Three actinosporean types (Myxozoa) from the oligochaete Branchiura sowerbyi in China
- 334 Downloads
- 9 Citations
Abstract
Three actinosporean types—raabeia, aurantiactinomyxon, and guyenotia—from the oligochaete Branchiura sowerbyi Beddard collected from a crucian carp (Carassius auratus gibelio) pond are described in this report. Compared with the actinospores described previously, the raabeia type presents similar spore shape with the actinospore of Myxobolus cultus, except a much longer caudal process, 250.8 μm (217.5–276.3). The aurantiactinomyxon and guyenotia type significantly differ from other actinospores in its same collective group with different caudal process shape (taper and leaf-like) and dimension, 170.8 μm (167.5–176.3) and 18.5 μm (16.5–20.6), respectively. The partial 18S rDNA sequences of raabeia and aurantiactinomyxon types, and myxospores M. cultus, Myxobolus wulii, Myxobolus pyramidis, and Thelohanellus wuhanensis detected from pond-reared crucian carp were determined. Based on DNA sequences analysis, the raabeia type showed high genetic similarity (99.5–100 %) with myxospore M. cultus Yokoyama, Ogawa & Wakabayashi, 1995 on the gills of crucian carp sampled from the same pond. The aurantiactinomyxon showed no more than 85.2 % sequence similarity with myxospores determined in this report and other myxozoans available from GenBank.
Keywords
Crucian Carp Polar Capsule Polar Filament Gibel Carp Caudal ProcessNotes
Acknowledgments
Valuable comments and helpful suggestions of the anonymous reviewers are greatly appreciated. The authors are also grateful to Dr. Xie and Dr. Cui (Institute of Hydrobiology, Chinese Academy of Sciences) for their assistance in the Oligochaeta identification and to Bo Liu and Qun-Lan Zhou for their assistance in sampling. The work was supported by the Natural Sciences Foundation of Jiangsu Province (no. BK2011182), project of China Postdoctoral Science Foundation and Freshwater Fisheries Research Center, CAFS Grant (project no. 2009JBFB03 and 2011JBFA07)
References
- Atkinson SD, Bartholomew JL (2009) Alternate spore stages of Myxobilatus gasterostei, a myxosporean parasite of three-spined sticklebacks (Gasterosteus aculeatus) and oligochaetes (Nais communis). Parasitol Res 104(5):1173–1181PubMedCrossRefGoogle Scholar
- Barta JR, Martin DS, Libetator PA, Dashkevicz M, Anderson JW, Feighner SD, Elbrecht A, Perkins-Barrow A, Jenkins MC, Danforth HD, Ruff MD, Profous-Juchelka H (1997) Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. J Parasitol 83:262–271Google Scholar
- Brinkhurst RO (1971) A guide for the identification of British aquatic Oligochaeta. Freshwater Biological Association, No. 22. Wilson & Son, TorontoGoogle Scholar
- Caffara M, Raimondi E, Florio D, Marcer F, Quaglio F, Fioravanti ML (2009) The life cycle of Myxobolus lentisuturalis (Myxozoa: Myxobolidae), from goldfish (Carassius auratus auratus), involves a Raabeia-type actinospore. Folia Parasitol 56:6–12PubMedGoogle Scholar
- Chen QL, Ma CL (1998) Myxozoa, myxosporea. Fauna Sinica. Committee of Fauna Sinica (ed). Science, Beijing (in Chinese)Google Scholar
- Dyková I, Fiala I, Nie P (2002) Myxobolus lentisuturalis sp. n. (Myxozoa: Myxobolidae), a new muscle-infecting species from the Prussian carp, Carassius gibelio from China. Folia Parasitol 49:253–258PubMedGoogle Scholar
- El-Mansy A, Székely C, Molnár K (1998a) Development of Myxobolus portucalensis Saraiva and Molnár (Myxosporea: Myxobolidae) in the oligochaete Tubifex tubifex (Muller). Syst Parasitol 41:95–103CrossRefGoogle Scholar
- El-Mansy A, Székely C, Molnár K (1998b) Studies on the occurrence of actinosporean stages of fish myxosporeans in a fish farm of Hungary, with the description of triactinomyxon, raabeia, aurantiactinomyxon and neoactinomyxon types. Acta Vet Hung 46:259–284PubMedGoogle Scholar
- El-Mansy A, Székely C, Molnár K (1998c) Studies on the occurrence of actinosporean stages of fish myxosporeans in a Lake Balaton, Hungary, with the description of triactinomyxon, raabeia, aurantiactinomyxon types. Acta Vet Hung 46:437–450PubMedGoogle Scholar
- Eszterbauer E, Marton S, Racz ZO, Letenyei M, Molnár K (2006) Morphological and genetic differences among actinosporean stages of fish-parasitic myxosporeans (Myxozoa): difficulties of species identification. Syst Parasitol 65:97–114PubMedCrossRefGoogle Scholar
- Fiala I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol 36:1521–1534PubMedCrossRefGoogle Scholar
- Hallett SL, Atkinson SD, El-Matbouli M (2002) Molecular characterization of two aurantiactinomyxon (Myxozoa) phenotypes reveal one genotype. J Fish Dis 25:627–631CrossRefGoogle Scholar
- Hallett SL, Atkinson SD, Erséus C, El-Matbouli M (2006) Myxozoa parasites disseminated via oligochaete worms as live food for aquarium fishes: descriptions of aurantiactinomyxon and raabeia actinospore types. Dis Aquat Org 69:213–225PubMedCrossRefGoogle Scholar
- Hallett SL, Erséus C, Lester RJG (1999) Actinosporeans (Myxozoa) from marine oligochaetes of the Great Barrier Reef. Syst Parasitol 44:49–57PubMedCrossRefGoogle Scholar
- Hallett SL, Atkinson SD, Erséus C, El-Matbouli M (2004) Molecular methods clarify morphometric variation in triactinomyxon spores released from different oligochaete hosts. Syst Parasitol 57:1–14PubMedCrossRefGoogle Scholar
- Hallett SL, Atkinson SD, Erséus C, El-Matbouli M (2005) Dissemination of triactinomyxons (Myxozoa) via oligochaetes used as live food for aquarium fishes. Dis Aquat Org 65:137–152PubMedCrossRefGoogle Scholar
- Holzer AS, Sommerville C, Wootten R (2004) Molecular relationships and phylogeny in a community of myxosporeans and actinosporeans based on their 18S rDNA sequences. Int J Parasitol 34:1099–1111PubMedCrossRefGoogle Scholar
- Janiszewska J (1955) Actinomyxidia. Morphology, ecology, history of investigations, systematics, development. Acta Parasitol Polon 2:405–407Google Scholar
- Janiszewska J (1957) Actinomyxidia. II. New systematics, sexual cycle, description of new genera and species. Zool Polon 8:3–34Google Scholar
- Kent ML, Andree KB, Bartholomew JL, El-Matbouli M, Desser SS, Devlin RH, Feist SW, Hedrick RP, Hoffmann RW, Khattra J, Hallett SL, Lester RJG, Longshaw M, Palenzeula O, Siddall ME, Xiao C (2001) Recent advances in our knowledge of the Myxozoa. J Eukaryot Microbiol 48:395–413PubMedCrossRefGoogle Scholar
- Køie M, Karlsbakk E, Nylund A (2007) A new genus Gadimyxa with three new species (Myxozoa, Parvicapsulidae) parasitic in marine fish (Gadidae) and the two-host life cycle of Gadimyxa atlantica n. sp. J Parasitol 93:1459–1467PubMedCrossRefGoogle Scholar
- Liu Y, Whipps CM, Gu ZM, Zeng C, Huang MJ (2012) Myxobolus honghuensis n. sp. (Myxosporea: Bivalvulida) parasitizing the pharynx of allogynogenetic gibel carp Carassius auratus gibelio (Bloch) from Honghu Lake, China. Parasitol Res 110:1331–1336PubMedCrossRefGoogle Scholar
- Lom J, McGeorge J, Feist SW, Morris D, Adams A (1997) Guidelines for the uniform characterization of the actinosporean stages of parasites of the phylum Myxozoa. Dis Aquat Org 30:1–9CrossRefGoogle Scholar
- Lom J, Dyková I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 53:1–36PubMedGoogle Scholar
- Lowers JM, Bartholomew JL (2003) Detection of myxozoan parasites in oligochaetes imported as food for ornamental fish. J Parasitol 89:84–91PubMedCrossRefGoogle Scholar
- Marcucci C, Caffara M, Goretti E (2009) Occurrence of actinosporean stages (Myxozoa) in the Nera River system (Umbria, central Italy). Parasitol Res 105:1517–1530PubMedCrossRefGoogle Scholar
- McGeorge J, Sommerville C, Wootten R (1997) Studies of actinosporean myxozoan stages parasitic in oligochaetes from sediments of a hatchery where Atlantic salmon harbour Sphaerospora truttae infection. Dis Aquat Org 30:107–119CrossRefGoogle Scholar
- Negredo C, Mulcahy MF (2001) Actinosporean infection in oligochaetes in a river system in southwest Ireland with descriptions of three new forms. Dis Aquat Org 46:67–77PubMedCrossRefGoogle Scholar
- Oumouna M, Hallett SL, Hoffmann RW, El-Matbouli M (2003) Seasonal occurrence of actinosporeans (Myxozoa) and oligochaetes (Annelida) at a trout hatchery in Bavaria, Germany. Parasitol Res 89:170–184PubMedGoogle Scholar
- Özer A, Wootten R, Shinn AP (2002) Survey of actinosporean types (Myxozoa) belonging to seven collective groups found in a freshwater salmon farm in Northern Scotland. Folia Parasitol 49:189–210PubMedGoogle Scholar
- Styer EL, Harrison LR, Rurtle GJ (1991) Experimental production of proliferative gill disease in channel catfish exposed to a myxozoan-infected oligochaete, Dero digitata. J Aquat Anim Health 3:288–291CrossRefGoogle Scholar
- Székely C, Avenant-Oldewage A, Molnár K (2004) Description of a new actinosporean type from South African freshwaters. Dis Aquat Org 61:95–102PubMedCrossRefGoogle Scholar
- Székely C, Eiras JC, Eszterbauer E (2005) Description of a new synactinomyxon type from River Souza, Portugal. Dis Aquat Org 66:9–14PubMedCrossRefGoogle Scholar
- Székely C, Hallett SL, Atkinson SD, Molnár K (2009) Complete life cycle of Myxobolus rotundus (Myxosporea: Myxobolidae), a gill myxozoan of common bream Abramis brama. Dis Aquat Org 85:147–155PubMedCrossRefGoogle Scholar
- Székely C, Rácz O, Molnár K, Eszterbauer E (2002a) Development of Myxobolus macrocapsularis (Myxosporea: Myxobolidae) in an oligochaete alternate host, Tubifex tubifex. Dis Aquat Org 48:117–123Google Scholar
- Székely C, Sitjà-Bobadilla A, Álvarez-Pellitero P (2000) First report on the occurrence of an actinosporean stage (Myxozoa) in Oligochaetes from Spanish freshwaters. Acta Vet Hung 48:433–441PubMedGoogle Scholar
- Székely C, Urawa S, Yokoyama H (2002b) Occurrence of actinosporean stages of myxosporeans in an inflow brook of a salmon hatchery in the Mena River System, Hokkaido, Japan. Dis Aquat Org 49:153–160PubMedCrossRefGoogle Scholar
- Székely C, Yokoyama H, Urawa S, Timm T, Ogawa K (2003) Description of two new actinosporean types from a brook of Fuji Mountain, Honshu, and from Chitose River, Hokkaido, Japan. Dis Aquat Org 53:127–132PubMedCrossRefGoogle Scholar
- Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
- Trouillier A, El-Matbouli M, Hoffmann W (1996) A new look at the life cycle of Hoferellus carassii in the goldfish (Carassius auratus) and its relation to ‘kidney enlargement disease’ (KED). Folia Parasitol 43:173–187Google Scholar
- Wang GT, Yao WJ (2000) First report on the actinosporean in oligochaetes in China. Acta Hydrobiol Sinica 24:198–200Google Scholar
- Wolf K, Markiw ME (1984) Biology contravenes taxonomy in the Myxozoa: new discoveries show alternation of invertebrate and vertebrate hosts. Science 225:1449–1452PubMedCrossRefGoogle Scholar
- Xi BW, Xie J, Zhou QL, Pan LK, Ge XP (2011) Mass mortality of pond-reared Carassius gibelio (Bloch) caused by Myxobolus ampullicapsulatus in China. Dis Aquat Org 93:257–260PubMedCrossRefGoogle Scholar
- Xiao C, Desser SS (1998a) Actinosporean stages of Myxozoan parasites of oligochaetes from Lake Sasajewun, Algonquin Park, Ontario: new forms of triactinomyxon and raabeia. J Parasitol 84:998–1009PubMedCrossRefGoogle Scholar
- Xiao C, Desser SS (1998b) Actinosporean stages of Myxozoan parasites of oligochaetes from Lake Sasajewun, Algonquin Park, Ontario: new forms of echinactinomyxon, neoactinomyxon, aurantiactinomyxon, guyenotia, synactinomyxon and antonactinomyxon. J Parasitol 84:1010–1018PubMedCrossRefGoogle Scholar
- Xiao C, Desser SS (1998c) The oligochaetes and their actinosporean parasites in Lake Sasajewun, Algonquin Park, Ontario. J Parasito 84:1020–1026CrossRefGoogle Scholar
- Yokoyam H, Ogawa K, Wakabayashi H (1993) Involvement of Branchiura sowerbyi (Oligochaeta: Annelida) in the transmission of Hoferellus carassii (Myxosporea: Myxozoa), the causative agent of kidney enlargement disease (KED) of goldfish Carassius auratus. Fish Pathol 28:135–139CrossRefGoogle Scholar
- Yokoyam H, Ogawa K, Wakabayashi H (1995) Myxobolus cultus n. sp. (Myxosporea: Myxobolidae) in the goldfish Carassius auratus transformed from the actinosporean stage in the oligochaete Branchiura sowerbyi. J Parasitol 81:446–451CrossRefGoogle Scholar
- Yokoyama H (2003) A review: gaps in our knowledge on Myxozoan parasites of fishes. Fish Pathol 38:125–136CrossRefGoogle Scholar
- Zhai YH, Zhou L, Gui JF (2012) Identification and characterization of one novel type of triactinospomyxon with short spore axis. Parasitol Res 110:2385–2393PubMedCrossRefGoogle Scholar
- Zhang JY, Yokoyama H, Wang JG, Li AH, Gong XN, Ryu-Hasegawa A, Iwashita M, Ogawa K (2010) Utilization of tissue habitats by Myxobolus wulii Landsberg et Lom, 1991 in different carp hosts and disease resistance in allogynogenetic gibel carp: redescription of M. wulii from China and Japan. J Fish Dis 33:57–68PubMedCrossRefGoogle Scholar