Abstract
Chloromyxum squali Gleeson and Adlard, 2012 originally described from Squalus acanthias Linnaeus, 1758 is reported for the first time from the gallbladder of Squalus blainville (Risso, 1827) caught from the eastern coast of Tunisia. In the present study, this chloromyxid was described based on morphological and ultrastructural features combined with molecular analysis of 18S rDNA. Young plasmodia were found attached to the gallbladder, while mature plasmodia and myxospores were observed floating free in the bile. Mature plasmodia were polysporic, subspherical in shape, measured 97.8 ± 0.5 µm long and 63.4 ± 0.4 µm wide. Mature myxospores were ovoid with a pointed anterior end, measuring 10.2 ± 0.5 µm long and 8.3 ± 0.5 µm wide. Two asymmetrical shell valves adhered together along an S-shaped suture line. Each valve has 5–7 elevated surface ridges parallel to suture line. A bundle of long caudal filaments extended from the basal end of shell valves. Four pyriform polar capsules equal in size, measuring 3.1 ± 0.4 µm long and 2.5 ± 0.3 µm wide, were situated at the same level in the anterior pole of the myxospore, each with a polar filament coiled in 7–8 turns. Pairwise comparisons among the SSU rDNA sequences revealed significant similarity between Chloromyxum squali infecting S. acanthias with the sequence obtained in this study. Phylogenetic analysis revealed that C. squali clustered in the clade of Chloromyxum species infecting the gallbladder of marine Chondrichthyes. Chloromyxum squali showed a seasonal variation of prevalence with significantly higher prevalence noted in summer and in autumn and absence of infection in winter.
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References
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, Hallett SL, Bartholomew JL (2007) The life cycle of Chloromyxum auratum (Myxozoa) from goldfish, Carassius auratus (L.), involves an antonactinomyxon actinospores. J Fish Dis 30:149–156
Azevedo C, Casal G, García P, Matos P, Teles-Grilo L, Matos E (2009) Ultrastructural and phylogenetic data of Chloromyxum riorajum sp. nov. (Myxozoa), a parasite of the stingray Rioraja agassizii in Southern Brazil. Dis Aquat Organ 85:41–51
Azizi R, Yemmen C, Rangel LF, Santos MJ, Bahri S (2020) Morphology, seasonality and molecular characterizationof Ceratomyxa draconis n. sp. parasite of Trachinus draco (L.) from the Bay of Bizerte. Tunisia Parasitol Res 119:2431–2438. https://doi.org/10.1007/s00436-020-06664-w
Bouderbala K, Yemmen C, Rangel LF, Santos MJ, Bahri S (2020) Ceratomyxa mennani n. sp. (Myxosporea: Bivalvulida) parasitizing the gallbladder of the dusky grouper Epinephelus marginatus (Serranidae) from Tunisian waters. Parasitol Res 119:1515–1522. https://doi.org/10.1007/s00436-020-06649-9
Bradaï MN, Saïdi B, Ghorbel M, Bouaïn A, Guélorget O, Capapé C (2002) Observations sur les requins du golfe de Gabès (Tunisie méridionale, Méditerranée centrale). Mésogée 60:61–77
Cannizzaro L, Rizzo P, Levi D, Gancitano S (1995) Age determination and growth of Squalus blainville (Risso, 1826). Fish Res 23:113–125
Cantatore DMP, Irigoitia MM, Holzer AS, Bartošová-Sojková P, Pecková H, Fiala I, Timi JT (2018) The description of two new species of Chloromyxum from skates in the Argentine Sea reveals that a limited geographic host distribution causes phylogenetic lineage separation of myxozoans in Chondrichthyes. Parasite 25:47
Capapé C (1974) Observations sur la sexualité, la reproduction et la fécondité de 16 Sélaciens pleurotrêmes vivipares aplacentaires des côtes tunisiennes. Archives Institut Pasteur Tunis 51:229–256
Chandran A, Sathianandan ZPU, TV, (2018) Morphological and molecular characterization of Chloromyxum argusi n.sp. (Myxosporea) infecting the urinary bladder of Scatophagus argus Linnaeus 1766 (Scatophagidae) from the south west coast of India. Parasitol Res 117:3145–3156
Compagno LJV, Dando M, Fowler S (2005) A field guide to the sharks of the world. Harper Collins, London
Eiras JC, Lu YS, Gibson DI, Fiala I, Saraiva A, Cruz C, Santos MJ (2012) Synopsis of the species Chloromyxum Mingazinni, 1890 (Myxozoa: Myxosporea: Chloromyxidae). Syst Parasitol 83:203–225
El-Matbouli M, McDowell TS, Antonio DB, Andree KB, Hedrick RP (1999) Effect of water temperature on the development, release and survival of the triactinomyxon stage of Myxobolus cerebralis in its oligochaete host. Int J Parasitol 29:627–641
Fiala I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol 36:1521–1534
Fiala I, Dyková I (2004) The phylogeny of marine and freshwater species of the genus Chloromyxum Mingazzini, 1890 (Myxosporea: Bivalvulida) based on small subunit ribosomal RNA gene sequences. Folia Parasitol (Praha) 51:211–214
Fontes I, Hallett SL, Mo TA (2015) Comparative epidemiology of myxozoan diseases. In: Okamura B, Gruhl A, Bartholomew JL (eds) Myxozoan evolution, ecology and development. Springer, Cham, pp 317–341
Gleeson RJ, Adlard RD (2012) Phylogenetic relationships amongst Chloromyxum Mingazzini, 1890 (Myxozoa: Myxosporea), and the description of six novel species from Australian elasmobranchs. Parasitol Int 61:267–274
Hallett SL, Diamant A (2001) Ultrastructure and small-subunit ribosomal DNA sequence of Henneguya lesteri n. sp. (Myxosporea), a parasite of sand whiting Sillago analis (Sillaginidae) from the coast of Queensland. Aust Dis Aquat Org 46:197–212
Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411–453
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 34:1099–1111
Holzer AS, Sommerville C, Wootten R (2006) Molecular identity, phylogeny and life cycle of Chloromyxum schurovi Shulman and Ieshko, 2003. Parasitol Res 99:90–96
Jirků M, Bartošová P, Kodádková A, Mutschmann F (2011) Another chloromyxid lineage: molecular phylogeny and redescription of Chloromyxum careni from the Asian horned frog Megophrysnasuta. J Euk Microbiol 58:50–59
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lisnerová M, Fiala I, Cantatore D, Irigoitia M, Timi J, Pecková H, Bartošová-Sojková P, Sandoval CM, Luer C, Morris J, Holzer AS (2020) Mechanisms and drivers for the establishment of life cycle complexity in myxozoan parasites. Biology 9(1):10. https://doi.org/10.3390/biology9010010
Liyanage YS, Yokoyama H, Wakabayashi H (2003) Evaluation of vectorcontrol strategy of haemorrhagic thelohanellosis in carp, caused by Thelohanellus hovorkai (Myxozoa). Dis Aquat Org 55(1):31–35
Liu XH, Voronin VN, Dudin AS, Morozova DA, Zhang JY (2017) Morphological and molecular characterization of a new cyprinid gallbladder-infecting Chloromyxum species, Chloromyxum peleci sp. n. (Myxozoa: Chloromyxidae), from Pelecus cultratus (L.) in Russia. Parasitol Res 116:2239–2248
Lom J, Arthur JR (1989) A guideline for preparation of species descriptions in Myxosporea. J Fish Dis 12(151):156
Lom J, Dyková I (1993) Scanning electron microscopic revision of common species of the genus Chloromyxum (Myxozoa: Myxosporea) infecting European freshwater fishes. Folia Parasitol 40:161–174
Lom J, Dyková I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 43:1–36
Marouani S, Chaâba R, Kadiri H, Saidi B, Bouain A, Maltaglati F, Last P, Séret B, Bradai MN (2012a) Taxonomie research on Squalus megalops (Macleay,1881) and Squalus blainvillei (Risso, 1827) (Chondrichthyes: Squalidae) in Tunisien waters (central Mediterranean Sea). Sci Mar 76(1):97–109
Marouani S, Kadri H, Saidi B, Morize E, Bouain A, Bradai MN (2012b) Age, growth, longevity, natural mortality and maturity of the longnose spurdog, Squalus blainvillei (Chondrichthyes: Squalidae), in the Gulf of Gabès (Central Mediterranean Sea). Cah Biol Mar 53:197–204
Quignard JP (1971) Recherches sur la biologie de Squalus blainvillei (Risso, 1826). Trav Lab Biol Halieut Univ Rennes 5:125–141
Reynolds ES (1963) The use of lead citrate at high pH as an electron opaque staining electron microscopy. J Cell Biol 17:208–212
Rocha S, Azevedo C (2012) Light and electron microscopy applied to the characterization of marine species belonging to the genus Chloromyxum, as a study model for myxosporean parasites. In: Méndez-Vilas A (eds) Current microscopy contributions to advances in science and technology. Formatex Research Center, Badajoz, pp 471–477
Rocha S, Casal G, Al-Quraishy S, Azevedo C (2013) Morphological and molecular characterization of a new myxozoan species (Myxosporea) infecting the gall bladder of Raja clavata (Chondrichthyes), from the Portuguese Atlantic Coast. Parasitol Res 99:307–317
Rocha S, Casal G, Al-Quraishy S, Azevedo C (2014) Morphological and ultrastructural redescription of Chloromyxum leydigi Mingazzini, 1890 (Myxozoa: Myxosporea), type species of the genus, infecting the gall bladder of the marine cartilaginous fish Torpedo marmorata Risso (Chondrichthyes: Torpedinidae), from the Portuguese Atlantic coast. Folia Parasitol (Praha) 61:1–10
Sanders JL, Jaramillo AG, Ashford JE, Feist SW, Lafferty KD, Kent ML (2015) Two myxozoans from the urinary tract of topsmelt. Atherinopsaffinis. J Parasitol 101(5):577–586
Serena F. (2005) Field identification guide to the sharks and rays of the Mediterranean and Black Sea. Food and Agriculture Organization of the United Nations (FAO) species identification guide for fishery purposes. FAO, Rome
Sion L, D’Onghia G, Tursi A, Mytilineou C (2003) First data on distribution and biology of Squalus blainvillei (Risso, 1826) from the eastern Mediterranean Sea. JNAFS 31:213–219
Whipps CM, Adlard RD, Bryant MS, Lester RGJ, 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(3):215–219
Yemmen C, Marton S, Bahri S, Eszterbauer E (2013) Morphology, seasonality and phylogeny of Zschokkella soleae sp. n. (Myxozoa, Myxosporea) parasite of Solea solea (L.) (Pleuronectiformes, Soleidae) from Ghar El Melh Lagoon. Tunisia J Fish Dis 36:871–879
Zhang JY, Zhao YL, Batueva MD, Luo D, Xing ZE, Zhang QQ, Lui XH (2017) Redescription of Chloromyxum ellipticum Li & Nie, 1973 (Myxosporea:Chloromyxidae) infecting the gall bladder of grasscarp Ctenopharyngodon idellus Valenciennes, 1844, supplemented by morphological and molecular characteristics. Parasitol Res 116:1479–1486
Acknowledgements
This work is a part of the PhD thesis of Houssem Eddine Snene supported by the University of Tunis El Manar and was supported by national funds through FCT—Foundation for Science and Technology within the scope of UIDB/04423/2020 and UIDP/04423/2020 to CIIMAR (Interdisciplinary Centre of Marine and Environmental Research) and FCT employment contract CEECIND/03501/2017.
All authors would like to thank Professor Jerri Bartholomew from Oregon State University for her help in English proofreading.
All applicable international, national and/or institutional guidelines for the care and use of animals were followed.
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Snene, H.E., Rangel, L.F., Quilichini, Y. et al. First description of Chloromyxum squali Gleeson and Adlard, 2012 (Myxozoa) in the Mediterranean Sea in a new host Squalus blainville (Chondrichthyes: Squalidae): morphological, ultrastructural and phylogenetic data. Parasitol Res 120, 2479–2491 (2021). https://doi.org/10.1007/s00436-021-07202-y
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DOI: https://doi.org/10.1007/s00436-021-07202-y