{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T13:37:54Z","timestamp":1789997874244,"version":"4.0.1"},"reference-count":38,"publisher":"Cambridge University Press (CUP)","issue":"7","license":[{"start":{"date-parts":[[2013,2,28]],"date-time":"2013-02-28T00:00:00Z","timestamp":1362009600000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/www.cambridge.org\/core\/terms"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Parasitology"],"published-print":{"date-parts":[[2013,6]]},"abstract":"<jats:title>SUMMARY<\/jats:title><jats:p>Class Rudimicrosporea Sprague 1977, with its single family Metchnikovellidae, comprises hyperparasites of gregarines from the guts of marine invertebrates. Metchnikovellids remain poorly studied in spite of their significance to the evolutionary history of microsporidia; their ultrastructure and life cycles require further investigation. Here we present results of the light- and electron-microscopy study of <jats:italic>Metchnikovella incurvata<\/jats:italic> Caulleri and Mesnil 1914, isolated from lecudinid gregarines, parasitizing polychaetes <jats:italic>Pygospio elegans<\/jats:italic> in the White Sea littoral zone, and yet described only on the light-microscopic level. The life cycle of this microsporidium includes 2 sporogonies: free (FS) and sac-bound (SBS). In FS, sporonts develop into multinuclear cells (sporogonial plasmodia), which generate sporoblasts and free spores residing in direct contact with the host cytoplasm. Electron microscopy revealed their metchnikovellidean structure: a horseshoe-shaped nucleus, short manubrium perpendicular to the long axis of the spore, and a polar cap in a separate membrane container. Merogony was not observed. The earliest stages of SBS were chains of binucleate cells. They underwent a series of nuclear and cell divisions, produced extracellular envelopes, and split into boomerang-shaped spore sacs, containing up to 16 spores each. Ultrastructure and sizes of sac-bounded spores were similar to those of free-living ones. An amended diagnosis of <jats:italic>M. incurvata<\/jats:italic> is provided.<\/jats:p>","DOI":"10.1017\/s0031182013000036","type":"journal-article","created":{"date-parts":[[2013,3,1]],"date-time":"2013-03-01T02:40:33Z","timestamp":1362105633000},"page":"855-867","source":"Crossref","is-referenced-by-count":24,"title":["Fine structure of <i>Metchnikovella incurvata<\/i> Caullery and Mesnil 1914 (microsporidia), a hyperparasite of gregarines <i>Polyrhabdina<\/i> sp. from the polychaete <i>Pygospio elegans<\/i>"],"prefix":"10.1017","volume":"140","author":[{"given":"Y. Y.","family":"SOKOLOVA","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"G. G.","family":"PASKEROVA","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Y. M.","family":"ROTARI","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"E. S.","family":"NASSONOVA","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"A. V.","family":"SMIRNOV","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"56","published-online":{"date-parts":[[2013,2,28]]},"reference":[{"key":"S0031182013000036_ref2","doi-asserted-by":"publisher","DOI":"10.1128\/9781555818227.ch14"},{"key":"S0031182013000036_ref17","doi-asserted-by":"publisher","DOI":"10.1016\/j.pt.2007.11.005"},{"key":"S0031182013000036_ref1","doi-asserted-by":"publisher","DOI":"10.1645\/GE-1177.1"},{"key":"S0031182013000036_ref21","first-page":"92","volume-title":"VI European Congress of Protistology, Berlin, 24\u201329 July 2011","author":"Nassonova","year":"2011"},{"key":"S0031182013000036_ref27","first-page":"144","volume-title":"Proceedings of the XIII International Congress of Protistology, Armacao dos Buzios, Brasil","author":"Simdianov","year":"2009"},{"key":"S0031182013000036_ref40","doi-asserted-by":"publisher","DOI":"10.1086\/BBLv187n2p255"},{"key":"S0031182013000036_ref29","doi-asserted-by":"publisher","DOI":"10.1111\/j.1550-7408.2001.tb00464.x"},{"key":"S0031182013000036_ref4","doi-asserted-by":"publisher","DOI":"10.1242\/jcs.03402"},{"key":"S0031182013000036_ref5","first-page":"960","article-title":"Sur un type nouveau (Metchnikovella n.g.) d'organismes parasites des Gr\u00e9garines","volume":"49","author":"Caullery","year":"1897","journal-title":"Comptes Rendus de Seances de la Societe de Biologie, Paris"},{"key":"S0031182013000036_ref37","first-page":"95","article-title":"\u00c9tude en microscopie photonique et \u00e9lectronique de diff\u00e9rents stades du cycle de Metchnikovella hovassei et observations sur la position syst\u00e9matique des Metchnikovellidae","volume":"9","author":"Vivier","year":"1973","journal-title":"Protistologica"},{"key":"S0031182013000036_ref7","first-page":"209","article-title":"Metchnikovellidae et autre Protistes des Gr\u00e9garines d'Ann\u00e9lides","volume":"33","author":"Caullery","year":"1919","journal-title":"Annales de l'Institut Pasteur"},{"key":"S0031182013000036_ref11","doi-asserted-by":"publisher","DOI":"10.14411\/fp.2009.012"},{"key":"S0031182013000036_ref10","first-page":"1","volume-title":"Toxoplasma gondii. The Model Apicomplexan: Perspectives and Methods","author":"Dubey","year":"2007"},{"key":"S0031182013000036_ref26","first-page":"67","article-title":"New data on hyperparasitic microsporidians from polychaetes of the White Sea","volume":"5","author":"Rotari","year":"2007","journal-title":"Proceedings of the V European Congress of Protistology and XI European Conference on Ciliate Biology, St. Petersburg. Protistology"},{"key":"S0031182013000036_ref22","first-page":"273","article-title":"Amphyamblys bhatiellae n. sp., microsporidie parasite de Bhatiella marphysae Setna, 1931, Eugr\u00e9garine d'Ann\u00e9lide Polych\u00e8te","volume":"17","author":"Ormi\u00e8res","year":"1981","journal-title":"Protistologica"},{"key":"S0031182013000036_ref15","doi-asserted-by":"publisher","DOI":"10.14411\/fp.2000.043"},{"key":"S0031182013000036_ref35","first-page":"6982","article-title":"\u00c9tude, au microscope \u00e9lectronique, de la spore de Metchnikovella hovassei n. sp.: appartenance des Metchnikovellidae aux Microsporidies","volume":"260","author":"Vivier","year":"1965","journal-title":"Comptes Rendus de Seances de la Societe de Biologie, Paris"},{"key":"S0031182013000036_ref13","first-page":"131","article-title":"Observations ultrastructurales sur le sporoblaste de Metchnikovella wohlfarthi, n.sp. (Microsporidies), parasite de la gr\u00e9garine Lecudina tuzetae","volume":"7","author":"Hildebrand","year":"1971","journal-title":"Protistologica"},{"key":"S0031182013000036_ref14","doi-asserted-by":"publisher","DOI":"10.1111\/j.1550-7408.1993.tb04880.x"},{"key":"S0031182013000036_ref3","doi-asserted-by":"publisher","DOI":"10.1111\/j.1550-7408.1990.tb05876.x"},{"key":"S0031182013000036_ref33","first-page":"289","article-title":"Gr\u00e9garines de Roscoff","volume":"3","author":"Tuzet","year":"1962","journal-title":"Cahiers de Biologie Marine"},{"key":"S0031182013000036_ref8","first-page":"67","article-title":"Liste actualis\u00e9e des esp\u00e8ces d'Ann\u00e9lides Polych\u00e8tes pr\u00e9sentes en Manche","volume":"44","author":"Dauvin","year":"2003","journal-title":"Cahiers de Biologie Marine"},{"key":"S0031182013000036_ref9","first-page":"435","article-title":"\u00c9tude ultrastructurale d'Amphiamblus laubieri n.sp. (Microsporidie, Metchnikovellidae) parasite d'un Gr\u00e9garine (Lecudina sp.) d'un Echiurien abyssal","volume":"15","author":"Desportes","year":"1979","journal-title":"Protistologica"},{"key":"S0031182013000036_ref12","first-page":"5","article-title":"Observations ultrastructurales sur le stade plasmodial de Metchnikovella wohlfarthi Hildebrand et Vivier 1971, microsporidie hyperparasite de la gr\u00e9garine Lecudina tuzetae","volume":"10","author":"Hildebrand","year":"1974","journal-title":"Protistologica"},{"key":"S0031182013000036_ref39","doi-asserted-by":"publisher","DOI":"10.1111\/j.1550-7408.1984.tb02948.x"},{"key":"S0031182013000036_ref16","doi-asserted-by":"publisher","DOI":"10.1016\/j.ejop.2006.07.001"},{"key":"S0031182013000036_ref20","doi-asserted-by":"publisher","DOI":"10.1111\/j.1550-7408.2010.00479.x"},{"key":"S0031182013000036_ref23","first-page":"190","volume-title":"The Illustrated Guide to the Protozoa","volume":"1","author":"Perkins","year":"2000"},{"key":"S0031182013000036_ref24","doi-asserted-by":"publisher","DOI":"10.1007\/s004360050538"},{"key":"S0031182013000036_ref25","unstructured":"Rotari Y. M. (1988). Microsporidia \u2013 hyperparasites of the White Sea polychaetes. M.S. dissertation. Biological Sciences, Department of Invertebrate Zoology, Leningrad State University, Leningrad USSR."},{"key":"S0031182013000036_ref28","doi-asserted-by":"publisher","DOI":"10.1007\/978-3-211-76310-0_38"},{"key":"S0031182013000036_ref30","first-page":"1","volume-title":"Comparative Pathobiology, Vol. 2. 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