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Pseudokabatana Alburnus N. Gen. N. Sp., (Microsporidia) from the Liver of Topmouth Culter Culter Alburnus (Actinopterygii, Cyprinidae) from China

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Pseudokabatana Alburnus N. Gen. N. Sp., (Microsporidia) from the Liver of Topmouth Culter Culter Alburnus (Actinopterygii, Cyprinidae) from China Parasitology Research (2019) 118:1689–1699 https://doi.org/10.1007/s00436-019-06303-z FISH PARASITOLOGY - REVIEW Pseudokabatana alburnus n. gen. n. sp., (Microsporidia) from the liver of topmouth culter Culter alburnus (Actinopterygii, Cyprinidae) from China X. H. Liu1,2 & G. D. Stentiford3,4 & V. N. Voronin5 & H. Sato6 & A. H. Li1,2 & J. Y. Zhang1,2 Received: 13 September 2018 /Accepted: 25 March 2019 /Published online: 11 April 2019 # Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract We describe the type species of a novel genus of microsporidian parasite, Pseudokabatana alburnus n. gen. n. sp., infecting the liver of topmouth culter, Culter alburnus Basilewsky, 1855, from Lake Poyang off Xingzi county, Jiangxi Province, China. The parasite elicits formation of spherical xenomas of up to 1.2 mm in diameter containing all observed life stages from early merogonal plasmodia to mature spores contained within the cytoplasm of host hepatocytes. Merogonal plasmodia existed in direct contact with the host cytoplasm and contained up to 20 visible nuclei. Plasmotomy of the multinucleate plasmodium led to formation of uninucleate cells in which the nucleus underwent further division to form bi-nucleate presporonts, sporonts (defined by cells with a thickened endospore) and eventually sporoblasts (containing pre-cursors of the spore extrusion apparatus). Mature spores were pyriform and monokaryotic, measuring 2.3 ± 0.19 μm long and 1.3 ± 0.10 μm wide. Spores possessed a bipartite polaroplast and 5– 6 coils of a polar filament, in a single rank. The obtained partial SSU rRNA gene sequence, 1383 bp in length, did not match any of microsporidia available in GenBank. SSU rDNA-based phylogenetic analysis indicated a new taxon branching with Kabatana rondoni, a parasite infecting the skeletal muscle of Gymnorhamphichthys rondoni from the Amazon River. Due to different host and tissue tropism, the novel taxon did not fit the diagnostic criteria for the genus Kabatana. Further, based on SSU rDNA-inferred phylogenetic analyses, different ultrastructural features of developmental stages, and ecological considerations, a new genus Pseudokabatana and type species Pseudokabatana alburnus n. sp. was erected for the parasite in topmouth culter. Keywords Kabatana . Pseudokabatana alburnus n. gen. n. sp. Ultrastructure . Xenoma Introduction Section Editor: Sascha L. Hallett * J. Y. Zhang Microsporidia are ubiquitous obligate intracellular parasites [email protected] that can infect diverse invertebrate (frequently arthropods) and vertebrate (including fish) hosts (Simakova et al. 2018; 1 Key Laboratory of Aquaculture Diseases Control, Ministry of Abdel-Ghaffar et al. 2012; Casal et al. 2016;Stentifordetal. Agriculture, State Key Laboratory of Freshwater Ecology and 2013a, 2015). At least 1600 species belonging to over 200 Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China recognized genera have been reported worldwide, and of them, more than 160 species in 21 genera are known to infect diverse 2 University of Chinese Academy of Sciences, Beijing 10049, China ornamental, marine, and freshwater fishes from wide-ranging 3 International Centre of Excellence for Aquatic Animal Health, Cefas niches (Lom and Nilsen 2003;Kentetal.2014; Stentiford et al. Weymouth Laboratory, Dorset, Weymouth DT4 8UB, UK 2013a). Among fish-infecting microsporidia, most are de- 4 Centre for Sustainable Aquaculture Futures, College of Life and scribed from bony fish, some of which are known to cause Environmental Sciences, Geoffrey Pope, University of Exeter, Stocker Road, Exeter EX4 4QD, UK important health issue in aquaculture (Kent et al. 2014). Despite the presence of diverse wild and cultured fish pop- 5 Berg State Research Institute on Lake and River Fisheries, St. Petersburg, Russia ulations, few studies on this important parasite group have been conducted in China. In the last century, several species 6 Laboratory of Parasitology, Joint Faculty of Veterinary Medicine, Yamaguchi University, Yamaguchi, Japan of Glugea and Pleistophora have been recorded from fish 1690 Parasitol Res (2019) 118:1689–1699 hosts in China (including Mylopharyngodon piceus, fish were anesthetized by an overdose of MS 222 Ctenopharyngodon idellus, Hypophthalmichthys molitrix, (Sigma, Germany) and necropsy was conducted. Aristichthys nobilis, Cyprinus carpio, Carassius auratus, Presumptive microsporidian xenomas were dissected Xenocypris argentea, Tilapia nilotica, Ophiocephalus from the surface of the liver using a dissection micro- maculatus, O. argus,andPseudorabora parva)(Chen1955; scope (Olympus SZ51) prior to wet mounting on clean Chen 1956a, b; Chen and Xie 1960;HeandLi1985). Further, glass slides and examination using light microscopy Agmasoma penaei was described infecting several penaeid Motic BA210 (Motic, China). Images were obtained shrimp hosts by He (1988) based solely on light microscopic using Olympus BX 53 microscope equipped with an observations. Since then, only sporadic reports of aquatic Olympus DP72 digital camera (Olympus, Japan). Other microsporidian infections have been made. More recently, xenomas were dissected from the surface of the liver several commercially important microsporidians have been and preserved in 95% ethanol and 2.5% glutaraldehyde described from intensive aquatic animal culture, including en- in 0.1 M sodium cacodylate buffer (PH 7.4) for molec- teric microsporidiosis of groupers (Xu et al. 2017, Yan et al. ular analyses and electron microscopy, respectively. 2018), slow growth syndrome in penaeids associated with Enterocytozoon hepatopanaei (Tourtip et al. 2009; Transmission electron microscopy Aranguren et al. 2017), and so-called toothpaste disease of swimming crab (Wang et al. 2017). Finally, several fish- Fortransmissionelectronmicroscopy(TEM),glutaraldehyde- infecting species of Glugea and Microsporidium were ultra- fixed xenomas were washed in sodium cacodylate buffer structurally and molecularly characterized from hosts collect- twice (10 min) and placed into 1% osmium tetroxide (OsO4) ed from wild marine hosts (Wu et al. 2005;Suetal.2014). solution for 1 h. After dehydration through a gradual ascend- However, the diversity of aquatic microsporidian in China is ing series of ethanol and propylene oxide series, samples were undoubtedly underestimated, especially within freshwater embedded in Spur resin. Ultrathin sections (70–90 nm) of habitats. these areas were mounted on uncoated copper grids and Lake Poyang, in the lower reaches of Yangtze River, is stained with uranyl acetate and lead citrate. Sections were 2 the largest freshwater lake in China at 4125 km . To date, examined using a Hitachi HT-7700 TEM. 134 fish species have been recorded from the lake, around one third of the amount of fish species in the Yangtze DNA extraction, PCR, and sequencing River basin (Cao 2011;Fangetal.2016). To the best of our knowledge, no microsporidian parasite has previously Four ethanol-fixed xenomas isolated from the infected been described from hosts collected from this natural wa- liver of two fish were washed with distilled water 2 times tershed. As part of ongoing survey work exploring diver- to remove all ethanol. Genomic DNA was extracted by a sity in freshwater microsporidia from China, we analyzed commercial tissue extraction kit (Qiagen, Hilden, specimens of the topmouth culter (Cluter alburnus)col- Germany). For amplification of SSU rDNA, V1f (5′- lected from Lake Poyang in 2016. We used morphologi- CACCAGGTTGATTCTGCC-3′) and 1492r (5′-GGTT cal, ultrastructural, and molecular data to characterize a ACCTTGTTACGACTT-3′) primers were used (Nilsen novel microsporidian parasite infecting the liver of 2000; Vossbrinck and Debrunner-Vossbrinck 2005). The C. alburnus.AnewtaxonPseudokabatana alburnus n. PCR was carried out in a 50 μl reaction mixture contain- gen. n. sp. was erected by comparing the C. alburnus par- ing PCR buffer, 200 mM dNTP, 2 mM MgCl ,1.25units asite to most closely related microsporidian genera (in- 2 Taq polymerase, 20 pm each primer, and 2 μlDNAtem- cluding Kabatana) within Clade 5 of the Microsporidia. plate. Thermocycler parameters were as follows: an initial denaturation step at 95 °C for 4 min, followed by 35 cy- Materials and methods cles of denaturation at 94 °C for 1 min, annealing at 46 °C for30s,elongationat72°Cfor2min,andafinalexten- Sample collections sion at 72 °C for 10 min. The target PCR products were Eight specimens of topmouth culter (C. alburnus)rang- Fig. 1 Photomicrographs of Pseudokabatana alburnus n. gen. n. sp. by light and transmission electron microscopy. a A whitish xenoma ingfrom23.0gto55.4ginbodyweightwerecaptured (arrow) at the surface of liver of host. b Fresh spores released from a by gill nets from Lake Poyang off Xingzi county, xenoma, showing some normal spores (arrowhead) and slightly ab- Jiangxi province, China (29°27′3″N, 116°01′32″E) dur- errant spores (arrow). c A rounded merogonal plasmodium d ing July 2016. Fish were transported to a local fish contained numerous nuclei (Nu) and some vacuoles (Va). A merogonal plasmodium surrounded by numerous sporoblasts (Sb). diseases laboratory for parasitological examination and e A dividing nucleus (arrow). f Late division stage of an isolated dissection. After visual examination of the body surface, nucleus to two unpaired nuclei (arrow) Parasitol Res (2019) 118:1689–1699 1691 1692 Parasitol Res (2019) 118:1689–1699 Fig. 2 Electron micrographs of sporogony of Pseudokabatana alburnus electron-dense
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