Abstract
A new species of Ceratomyxa infecting the gallbladder of the marine ornamental fish Acanthurus xanthopterus collected from the Vizhinjam coast of Kerala is described. The parasite exhibited a prevalence of 100%. Mature spores recovered from the gallbladder were slightly crescentic with rounded lateral extremities and possessed convex anterior and slightly concave to straight posterior margins. Spore valves two, equal, joined by a straight and prominent suture. Myxospores measured 5.5 ± 0.6 μm in length and 15.9 ± 2.3 μm in thickness. Polar capsules two, equal, spherical, positioned anteriorly on either sides of the suture, 2.3 ± 0.2 μm long and 2.2 ± 0.2 μm wide. Polar filament with four to five coils, 21.2 ± 0.6 μm when extruded. Posterior angle 173.6 ± 5.2°. Early sporogonic stages and monosporic, disporic, and multisporic plasmodial stages were spherical to irregular in shape, with or without filopodia. Histopathologic analysis revealed that spores and developing stages were attached to the gallbladder wall as well as found free in the lumen. Morphologic and morphometric comparison of the present parasite with known species of Ceratomyxa indicated significant differences. In molecular and phylogenetic analyses, the present myxosporean revealed high divergence with related forms and occupied an independent position within the Ceratomyxa clade with high nodal support. Considering the morphological, morphometric, molecular, and phylogenetic dissimilarities with the previously described species of Ceratomyxa and the differences in host and geographic locations, the present species of myxosporean is treated as new and is named Ceratomyxa xanthopteri n. sp.
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Abdel-Ghaffar F, Ali MA, Al Quraishy S, Al Rasheid K, Al Farraj S, Abdel-Baki AS, Bashtar AR (2008) Four new species of Ceratomyxa Thelohan 1892 (Myxozoa: Myxosporea: Ceratomyxidae) infecting the gallbladder of some Red Sea fishes. Parasitol Res 103(3):559–565
Alama-Bermejo G, Raga JA, Holzer AS (2011) Host–parasite relationship of Ceratomyxa puntazzi n. sp. (Myxozoa: Myxosporea) and sharpsnout seabream Diplodus puntazzo (Walbaum, 1792) from the Mediterranean with first data on ceratomyxid host specificity in sparids. Vet Parasitol 182(2-4):181–192
Alama-Bermejo G, Sima R, Raga JA, Holzer AS (2013) Understanding myxozoan infection dynamics in the sea: seasonality and transmission of Ceratomyxa puntazzi. Int J Parasitol 43:771–780
Atkinson SD, Bartholomew JL, Lotan T (2018) Myxozoans: ancient metazoan parasites find a home in phylum Cnidaria. Zoology 129:66–68
Barta JR, Martin DS, Liberator PA, Dashkevicz M, Anderson JW, Feighner SD, Elbrecht A, Perkins-Barrow A, Jenkins MC, Danforth HD, Ruff MD (1997) Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. J Parasitol 83(2):262–271
Cho JB, Kwon SR, Kim SK, Nam YK, Kim KH (2004) Ultrastructure and development of Ceratomyxa protopsettae Fujita, 1923 (Myxosporea) in the gall bladder of cultured olive flounder, Paralichthys olivaceus. Acta Protozool 43:241–250
Eiras JC (2006) Synopsis of the species of Ceratomyxa Thélohan, 1892 (Myxozoa: Myxosporea: Ceratomyxidae). Syst Parasitol 65(1):49–71
Eiras JC, Cruz C, Saraiva A (2018) Synopsis of the species of Ceratomyxa Thélohan, 1892 (Cnidaria, Myxosporea, Ceratomyxidae) described between 2007 and 2017. Syst Parasitol 95(5):427–446
Fiala I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol 36(14):1521–1534
Fiala I, Hlavničková M, Kodádková A, Freeman MA, Bartošová-Sojková P, Atkinson SD (2015) Evolutionary origin of Ceratonova shasta and phylogeny of the marine myxosporean lineage. Mol Phylogenet Evol 86:75–89
Gaevskaya AV, Kovaleva AA (1979) Two new species of Myxosporidia Davisia donecae n. sp. and Ceratomyxa australis n, sp., from the horse mackerel in the south-eastern Atlantic (In Russian). Biol Morya (Vladivostok) 3:80–83
Gleeson R, Adlard R (2011) Morphological and genetic analysis of three new species of Ceratomyxa Thélohan, 1892 (Myxozoa: Myxosporea) from carcharhinid sharks off Australia. Syst Parasitol 80(2):117–124
Gunter NL, Adlard RD (2008) Bivalvulidan (Myxozoa: Myxosporea) parasites of damselfishes with description of twelve novel species from Australia’s Great Barrier Reef. Parasitol 135(10):1165–1178
Gunter NL, Adlard RD (2009) Seven new species of Ceratomyxa Thélohan, 1892 (Myxozoa) from the gall-bladders of serranid fishes from the Great Barrier Reef, Australia. Syst Parasitol 73(1):1–11
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(2):81–104
Gunter NL, Whipps CM, Adlard RD (2009) Ceratomyxa (Myxozoa: Bivalvulida): robust taxon or genus of convenience? Int J Parasitol 39(12):1395–1405
Gunter NL, Burger MA, Adlard RD (2010) Morphometric and molecular characterisation of four new Ceratomyxa species (Myxosporea: Bivalvulida: Ceratomyxidae) from fishes off Lizard Island, Australia. Folia Parasitol 57(1):1–10
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Heiniger H, Adlard R (2013) Molecular identification of cryptic species of Ceratomyxa Thélohan, 1892 (Myxosporea: Bivalvulida) including the description of eight novel species from apogonid fishes (Perciformes: Apogonidae) from Australian waters. Acta Parasitol 58(3):342–360
Heiniger H, Gunter NL, Adlard RD (2008) Relationships between four novel ceratomyxid parasites from the gall bladders of labrid fishes from Heron Island, Queensland, Australia. Parasitol Int 57(2):158–165
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(10):1099–1111
Holzer AS, Wootten R, Sommerville C (2007) The secondary structure of the unusually long 18S ribosomal RNA of the myxozoan Sphaerospora truttae and structural evolutionary trends in the Myxozoa. Int J Parasitol 37(11):1281–1295
Hsieh SR, Chen CL (1984) A new species of myxosporidian parasite (Ceratomyxa hongzensis) from freshwater fishes of China. Acta Zootaxon Sin 9:337–338
Kent ML, Margolis L, Whitaker DJ, Hoskins GE, McDonald TE (1994) Review of Myxosporea of importance in salmonid fisheries and aquaculture in British Columbia. Folia Parasitol 41(1):27–37
Kent ML, Andree KB, Bartholomew JL, El-Matbouli M, Desser SS, Devlin RH, Feist SW, Hedrick RP, Hoffmann RW, Khattra J, Hallett SL, Lester RJ, Longshaw M, Palenzeula O, Siddall ME, Xiao C (2001) Recent advances in our knowledge of the Myxozoa. J Eukaryot Microbiol 48(4):395–413
Kpatcha TK, Diebakate C, Faye N, Toguebaye BS (1996) Quelques nouvelles espèces de Myxosporidies, du genre Ceratomyxa Thélohan, 1895 parasites des poissons marins du Sénégal, Afrique de l’Ouest. Parasite 3:223–228
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
Lom J, Arthur JR (1989) A guideline for the preparation of species descriptions in Myxosporea. J Fish Dis 12(2):151–156
Lom J, Dyková I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 53:1–36
Mackenzie K, Kalavati C (2014) Myxosporean parasites of marine fishes: their distribution in the world’s oceans. Parasitology 141(13):1709–1717
Moser M, Kent ML, Dennis D (1989) Gall-bladder Myxosporea in coral-reef fishes from Heron Island, Australia. Aust J Zool 37(1):1–13
Palenzuela O, Sitjà-Bobadilla A, Álvarez-Pellitero P (1997) Ceratomyxa sparusaurati (Protozoa: Myxosporea) infections in cultured gilthead sea bream Sparus aurata (Pisces: Teleostei) from Spain: aspects of the host-parasite relationship. Parasitol Res 83(6):539–548
Qiao Y, Shao Y, Pengsakul T, Chen C, Zheng S, Wu W, Hardjo TB (2019) Morphological and molecular characterization of Ceratomyxa batam n. sp.(Myxozoa: Ceratomyxidae) infecting the gall bladder of the cultured Trachinotus ovatus (Perciformes: Carangidae) in Batam Island, Indonesia. Parasitol Res 118(5):1647–1651
Rambaut A. (2016) FigTree v1.4.3. Mol. Evol. phylogenetics Epidemiol. http://tree.bio.ed.ac.uk/software/figtree.
Reed CC, Basson L, Van As LL, Dyková I (2007) Four new myxozoans (Myxosporea: Bivalvulida) from intertidal fishes along the south coast of Africa. Folia Parasitol 54(4):283–292
Rocha S, Rangel LF, Castro R, Severino R, Azevedo C, Santos MJ, Casal G (2016) Ultrastructure and phylogeny of Ceratomyxa diplodae (Myxosporea: Ceratomyxidae), from gall bladder of European seabass Dicentrarchus labrax. Dis Aquat Org 121(2):117–128
Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542
Sanil NK, Chandran A, Shamal P, Binesh CP (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(2):529–537
Sitja-Bobadilla A, Alvarez-Pellitero P (1993) Population dynamics of Sphaerospora dicentrarchi Sitja-Bobadilla et Alvarez-Pellitero, 1992 and S. testicularis Sitja-Bobadilla et Alvarez-Pellitero, 1990 (Myxosporea: Bivalvulida) infections in wild and cultured Mediterranean sea bass (Dicentrarchus labrax L.). Parasitology 106(1):39–45
Su XQ, White RWG (1994) New Myxosporeans [Myxozoa: Myxosporea] from marine fishes of Tasmania, Australia. Acta Protozool 33:251–259
Suvarna K, Layton C, Bancroft J (2018) Bancroft’s theory and practice of histological techniques, 8th edn. Elsevier, United Kingdom, pp 126–139
Thabet A, Abdel-Baki AAS, Harrath AH, Mansour L (2019) Morphological and molecular aspects of Ceratomyxa ghannouchensis n. sp. and C. pallida Thélohan 1894 infecting the bogue, Boops boops (l.). J Nat Hist 53(9-10):541–556
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680
Whipps CM, Adlard RD, Bryant MS, Lester RJG, Findlav V, Kent ML (2003) First report of three Kudoa species from eastern Australia: Kudoa thyrsites from Mahi mahi (Coryphaena hippurus), Kudoa amamiensis and Kudoa minithyrsites n. sp. from sweeper (Pempheris ypsilychnus). J Eukaryot Microbiol 50:215–219
Wolf K, Markiw ME (1984) Biology contravenes taxonomy in the Myxozoa: new discoveries show alternation of invertebrate and vertebrate hosts. Science 225(4669):1449–1452
Yokoyama H, Fukuda Y (2001) Ceratomyxa seriolae n. sp. and C. buri n. sp.(Myxozoa: Myxosporea) from the gall-bladder of cultured yellowtail Seriola quinqueradiata. Syst Parasitol 48(2):125–130
Zhao Y, Al-Farraj SA, Al-Rasheid KA, Song W (2015) Data on ten new myxosporean parasites (Myxozoa, Myxosporea, Bivalvulida) from the Yellow Sea, China. Acta Protozool 54(4):305–323
Acknowledgements
The authors wish to thank the Director, Central Marine Fisheries Research Institute, Cochin, and the Indian Council of Agricultural Research, New Delhi, for providing necessary facilities for undertaking this work.
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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
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The authors declare no competing interests.
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The present study was supported by the Council of Scientific and Industrial Research, New Delhi, through a Junior Research Fellowship for the first author (No. 09/1135(0017)/2019-EMR-I).
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Surendran, S., Chandran, A., Vijayagopal, P. et al. Morphological and molecular characterization of Ceratomyxa xanthopteri n. sp. (Myxosporea: Ceratomyxidae) from the marine ornamental fish Acanthurus xanthopterus Valenciennes 1835 (Acanthuridae) off Vizhinjam coast, Kerala. Parasitol Res 120, 2445–2453 (2021). https://doi.org/10.1007/s00436-021-07168-x
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DOI: https://doi.org/10.1007/s00436-021-07168-x