Abstract
A new myxobolid, Thelohanellus gabori (Myxosporea: Myxozoa) parasitizing gill filaments of Crossocheilus latius (Hamilton, 1822) has been described using light microscopy, histopathology, and molecular analyses. A total of 80 live specimens of C. latius were examined, revealing a prevalence of infection of 25.66% (21 of 80 fish sampled). The plasmodia were of intrafilamental epithelial type, FE as per their location in the gill filaments of the fish host. The plasmodia were cylindrical and creamy-white, 1.0–1.7 mm in diameter containing about 500–700 myxospores. The myxospores had a mean length of 8.56 ± 0.21 μm, width 3.66 ± 0.08 μm, mean length of polar capsule 5.50 ± 0.28 μm, and width 2.50 ± 0.14 μm. The 18S rDNA of Thelohanellus gabori sp. nov. (accession number KX757025) clustered phylogenetically with other related myxozoan parasites being T. pathankotensis and T. boggoti the most closely related species with 97% sequence similarity followed by T. sp. FCO with 89% sequence similarity. The mean abundance (gill plasmodial index) was calculated by counting the number of plasmodia on each side of the gill apparatus per host and was found to be 4 indicating severe infection causing fusion of many large-sized plasmodia in the gill filament. During the present study, it was found that the phylogenetic tree for Thelohanellus spp. depends upon the tissue location, vertebrate host group, and geographical region.
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Abdel-Baki AA, Sakran T, Fayed H, Zayed E (2014) Redescription of Myxobolus niloticus infecting Labeo niloticus and their seasonal variation and histological impacts. Parasitol Res 106:1365–1369
Abdel-Ghaffar F, Abdel-Gaber R, Maher S, Al-Quraishy S, Mehlhorn H (2016) Morphological re-description and molecular characterization of Kudoa pagrusi (Myxosporea: Multivalvulida) infecting the heart muscles of the common sea bream fish Pagrus pagrus (Perciformes: Sparidae) from the Red Sea, Egypt. Parasitol Res 115:3175–3184
Abdel-Ghaffar F, Abdel-Gaber R, Maher S, El-Deeb N, Kamel R, Al-Quraishy S, Mehlhorn H (2017) Morphological and ultrastructural characteristics of Myxobolus ridibundae n. sp. (Myxosporea: Bivalvulida) infecting the testicular tissue of the marsh frog Rana ridibunda (Amphibia: Ranidae) in Egypt. Parasitol Res 116:133–141
Acharya S, Dutta T (2007) Thelohanellus habibpuri sp. n. (Myxozoa: Bivalvulida) from the tropical freshwater fishes rohu, Labeo rohita (Hamilton-Buchanan, 1882) in West Bengal, India: light and electron microscope observations. Anim Biol 57:293–300
Akhmerov AK (1960) Myxosporidia of fishes from the Amur River basin. Rybn Khoz Venutr Vodoemov Latv SSSR 5:240–307
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Andree KB, Székely C, Molnár K, Gresoviac SJ, Hedrick PP (1999) Relationships among members of the genus Myxobolus (Myxozoa: Bivalvidae) based on small subunit ribosomal DNA sequences. J Parasitol 85:68–74
Attri R (2015) Taxonomic evaluation of myxozoan parasites infecting fresh water fishes in Punjab. Ph.D. thesis, Punjabi University, Patiala (Punjab), India
Basu S, Haldar DP (1999) Thelohanellus bifurcata n. sp. a new species of the genus Thelohanellus from hybrid carps and checklist of the species of the genus described from Indian fishes. Proc Zool Soc Calcutta 52:115–124
Fiala I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol 36 (14):1521-1534
Fomena A, Bouix G (1987) Contribution al’etude des myxosporidies des poissons d’eau douce du Cameroun. III. Especes nouvelles du genre Henneguya Thélohan, 1892 Thelohanellus Kudo, 1933. J Afr Zool 101: 43–53
Fomena A, Marques A, Bouix G, Njine T (1994) Myxobolus bilongi n. sp., Thelohanellus assambai n. sp., T. sanagaensis n. sp., Myxosporidies parasites de Labeo sp. (Teleosteen: Cyprinidae) du Bassin de la Sanaga au Cameroun (Afrique Centrale). Annales de la Faculte des Sciences de Yaounde 1: 131–142
Gupta A, Kaur H (2016a) Morphological and histopathological description of Myxobolus adlardi n. sp. (Cnidaria: Myxosporea: Myxozoa) infecting an Indian major carp, Labeo rohita Hamilton, 1822 from a cold water wetland in Punjab (India). Bull Pure Appl Sci 35:39–52
Gupta A, Kaur H (2016b) 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 41:1–10. https://doi.org/10.1007/s12639-016-0856-4
Gupta A, Kaur H (2017a) Morphological and molecular characterization of Myxobolus puntiusii n. sp. (Cnidaria: Myxosporea) infecting Puntius sophore Hamilton, 1822 from Ranjit Sagar Wetland, Punjab (India). Turk J Zool 41:791–799. https://doi.org/10.3906/zoo-1606-47
Gupta A, Kaur H (2017b) A new pathogen, Myxobolus holzerae (Myxosporea: Myxozoa) causing severe gill disease in an Indian major carp Labeo rohita in a cold water wetland, Punjab (India). Microb Pathog 111:244–251
Gupta A, Kaur H (2017c) Record of new host, site of infection and locality of two myxobolids infecting freshwater fishes in Ranjit Sagar Wetland of Punjab (India). Int J Biol Res 2(4):06–11
Hall T (2011) BioEdit: an important software for molecular biology. GERF Bull Biosci 2:60–61
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, Punjab (India). Parasitol Res 114:4161–4167
Kaur H, Gupta A (2015) Genetic relatedness provides support for a species complex of myxosporeans infecting the Indian major carp, Labeo rohita. Anim Biol 65:337–347
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 Comm 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 Biol Biotech 5:21–28
Kaur H, Gupta A (2017c) Morphological, histopathological and molecular characterization of Thelohanellus pathankotensis n. sp. (Cnidaria: Myxosporea: Myxozoa) infecting an Indian minor carp, Labeo dero Hamilton, 1822 from a cold water wetland in Punjab (India). Zootaxa 4353:161–173
Kaur H, Gupta A (2017d) 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 Comm 6(1):13–21
Kaur H, Dar SA, Katoch A (2014a) Thelohanellus dykovi n. sp. (Myxozoa: Bivalvulidae), a pathogenic gill parasite in cultured Indian major carp, Labeo rohita (Hamilton, 1822) in Punjab (India). Species 10:24–30
Kaur H, Katoch A, Gupta M (2014b) Thelohanellus filli sp. n., a pathogenic myxosporean infecting gills of cultured carp, Labeo rohita (Hamilton, 1822) in Punjab, India. Species 10:31–38
Kaur H, Singh R, Katoch A, Attri R, Dar SA, Gupta A (2016) Species diversity of the genus Thelohanellus Kudo, 1933 (Myxozoa: Bivalvulida) parasitizing fishes in Indian subcontinent. J Parasit Dis 41:1–8. https://doi.org/10.1007/s12639-016-0836-8
Kimura M (1980) A simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kumar A, Sati JP, Tak PC, Alfred JRB (2006) Handbook on Indian wetland birds and their conservation. Zoological Survey of India pp 1–472
Lalitha Kumari PS (1969) Studies on parasitic protozoa (Myxosporidia) of fresh water fishes of Andhra Pradesh, India. Riv Parassitol 30:153–226
Luna LG (1968) Manual of histologic staining methods of the armed Forces Institute of Pathology. Mcgraw-Hill, New York, pp 114–115
Molnar K (2002) Site preference of fish myxosporeans in the gill. Dis Aquat Org 48:197–207
Morsy K, Semmler M, Al-Olayan E, Mehlhorn H (2015) Testicular myxosporidiasis and ultrastructural characteristics of Myxobolus bufonis (Myxobolidae) infecting the Egyptian toad Bufo regularis (Bufonidae). A light and electron microscopic study. Parasitol Res 114:3989–3997
Morsy K, Semmler M, Al-Olayan E, Mehlhorn H (2016) Henneguya collaris sp. nov., (Myxosporidia), parasite of the Greenband parrotfish Scarus collana Rüppell, 1835 (Actinopterygii: Scaridae) from the Red Sea, Egypt. A light and electron microscopic study. Parasitol Res 115:2253–2261
Mukhopadhyay D, Haldar DP (2004) Thelohanellus endodermitus sp. n.—a new myxozoan (Myxozoa: Bivalvulida) from the major carp, Labeo rohita (Hamilton, 1822) in a sewage farm in West Bengal, India. Env. Ecol 22:139–142
Okamura B, Gruhl A (2015) Myxozoan affinities and route to endoparasitism. In: Okamura B, Gruhl A, Bartholomew JL (eds) Myxozoan evolution, ecology and development. Springer, Berlin, pp 23–44
Pagarkar AU, Das M (1993) Two new species of Myxozoa, Thelohanellus caudatus n. sp. and Myxobolus serrata n. sp. from cultural carps. J Inland Fish Soc of India 25:30–35
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
Qadri SS (1962) A new Myxosporidia from the Indian fresh water fish, Labeo fimbricatus II. Thelohanellus andhrae sp. n. Z Parasitenkd, 21: 517–520
Sarkar NK (1985) Some Myxosporidia (Myxozoa: Myxosporea) of anabantid fishes of West Bengal, India. Acta Protozool 24:175–180
Sarkar NK (1994) Three new species of Myxosporidia (Myxozoa: Bivalvulida) infecting some freshwater fishes of West Bengal, India. Proc Zool Soc Calcutta 47:63–69
Sarkar NK, Mazumdar S (1983) Studies on myxosporidian parasites (Myxozoa: Myxosomatidae) from marine fishes in West Bengal, India. Description of three new species from Tachysurus sp. Arch Protistenkd 127:59–63
Singh R, Kaur H (2012a) Biodiversity of myxozoan parasites infecting freshwater fishes of three main wetlands of Punjab, India. Protistol 7:79–89
Singh R, Kaur (2012b) Thelohanellus (Myxozoa: Myxosporea: Bivalvulida) infections in major carp fish from Punjab wetlands (India). Protistol 7:178–188
Singh R, Kaur H (2012c) Myxosporean species of the genus Thelohanellus Kudo, 1933 (Myxozoa: Myxosporea: Bivalvulida) from freshwater fishes of Punjab wetlands, India. Protistol 7:208–217
Singh R, Kaur H (2012d) Two new Thelohanellus Kudo, 1933 (Myxozoa: Myxosporea: Bivalvulida) infecting fins of major carps in wetlands of Punjab. Trends Parasitol Res 1:34–43
Singh R, Kaur H (2014) Two new and two already known species of genus Thelohanellus Kudo, 1933 (Myxozoa: Myxosporea: Bivalvulida) infecting Indian major carp fishes in Punjab wetlands (India). J Parasit Dis 38:49–60
Singh R, Kaur H (2015) Two new and one already known species of the genus Thelohanellus Kudo, 1933 (Myxozoa: Myxosporea: Bivalvulida) parasitizing fresh water fishes in wetlands of Punjab, India. Biologia 70:85–93
Szekely C, Shaharom-Harrison F, Cech G, Mohamed K, Molnar K (2009) Myxozoan pathogens of Malaysian fishes cultured in ponds and net-cages. Dis Aquat Org 83:49–57
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tripathi YR (1952) Studies on the parasites of Indian fishes. Protozoa: Myxosporidia together with a checklist of parasitic protozoa described from Indian fishes. Rec Indian Museum 50:63–88
Walker J, Winton R (2010) Emerging viral diseases of fish and shrimp. Vet Res 41:51
Yuan S, Xi BW, Wang JG, Xie J, Zhang JY (2015) Thelohanellus wangi n. sp. (Myxozoa: Myxosporea), a new gill parasite of allogynogenetic gibel carp (Carassius auratus gibelio Bloch) in China, causing severe gill myxosporidiosis. Parasitol Res 114:37–45
Zhang JY, Gu ZM, Kalavati C, Eiras JC, Liu Y, Guo QY, Molnar K (2013) Synopsis of the species of Thelohanellus Kudo, 1933 (Myxozoa: Myxosporea: Bivalvulida). Sys Parasitol 86:235–256
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This study received a financial support by the University Grants Commission (UGC), Govt. of India, under UGC-CAS-II and DST-Purse grant to the department of Zoology, Panjab University, Chandigarh.
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Gupta, A., Kaur, H. Thelohanellus gabori sp. nov. (Myxosporea: Myxozoa) infecting gill filaments of a Cyprinid fish Crossocheilus latius (Hamilton, 1822) inhabiting a cold water wetland in Punjab (India). Parasitol Res 117, 2715–2723 (2018). https://doi.org/10.1007/s00436-018-5960-1
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DOI: https://doi.org/10.1007/s00436-018-5960-1