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Morphological Redescription and Phylogenetical Position of Ceratomyxa truncata Thelohan (1895) and Coccomyxa morovi Léger and Hesse, 1907 (Myxozoa: Myxosporea) Infecting the Gall Bladder of Sardina pilchardus (Walbaum) from Tunisian Coast

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Abstract

Purpose

Two myxosporean species have been, so far, independently reported from the gallbladder of the European pilchard, Sardina pilchardus (Walbaum) (synonym Clupea pilchardus) in the Northern shore of the Mediterranean Sea; Ceratomyxa truncata Thélohan, and Coccomyxa morovi Léger and Hesse, 1907. The two species were described with incomplete morphological data and based only on line drawings of their mature myxospores.

Methods

During a parasitological survey in the Southern shores of the Mediterranean coast in the gulf of Gabès off Tunisia, two coelozoic myxosporean species were found in the European pilchard and described using morphological and molecular phylogenetic tools. Morphological characterization was based on the mature myxospore study and some vegetative stages. The SSU rDNA sequences were performed for molecular and phylogenetic study.

Results

The most frequently encountered species belongs to the genus Ceratomyxa Thelohan, 1892. The second species belongs to the genus Coccomyxa. Morphological examinations, allowed us to match these two recorded species with Ceratomyxa truncata and Coccomyxa morovi, respectively, as previously described in the same host species referring to the original manuscripts instead of some morphological differences. Molecular analyses based on the partial SSU rDNA sequences did not much with any of the previously reported myxozoan sequences. Phylogenetic analysis positioned C. truncate in a well-supported clade including Ceratomyxa ssp. from Mediterranean Sea, while C. morovi was positioned on the basis of the subclade grouping all Coccomyxidae species.

Conclusion

We provided herein a first morphological redescription of Ceratomyxa truncata and Coccomyxa morovi parasite of Sardina pilchardus from the Southern shores of the Mediterranean Sea and we successfully obtained the SSU rDNA sequences of these two species and positioned them in the phylogenetic tree.

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References

  1. Kent ML, Andree KB, Bartholomew JL, El-Matbouli M, Desser SS, Devlin RH et al (2001) Recent advances in our knowledge of the Myxozoa. J Eukaryot Microbiol 48(4):395–413

    Article  CAS  PubMed  Google Scholar 

  2. Fiala I, Bartošová-Sojková P, Okamura B, Hartikainen H (2015) Adaptive radiation and evolution within the Myxozoa. In: Okamura B, Gruhl A, Bartholomew JL (eds) Myxozoan evolution, ecology and development. Springer International Publishing, Cham, pp 69–84

    Chapter  Google Scholar 

  3. Fiala I, Hlavnickova M, Kodadkova A, Freeman MA, Bartosova-Sojkova P, Atkinson SD (2015) Evolutionary origin of Ceratonova shasta and phylogeny of the marine myxosporean lineage. Mol Phylogenet Evol 86:75–89

    Article  PubMed  Google Scholar 

  4. Canning EU, Okamura B (2004) Biodiversity and evolution of the Myxozoa. Adv Parasitol 56:43–131

    Article  PubMed  Google Scholar 

  5. Holzer AS, Bartosova-Sojkova P, Born-Torrijos A, Lovy A, Hartigan A, Fiala I (2018) The joint evolution of the Myxozoa and their alternate hosts: A cnidarian recipe for success and vast biodiversity. Mol Ecol 27(7):1651–1666. https://doi.org/10.1111/mec.14558

    Article  PubMed  Google Scholar 

  6. Shpirer E, Diamant A, Cartwright P, Huchon D (2018) A genome wide survey reveals multiple nematocyst-specific genes in Myxozoa. BMC Evol Biol 18(1):138–138. https://doi.org/10.1186/s12862-018-1253-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Foox J, Siddall ME (2015) The road to cnidaria: history of phylogeny of the Myxozoa. J Parasitol 101(3):269–274

    Article  PubMed  Google Scholar 

  8. Atkinson SD, Bartholomew JL, Lotan T (2018) Myxozoans: ancient metazoan parasites find a home in phylum Cnidaria. Zoology 129:66–68. https://doi.org/10.1016/j.zool.2018.06.005

    Article  PubMed  Google Scholar 

  9. Evans NM, Holder MT, Barbeitos MS, Okamura B, Cartwright P (2010) The phylogenetic position of Myxozoa: exploring conflicting signals in phylogenomic and ribosomal data sets. Mol Phylogenet Evol 27(12):2733–2746. https://doi.org/10.1093/molbev/msq159

    Article  CAS  Google Scholar 

  10. Okamura B, Hartigan A, Naldoni J (2018) Extensive uncharted biodiversity: the parasite dimension. Integr Comp Biol 58:1132–1145

    PubMed  Google Scholar 

  11. Ji L, Dyková I (1992) Protozoan parasites of fishes. Elsevier, Amsterdam, New York

    Google Scholar 

  12. Lom J, Dykova I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol (Praha) 53(1):1–36

    Article  Google Scholar 

  13. Santojanni A, Cingolani N, Arneri E, Kirkwood G, Belardinelli A, Giannetti G et al (2005) Stock assessment of sardine (Sardina pilchardus, Walb) in the Adriatic Sea with an estimate of discards. Sci Mar 69(4):603–617

    Article  Google Scholar 

  14. Gaamour A, Khemiri S (2010) Evaluation of growth differences in populations of Sardina pilchardus (Walbum, 1792) from two regions along the Tunisian costs. Cah Biol Mar 51:101–108

    Google Scholar 

  15. Thélohan P (1895) Recherches sur les Myxosporidies. Bull Sci Fr Belg 5:100–394

    Google Scholar 

  16. Léger H, Hesse E (1907) Sur une nouvelle Myxosporidie parasite de la sardine. C R Acad Sci Paris 145:85–87 (in Frensh)

    Google Scholar 

  17. Lom J, Arthur J (1989) A guideline for the preparation of species descriptions in Myxosporea. J F Dis 12(2):151–156

    Article  Google Scholar 

  18. Mansour L, Thabet A, Chourabi K, Harrath AH, Gtari M, Al Omar SY et al (2013) Kudoa azevedoi n. sp. (Myxozoa, Multivalvulida) from the oocytes of the Atlantic horse mackerel Trachurus trachurus (Perciformes, Carangidae) in Tunisian coasts. Parasitol Res 112(4):1737–1747. https://doi.org/10.1007/s00436-013-3332-4

    Article  PubMed  Google Scholar 

  19. Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philos Trans R Soc Lond B Biol Sci 360(1462):1847–1857. https://doi.org/10.1098/rstb.2005.1716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948. https://doi.org/10.1093/bioinformatics/btm404

    Article  CAS  PubMed  Google Scholar 

  22. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542

    Article  PubMed Central  PubMed  Google Scholar 

  23. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. 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 (Paris, France) 3(3):223–228

    Article  Google Scholar 

  25. Gaevskaya A, Kovaleva A (1979) New and rarely occurring myxosporidia species from the Celtic Sea fishes. Parazitologiya 13:159–165 (in Russian)

    Google Scholar 

  26. 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 (Praha) 57(1):1–10

    Article  Google Scholar 

  27. Fiala I, Sojková P, Whipps C (2015) Classification and phylogenetics of Myxozoa. In: Gruhl A, Bartholomew JL, Okamura B (eds) Myxozoan evolution, ecology and Development. Springer, Cham, pp 85–110

    Chapter  Google Scholar 

  28. Heiniger H, Adlard RD (2014) Relatedness of novel species of Myxidium Butschli, 1882, Zschokkella Auerbach, 1910 and Ellipsomyxa Koie, 2003 (Myxosporea: Bivalvulida) from the gall bladders of marine fishes (Teleostei) from Australian waters. Sys parasit 87(1):47–72. https://doi.org/10.1007/s11230-013-9454-3

    Article  Google Scholar 

  29. Mansour L, Harrath AH, Abd-Elkader OH, Alwasel S, Abdel-Baki AA, Al Omar SY (2014) Structural and molecular characterization of Kudoa quraishii n. sp. from the trunk muscle of the Indian mackerel Rastrelliger kanagurta (Perciforme, Scombridae) in Saudi Arabia coasts. Parasitol Res 113(4):1361–1370. https://doi.org/10.1007/s00436-014-3775-2

    Article  PubMed  Google Scholar 

  30. Abdel-Baki AAS, Al-Qahtani HA, Almalki E, Al-Quraishy S, Al Ghamdi A, Mansour L (2018) Morphometeric criteria and partial sequence of the 18S rRNA gene of Ceratomyxa sultani n. sp. from the gallbladder of Upeneus margarethae in the Arabian Gulf, with a note on its seasonal prevalence. Saudi J Biol Sci 25(3):597–603. https://doi.org/10.1016/j.sjbs.2017.12.001

    Article  CAS  PubMed  Google Scholar 

  31. Thabet A, Tlig-Zouari S, Al Omar SY, Mansour L (2016) Molecular and morphological characterisation of two species of the genus Ellipsomyxa Køie, 2003 (Ceratomyxidae) from the gall-bladder of Liza saliens (Risso) off Tunisian coasts of the Mediterranean. Sys parasitol 93(6):601–611. https://doi.org/10.1007/s11230-016-9647-7

    Article  Google Scholar 

  32. Mansour L, Azevedo C, Alves Â, Al-Quraishy S, Abdel-Baki A-AS (2017) Ultrastructural aspects and molecular phylogeny of Auerbachia maamouni n. sp. (Myxosporea: Bivalvulida) from the gallbladder of Gnathanodon speciosus Forsskål (Actinopterygii: Carangidae) in the Red Sea. Syst parasitol 94(1):123–131. https://doi.org/10.1007/s11230-016-9684-2

    Article  PubMed  Google Scholar 

  33. Thabet A, Abdel-Baki A-AS, 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. https://doi.org/10.1080/00222933.2019.1597202

    Article  Google Scholar 

  34. Whipps CM, El-Matbouli M, Hedrick RP, Blazer V, Kent ML (2004) Myxobolus cerebralis internal transcribed spacer 1 (ITS-1) sequences support recent spread of the parasite to North America and within Europe. Dise Aquatic Org 60(2):105–108

    Article  CAS  Google Scholar 

  35. Liu Y, Gu Z, Zhang Y, Zeng L (2011) Redescription and molecular analysis of Myxobolus shantungensis Hu, 1965 (Myxozoa: Myxosporea) infecting common carp Cyprinus carpio haematopterus. Parasitol Res 109(6):1619–1623. https://doi.org/10.1007/s00436-011-2450-0

    Article  PubMed  Google Scholar 

  36. Zhao YJ, Li NN, Tang FH, Dong JL (2013) Remarks on the validity of Myxobolus ampullicapsulatus and Myxobolus honghuensis (Myxozoa: Myxosporea) based on SSU rDNA sequences. Parasitol Res 112(11):3817–3823. https://doi.org/10.1007/s00436-013-3569-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Whipps CM, Grossel G, Adlard RD, Yokoyama H, Bryant MS, Munday BL et al (2004) Phylogeny of the multivalvulidae (Myxozoa: Myxosporea) based on comparative ribosomal DNA sequence analysis. J parasitol 90(3):618–622. https://doi.org/10.1645/ge-153r

    Article  CAS  PubMed  Google Scholar 

  38. Griffin MJ, Goodwin AE (2011) Thelohanellus toyamai (Syn. Myxobolus toyamai) infecting the gills of Koi Cyprinus carpio in the Eastern United States. J Parasitol 97(3):493–502. https://doi.org/10.1645/ge-2674.1

    Article  CAS  PubMed  Google Scholar 

  39. Heiniger H, Gunter NL, Adlard RD (2011) Re-establishment of the family Coccomyxidae and description of five novel species of Auerbachia and Coccomyxa (Myxosporea: Bivalvulida) parasites from Australian fishes. Parasitol 138(4):501–515. https://doi.org/10.1017/S0031182010001447

    Article  CAS  Google Scholar 

  40. Chaganti K, Mackenzie K (1999) The genera Ceratomyxa Thelohan, 1892, Leptotheca Thelohan, 1895 and Sphaeromyxa Thelohan, 1892 (Myxosporea: Bivalvulida) in gadid fish of the Northeast Atlantic. Syst Parasitol 43:209–216. https://doi.org/10.1023/A:1006144721096

    Article  Google Scholar 

  41. Laamiri S (2014) New observations on Myxozoa of the goldline sea bream Sarpa salpa L. 1758 (Teleostei: Sparidae) from the Mediterranean coast of Tunisia. Zootaxa 3887(2):157–190. https://doi.org/10.11646/zootaxa.3887.2.3

    Article  PubMed  Google Scholar 

  42. Sojková P, Lövy Kodádková A, Reed C, Lisnerová M, Tomková T, Holzer A et al (2018) Life in a rock pool: radiation and population genetics of myxozoan parasites in hosts inhabiting restricted spaces. PLoS ONE 13:e0194042. https://doi.org/10.1371/journal.pone.0194042

    Article  CAS  Google Scholar 

  43. Lom J, Noble RE (1984) Revised classification of the class Myxosporea Butschli, 1881. Folia Parasitol (Praha) 31(3):193–205

    Google Scholar 

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Acknowledgements

The authors extend their appreciation to the Deanship of Scientific Research at King Saud University for funding this work through research group RG-1435-023.

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Authors and Affiliations

  1. Zoology Department, College of Science, King Saud University, P.O. Box 2455, Riyadh, 11451, Saudi Arabia

    Lamjed Mansour, Jameel Al-Tamimi, Saber Nahdi & Suliman Alomar

  2. Laboratory of Biodiversity and Parasitology of Aquatic Ecosystems (LR18ES05), Department of Biology, Faculty of Science of Tunis, University of Tunis El Manar, University Campus, 2092, Tunis, Tunisia

    Lamjed Mansour & Aouatef Thabet

  3. Zoology Department, Faculty of Science, Beni-Suef University, Beni-Suef, 62521, Egypt

    Abdel-Azeem S. Abdel-Baki

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  1. Lamjed Mansour
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Mansour, L., Thabet, A., Al-Tamimi, J. et al. Morphological Redescription and Phylogenetical Position of Ceratomyxa truncata Thelohan (1895) and Coccomyxa morovi Léger and Hesse, 1907 (Myxozoa: Myxosporea) Infecting the Gall Bladder of Sardina pilchardus (Walbaum) from Tunisian Coast. Acta Parasit. 67, 288–297 (2022). https://doi.org/10.1007/s11686-021-00462-9

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