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Licensed Unlicensed Requires Authentication Published by De Gruyter July 4, 2018

First molecular evidence of Thelohanellus wallagoiSarkar, 1985 (Myxozoa) from economically important food fish, freshwater shark Wallago attu (Siluridae) in India

Abhishek Gupta, Anshu Chaudhary, Anupma Garg, Chandni Verma, Hridaya S. Singh and Bindu Sharma
From the journal Acta Parasitologica

Abstract

The freshwater shark Wallago attu (Bl. and Schn.) is a frequent silurid in the River Ganga and one of the most commercially exploit fish in India. In a survey on its infection with myxosporeans, spore type belongs to Thelohanellus species was found in the gills, kidney and intestine respectively. Through morphological and molecular investigations, we identified the spore as Thelohanellus wallagoiSarkar, 1985. They were pyriform in valvular view and slim in sutural view, and had one pyriform polar capsule with four to five turns. The spores measured 8.0 × 4.0 × 2.3 μm. T. wallagoi developed in small cysts in the gill lamellae, whereas cyst and scattered spores of T. wallagoi were also found in the kidney and intestine respectively. The 18S rDNA sequence of T. wallagoi isolates recovered from gills, kidney and intestine were found similar to each other and differed from any other Thelohanellus species available in GenBank and validated its status after 32 years of original description. Phylogenetic analysis signified that T. wallagoi was placed sister to Myxobolus species in the clade that indicated the polyphyletic nature of the genus Thelohanellus.

Acknowledgements

The authors thank to the Head, Department of Zoology, Chaudhary Charan Singh University, Meerut, for providing laboratory facilities. The authors declare that they have no conflict of interest.

References

Adriano E.A., Arana S., Alves A.L., Silva M.R., Ceccarelli P.S., Henrique-Silva F., Maia A.A. 2009. Myxobolus cordeiroi n. sp., a parasite of Zungaro jahu (Siluriformes: Pimelodiade) from Brazilian Pantanal: Morphology, phylogeny and histopathology. Veterinary Parasitology, 162, 221–229. 10.1016/j.vetpar.2009.03.030Search in Google Scholar PubMed

Atkinson S., Bartošová-Sojková P., Whipps C., Bartholomew J. 2015. Approaches for characterizing myxozoan species, Chapter 6. In: (Eds B. Okamura, A. Gruhl, J.L. Bartholomew) Myxozoan Evolution, Ecology and Development. Springer International Publishing, pp. 111–12310.1007/978-3-319-14753-6_6Search in Google Scholar

Banerjee S., Patra A., Adikesavalu H., Joardar S.N., Abraham T.J. 2015. Molecular and phylogenetic characterization of Thelohanellus qadrii (Myxozoa, Myxosporea, Bivalvulida) infecting the secondary gill epithelium of Indian major carp, Catla catla (Hamilton, 1822). Molecular Biology Research Communications, 4, 83–91Search in Google Scholar

Barta J.R., Martin D.S., Libetator P.A., Dashkevicz M., Anderson J.W., Feighner S.D., et al. 1997. Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. Journal of Parasitology, 83, 262–27110.2307/3284453Search in Google Scholar

Basu S., Modak B.K., Haldar D.P. 2006. Synopsis of the Indian species of the genus Thelohanellus Kudo, 1933 along with description of Thelohanellus disporomorphus sp.n. Journal of Parasitology and Applied Animal Biology, 15, 81–94Search in Google Scholar

Cech G., Molnár K., Székely C. 2012. Molecular genetic studies on morphologically indistinguishable Myxobolus spp. infecting cyprinid fishes, with the description of three new species, M. alvarezae sp. nov., M. sitjae sp. nov. and M. eirasianus sp. nov. Acta Parasitologica, 57, 354–366.10.2478/s11686-012-0045-2Search in Google Scholar PubMed

Chaudhary A., Molnár K., Gupta A., Cech G., Singh H.S., Székely C. 2017. Redescription of Henneguya chaudhuryi (Bajpai & Haldar, 1982) (Myxosporea: Myxobolidae), infecting the gills of the freshwater fish Channapunctata (Bloch) (Perciformes: Channidae) in India. Systematic Parasitology, 94, 403– 411.10.1007/s11230-017-9705-9Search in Google Scholar PubMed

Chen C.L., Ma C.L. 1998. Fauna Sinica. Myxozoa. Myxosporea.Science Press, Beijing, pp. 993. (In Chinese)Search in Google Scholar

Eszterbauer E., Benkő M., Dán Á., Molnár K. 2001. Identification of fish parasitic Myxobolus (Myxosporea) species using a combined PCR-RFLP method. Diseases of Aquatic Organisms, 44, 35–39. 10.3354/dao044035Search in Google Scholar PubMed

Eszterbauer E., Székely C. 2004. Molecular phylogeny of the kidney parasitic Sphaerospora renicola from common carp (Cyprinus carpio) and Sphaerospora sp. from goldfish (Carassius auratus auratus). Acta Veterinaria Hungarica, 52, 469–478.10.1556/AVet.52.2004.4.9Search in Google Scholar PubMed

Fiala I., Bartošová P. (2010) History of myxozoan character evolution on the basis of rDNA and EF-2 data. BMC Evolutionary Biology, 10, 228. 10.1186/1471-2148-10-228Search in Google Scholar PubMed PubMed Central

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, 95–98Search in Google Scholar

Kalavati C., Nandi N.C.(Eds) 2007. Handbook on myxosporean parasites of Indian fishes. Zoological Survey of India, Kolkata, India, pp. 294Search in Google Scholar

Kaur H., Gupta A. 2017. Molecular and phylogenetic characterization of Thelohanellus boggoti Qadri, 1962 (Cnidaria, Myxosporea, Bivalvulida) infecting the fin of Indian minor carp Labeo dero (Hamilton, 1822). Molecular Biology Research Communications, 6, 13–21Search in Google Scholar

Kaur H., Singh R., Katoch A., Attri R., Dar S.A., Gupta A. 2016. Species diversity of the genus Thelohanellus Kudo, 1933 (Myxozoa: Bivalvulida) parasitizing fishes in Indian subcontinent. Journal of Parasitic Diseases, 41, 305–312. 10.1007/s12639-016-0836-8Search in Google Scholar PubMed PubMed Central

Kudo R.R. 1933. A taxonomic consideration of myxosporidia. Transactions of the American Microscopical Society, 52, 195–21610.2307/3222254Search in Google Scholar

Lalitha-Kumari P.S. 1969. Studies on parasitic protozoa (Myxosporidia) of freshwater fishes of Andhra Pradesh, India. Rivista Di Parassitologia, 30, 154–225Search in Google Scholar

Liu Y., Whipps C.M., Gu Z.M., Zeng L.B. 2010. Myxobolus turpisrotundus (Myxosporea: Bivalvulida)spores with caudal appendages: investigating the validity of the genus Henneguya with morphological and molecular evidence. Parasitology Research, 107, 699–706.10.1007/s00436-010-1924-9Search in Google Scholar PubMed

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, 1331–1336. 10.1007/s00436-011-2629-4Search in Google Scholar PubMed

Liu Y., Whipps C.M., Gu Z.M., Huang M.J., He C., Yang H.L., Molnár K. 2013. Myxobolus musseliusae (Myxozoa: Myxobolidae) from the gills of common carp Cyprinus carpio and revision of Myxobolus dispar recorded in China. Parasitology Research, 112, 289–296. 10.1007/s00436-012-3136-ySearch in Google Scholar PubMed

Liu Y., Jia L., Huang M.J., Gu Z.M. 2014.Thelohanellus testudineus n. sp. (Myxosporea: Bivalvulida) infecting the skin of allogynogenetic gibel carp Carassius auratus gibelio (Bloch) in China. Journal of Fish Diseases, 37, 535–542.10.1111/jfd.12141Search in Google Scholar PubMed

Liu Y., Zhai Y., Gu Z. 2016. Morphological and molecular characterization of Thelohanellus macrovacuolaris n. sp. (Myxosporea: Bivalvulida) infecting the palate in the mouth of common carp Cyprinus carpio L. in China. Parasitology International, 65, 303–307. 10.1016/j.parint.2016.02.013Search in Google Scholar PubMed

Lom J., Arthur J.R. 1989. A guideline for preparation ofspecies descriptions in Myxosporea. Journal of Fish Diseases, 12, 151–15610.1111/j.1365-2761.1989.tb00287.xSearch in Google Scholar

Lom J., Dyková I. 2006. Myxozoan Genera: Definition and Notes on Taxonomy, Life-cycle Terminology and Pathogenic Species. Folia Parasitologica, 53, 1–3610.14411/fp.2006.001Search in Google Scholar

Marton S., Eszterbauer E.2011. The development of Myxobolus pavlovskii (Myxozoa: Myxobolidae) includes an echinactinomyxon-type actinospore. Folia Parasitologica, 58: 157–16310.14411/fp.2011.015Search in Google Scholar PubMed

Milne I., Lindner D., Bayer M., Husmeier D., McGuire G., Marshall D.F., Wright F. 2008. TOPALi v2: as rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics, 25, 126–127.10.1093/bioinformatics/btn575Search in Google Scholar PubMed PubMed Central

Molnár, K., Eszterbauer, E. 2015. Specificity of infection sites in vertebrate hosts. In: Myxozoan Evolution, Ecology and Development. (Ed.) Spinger International Publishing, London, pp. 295–313.10.1007/978-3-319-14753-6_16Search in Google Scholar

Molnár K., Eszterbauer E., Marton S., Cech G., Szekély C. 2009. Myxobolus erythrophthalmi sp. n. and Myxobolus shaharomae sp. n. (Myxozoa: Myxobolidae) from the internal organs of rudd, Scardinius erythrophthalmus (L.), and bleak, Alburnus alburnus (L.).Journal of Fish Diseases, 32, 219–231 .10.1111/j.1365-2761.2008.00976.xSearch in Google Scholar PubMed

Molnár K., Marton S., Szekély C., Eszterbauer E. 2010. Differentiation of Myxobolus spp. (Myxozoa: Myxobolidae) infecting roach (Rutilus rutilus) in Hungary. Parasitology Research, 107, 1137–1150.10.1007/s00436-010-1982-zSearch in Google Scholar PubMed

Rajesh S.C., Banerjee S., Patra A., Dash G., Abraham T.J. 2014. Molecular characterization of Myxobolus cuttacki (Myxozoa, Myxosporea, Bivalvulida) infecting gill lamellae of minor carp Labeo bata (Ham.). Molecular Biology Research Communications, 3, 231–239Search in Google Scholar

Saha M., Bandyopadhyay P.K. 2017. Parasitological and histological analysis of a new species of the genus Thelohanellus and description of a myxozoan parasite (Myxosporea: Bivalvulida) from cultured ornamental goldfish, Carassius auratus L. Aquaculture Reports, 8, 8–15. 10.1016/j.aqrep.2017.07.001Search in Google Scholar

Sarkar N.K. 1985. Some coelozoic Myxosporida (Myxozoa: Myxosporea) from a freshwater water teleost fish of River Padma. Acta Protozoologica, 24, 47–53.Search in Google Scholar

Singh R., Kaur H. 2012. Myxosporean species of the genus Thelohanellus Kudo, 1933 (Myxozoa: Myxosporea: Bivalvulida) from freshwater fishes of Punjab wetlands, India. Protistology, 7, 209–217.Search in Google Scholar

Singh R., Kaur H. 2015. Two new and one already known species of the genus Thelohanellus (Myxozoa: Myxosporea: Bivalvulida) parasitizing fresh water fishes in wetlands of Punjab, India. Biologia, 70, 85–93. 10.1007/s12639-012-0190-4Search in Google Scholar PubMed PubMed Central

Székely C., Cech G., Chaudhary A., Borzák R., Singh H.S., Molnár K. 2015. Myxozoan infections of the three Indian major carps in fish ponds around Meerut, UP, India, with descriptions of three new species, Myxobolus basuhaldari sp. n., M. kalavatiae sp. n. and M. meerutensis sp. n., and the redescription of M. catlae and M. bhadrensis. Parasitology Research, 114, 1301–1311.10.1007/s00436-014-4307-9Search in Google Scholar PubMed

Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.10.1093/molbev/mst197Search in Google Scholar PubMed PubMed Central

Thelohan P. 1892. Observation sur les myxosporidies et essai de classificationde ces organismes. Bulletin de la Société Philomathiquede Paris, 4, 165–178. ( In French)Search in Google Scholar

Thompson J.D., Higgins D.G., Gibson T.J. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–468010.1093/nar/22.22.4673Search in Google Scholar PubMed PubMed Central

Zhang J.Y., Gu Z.M., Kalavati C., Eiras J.C., Liu Y., Guo Q.Y., Molnar K. 2013. A synopsis of the species of Thelohanellus Kudo, 1933 (Myxozoa: Myxosporea: Bivalvulida). Systematic Parasitology, 86, 235–256. 10.1007/s11230-013-9449-0Search in Google Scholar PubMed

Received: 2018-01-03
Revised: 2018-04-11
Accepted: 2018-04-12
Published Online: 2018-07-04
Published in Print: 2018-09-25

© 2018 W. Stefański Institute of Parasitology, PAS