associated with filamentous structures (= cross-linking protein complexes), presumably of actin nature.

Department of Botany and Zoology Faculty of Science Masaryk University Kotlářská 2 Brno Czech Republic

Department of Invertebrate Zoology Faculty of Biology Lomonosov Moscow State University Leninskiye Gory 1 12 Moscow Russian Federation

Department of Invertebrate Zoology Faculty of Biology Saint Petersburg State University Universitetskaya emb 7 9 St Petersburg Russian Federation

Institute of Scientific Instruments of the CAS v v i Královopolská 147 Brno Czech Republic

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Adl SM, Simpson AG, Lane CE, Lukeš J, Bass D, Bowser SS, et al. The revised classification of eukaryotes. J Eukaryot Microbiol. 2012; 59:429–493. doi: 10.1111/j.1550-7408.2012.00644.x PubMed DOI PMC

Morrissette NS, Sibley LD. Cytoskeleton of apicomplexan parasites. Microbiol Mol Biol R. 2002; 66:21–38. PubMed PMC

Valigurová A, Vaškovicová N, Musilová N, Schrével J. The enigma of eugregarine epicytic folds: Where gliding motility originates? Front Zool. 2013; 10:57 doi: 10.1186/1742-9994-10-57 PubMed DOI PMC

Heintzelman MB, Mateer MJ. GpMyoF, a WD40 repeat-containing myosin associated with the myonemes of Gregarina polymorpha. J Parasitol. 2008; 94:158–168. doi: 10.1645/GE-1339.1 PubMed DOI

Kuhni-Boghenbor K, Ma M, Lemgruber L, Cyrklaff M, Frischknecht F, Gaschen V, et al. Actin-mediated plasma membrane plasticity of the intracellular parasite Theileria annulata. Cell Microbiol. 2012; 14:1867–1879. doi: 10.1111/cmi.12006 PubMed DOI

Frénal K, Polonais V, Marq JB, Stratmann R, Limenitakis J, Soldati-Favre D. Functional dissection of the apicomplexan glideosome molecular architecture. Cell Host Microbe. 2010; 8:343–357. doi: 10.1016/j.chom.2010.09.002 PubMed DOI

Daher W, Soldati-Favre D. Mechanisms controlling glideosome function in apicomplexans. Curr Opin Microbiol. 2009; 12:408–414. doi: 10.1016/j.mib.2009.06.008 PubMed DOI

Bullen HE, Tonkin CJ, O'Donnell RA, Tham WH, Papenfuss AT, Gould S, et al. A novel family of apicomplexan glideosome-associated proteins with an inner membrane-anchoring role. J Biol Chem. 2009; 284:25353–25363. doi: 10.1074/jbc.M109.036772 PubMed DOI PMC

Santos JM, Lebrun M, Daher W, Soldati D, Dubremetz JF. Apicomplexan cytoskeleton and motors: Key regulators in morphogenesis, cell division, transport and motility. Int J Parasitol. 2009; 39:153–162. doi: 10.1016/j.ijpara.2008.10.007 PubMed DOI

Boucher LE, Bosch J. The apicomplexan glideosome and adhesins–Structures and function. J Struct Biol. 2015; 190:93–114. doi: 10.1016/j.jsb.2015.02.008 PubMed DOI PMC

Tardieux I, Baum J. Reassessing the mechanics of parasite motility and host-cell invasion. J Cell Biol. 2016; 214:507–515. doi: 10.1083/jcb.201605100 PubMed DOI PMC

Heintzelman MB. Actin and myosin in Gregarina polymorpha. Cell Motil Cytoskel. 2004; 58:83–95. PubMed

Mackenzie C, Walker MH. Substrate contact, mucus, and eugregarine gliding. J Protozool. 1983; 30:3–8.

Chen WJ, Fan-Chiang MH. Directed migration of Ascogregarina taiwanensis (Apicomplexa: Lecudinidae) in its natural host Aedes albopictus (Diptera: Culicidae). J Eukaryot Microbiol. 2001; 48:537–541. doi: 10.1111/j.1550-7408.2001.tb00189.x PubMed DOI

Ghazali M, Schrével J. Myosin-like protein (Mr 175,000) in Gregarina blaberae. J Eukaryot Microbiol. 1993; 40:345–354. PubMed

Ghazali M, Philippe M, Deguercy A, Gounon P, Gallo JM, Schrével J. Actin and spectrin-like (Mr = 260–240 000) proteins in gregarines. Biol Cell. 1989; 67:173–184.

Schrével J, Caigneaux E, Gros D, Philippe M. The three cortical membranes of the gregarines. I. Ultrastructural organization of Gregarina blaberae. J Cell Sci. 1983; 61:151–174. PubMed

Walker MH, Lane NJ, Lee WM. Freeze-fracture studies on the pellicle of the eugregarine, Gregarina garnhami (Eugregarinida, Protozoa). J Ultrastruct Res. 1984; 88:66–76.

Schewiakoff W. Über die Ürsache der fortschreitenden Bewegung der Gregarinen. Z Wis Zool. 1894; 58:340–354.

Richter IE. Bewegungsphysiologische Untersuchungen an polycystiden Gregarinen unter Anwendung des Mikrozeitrafferfilmes. Protoplasma. 1959; 51:197–241.

Baines I, King CA. Demonstration of actin in the protozoan Gregarina. Cell Biol Int Rep. 1989; 13:679–686. PubMed

King CA. Cell surface interaction of the protozoan Gregarina with concanavalin A beads—Implications for models of gregarine gliding. Cell Biol Int Rep. 1981; 5:297–305. PubMed

King CA, Lee K. Effect of trifluoperazine and calcium ions on gregarine gliding. Experientia. 1982; 38:1051–1052.

Crawley H. The movements of gregarines. P Acad Nat Sci Philadelphia. 1905; 57:89–99.

Hildebrand HF. Electron-microscopic investigation on evolution stages of trophozoite of Didymophyes gigantea (Sporozoa, Gregarinida). III. The fine structure of the epicyte with emphasis on the contractile elements. Z Parasitenkd. 1980; 64:29–46. PubMed

Diakin A, Paskerova GG, Simdyanov TG, Aleoshin VV, Valigurová A. Morphology and molecular phylogeny of coelomic gregarines (Apicomplexa) with different types of motility: Urospora ovalis and U. travisiae from the polychaete Travisia forbesii. Protist. 2016; 167:279–301. doi: 10.1016/j.protis.2016.05.001 PubMed DOI

Desportes I, Schrével J. Treatise on zoology—Anatomy, taxonomy, biology The gregarines (2 vols): The early branching Apicomplexa: Brill; 2013.

MacMillan WG. Conformational changes in the cortical region during peristaltic movements of a gregarine trophozoite. J Protozool. 1973; 20:267–274.

Leander BS, Lloyd SAJ, Marshall W, Landers SC. Phylogeny of marine gregarines (Apicomplexa)—Pterospora, Lithocystis and Lankesteria—and the origin(s) of coelomic parasitism. Protist. 2006; 157:45–60. doi: 10.1016/j.protis.2005.10.002 PubMed DOI

Warner FD. The fine structure of Rhynchocystis pilosa (Sporozoa, Eugregarinida). J Protozool. 1968; 15:59–73.

Miles HB. The fine structure of the epicyte of the acephaline gregarines Monocystis lumbriciolidi, and Nematocystis magna: Observations by electron microscope. Rev Iber Parasitol. 1968; 28:455–465.

Miles HB. The contractile system of the acephaline gregarine Nematocystis magna: Observations by electron microscope. Rev Iber Parasitol. 1966; 26:361–368.

Landers SC. Pterospora floridiensis, a new species of acephaline gregarine (Apicomplexa) from the maldanid polychaete Axiothella mucosa in St. Andrew Bay, Florida. Syst Parasitol. 2001; 48:55–59. PubMed

Fowell RR. The fibrillar structures of protozoa, with special reference to schizogregarines of the genus Selenidium. J R Micr Soc. 1936; 56:12–28.

Vivier E, Schrével J. Etude au microscope électronique d'une grégarine du genre Selenidium parasite de Sabellaria alveolata L. J Microsc. 1964; 3:651–670.

Schrével J. Observations biologiques et ultrastructurales sur les Selenidiidae et leurs conséquences sur la systématique des Grégarinomorphes. J Protozool. 1971; 18:448–470.

Schrével J, Valigurová A, Prensier G, Chambouvet A, Florent I, Guillou L. Ultrastructure of Selenidium pendula, the type species of archigregarines, and phylogenetic relations to other marine Apicomplexa. Protist. 2016; 167:339–368. doi: 10.1016/j.protis.2016.06.001 PubMed DOI

Schrével J, Buissonnet S, Métais M. Action de l'urée sur la motilité et les microtubules sous-pelliculaires du Protozoaire Selenidium hollandei. C R Acad Sci. 1974; 278:2201–2204.

Wakeman KC, Heintzelman MB, Leander BS. Comparative ultrastructure and molecular phylogeny of Selenidium melongena n. sp. and S. terebellae Ray 1930 demonstrate niche partitioning in marine gregarine parasites (Apicomplexa). Protist. 2014; 165:493–511. doi: 10.1016/j.protis.2014.05.007 PubMed DOI

Schrével J. Contribution a l'étude des Selenidiidae parasites d'annélides polychètes. II. Ultrastructure de quelques trophozoïtes. Protistologica. 1971; 7:101–130.

Stebbings H, Boe GS, Garlick PR. Microtubules and movement in the archigregarine, Selenidium fallax. Cell Tissue Res. 1974; 148:331–345. PubMed

Mellor JS, Stebbings H. Microtubules and the propagation of bending waves by the archigregarine, Selenidium fallax. J Exp Biol. 1980; 87:149–161. PubMed

Gunderson J, Small EB. Selenidium vivax n. sp. (Protozoa, Apicomplexa) from the sipunculid Phascolosoma agassizii Keferstein, 1867. J Parasitol. 1986; 72:107–110.

Chatton E, Villeneuve F. La sexualité et le cycle évolutif des Siedleckia d'après l'étude de S. caulleryi, n.sp. hologrégarines et blastogrégarines. Sporozoaires hologamétogènes et blastogamétogènes. C R Acad Sci. 1936; 203:505–508.

Hayat M. Principles and techniques of electron microscopy: Biological applications. 4th Edn. Cambridge: Cambridge University Press; 2000.

Valigurová A. Sophisticated adaptations of Gregarina cuneata (Apicomplexa) feeding stages for epicellular parasitism. PLoS ONE. 2012; 7(8):e42606 doi: 10.1371/journal.pone.0042606 PubMed DOI PMC

Valigurová A, Michalková V, Koudela B. Eugregarine trophozoite detachment from the host epithelium via epimerite retraction: Fiction or fact? Int J Parasitol. 2009; 39:1235–1242. doi: 10.1016/j.ijpara.2009.04.009 PubMed DOI

Branton D, Bullivant S, Gilula NB, Karnovsky MJ, Moor H, Muhlethaler K, et al. Freeze etching nomenclature. Science. 1975; 190:54–56. PubMed

Dubremetz JF, Torpier G. Freeze fracture study of the pellicle of an eimerian sporozoite (Protozoa, Coccidia). J Ultrastruct Res. 1978; 62:94–109. PubMed

McLaren DJ, Bannister LH, Trigg PI, Butcher GA. Freeze fracture studies on the interaction between the malaria parasite and the host erythrocyte in Plasmodium knowlesi infections. Parasitology. 1979; 79:125–139. PubMed

Chatton F, Dehorne L. Sporozoaires du genre Siedleckia, S. dogieli n.sp. et S. mesnili n.sp. Bull Zool Soc Fr. 1929; 54:28–33.

Chatton E, Dehorne L. Observations sur les Sporozoaires du genre Siedleckia, S. dogieli n.sp. et S. mesnili n.sp. Arch Anat Microsc. 1929; 25:530–543.

Schüler H, Matuschewski K. Regulation of apicomplexan microfilament dynamics by a minimal set of actin-binding proteins. Traffic. 2006; 7:1433–1439. doi: 10.1111/j.1600-0854.2006.00484.x PubMed DOI

Gould SB, Tham WH, Cowman AF, McFadden GI, Waller RF. Alveolins, a new family of cortical proteins that define the protist infrakingdom Alveolata. Mol Biol Evol. 2008; 25:1219–1230. doi: 10.1093/molbev/msn070 PubMed DOI

Kumpula EP, Kursula I. Towards a molecular understanding of the apicomplexan actin motor: on a road to novel targets for malaria remedies? Acta Crystallogr F Struct Biol Commun. 2015; 71:500–513. doi: 10.1107/S2053230X1500391X PubMed DOI PMC

Egarter S, Andenmatten N, Jackson AJ, Whitelaw JA, Pall G, Black JA, et al. The Toxoplasma Acto-MyoA motor complex is important but not essential for gliding motility and host cell invasion. PLoS ONE. 2014; 9(3):e91819 doi: 10.1371/journal.pone.0091819 PubMed DOI PMC

Whitelaw JA, Latorre-Barragan F, Gras S, Pall GS, Leung JM, Heaslip A, et al. Surface attachment, promoted by the actomyosin system of Toxoplasma gondii is important for efficient gliding motility and invasion. BMC Biol. 2017; 15(1):1 doi: 10.1186/s12915-016-0343-5 PubMed DOI PMC

Leander BS. Molecular phylogeny and ultrastructure of Selenidium serpulae (Apicomplexa, Archigregarinia) from the calcareous tubeworm Serpula vermicularis (Annelida, Polychaeta, Sabellida). Zool Scripta. 2007; 36:213–227.

Caullery M, Mesnil F. Sur un Sporozoaire aberrant (Siedleckia n. g.). C R Soc Biol. 1898; 5:1093–1095.

Hakansson S, Morisaki H, Heuser J, Sibley LD. Time-lapse video microscopy of gliding motility in Toxoplasma gondii reveals a novel, biphasic mechanism of cell locomotion. Mol Biol Cell. 1999; 10:3539–3547. PubMed PMC

Vanderberg JP. Studies on the motility of Plasmodium sporozoites. J Protozool. 1974; 21:527–537. PubMed

Valigurová A, Paskerova GG, Diakin A, Kováčiková M, Simdyanov TG. Protococcidian Eleutheroschizon duboscqi, an unusual apicomplexan interconnecting gregarines and cryptosporidia. PLoS ONE. 2015; 10:e0125063 doi: 10.1371/journal.pone.0125063 PubMed DOI PMC

Beams HW, Tahmisian TN, Devine RL, Anderson E. Studies on the fine structure of a gregarine parasitic in the gut of the grasshopper, Melanoplus differentialis. J Protozool. 1959; 6:136–146.

Hliscs M, Millet C, Dixon MW, Siden-Kiamos I, McMillan P, Tilley L. Organization and function of an actin cytoskeleton in Plasmodium falciparum gametocytes. Cell Microbiol. 2015; 17:207–225. doi: 10.1111/cmi.12359 PubMed DOI

Sampathkumar A, Lindeboom JJ, Debolt S, Gutierrez R, Ehrhardt DW, Ketelaar T, et al. Live cell imaging reveals structural associations between the actin and microtubule cytoskeleton in Arabidopsis. Plant Cell. 2011; 23:2302–2313. doi: 10.1105/tpc.111.087940 PubMed DOI PMC

Kobayashi H, Fukuda H, Shibaoka H. Interrelation between the spatial disposition of actin filaments and microtubules during the differentiation of tracheary elements in cultured Zinnia cells. Protoplasma. 1988; 143:29–37.

Morrissette NS, Mitra A, Sept D, Sibley LD. Dinitroanilines bind α-tubulin to disrupt microtubules. Mol Biol Cell. 2004; 15:1960–1968. doi: 10.1091/mbc.E03-07-0530 PubMed DOI PMC

Morrissette NS, Sibley LD. Disruption of microtubules uncouples budding and nuclear division in Toxoplasma gondii. J Cell Sci. 2002; 115:1017–1025. PubMed

Beck JR, Rodriguez-Fernandez IA, Cruz de Leon J, Huynh M-H, Carruthers VB, Morrissette NS, et al. A novel family of Toxoplasma IMC proteins displays a hierarchical organization and functions in coordinating prasite division. PLoS Pathog. 2010; 6(9):e1001094 doi: 10.1371/journal.ppat.1001094 PubMed DOI PMC

Dostál V, Libusová L. Microtubule drugs: action, selectivity, and resistance across the kingdoms of life. Protoplasma. 2014; 251:991–1005. doi: 10.1007/s00709-014-0633-0 PubMed DOI

Tran JQ, Li C, Chyan A, Chung L, Morrissette NS. SPM1 Stabilizes subpellicular microtubules in Toxoplasma gondii. Eukaryot Cell. 2012; 11:206–216. doi: 10.1128/EC.05161-11 PubMed DOI PMC

Leander BS. Ultrastructure of the archigregarine Selenidium vivax (Apicomplexa)—A dynamic parasite of sipunculid worms (host: Phascolosoma agassizii). Mar Biol Res. 2006; 2:178–190.

Macgregor HC, Thomasson PA. The fine structure of two archigregarines, Selenidium fallax and Ditrypanocystis cirratuli. J Protozool. 1965; 12:438–443.

Raibaud A, Lupetti P, Paul RE, Mercati D, Brey PT, Sinden RE, et al. Cryofracture electron microscopy of the ookinete pellicle of Plasmodium gallinaceum reveals the existence of novel pores in the alveolar membranes. J Struct Biol. 2001; 135:47–57. doi: 10.1006/jsbi.2001.4396 PubMed DOI

Harding CR, Meissner M. The inner membrane complex through development of Toxoplasma gondii and Plasmodium. Cellular Microbiol. 2014; 16:632–641. PubMed PMC

Mann T, Beckers C. Characterization of the subpellicular network, a filamentous membrane skeletal component in the parasite Toxoplasma gondii. Mol Biochem Parasitol. 2001; 115:257–268. PubMed

Menard R. Gliding motility and cell invasion by Apicomplexa: insights from the Plasmodium sporozoite. Cell Microbiol. 2001; 3:63–73. PubMed

Dallai R, Talluri MV. Freeze-fracture study of the gregarine trophozoite: I. The top of the epicyte folds. Ital J Zool. 1983; 50:235–244.

Simdyanov TG, Kuvardina ON. Fine structure and putative feeding mechanism of the archigregarine Selenidium orientale (Apicomplexa: Gregarinomorpha). Eur J Protistol. 2007; 43:17–25. doi: 10.1016/j.ejop.2006.09.003 PubMed DOI

Guha-Niyogi A, Sullivan DR, Turco SJ. Glycoconjugate structures of parasitic protozoa. Glycobiology. 2001; 11:45R–59R. PubMed

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