Abstract
Henneguya doneci Schulman, 1962 was collected from the gill filaments of Carassius auratus gibelio (Bloch) in Hubei Province, China. The plasmodia located on the surface of the gill arches deformed the neighboring gill filaments. The size of the plasmodia ranged from 0.6 to 4.5 mm in diameter in different months. The myxospores in the plasmodia measured 10.1 (9.2–11.5) μm long × 8.0 (7.5–8.5) μm wide × 7.5 (7–8) μm thick, with two equal capsules at 4.7 (4–5.5) μm long × 3.3 (2.5–4) μm wide, and two caudal processes 32.7 (24–38.5) μm long, respectively. Polar filaments were coiled 5–6 turns. Ultrastructural observation of the plasmodia showing the capsulogenesis of H. doneci is described briefly. The external tubule initially invaginated into the polar capsule. The rudimentary polar filaments were observed to undergo a series of considerable modification, finally developing into mature polar filaments. Molecular analysis demonstrated that although the myxosporean species were collected from different tissues of hosts in various geographic locations, they clustered with the Cyprinidae-infecting myxosporean species in the phylogenetic tree.
Similar content being viewed by others
References
Abdel-Ghaffar F, Abdel-Baki AA, Garhy ME (2005) Ultrastructural characteristics of the sporogenesis of genus Myxobolus infecting some Nile fishes in Egypt. Parasitol Res 88:617–626
Abdel-Ghaffar F, Abdel-Baki AAS, Bayoumy EM, Bashtar AR, Qurieshy SAI, Morsey KS, Alghamdy A, Mehlhorn H (2008) Light and electron microscopic study on Henneguya suprabranchiae Landsberg, 1987 (Myxozoa: Myxosporea) infecting Oreochromis niloticus, a new host record. Parasitol Res 103:609–617
Adriano EA, Arana S, Cordeiro NS (2005) Histology, ultrastructure and prevalence of Henneguya piaractus (Myxosporea) infecting the gills of Piaractus mesopotamicus (Characidae) cultivated in Brazil. Dis Aquat Org 64:229–235
Andree KB, Szekely C, Molnar K, Gresoviac SJ, Hedrick RP (1999) Relationships among members of the genus Myxobolus (Myxozoa: Bilvalvidae) based on small subunit ribosomal DNA sequences. J Parasitol 85:68–74
Astrid S, Holzer C, Sommerville RW (2004) Molecular relationships and phylogeny in a community of myxosporeans and actinosporeans based on their 18S rDNA sequences. Int J Parasitol 34:1099–1111
Azevedo C, Acasal G, Matos P, Matosa E (2008) New species of Myxozoa, Henneguya rondoni n. sp. (Myxozoa), from the peripheral nervous system of the Amazonian fish, Gymnorhamphichthys rondoni (Teleostei). J Eukaryot Microbiol 55:229–234
Bahri S, Andree KB, Hedrick RP (2003) Morphological and phylogenetic studies of marine Myxobolus spp. from Mullet in Ichkeul Lake, Tunisia. J Eukaryot Microbiol 50:463–470
Bahri S, Marton S, Marques A, Eszterbauer E (2010) Henneguya tunisiensis n. sp. (Myxosporea: Bivalvulida), a new gill parasite of Symphodus tinca (L.) (Teleostei: Labridae) off Tunisia. Syst Parasitol 76:93–101
Barta JR, Martin DS, Liberator 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 83:262–271
Canning EU, Curry A, Feist SW, Longshaw M, Okamura B (2000) A new class and order of Myxozoans to accommodate parasites of Bryozoans with ultrastructural observations on Tetracapsula bryosalmonae (PKX organism). J Eukaryot Microbiol 47:456–468
Chen QL, Ma CL (1998) Fauna Sinica: Myxozoa, myxosporea. Science Press, Beijing, pp 533–558, in Chinese with English summary
Desser SS, Molnar K, Weller I (1983) Ultrastructure of sporogenesis of Thelohanellus nikolskii Akhmerov, 1955 (Myxozoa: Myxosporea) from the common carp, Cyprinus carpio. J Parasitol 69:504–518
Eiras JC (2002) Synopsis of the species of the genus Henneguya Thélohan, 1892 (Myxozoa: Myxosporea: Myxobolidae). Syst Parasitol 52:43–54
El-Matbouli M, Fischer-Scherl T, Hoffmann RW (1990) Light and electron microscopic studies on Myxobolus cotti El-Matbouli and Hoffmann, 1987 infecting the central nervous system of the bullhead (Cottus gobio). Parasitol Res 75:461–464
Eszterbauer E (2004) Genetic relationship among gill-infecting Myxobolus species (Myxosporea) of cyprinids: molecular evidence of importance of tissue-specificity. Dis Aquat Org 58:35–40
Fiala I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol 36:1521–1524
Hall TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98
Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411–453
Kageyama T, Yanagida T, Ohara K, Yokoyama H (2009) Henneguya pseudorhinogobii n. sp. (Myxozoa: Myxosporea) parasitizing the gills of the freshwater goby Rhinogobius sp. OR from the Nagara River and redescription of Henneguya rhinogobii. Fisheries Sci 75:657–663
Kallert DM, Eszterbauer E, El-Matbouli M, Erséus C, Haas W (2005) The life cycle of Henneguya nuesslini Schuberg & Schröder, 1905 (Myxozoa) involves a triactinomyxon-type actinospore. J Fish Dis 28:71–79
Kent ML, Khattra J, Hervio DML, Devlin RH (1998) Ribosomal DNA sequence analysis of isolates of the PKX myxosporean and their relationship to members of the genus Sphuerosporu. J Aquat Anim Health 10:12–21
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 CX (2001) Recent advances in our knowledge of the Myxozoa. J Eukaryot Microbiol 48:395–413
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings Bioinform 5:150–163
Lebbad M, Willcox M (1998) Spores of Henneguya salminicola in human stool specimens. J Clin Microbiol 36:1820
Lin DJ, Hanson LA, Pote LM (1999) Small subunit ribosomal RNA sequence of Henneguya exilis (Class Myxosporea) identifies the Actinosporean stage from an Oligochaete host. J Eukaryot Microbiol 46:66–68
Lom J (1990) Phylum Myxozoa. In: Margulis L, Corliss JO, Melkonian M, Chapman DJ (ed.), Handbook of Protoctista. Jones & Barlett, Boston. p. 36–52
Lom J, Arthur R (1989) A guideline for the preparation of species descriptions in Myxosporea. J Fish Dis 12:151–156
Lom J, Dykova I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitolog 53:1–36
Ma CL, Dong XM, Wang CS (1999) The myxosporida of freshwater fishes from Sichuan Province (IV): Henneguya Thelohan and Thelohanellus Kudo (Myxosporidia: Bivalvulidi). Journal of Chongqing Teachers College (Natural Science Edition) 16:12–15 (in Chinese)
McClelland RS, Murphy DM, Cone DK (1997) Report of spores of Henneguya salminicola (Myxozoa) in human stool specimens: possible source of confusion with human spermatozoa. J Clin Microbiol 35:2815–2818
Molnár K (1994) Comment on the host, organ and tissue specificity of fish myxosporeans and on the types of their intrapiscine development. Parasitologica Hungarica 27:5–20
Molnár K (2002) Site preference of fish myxosporeans in the gill. Dis Aquat Organ 48:197–207
Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York, New York, p 333
Okamura B, Canning EU (2003) Orphan worms and homeless parasites enhance bilaterian diversity. Trends Ecol Evol 18:633–639
Okamura B, Curry A, Wood TS, Canning EU (2000) Ultrastructure of Buddenbrockia identifies it as a myxozoan and verifies the bilaterian origin of the Myxozoa. Parasitology 124:215–223
Pote LM, Hanson LA, Shivaji R (2000) Small subunit ribosomal RNA sequences link the cause of proliferative gill disease in channel catfish to Henneguya n. sp. (Myxozoa: Myxosporea). J Aquat Anim Health 12:230–240
Quraishy SAl, Koura E, Abdel-Baki AS, Bashtar AR, Deed NEl, Rasheid KAl, Ghaffar FA (2008) Light and electron microscopic studies on Kudoa pagrusi sp. n. (Myxosporea: Multivalvulida) infecting the heart of sea bream Pagrus pagrus (L.) from the Red Sea. Parasitol Res 102:205–209
Rzhetsky A, Nei M (1992) A simple method for estimating and testing minimum-evolution trees. Mol Biol Evol 9:945–967
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Schlegel M, Lom J, Stechmann A, Bernhard D, Leipe D, Dykova I, Sogin ML (1996) Phylogenetic analysis of complete small subunit ribosomal RNA coding region of Myxidium lieberkuehni: evidence that Myxozoa are Metazoa and related to the Bilateria. Arch Protist 147:1–9
Schulman SS (1966) Myxosporidia of the fauna of the USSR. Nauka, Moscow, pp 1–504, in Russian
Shostak S (1993) A symbiogenetic theory for the origins of cnidocysts in Cnidaria. Biosystems 29:49–58
Siddall ME, Martin DS, Bridge D, Cone DM, Desser SS (1995) The demise of a phylum of protists: phylogeny of Myxozoa and other parasitic Cnidaria. J Parasitol 81:961–967
Siddall ME, Whiting MF (1999) Long-branch abstractions. Cladistics 15:9–24
Smothers JF, Dohlen CD, Smith LH, Spall RD (1994) Molecular evidence that the myxozoan protists are metazoans. Science 265:1719–1721
Sun CY, Zhao YJ, Chen ZG (2006) Genetic diversity among populations of Henneguya doneci (Schulman) revealed by RAPD. Chinese High Technology Letters 16:1096–1100 (in Chinese with English summary)
Swofford DL (1998) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Ver. 4. Sinauer Associates, Sunderland, MA
Székely C, Shaharom-Harrison F, Cech G, Mohamed K, Molnár K (2009) Myxozoan pathogens of Malaysian fishes cultured in ponds and net-cages. Dis Aquat Org 83:49–57
Tamura KJ, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. P Natl Acad Sci USA 101:11030–11035
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882
Vita P, Corral L, Matos E, Azevedo C (2003) Ultrastructural aspects of the myxosporean Henneguya astyanax n. sp. (Myxozoa:Myxobolidae), a parasite of the Amazonian teleost Astyanax keithi (Characidae). Dis Aquat Org 53:55–60
Yokoyama H, Kawakami H, Yasuda H, Tanaka S (2003) Henneguya lateolabracis sp. n. (Myxozoa: Myxosporea), the causative agent of cardiac henneguyosis in Chinese sea bass Lateolabrax sp. Fisheries Sci 69:1116–1120
Acknowledgements
The present study was financially supported by the earmarked fund for China Agriculture Research System (Grant no. CARS-46-08) and the National Program on Key Basic Research Project (Grant no. 2009CB118705). The authors thank Dr. Guo Xiang Liu for his help in photographing the fresh spores and Mr. Ao for his help in collecting the fish.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ye, L.T., Li, W.X., Wu, S.G. et al. 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. Parasitol Res 110, 1509–1516 (2012). https://doi.org/10.1007/s00436-011-2655-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-011-2655-2