##plugins.themes.bootstrap3.article.main##

Abhishek Gupta Anshu Chaudhary Anju Tyagi Bindu Sharma Hridaya S. Singh

Abstract

A substantial literature on myxosporea has been published to date using morphological characters and specificity of host tissue. Currently, there are some 2400 nominal species of myxosporea classified to 17 families and 64 genera. Approximately 300 species have been described from India and most of them have been described solely on the basis of morphological characteristics. Molecular markers like small subunit ribosomal (SSU) and large subunit ribosomal (LSU) DNA have been used worldwide for the identification and validation of fish myxosporeans. Maximum likelihood phylogenetic tree based on SSU rDNA sequences was used to study the phylogenetic relationship among myxosporeans infecting Indian fishes. Myxospore phylogenies disagree with traditional spore-based classification systems, probably due to extreme plasticity in myxospores morphologies that have resulted in extensive convergence. Morphological similarities exist among myxosporea that encounter several problems in categorizing them. That’s why present-day research has shifted to molecular techniques for identification and correct systematics of myxosporeans. Molecular studies of myxozoans in India are still scarce and in infancy. To address persisting taxonomic and phylogenetic discrepancies, validation of these species by molecular tools is needed, because earlier species were reported only on the basis of morphological data. Therefore, the present study has summarized existing molecular data and current status of molecular taxonomy of myxosporeans parasitizing fresh and marine water fishes of India along with the approaches of myxozoan phylogenetics and information about the molecular markers, their interpretation in the identification of myxozoans parasitizing fishes.

##plugins.themes.bootstrap3.article.details##

##plugins.themes.bootstrap3.article.details##

Keywords

Myxosporea, Systematics, Fish parasites, Molecular marker, Phylogenetic analysis, Validation

References
Abdel-Gaber, R., Abdel-Ghaffar, F., Maher, S., El-Mallah, A. M., Al Quraishy, S., & Mehlhorn, H. (2017). Morphological re-description and phylogenetic relationship of five myxosporean species of the family Myxobolidae infecting Nile tilapia. Dis. Aquat. Org., 124, 201-214. https://doi.or g/10.3354/dao03118
Abidi, R., Fariya, N. & Chauhan, U. K. (2015). Development and standardization of PCR technique to detect myxozoan parasites and its use in identification of two exotic Myxobolus species from Indian catfish Clarias batrachus (linn.). Int. J. Fish. Aquat. Stud., 2, 374-377.
Abraham, T. J., Banerjee, S., Patra, A., Sarkar, A., Adikesavalu, H., & Dash, G. (2015). Molecular phylogeny of Myxobolus orissae (Myxosporea: Myxobolidae) infecting the gill lamellae of mrigal carp Cirrhinus mrigala (Actinopterygii: Cyprinidae). Mol. Biol. Res. Commun., 4, 15-24.
Andree, K. B., Székely, C., Molnár, K., Gresoviac, S. J., & Hedrick, R. P. (1999). Relationships among members of the genus Myxobolus (Myxozoa: Bilvalvidae) based on small subunit ribosomal DNA sequences. J. Parasitol., 85, 68-74. https://doi.org/10.2307/3285702
Anjan, M., Sayani, B., Avijit, P., Harresh, A., Raghu, R. K., Gadadhar, D. and Jawahar, A. T. (2014). Molecular & morphometric characterization of Thelohanellus caudatus (Myxosporea: Myxobolidae) infecting the caudal fin of Labeo rohita (Hamilton). Protistol., 8, 41-52.
Banerjee, S., Patra, A., Adikesavalu, H., Joardar, S. N. & Abraham, T. J. (2015a). Molecular and phylogenetic characterization of Thelohanellus qadrii (Myxozoa, Myxosporea, Bivalvulida) infecting the secondary gill epithelium of Indian major carp, Catla catla (Hamilton, 1822). Mol. Biol. Res. Commun., 4, 83-91.
Banerjee, S., Patra, A., Adikesavalu, H., Mondal, A. & Abraham, T. J. (2015b). The phylogenetic position of Myxobolus carnaticus (Myxozoa, Myxosporea, Bivalvulida) infecting gill lamellae of Cirrhinus mrigala (Hamilton, 1822) based on 18S rRNA sequence analysis. Mol. Biol. Res. Commun., 4, 125-132.
Banerjee, S., Patra, A., Mondal, A., Adikesavalu, H., Ramudu, K. R., Dash, G. and Abraham, T. J. (2017). Molecular characterization of Myxobolus catmrigalae (Myxosporea: Myxobolidae) infecting the gill lamellae of carp Cirrhinus mrigala (Hamilton). J. Parasit. Dis. 41, 62-70.
Bartošová, P., Fiala, I., & Hypša, V. (2009). Concatenated SSU and LSU rDNA data confirm the main evolutionary trends within myxosporeans (Myxozoa: Myxosporea) and provide an effective tool for their molecular phylogenetics. Mol. Phylogenet. Evol., 53, 81-93. https://doi.org/10.1016/j.ympev.2009.05.018
Bartošová, P., Fiala, I., Jirk?, M., Cinková, M., Caffara, M., Fioravanti, M. L., & Holzer, A. S. (2013). Sphaerospora sensu stricto: taxonomy, diversity and evolution of a unique lineage of myxosporeans (Myxozoa). Mol. Phylogenet. Evol., 68, 93-105. https://doi.org/10.1016/j.ympev.2013.02.026
Chandran, A., Zacharia, P. U. & Sanil, N. K. (2020). Ortholinea scatophagi (Myxosporea: Ortholineidae), a novel myxosporean infecting the spotted scat, Scatophagus argus (Linnaeus 1766) from southwest coast of India. Parasitol. Int., 75, 102020. https://doi.org/10.1016/j.parint.2019.102020
Chandran, A., Zacharia, P. U., Sathianandan, T. V., Shamal, P., Binesh, C. P., Kaur, P. & Sanil, N. K. (2018). Morphological and molecular characterization of Chloromyxum argusi n. sp. (Myxosporea) infecting the urinary bladder of Scatophagus argus Linnaeus 1766 (Scatophagidae) from the southwest coast of India. Parasitol. Res., 117, 3145-3156. https://doi.org/10.1007/s00436-018-6013-5
Chaudhary, A., Goswami, U., Gupta, A., Cech, G., Singh, H. S., Molnár, K., Szekely, C. & Sharma, B. (2018). Morphological, histological, and molecular description of Myxobolus ompok n. sp. (Myxosporea: Myxobolidae), a kidney myxozoan from Pabdah catfish Ompok pabda (Hamilton, 1822) (Siluriformes: Siluridae) in India. Parasitol. Res., 117, 1899-1905. https://doi.org/10.1007/s0 0436-018-5882-y
Chaudhary, A., Gupta, A., Goswami, U., Cech, G., Molnár, K., Singh, H. S. & Székely, C. (2019). Molecular Genetic Studies on Myxobolus cylindricus and Henneguya mystasi (Myxosporea: Myxobolidae) Infecting Two Indian Fish Species, Channa gachua and Mystus vittatus, Respectively. Acta Parasitol., 64, 129-137. https://doi.org/10.2478/s11686-018-00014-8
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 Channa punctata (Bloch) (Perciformes: Channidae) in India. Syst. Parasitol., 94, 403-411. https://doi.org/10.1007/s11230-017-9705-9
Evans, N. M., Holder, M. T., Barbeitos, M. S., Okamura, B., and Cartwright, P. (2010). The phylogenetic position of Myxozoa: exploring conflicting signals in phylogenomic and ribosomal data sets. Mol. Biol. Evol., 27, 2733-2746. https://doi.org/10.1093/molbev/msq159
Fariya, N., Ali, D., Abide, R., Falodah, F. A., Alarifi, S. & Alkahtani, S. (2020). Morphological and molecular evidence for Myxobolus toyami as an evolutionary link between Thelohanellus and Myxobolus genera of myxozoan parasites. Fresenius. Environ. Bull., 29, 633-639.
Fiala, I. (2006). The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int. J. Parasitol., 36, 1521-1534. https://doi.org/10.1016/j.ijpara.2006.06.016
Fiala, I. & Bartošová, P. (2010). History of myxozoan character evolution on the basis of rDNA and EF-2 data. BMC Evol. Biol., 10, 228-235. https://doi.org/10.1186/1471-2148-10-228
Fiala, I., Bartošová-Sojková, P., Okamura, B., & Hartikainen, H. (2015). Adaptive radiation and evolution within the Myxozoa. In Myxozoan evolution, ecology and development, pp 69-84. https://doi.org/10.1007/978-3-319-14753-6_4
Jirku, M., Fiala, I., & Modrý, D. (2007). Tracing the genus Sphaerospora: rediscovery, redescription and phylogeny of the Sphaerospora ranae (Morelle, 1929) n. comb. (Myxosporea, Sphaerosporidae), with emendation of the genus Sphaerospora. Parasitology, 134, 1727-1739. https://doi.org/10.1017/s0031182007003241
Gunter, N., & Adlard, R. (2010). The demise of Leptotheca Thélohan, 1895 (Myxozoa: Myxosporea: Ceratomyxidae) and assignment of its species to Ceratomyxa Thélohan, 1892 (Myxosporea: Ceratomyxidae), Ellipsomyxa Køie, 2003 (Myxosporea: Ceratomyxidae), Myxobolus Bütschli, 1882 and Sphaerospora Thélohan, 1892 (Myxosporea: Sphaerosporidae). Syst. Parasitol 75, 81-104. https://doi.org/10.1007/s11230-009-9227-1
Gupta, A. & Kaur, H. (2017). Morphological, histopathological and molecular characterization of Thelohanellus theinensis n. sp. (Cnidaria: Myxosporea) infecting an Indian major carp, Labeo bata in a cold water wetland in Punjab (India). J. Parasit. Dis., 41, 629-638. https://doi.org/10.1007/s12639-016-0856-4
Gupta, A., Chaudhary, A., Garg, A., Verma, C., Singh, H. S. & Sharma, B. (2018). First molecular evidence of Thelohanellus wallagoi Sarkar, 1985 (Myxozoa) from economically important food fish, freshwater shark Wallago attu (Siluridae) in India. Acta Parasitol., 63, 647-653. https://doi.org/10.1515/ap-2018-0075
Heiniger, H., Gunter, N. L., & D ADLARD, R. O. B. E. R. T. (2011). Re-establishment of the family Coccomyxidae and description of five novel species of Auerbachia and Coccomyxa (Myxosporea: Bivalvulida) parasites from Australian fishes. Parasitology, 138, 501-515. https://doi.org/10.1017/s003118 201 0001447
Hartikainen, H., Gruhl, A., & Okamura, B. (2014). Diversification and repeated morphological transitions in endoparasitic cnidarians (Myxozoa: Malacosporea). Mol. Phylogenet. Evol., 76, 261-269.https://doi.org/10.1016/j.ympev.20 14.03.010
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. Int. J. Parasitol., 34,1099-1111.https://doi.org/10.1016/j.ijpara.2 004.06.002
Kalavati, C. & Nandi, N. C. (2007). Handbook on myxosporean parasites of Indian fishes. New Delhi: Zoological Survey of India, Kolkata, India, pp-294.
Kaur, H. (2014). Myxozoan infestation in freshwater fishes in wetlands and aquaculture in Punjab (India). Adv. Anim. Vet. Sci., 2, 488-502. https://doi.org/10.14737/journal.aavs/2014/2.9.488.502
Kaur, H. & Attri, R. (2015). Morphological and molecular characterization of Henneguya bicaudi n. sp.(Myxosporea: Myxobolidae) infecting gills of Cirrhinus mrigala (Ham.) in Harike Wetland, Punja (India). Parasitol. Res., 114, 4161-4167. https://doi. org/10.1007/s00436-015-4647-0
Kaur, H. & Gupta, A. (2017a). Molecular and phylogenetic characterization of Thelohanellus boggoti Qadri, 1962 (Cnidaria, Myxosporea, Bivalvulida) infecting the fin of Indian minor carp Labeo dero (Hamilton, 1822). Mol. Biol. Res. Commun., 6, 13-21.
Kaur, H. & Gupta, A. (2017b). Morphological, histopathological and molecular characterization of Thelohanellus muscularis n. sp. (Cnidaria: Myxosporea) infecting head muscles of Labeo rohita from Ranjit sagar wetland, Punjab (India). J. Appl. Bio. Biotechnol., 5, 21-28. https://doi.org/10.7324/jabb.2 017.50104
Kaur, H. & Singh, R. (2012). A synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Bivalvulida) parasitizing Indian fishes and a revised dichotomous key to myxosporean genera. Syst. Parasitol., 81, 17-37. https://doi.org/10.1007/s11230-011-9321-z
Kaur, H., Katoch, A. & Gupta, M. (2014). Thelohanellus filli sp. n., a pathogenic myxosporean infecting gills of cultured carp, Labeo rohita (Hamilton 1822) in Punjab, India. Species, 10, 31-38.
Kent, M. L., Andree, K. B., Bartholomew, J. L., El-Matbouli, M., Desser, S. S., Devlin, R. H. & Hallett, S. L. (2001). Recent advances in our knowledge of the Myxozoa. J. Eukaryot. Microbiol., 48, 395-413. https://doi.org/10.1111/j.1550-7408.2001.tb00173.x
Kosakyan, A., Alama-Bermejo, G., Bartošová-Sojková, P., Born-Torrijos, A., Šíma, R., Nenarokova, A. & Holzer, A. S. (2019). Selection of suitable reference genes for gene expression studies in myxosporean (Myxozoa, Cnidaria) parasites. Sci. Rep., 9, 1-14. https://doi.org/10.1038/s41598-019-51479-0
Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol., 35, 1547-1549. https://doi.org/10.1093/molbev/msy096
Lom, J. & Dyková, I. (2006). Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol., 53, 1-36. https://doi.org/10.14411/fp.2006.001
Molnár, K. (1994). Comments on the host, organ and tissue specificity of fish myxosporeans and on the types of their intrapiscine development. Parasitol. Hung., 27, 5-20.
Naldoni, J., Maia, A. A., Correa, L. L., da Silva, M. R., & Adriano, E. A. (2018). New myxosporeans parasitizing Phractocephalus hemioliopterus from Brazil: morphology, ultrastructure and SSU-rDNA sequencing. Diseases of aquatic organisms, 128(1), 37-49. https://doi.org/10.3354/dao03210
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. Parasitol., 124, 369-379. https://doi.org/10.1017/s0031182001001354
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.).  Mol. Biol. Res. Commun., 3, 231-239.
Sanil, N. K., Chandran, A., Shamal, P. & Binesh, C. P. (2017). Molecular and morphological descriptions of Ceratomyxa collarae n. sp. and Ceratomyxa leucosternoni n. sp. from marine ornamental fishes of Indian waters. Parasitol. Res., 116, 529-537. https://doi.org/10.1007/s00436-016-5317-6
Saulnier, D., Philippe, H., & Kinkelin, P. (1999). Molecular evidence that the proliferative kidney disease organism unknown (PKX) is a myxosporean. Dis. Aquat. Org., 36, 209-212. https://doi.org/10.3354/dao036209
Singh, R. & Kaur, H. (2012). Biodiversity of myxozoan parasites infecting freshwater fishes of three main wetlands of Punjab, India. Protistol., 7, 79-89.
Smothers, J. F., Von Dohlen, C. D., Smith, L. J., & Spall, R. D. (1994). Molecular evidence that the myxozoan protists are metazoans. Science, 265, 1719-1721. https://doi.org/10.1126/science.8085160
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. Parasitol. Res., 114, 1301-1311. DOI:10.10 07/s00436-014-4307-9
Whipps, C. M., & Kent, M. L. (2006). Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea). J. Eukaryot. Microbiol., 53, 364-373. https://doi.org/10.1111/j.1550-7408.2006.00114.x
Whipps, C. M., Grossel, G., Adlard, R. D., Yokoyama, H., Bryant, M. S., Munday, B. L., & Kent, M. L. (2004). Phylogeny of the Multivalvulidae (Myxozoa: Myxosporea) based on comparative ribosomal DNA sequence analysis. J. Parasitol., 90, 618-622. https://doi.org/10.1645/ge-153r
Ye, L., Lu, M., Quan, K., Li, W., Zou, H., Wu, S., & Wang, G. (2017). 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. Chin. J. Oceanol. Limn., 35, 587-596. https://doi.org/10.1007/s00343-017-5312-5
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. Parasitol. Res., 112, 3817-3823. https://doi.org/10.1007/s00436-013-3569-y
Section
Research Articles

How to Cite

Molecular tools for identification and classification of Myxozoan parasites (Cnidaria: Myxosporea) in India: Current status. (2021). Journal of Applied and Natural Science, 13(1), 51-58. https://doi.org/10.31018/jans.v13i1.2451