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Taxonomy and Systematics of Two New Species of Myxobolus (Cnidaria: Myxobolidae) Parasitizing the Gills of Mugil curema (Mugilidae) from the Brazilian Coast

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Abstract

Purpose

We describe two new species of Myxobolus (Myxobolidae) found parasitizing Mugil curema from two locations in Brazil: Myxobolus curemae n. sp. from gill arch and rays and Myxobolus maceioensis n. sp. from gill lamellae.

Methods

We based the descriptions on myxospore morphology, histology, and small-subunit ribosomal DNA sequences.

Results

Myxospores of the two new species had similar morphology and morphometry but differed in spore body width and length, and ssrDNA sequences differed by 10.5%. These data supported the diagnosis of the parasites as distinct and novel species. The phylogenetic analysis showed a subclade formed by species that parasitize Mugiliformes, with M. maceioensis n. sp. as a sister species of Myxobolus episquamalis and Myxobolus bizerti, while there is a group of six species that are sister related to M. curemae n. sp. Our analysis was consistent with previous studies suggesting that orders of the hosts are strongly correlated with phylogenetic signals in the Myxobolidae.

Conclusions

Myxobolus curemae n. sp. and M. maceioensis n. sp. are new species identified parasitizing M. curema.

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Data Availability

The data used in this study are included in the manuscript.

References

  1. Kent ML, Andree KB, Bartholomew JL et al (2001) Recent advances in our knowledge of the Myxozoa. J Eukaryot Microbiol 48:395–413. https://doi.org/10.1111/j.1550-7408.2001.tb00173.x

    Article  CAS  PubMed  Google Scholar 

  2. Lom J, Dyková I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 53:1–36. https://doi.org/10.14411/fp.2006.001

    Article  Google Scholar 

  3. Fiala I, Bartoŝová P (2010) History of myxozoan character evolution on the basis of rDNA and EF-2 data. BMC Evol Biol 10:5–7. https://doi.org/10.1186/1471-2148-10-228

    Article  CAS  Google Scholar 

  4. Eiras JC, Molnár K, Lu YS (2005) Synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea: Myxobolidae). Syst Parasitol 61:1–46. https://doi.org/10.1007/s11230-004-6343-9

    Article  CAS  PubMed  Google Scholar 

  5. 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. https://doi.org/10.1007/s11230-014-9484-5

    Article  PubMed  Google Scholar 

  6. Eiras JC, Cruz CF, Saraiva A, Adriano EA (2021) Synopsis of the species of Myxobolus (Cnidaria, Myxozoa, Myxosporea) described between 2014 and 2020. Folia Parasitol 68:012. https://doi.org/10.14411/fp.2021.012

    Article  Google Scholar 

  7. Ibañez Aguirre AL (1993) Coexistence of Mugil cephalus and M. curema in a coastal lagoon in the Gulf of Mexico. J Fish Biol 42:959–961. https://doi.org/10.1006/jfbi.1993.1101

    Article  Google Scholar 

  8. Trape S, Durand JD, Vigliola L, Panfili J (2017) Recruitment success and growth variability of mugilids in a West African estuary impacted by climate change. Estuar Coast Shelf Sci 198:53–62. https://doi.org/10.1016/j.ecss.2017.08.037

    Article  Google Scholar 

  9. Mai ACG, dos Santos ML, Lemos VM, Vieira JP (2018) Discrimination of habitat use between two sympatric species of mullets, Mugil curema and Mugil liza (Mugiliformes: Mugilidae) in the rio Tramandaí Estuary, determined by otolith chemistry. Neotrop Ichthyol 16:1–8. https://doi.org/10.1590/1982-0224-20170045

    Article  Google Scholar 

  10. Marin EBJ, Quintero A, Bussière D, Dodson JJ (2003) Reproduction and recruitment of white mullet (Mugil curema) to a tropical lagoon (Margarita Island, Venezuela) as revealed by otolith microstructure. Fish Bull 101:809–821

    Google Scholar 

  11. Heras S, González Castro M, Roldán MI (2006) Mugil curema in Argentinean waters: combined morphological and molecular approach. Aquaculture 261:473–478. https://doi.org/10.1016/j.aquaculture.2006.07.003

    Article  CAS  Google Scholar 

  12. Avigliano E, Ibañez A, Fabré N et al (2020) White mullet Mugil curema population structure from Mexico and Brazil revealed by otolith chemistry. J Fish Biol 97:1187–1200. https://doi.org/10.1111/jfb.14500

    Article  CAS  PubMed  Google Scholar 

  13. Albieri RJ, Araújo FG, Uehara W (2010) Differences in reproductive strategies between two co-occurring mullets Mugil curema Valenciennes 1836 and Mugil liza Valenciennes 1836 (Mugilidae) in a tropical bay. Trop Zool 23:51–62

    Google Scholar 

  14. Lima ARB, Torres RA, Jacobina UP et al (2019) Genomic damage in Mugil curema (Actinopterygii: Mugilidae ) reveals the effects of intense urbanization on estuaries in northeastern Brazil. Mar Pollut Bull 138:63–69. https://doi.org/10.1016/j.marpolbul.2018.07.037

    Article  CAS  PubMed  Google Scholar 

  15. Yurakhno VM, Ovcharenko MO (2014) Study of Myxosporea (Myxozoa), infecting worldwide mullets with description of a new species. Parasitol Res 113:3661–3674. https://doi.org/10.1007/s00436-014-4031-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Ovcharenko M (2015) Microparasites of worldwide mullets. Ann Parasitol 61:229–239. https://doi.org/10.17420/ap6104.12

    Article  PubMed  Google Scholar 

  17. 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. https://doi.org/10.1017/S0031182018001671

    Article  CAS  PubMed  Google Scholar 

  18. Sharon G, Ucko M, Tamir B, Diamant A (2019) Co-existence of Myxobolus spp. (Myxozoa) in gray mullet (Mugil cephalus) juveniles from the Mediterranean Sea. Parasitol Res 118:159–167. https://doi.org/10.1007/s00436-018-6151-9

    Article  PubMed  Google Scholar 

  19. Faye N, Kpatcha TK, Fall M, Toguebaye BS (1997) Heart infections due to myxosporean (Myxozoa) parasites in marine and estuarine fishes from Senegal. Bull Eur Assoc Fish Pathol 17:115–117

    Google Scholar 

  20. Faye N, Kpatcha TK, Debakate C, Fall M, Toguebaye BS (1999) Gill infections due to myxosporean (Myxozoa) parasites in fishes from Senegal with description of Myxobolus hani sp. n. Bull Eur Assoc Fish Pathol 19:14–16

    Google Scholar 

  21. Lom J, Arthur JR (1989) A guideline for the preparation of species descriptions in Myxosporea. J Fish Dis 12:151–156. https://doi.org/10.1111/j.1365-2761.1989.tb00287.x

    Article  Google Scholar 

  22. Kearse M, Moir R, Wilson A et al (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  24. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256. https://doi.org/10.1093/molbev/msn083

    Article  CAS  PubMed  Google Scholar 

  25. Rambaut A (2012) FigTree v1.4. Molecular evolution, phylogenetics and epidemiology. http://tree.bio.ed.ac.uk/. Accessed 19 Dec 2021

  26. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Naldoni J, Maia AAM, Correa LL et al (2018) New myxosporeans parasitizing Phractocephalus hemioliopterus from Brazil: morphology, ultrastructure and SSU-rDNA sequencing. Dis Aquat Organ 128:37–49. https://doi.org/10.3354/dao03210

    Article  CAS  PubMed  Google Scholar 

  28. Vieira DHMD, Rangel LF, Tagliavini VP et al (2020) Morphological and molecular analysis of Henneguya tietensis n. sp. (Cnidaria: Myxosporea), parasitizing the gill filaments of Prochilodus lineatus (Valenciennes, 1837) from Brazil. Parasitol Res 120:27–36. https://doi.org/10.1007/s00436-020-06918-7

    Article  PubMed  Google Scholar 

  29. Vieira DHMD, Rangel LF, Tagliavini VP et al (2020) A new species, Henneguya lacustris n. sp. (Cnidaria: Myxosporea), infecting the gills of Astyanax lacustris from Brazil. Parasitol Res 119:4259–4265. https://doi.org/10.1007/s00436-020-06871-5

    Article  PubMed  Google Scholar 

  30. Molnár K, Cech G, Székely C (2008) Myxobolus species infecting the cartilaginous rays of the gill filaments in cyprinid fishes. Acta Parasitol 53:330–338. https://doi.org/10.2478/s11686-008-0054-3

    Article  CAS  Google Scholar 

  31. Molnár K, Eszterbauer E, Marton S et al (2009) Myxobolus erythrophthalmi sp. n. and Myxobolus shaharomae sp. n. (Myxozoa: Myxobolidae) from the internal organs of rudd, Scardinius erythrophthalmus (L.), and bleak, Alburnus alburnus (L.). J Fish Dis 32:219–231. https://doi.org/10.1111/j.1365-2761.2008.00976.x

    Article  CAS  PubMed  Google Scholar 

  32. Molnár K, Marton S, Székely C, Eszterbauer E (2010) Differentiation of Myxobolus spp. (Myxozoa: Myxobolidae) infecting roach (Rutilus rutilus) in Hungary. Parasitol Res 107:1137–1150. https://doi.org/10.1007/s00436-010-1982-z

    Article  PubMed  Google Scholar 

  33. Liu Y, Whipps CM, Gu ZM et al (2013) Myxobolus musseliusae (Myxozoa: Myxobolidae) from the gills of common carp Cyprinus carpio and revision of Myxobolus dispar recorded in China. Parasitol Res 112:289–296. https://doi.org/10.1007/s00436-012-3136-y

    Article  CAS  PubMed  Google Scholar 

  34. Negrelli DC, Vieira DHMD, Tagliavini VP et al (2019) Molecular and morphological analysis of Henneguya jundiai n. sp. (Cnidaria: Myxosporea), a new parasite of the gills of Rhamdia quelen in Brazil. Acta Trop 197:105053. https://doi.org/10.1016/j.actatropica.2019.105053

    Article  CAS  PubMed  Google Scholar 

  35. Molnár K (2002) Site preference of fish myxosporeans in the gill. Dis Aquat Organ 48:197–207. https://doi.org/10.3354/dao048197

    Article  PubMed  Google Scholar 

  36. Bahri S (2008) Abnormal forms of Myxobolus bizerti and Myxobolus mulleri (Myxosporea: Bivalvulida) spores with caudal appendages. Bull Eur Assoc Fish Pathol 28:252–255

    Google Scholar 

  37. Liu Y, Whipps CM, Gu ZM et al (2010) Myxobolus turpisrotundus (Myxosporea: Bivalvulida) spores with caudal appendages: investigating the validity of the genus Henneguya with morphological and molecular evidence. Parasitol Res 107:699–706. https://doi.org/10.1007/s00436-010-1924-9

    Article  PubMed  Google Scholar 

  38. Liu Y, Lövy A, Gu Z, Fiala I (2019) Phylogeny of Myxobolidae (Myxozoa) and the evolution of myxospore appendages in the Myxobolus clade. Int J Parasitol 49:523–530. https://doi.org/10.1016/j.ijpara.2019.02.009

    Article  PubMed  Google Scholar 

  39. Liu XH, Zhang JY, Batueva MD, Voronin VN (2016) Supplemental description and molecular characterization of Myxobolus miyarii Kudo, 1919 (Myxosporea: Myxobolidae) infecting intestine of Amur catfish (Silurus asotus). Parasitol Res 115:1547–1556. https://doi.org/10.1007/s00436-015-4889-x

    Article  CAS  PubMed  Google Scholar 

  40. Zhang JY, Al-Quraishy S, Abdel-Baki AAS (2014) The morphological and molecular characterization of Myxobolus khaliji n. sp. (Myxozoa: Myxosporea) from the double bar seabream Acanthopagrus bifasciatus (Forsskål, 1775) in the Arabian Gulf. Saudi Arabia Parasitol Res 113:2177–2183. https://doi.org/10.1007/s00436-014-3870-4

    Article  PubMed  Google Scholar 

  41. 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. https://doi.org/10.2307/3284453

    Article  CAS  PubMed  Google Scholar 

  42. 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, Australia. Dis Aquat Organ 46:197–212. https://doi.org/10.3354/dao046197

    Article  CAS  PubMed  Google Scholar 

  43. Kent ML, Khattra J, Hedrick RP, Devlin RH (2000) Tetracapsula renicola n. sp. (Myxozoa: Saccosporidae); the PKX myxozoan—the cause of proliferative kidney disease of salmonid fishes. J Parasitol 86:103–111. https://doi.org/10.2307/3284917

    Article  CAS  PubMed  Google Scholar 

  44. Eszterbauer E (2004) Genetic relationship among gill-infecting Myxobolus species (Myxosporea) of cyprinids: molecular evidence of importance of tissue-specificity. Dis Aquat Organ 58:35–40. https://doi.org/10.3354/dao058035

    Article  PubMed  Google Scholar 

  45. Andree KB, Szekely C, Molnár K et al (1999) Relationships among members of the genus Myxobolus (Myxozoa: Bilvalvidae) based on small subunit ribosomal DNA sequences. J Parasitol 85:68–74. https://doi.org/10.2307/3285702

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) [Grant numbers 2020/05412-9 and 2019/25223-9], Fundação de Amparo à Pesquisa do Estado de Alagoas (FAPEAL) [Grant number 60030.0000000464/2020] and Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq [Grant number 309125/2017-0].

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Authors and Affiliations

  1. Division of Parasitology, Institute of Biosciences, São Paulo State University (Unesp), Botucatu, SP, 18618-689, Brazil

    Diego Henrique Mirandola Dias Vieira, Beatriz Narciso Agostinho, Débora Caroline Negrelli & Reinaldo José da Silva

  2. Análise de Sistemas Ambientais, Centro Universitário CESMAC, Maceió, AL, Brazil

    Rodney Kozlowiski de Azevedo & Vanessa Doro Abdallah

  3. Instituto de Ciências Biológicas E da Saúde, Setor de Parasitologia e Patologia, Universidade Federal de Alagoas, Maceió, AL, 57072-970, Brasil

    Vanessa Doro Abdallah

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  1. Diego Henrique Mirandola Dias Vieira
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  2. Beatriz Narciso Agostinho
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  3. Débora Caroline Negrelli
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  4. Reinaldo José da Silva
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All the authors have contributed equally to the manuscript.

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Correspondence to Diego Henrique Mirandola Dias Vieira.

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During the present research work, all applicable international, national or institutional guidelines for the care and use of animals were followed. All the protocols used have been approved by Animal Ethical Committee.

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Vieira, D.H.M.D., Agostinho, B.N., Negrelli, D.C. et al. Taxonomy and Systematics of Two New Species of Myxobolus (Cnidaria: Myxobolidae) Parasitizing the Gills of Mugil curema (Mugilidae) from the Brazilian Coast. Acta Parasit. 67, 1206–1216 (2022). https://doi.org/10.1007/s11686-022-00569-7

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