First molecular data on the validity of Myxobolus ichkeulensis (Cnidaria: Myxosporea) from Mugil cephalus (Mugilidae) in Turkish waters

Abstract

To date, there is no report on molecular characterisation of Myxobolus ichkeulensis in Mugil cephalus (Mugilidae) in Turkish marine waters. The aim of the current research was to provide the first molecular data on M. ichkeulensis from M. cephalus in Turkish Black Sea coasts. A total of 40 M. cephalus specimens were examined for the presence of M. ichkeulensis in the Turkish Black Sea coasts during January 2017 and April 2017. In the present study, M. ichkeulensis was identified based upon the myxospore morphology, host and tissue specificity, and SSU rRNA sequence. Phylogenetic analysis using neighbor-joining also revealed that our isolate (#GZP-2018-Samsun1) was clustered with other Myxobolus species that infect M. cephalus. The current study includes the morphological and histopathological descriptions and first molecular data on M. ichkeulensis in M. cephalus in Turkish marine waters. M. ichkeulensis was also reported from the M. cephalus in the coast of the Black Sea in Turkey for the first time. Moreover, our current genetic data was recorded as the new valid SSU rRNA sequence (MH374629) for M. ichkeulensis in the GenBank database.

Keywords

• Histopathology,Morphology,Myxobolus ichkeulensis,SSU rRNA,Turkey

References

1. 1. Altschul S, Madden T, Schaffer A, et al (1997): Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res, 258, 3389-3402.
2. 2. Altunel FN (1983): Parasitism on mullets (Mugil spp.). J Fac Sci Ege Univ B, 1, 364-378.
3. 3. Bahri S, Andree KB, Hedrick RP (2003): Morphological and phylogenetic studies of marine Myxobolus spp. from mullet in Ichkeul Lake, Tunisia. J Eukaryot Microbiol, 50, 463-470.
4. 4. Bahri S, Marques A (1996): Myxosporean parasites of the genus Myxobolus from Mugil cephalus in Ichkeul lagoon, Tunisia: description of two new species. Dis Aquat Organ, 27, 115-122.
5. 5. Barta JR, Martin DS, Liberator PA, et al (1997): Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. J Parasitol, 83, 262-271.
6. 6. Demirkale I, Cengizler I (2016): Identification of the infested gray mullets (Mugil cephalus L. 1758) by Myxobolus ichkeulensis level in the coast of Adana. TURJAF, 4, 805-812.
7. 7. Eiras JC, Molnár K, Lu YS (2005): Synopsis of the genus Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea: Myxobolidae). Syst Parasitol, 61, 1-46.
8. 8. Eiras JC, Zhang J, Molnár K (2014). Synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea, Myxobolidae) described between 2005 and 2013. Syst Parasitol, 88, 11-36.

9. 9. Fall M, Kpatcha KP, Diebakate C, et al (1997): Observations sur des Myxosporidies (Myxozoa) du genre Myxobolus parasites de Mugil cephalus (Poisson, Téléostéen) du Sénégal. Parasite, 2, 173-180.
10. 10. Felsenstein J (1985): Confidence intervals on phylogenies: an approach using the bootstrap. Evolution, 39, 783-791.
11. 11. Fiala I, Bartošová–Sojková P, Okamura B, et al (2015): Adaptive Radiation and Evolution within the Myxozoa. 69-84. In: B Okamura, Gruhl A, Bartholomew JL (Eds), Myxozoan Evolution, Ecology and Development. Springer International Publishing, Switzerland.
12. 12. Fiala I (2006): The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol, 36, 1521-1534.
13. 13. Hillis DM, Bull JJ (1993): An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol, 42, 182-192.
14. 14. Kent ML, Andree KB, Bartholomew JL, et al (2001): Recent advances in our knowledge of the Myxozoa. J Eukaryotic Microbiol, 48, 395-413.
15. 15. Kim WS, Kim JH, Oh MJ (2013): Morphologic and genetic evidence for mixed infection with two Myxobolus species (Myxozoa: Myxobolidae) in gray mullets, Mugil cephalus, from Korean waters. Korean J Parasitol, 51, 369-373.
16. 16. Kumar S, Stecher G, Tamura K (2016): MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol, 33, 1870-1874.
17. 17. Lom J, Arthur JR (1989): A guideline for the preparation of species description in Myxosporea. J Fish Dis, 12, 151-156.
18. 18. Lom J, Dyková I (1992): Protozoan Parasites of Fishes. Elsevier, Amsterdam.
19. 19. Lom J, Dyková I (2006): Myxozoan genera: definition and note on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol, 53, 1-36.
20. 20. Molnár K, Eszterbauer E (2015): Specificity of Infection Sites in Vertebrate Hosts. 295-313. In: B Okamura, Gruhl A, Bartholomew JL (Eds), Myxozoan Evolution, Ecology and Development. Springer International Publishing, Switzerland.
21. 21. Molnár K (2002): Site preference of myxosporeans in the gill. Dis Aquat Organ, 48, 197-207.
22. 22. Ovcharenko M (2015): Microparasites of worldwide mullets. Ann Parasitol, 61, 229-239.
23. 23. Ozak AA, Demirkale I, Cengizler I (2012): Two new records of Myxobolus Bütschli, 1882 (Myxozoa, Myxosporea, Myxobolidae) species from Turkey. Turk J Zool, 36, 191-199.
24. 24. Pedro-Andrĕs MB, Marques A, Gracia-Royo MP (2011): Myxosporean infection of grey mullet in the Ebro Delta: identification and ultrastructure of Myxobolus ichkeulensis Bahri & Marques, 1996 infecting the gills of Mugil cephalus L. Acta Protozool, 50, 67-71.
25. 25. Pekmezci GZ, Yardimci B, Yilmaz S, et al (2014): Myxobolus anatolicus sp. nov. (Myxozoa) infecting the gill of Anatolian khramulya Capoeta tinca (Cyprinidae) in Turkey. Dis Aquat Organ, 109, 213-222.
26. 26. Pekmezci GZ, Yardimci B, Yilmaz S (2015): Supplementary studies and the first molecular data on Myxobolus scardinii Reuss, 1906 (Myxozoa: Myxosporea) infecting the gill filaments of rudd, Scardinius erythrophthalmus (L.). Parasitol Res, 114, 3619-3625.
27. 27. Rocha S, Azevedo C, Oliveira E, et al (2019): Phylogeny and comprehensive revision of mugiliform-infecting myxobolids (Myxozoa, Myxobolidae), with the morphological and molecular redescription of the cryptic species Myxobolus exiguus. Parasitology, 146, 479-496.
28. 28. Sharon G, Ucko M, Tamir B, et al (2019): Co-existence of Myxobolus spp. (Myxozoa) in gray mullet (Mugil cephalus) juveniles from the Mediterranean Sea. Parasitol Res, 118, 159-167.
29. 29. Thompson JD, Higgins DG, Gibson TJ (1994): CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res, 2, 4673-4680.
30. 30. Umur S, Pekmezci GZ, Beyhan YE, et al (2010): First record of Myxobolus muelleri (Myxosporea: Myxobolidae) in flathead grey mullet Mugil cephalus (Teleostei, Mugilidae) from Turkey. Ankara Univ Vet Fak Derg, 57, 205-207.
31. 31. Yurakhno VM, Ovcharenko MO (2014): Study of Myxosporea (Myxozoa), infecting worldwide mullets with description of a new species. Parasitol Res, 113, 3661-3674.