Cite this paper:
YE Lingtong, LU Mingmiao, QUAN Keyan, LI Wenxiang, ZOU Hong, WU Shangong, WANG Jiangyong, WANG Guitang. Intestinal disease of scattered mirror carp Cyprinus carpio caused by Thelohanellus kitauei and notes on the morphology and phylogeny of the myxosporean from Sichuan Province, southwest China[J]. Journal of Oceanology and Limnology, 2017, 35(3): 587-596

Intestinal disease of scattered mirror carp Cyprinus carpio caused by Thelohanellus kitauei and notes on the morphology and phylogeny of the myxosporean from Sichuan Province, southwest China

YE Lingtong1, LU Mingmiao2, QUAN Keyan3, LI Wenxiang2, ZOU Hong2, WU Shangong2, WANG Jiangyong1, WANG Guitang2
1 Key Laboratory of Fishery Ecology and Environment, Guangdong Province; Key Laboratory of South China Sea Fishery Resources Exploitation & Utilization, Ministry of Agriculture; South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou 510300, China;
2 Key Laboratory of Aquatic Biodiversity and Conservation, and the Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China;
3 Sichuan Fisheries School, Chengdu 611730, China
The mass mortality of pond-reared scattered mirror carp, Cyprinus carpio, caused by Thelohanellus kitauei, occurred at fish farms in Sichuan Province, southwest China. Morphological and molecular analyses were supplemented with histological evaluation of infected tissues to better understand the route of infection and the pathological effects of T. kitauei on the fish host. The intestine of the diseased host was full of large cysts of the myxosporean. The cysts range from 2 cm to 3.6 cm in diameter. Histopathology indicated that T. kitauei first invaded the submucosa of the host intestine and then moved into the mucosa layers with the development of their spores, finally entering into the enteric cavity of the hosts after the disruption of mucosa layers. The pyriform spores of T. kitauei were surrounded by the transparent spore sheath, measuring 25.98 μm±0.95 μm in body length, 8.72 μm±0.51 μm in body width, and 7.86 μm±0.26 μm in body thickness. The single polar capsule was pyriform, measuring 14.73 μm±0.92 μm in length and 6.82 μm±0.45 μm in width, with eight to 10 turns of filament coils winding inside. Phylogenetic analysis based on the 18S small-subunit ribosomal DNA sequences indicated that minimal genetic differences were present between T. kitauei samples from South Korea and from China. Close affinity was found between the genus Thelohanellus and Myxobolus. Additionally, two polar capsule nuclei were found at the anterior end of the single polar capsule in spores of T. kitauei stained with hematoxylin and eosin, which suggested the separation of the genus Thelohanellus from Myxobolus.
Key words:    intestinal disease|scattered mirror carp|Thelohanellus kitauei|host-specific tropism|morphology|phylogeny   
Received: 2015-12-09   Revised: 2016-02-01
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Articles by YE Lingtong
Articles by LU Mingmiao
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Ali M A, Abdel-Baki A S, Sakran T, Entzeroth R, AbdelGhaffar F. 2007. Myxobolus lubati n. sp. (Myxosporea: Myxobolidae), a new parasite of haffara seabream Rhabdosargus haffara (Forsskal, 1775), Red Sea, Egypt: a light and transmission electron microscopy. Parasitology Research, 100(4): 819-827.
Ali M A, Al-Rasheid K A, Sakran T, Abdel-Baki A A, AbdelGhaffar F A. 2002. Some species of the genus Myxobolus (Myxozoa: Myxosporea) infecting freshwater fish of the River Nile, Egypt, and the impact on their hosts. Parasitology Research, 88(1): 9-15.
Ali M A. 1999. Henneguya ghaffari sp. n. (Myxozoa: Myxosporea), infecting the Nile perch Lates niloticus (Teleostei: Centropomidae). Diseases of Aquatic Organisms, 38(3): 225-230.
Andree K B, El-Matbouli M, Hoffman R W, Hedrick R P. 1999. Comparison of 18S and ITS-1 rDNA sequences of selected geographic isolates of Myxobolus cerebralis. International Journal for Parasitology, 29(5): 771-775.
Barta J R, Martin D S, Liberator P A, Dashkevicz M, Anderson J W, Feighner S D, Elbrecht A, Perkins-Barrow A, Jenkins M C, Danforth H D, Ruff M D, Profous-Juchelka H. 1997. Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. The Journal of Parasitology, 83(2): 262-271.
Chen Q L, Ma C L. 1998. Fauna Sinica: Myxozoa, Myxosporea. Science Press, Beijing. p.1-993. (in Chinese)
Diamant A, Lom J, Dyková I. 1994. Myxidium leei n. sp., a pathogenic myxosporean of cultured sea bream Sparus aurata. Diseases of Aquatic Organisms, 20(2): 137-141.
Egusa S, Nakajima K. 1981. A new myxozoa Thelohanellus kitauei, the cause of intestinal giant cystic disease of carp. Fish Pathology, 15(3-4): 213-218.
Fiala I, Bartošová P. 2010. History of myxozoan character evolution on the basis of rDNA and EF-2 data. BMC Evolutionary Biology, 10(1): 228.
Fiala I. 2006. The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. International Journal for Parasitology, 36(14): 1 521-1 534.
Fleurance R, Sauvegrain C, Marques A, Le Breton A, Guereaud C, Cherel Y, Wyers M. 2008. Histopathological changes caused by Enteromyxum leei infection in farmed sea bream Sparus aurata. Diseases of Aquatic Organisms, 79(3): 219-228.
Griffin M J, Goodwin A E. 2011. Thelohanellus toyamai (Syn. Myxobolus toyamai) infecting the gills of koi Cyprinus carpio in the eastern United States. Journal of Parasitology, 97(3): 493-502.
Hall T A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41: 95-98.
Hallett S L, O'Donoghue P J, Lester R J G. 1997. Infections by Kudoa ciliatae (Myxozoa: Myxosporea) in Indo-Pacific whiting Sillago spp. Diseases of Aquatic Organisms, 30(1): 11-16.
Hogge C, Campbell M, Johnson K. 2004. Discriminating between a neurotropic Myxobolus sp. and M. cerebralis, the causative agent of salmonid whirling disease. Journal of Aquatic Animal Health, 16(3): 137-144.
Holzer A S, Sommerville C, Wootten R. 2004. Molecular relationships and phylogeny in a community of myxosporeans and actinosporeans based on their 18S rDNA sequences. International Journal for Parasitology, 34(10): 1 099-1 111.
Kent M L, Andree K B, Bartholomew J L, El-Matbouli M, Desser S S, Devlin R H, Feist S W, Hedrick R P, Hoffmann R W, Khattra J, Hallett S L, Lester R J G, Longshaw M, Palenzeula O, Siddall M E, Xiao C X. 2001. Recent advances in our knowledge of the Myxozoa. The Journal of Eukaryotic Microbiology, 48(4): 395-413.
Kitaue K. 1980. Intestinal giant-cystic disease affecting the carp, caused by Thellohanellus sp. Fish Pathology, 14(3): 145-146.
Liu Y, Whipps C M, Gu Z M, Zeng C, Huang M J. 2012. Myxobolus honghuensis n. sp. (Myxosporea: Bivalvulida) parasitizing the pharynx of allogynogenetic gibel carp Carassius auratus gibelio (Bloch) from Honghu Lake, China. Parasitology Research, 110(4): 1 331-1 336.
Liu Y, Whipps C M, Liu W S, Zeng L B, Gu Z M. 2011. Supplemental diagnosis of a myxozoan parasite from common carp Cyprinus carpio: synonymy of Thelohanellus xinyangensis with Thelohanellus kitauei. Veterinary Parasitology, 178(3-4): 355-359.
Lom J, Arthur J R. 1989. A guideline for the preparation of species descriptions in Myxosporea. Journal of Fish Diseases, 12(2): 151-156.
Lom J, Dyková I. 2006. Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica, 53(1): 1-36.
Lom J. 1987. Myxosporea: a new look at long-known parasites of fish. Parasitology Today, 3(11): 327-332.
Longshaw M, Frear P A, Feist S W. 2005. Descriptions, development and pathogenicity of myxozoan (Myxozoa: Myxosporea) parasites of juvenile cyprinids (Pisces: Cyprinidae). Journal of Fish Diseases, 28(8): 489-508.
Lou Y D. 2007. Close hybridization of fish and its application in aquaculture. Journal of Fisheries of China, 31(4): 532-538. (in Chinese with English abstract)
Maeno Y, Nagasawa K, Sorimachi M. 1993. Kudoa intestinalis n. sp. (Myxosporea: Multivalvulida) from the intestinal musculature of the striped mullet, Mugil cephalus, from Japan. The Journal of Parasitology, 79(2): 190-192.
Masoumian M, Baska F, Molnár K. 1996. Myxobolus nodulointestinalis sp. n. (Myxosporea, Myxobolidae), a parasite of the intestine of Barbus sharpeyi. Diseases of Aquatic Organisms, 24(1): 35-39.
Molnár K, Marton S, Eszterbauer E, Székely C. 2006. Comparative morphological and molecular studies on Myxobolus spp. infecting chub from the River Danube, Hungary, and description of M. muellericus sp. n. Diseases of Aquatic Organisms, 73(1): 49-61.
Molnár K. 1994. Comments on the host, organ and tissue specificity of fish myxosporeans and on the types of their intrapiscine development. Parasitologia Hungarica, 27: 5-20.
Molnár K. 2002. Site preference of fish myxosporeans in the gill. Diseases of Aquatic Organisms, 48(3): 197-207.
Palenzuela O, Redondo M J, Alvarez-Pellitero P. 2002. Description of Enteromyxum scophthalmi gen. nov., sp. nov. (Myxozoa), an intestinal parasite of turbot (Scophthalmus maximus L.) using morphological and ribosomal RNA sequence data. Parasitology, 124(Pt 4): 369-379.
Posada D, Crandall K A. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics, 14(9): 817-818.
Redondo M J, Palenzuela O, Riaza A, Macías Á, ÁlvarezPellitero P. 2002. Experimental transmission of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of turbot Scophthalmus maximus. Journal of Parasitology, 88(3): 482-488.
Rhee J K, Kim J O, Park B K. 1990. Prophylactic and therapeutic studies on intestinal giant-cystic disease of the Israel carp caused by Thelohanellus kitauei. II. Effects of physical and chemical factors on T. Kitauei spores in vitro. The Korean Journal of Parasitology, 28(4): 241-252.
Ronquist F, Huelsenbeck J P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19(12): 1 572-1 574.
Shulman S S. 1966. Myxosporidia of the Fauna of the USSR. Nauka, Moscow. p.1-504. (in Russian)
Sitja-Bobadilla A, Alvarez-Pellitero P. 1992. Light and electron microscopic description of Sphaerospora dicentrarchi n. sp. (Myxosporea: Sphaerosporidae) from wild and cultured sea bass, Dicentrarchus labrax L. Journal of Eukaryotic Microbiology, 39(2): 273-281.
Thompson J D, Gibson T J, Plewniak F, Jeanmougin F, Higgins D G. 1997. The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25(24): 4 876-4 882.
Wang G T, Yao W J, Gong X N, Wang J G, Nie P. 2003. Seasonal fluctuation of Myxobolus gibelioi (myxosporea) plasmodia in the gills of the farmed allogynogenetic gibel carp in China. Chinese Journal of Oceanology and Limnology, 21(2): 149-153.
Wang G T, Yao W J, Wang J G, Lu Y S. 2001. Occurrence of thelohanellosis caused by Thelohanellus wuhanensis (Myxosporea) in juvenile allogynogenetic silver crucian carp, Carassius auratus gibelio (Bloch), with an observation on the efficacy of fumagillin as a therapeutant. Journal of Fish Diseases, 24(1): 57-60.
Whipps C M, Kent M L. 2006. Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea). The Journal of Eukaryotic Microbiology, 53(5): 364-373.
Xi B W, Xie J, Zhou Q L, Pan L K, Ge X P. 2011. Mass mortality of pond-reared Carassius gibelio caused by Myxobolus ampullicapsulatus in China. Diseases of Aquatic Organisms, 93(3): 257-260.
Xia X, Xie Z. 2001. DAMBE: software package for data analysis in molecular biology and evolution. Journal of Heredity, 92(4): 371-373.
Xie X R, Gong X N, Xiao W H, Guo Q L, Li L C, Guo X S. 2000. Studies on Thelohanellionsis (Myxosporidiosis) parasitized freshwater fish in China. I. Thelohanelliosis (Myxosporidiosis) parasitized Carp in Xinyang, Henan Province. Journal of Xinyang Agricultural College, 10(2): 1-5. (in Chinese with English abstract)
Yanagida T, Nomura Y, Kimura T, Fukuda Y, Yokoyama H, Ogawa K. 2004. Molecular and morphological redescriptions of enteric myxozoans, Enteromyxum leei (formerly Myxidium sp. TP) and Enteromyxum fugu comb. n. (syn. Myxidium fugu) from cultured tiger puffer. Fish Pathology, 39(3): 137-144.
Ye L T, Li W X, Wang W W, Wu S G, Wang G T. 2014. Updated morphology, histopathology and molecular phylogeny of Myxobolus hearti, cardiac myxosporea in gibel carp, Carassius gibelio (Bloch). Journal of Fish Diseases, 37(1): 11-20.
Ye L T, Li W X, Wu S G, Wang G T. 2012. Supplementary studies on Henneguya doneci Schulman, 1962 (Myxozoa: Myxosporea) infecting the gill filaments of Carassius auratus gibelio (Bloch) in China: histologic, ultrastructural, and molecular data. Parasitology Research, 110(4): 1 509-1 516.
Yoon J M. 2001. Genetic similarity and difference between common carp and Israeli carp (Cyprinus carpio) based on random amplified polymorphic DNAs analyses. Korean Journal of Biological Sciences, 5(4): 333-339.
Zhai Y H, Gu Z M, Guo Q X, Wu Z Z, Wang H M, Liu Y. 2016. New type of pathogenicity of Thelohanellus kitauei Egusa & Nakajima, 1981 infecting the skin of common carp Cyprinus carpio L. Parasitology International, 65(1): 78-82.
Zhang J Y, Gu Z M, Kalavati C, Eiras J C, Liu Y, Guo Q Y, Molnár K. 2013. Synopsis of the species of Thelohanellus Kudo, 1933 (Myxozoa: Myxosporea: Bivalvulida). Systematic Parasitology, 86(3): 235-256.
Zhang J Y, Yokoyama H, Wang J G, Li A H, Gong X N, RyuHasegawa A, Iwashita M, Ogawa K. 2010. Utilization of tissue habitats by Myxobolus wulii Landsberg & Lom, 1991 in different carp hosts and disease resistance in allogynogenetic gibel carp: redescription of M. wulii from China and Japan. Journal of Fish Diseases, 33(1): 57-68.
Zhao Y J, Li N N, Tang F H, Dong J L. 2013. Remarks on the validity of Myxobolus ampullicapsulatus and Myxobolus honghuensis (Myxozoa: Myxosporea) based on SSU rDNA sequences. Parasitology Research, 112(11): 3 817-3 823.
Zhao Y J, Song W B. 1999. Redescription of Thelohanellus kitauei Egusa & Nakajima, 1981 (Mxospores: Thelohanellidae), parasitic in marine fishers from the Yellow Sea, China. Journal of the Yellow Sea, 5: 73-76.
Zhou L, Gong Q L, Yu K K, Meng Q X. 1998. A preliminary study on the disease of Myxozoa, Thelohanellus Kitauei of Jian Carp (Cyprinus Carpio Var. Jian). Journal of Ocean University of Qingdao, 28(1): 59-62. (in Chinese with English abstract)
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