Skip to main content
SpringerLink
Log in

Sphaeromyxa azevedoi n. sp. (Myxozoa: Sphaeromyxidae) infecting the gall bladder of Gobioides grahamae (Perciformes: Gobiidae) in the Amazon region

  • Fish Parasitology - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Sphaeromyxa azevedoi n. sp. is described from the gall bladder of the goby Gobioides grahamae (Gobiidae) captured on the Paracauari River in Salvaterra, on Marajó Island, northern Brazil. A total of 50 G. grahamae specimens were analysed, and 15 (30%) were parasitised by the plasmodia and myxospore of Sphaeromyxa azevedoi n. sp. Large plasmodia were observed floating in the bile. These plasmodia were flat, rounded, oval or elongated, and of varying sizes. The mature myxospores, found singly or in pairs, were 27.1 ± 2.7 (20.5–30.1) μm Length and 3.8 ± 0.2 (3.5–4.4) μm Width in the valvular view. The myxospore has two polar capsules of equal size, 8.1 ± 0.6 (7.4–9.4) μm in length and 2.9 ± 0.2 (2.3–3.3) μm in width. A polar tubule was observed in each capsule, arranged perpendicularly to the principal axis, with three or four coils. The histological analysis showed that the plasmodia and myxospore are located in the lumen of the gall bladder, arranged in pairs, and the epithelium of the gall bladder presented multifocal necrosis. The SSU rDNA of Sphaeromyxa azevedoi n. sp. clusters in the ‘balbianii’ group of the Sphaeromyxa clade. The morphological characteristics and molecular phylogeny of Sphaeromyxa azevedoi n. sp. support its classification as a new species of the genus Sphaeromyxa, which represents an important advancement in the understanding of the diversity of the myxozoan parasite fauna of Brazilian fishes, especially considering that the new species may be detrimental to the host, a commercially important Brazilian fish species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Azevedo C, Rocha S, Matos E, Oliveira E, Matos P, Al-Quraishy S, Casal G (2016) Ultrastructural and phylogenetic description of Kudoa orbicularis n. sp. (Myxosporea: Multivalvulida): a parasite infecting the muscle of the fish Chaetobranchopsis orbicularis (Teleostei: Cichlidae) in the Amazon region. J Eukaryot. Microbiol. 63(1), 27–36. https://doi.org/10.1111/jeu.12244

  • Azevedo C, Videira M, Casal G, Matos P, Oliveira E, Al-quraishy S, Matos E (2013) Fine structure of the plasmodia and myxospore of Ellipsomyxa gobioides n. sp. (Myxozoa) found in the gallbladder of Gobioides broussonnetii (Teleostei: Gobiidae) from the lower Amazon River. J Eukaryot Microbiol 60(5): 490–496. https://doi.org/10.1111/jeu.12056

  • Barthem RB (1990) Descrição da pesca da piramutaba (Brachyplatystoma vaillantii. Pimelodidae) no estuário e na calha do rio Amazonas. Bol Mus Para Emlio Goeldi sér.Antropol 6(1):117–13

  • Bartošová-Sojková P, Kodádková A, Pecková H, Kuchta R, Reed CC (2015) Morphology and phylogeny of two new species of Sphaeromyxa Thélohan, 1892 (Cnidaria: Myxozoa) from marine fish (Clinidae and Trachichthyidae). Parasitology 142(5):660–674. https://doi.org/10.1017/S0031182014001723

    Article  PubMed  Google Scholar 

  • Brassard P, Rau ME, Curtis MA (1982) Parasite-induced susceptibility to predation in diplostomiasis. Parasitology 85:495–501. https://doi.org/10.1017/S0031182000056274

    Article  Google Scholar 

  • Chen W, Yang C, Whipps CM, Peng Z, Zhao Y (2020) Taxonomy on three novel species of Sphaeromyxa Thélohan 1892 (Myxozoa, Bivalvulida, Sphaeromyxidae) with insight into the evolution of the genus. Parasitol Res 119(5):1493–1503. https://doi.org/10.1007/s00436-020-06656-w

    Article  PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772. https://doi.org/10.1038/nmeth.2109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diamant A, Whipps CM, Kent ML (2004) A new species of Sphaeromyxa (Myxosporea: Sphaeromyxina: Sphaeromyxidae) in devil firefish, Pterois miles (Scorpaenidae), from the northern red sea: morphology, ultrastructure, and phylogeny. J Parasitol 90(6):1434–1442. https://doi.org/10.1645/GE-336R

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66(4):411–453

    Article  CAS  Google Scholar 

  • Kalavati C, Vaidehi J (1991) Two new species of myxosporidians from fishes of Chilika Lake: genus Sphaeromyxa Thelohan and genus Zschokkella Auerbach. Uttar Pradesh Journal of Zoology 11(2):146–150

    Google Scholar 

  • Karlsbakk E, Einen AC, Bartosová P (2013) Sphaeromyxa artedielli sp. n. (Myxozoa: Sphaeromyxidae) a parasite of sculpins (Cottidae) in northern Norway. Folia Parasitol 60(5):425–432. https://doi.org/10.14411/fp.2013.045

  • Kristmundsson A, Freeman MA (2013) Sphaeromyxids form part of a diverse group of myxosporeans infecting the hepatic biliary systems of a wide range of host organisms. Parasit Vectors 6:51. https://doi.org/10.1186/1756-3305-6-51

    Article  PubMed  PubMed Central  Google Scholar 

  • Laird M (1953) The protozoa of New Zealand intertidal zone fishes. Transactions of the Royal Society of New Zealand 81:79–143

    Google Scholar 

  • Lom J, Arthur JR (1989) A guideline for the preparation of species descriptions in Myxosporea. J Fish Dis 12(2):151–156. https://doi.org/10.1111/j.1365-2761.1989.tb00287.x

    Article  Google Scholar 

  • Lom J (1969) Notes on the ultrastructure and sporoblast development in fish parasitizing myxosporidian of the genus Sphaeromyxa. Z Zellforsch 97(3):416–437. https://doi.org/10.1007/BF00968848

    Article  CAS  PubMed  Google Scholar 

  • Lom J (2004) Morphology and ultrastructure of Sphaeromyxa noblei sp. n. (Myxozoa), parasite of Heteroclinus whiteleggii (Pisces) from Australian New South Wales coast. Folia Parasitologica 51: 19–26. https://doi.org/10.14411/fp.2004.003

  • Lom J, Dyková I (1992) Protozoan parasites of fishes. Elsevier, Amsterdam, p 315

    Google Scholar 

  • Luna LG (1968) Manual of histologic staining methods of the armed forces institute of pathology. McGraw-Hill, New York

    Google Scholar 

  • Mathews PD, Silva MR, Maia AA, Adriano EA (2015) Ultrastructure and ssrRNA sequencing of Myxidium amazonense n. sp. a myxosporean parasite of Corydoras melini from the Rio Negro river, Amazonas state, Brazil. Parasitol Res 114 (12): 4675–4683. https://doi.org/10.1007/s00436-015-4715-5

  • Matos PS, Silva DT, Hamoy I, Matos E (2018) Morphological features and molecular phylogeny of Hoferellus azevedoi n. sp. (Myxozoa: Myxobilatidae) found in Chaetobranchus flavescens Heckel, 1840 (Teleostei: Cichlidae) from Marajó Island, northern Brazil. Parasitol Res 117(4): 1087-1093. https://doi.org/10.1007/s00436-018-5785-y

  • Mendes FLS, Barthem RB (2010) Hábitos alimentares de bagres marinhos (Siluriformes: Ariidae) do estuário amazônico. Amazônia: Ci & Desenv 5 (10).

  • Miller TL, Barnett SK, Seymour JE, Jenkins TP, Mcnamara M, Adlard RD (2018) Biliary tract-infecting myxosporeans from estuarine and reef stonefish (Scorpaeniformes: Synanceiidae) off eastern Australia, with descriptions of Sphaeromyxa horrida n. sp. and Myxidium lapipiscis n. sp. (Myxosporea: Bivalvulida). J Parasitol 104(3): 254–261. https://doi.org/10.1645/17-79

  • Miller KM, Teffer A, Tucker S, Li S, Schulze AD, Trudel M, Juanes F, Tabata A, Kaukinen KH, Ginther NG, Ming TJ, Cooke SJ, Hipfner JM, Patterson DA, Hinch SG (2014) Infectious disease, shifting climates, and opportunistic predators: cumulative factors potentially impacting wild salmon declines. Evol Appl 7:812–855. https://doi.org/10.1111/eva.12164

    Article  PubMed  PubMed Central  Google Scholar 

  • Molnár K, Eszterbauer E, Szckely C, Dán A, Harrach B (2002) Morphological and molecular biological studies on intramuscular Myxobolus spp. of cyprinid fish. J Fish Dis 25:643–652. https://doi.org/10.1046/j.1365-2761.2002.00409.x

    Article  Google Scholar 

  • Moser M, Noble ER (1977) Three genera of myxosporida (Protozoa) in macrourid fishes. Int J Parasitol 7(2):93–96. https://doi.org/10.1016/0020-7519(77)90072-8

    Article  CAS  PubMed  Google Scholar 

  • Murdy EO (1998) A review of the genus Gobioides. Ichthyol Res 45(2):121–133. https://doi.org/10.1007/BF02678554

    Article  Google Scholar 

  • Naidenova NN (1970) Parasitofauna of fishes from family Gobiidae from the Azov Sea. Biologiya Morya 20:84–113 ((In Russian))

    Google Scholar 

  • Nekouei O, Vanderstichel R, Ming T, Kaukinen KH, Thakur K, Tabata A, Laurin E, Tucker S, Beacham TD, Miller KM (2018) Detection and assessment of the distribution of infectious agents in juvenile Fraser River Sockeye Salmon, Canada, in 2012 and 2013. Frontiers in Microbiology 9:3221. https://doi.org/10.3389/fmicb.2018.03221

  • Pinto C (1928) Myxosporideos e outros protozoários intestinais de peixes observados na América do Sul. Arch Inst Biol 1:102–136

    Google Scholar 

  • Rambaut A (2012) FigTree v1.4.0. University of Oxford, Oxford, UK. http://tree.bio.ed.ac.uk/software/figtree.

  • Rambaut A, Drummond AJ (2007) Trace v1.4, available from http://beast.bio.ed.ac.uk/Tracer

  • 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 63(3): 539–42. https://doi.org/10.1093/sysbio/sys029

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574. https://doi.org/10.1093/bioinformatics/btg180

    Article  CAS  PubMed  Google Scholar 

  • Sears BF, Anderson P, Greiner EC (2011) A new species of myxosporean (Sphaeromyxidae), a parasite of lined seahorses, Hippocampus erectus, from the Gulf of Mexico. J Parasitol 97(4):713–716. https://doi.org/10.1645/GE-2565.1

    Article  CAS  PubMed  Google Scholar 

  • Tripathi YR (1953) Studies on parasites of Indian fishes. I. Protozoa Myxosporidia together with a check list of parasitic protozoa described from Indian fishes. Records of the Indian Museum 50:63–88

    Google Scholar 

  • Swofford DL PAUP* (2003) Phylogenetic analysis using parsimony (*and other methods). v. 4.0 beta 10. Sinauer associates, Sunderland.

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL–X window interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25(24):4876–4882. https://doi.org/10.1093/nar/25.24.4876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Velasco M, Matos P, Sanches O, São Clemente SC, Videira M, Santos P, Matos E (2012) Necrotizing myositis associated with parasitism by Myxobolus sp. (Myxozoa) in the palate of the violet goby, Gobioides broussonnetii (Gobiidae), from Marajó Island. Brazil Aquaculture 358–359:129–131. https://doi.org/10.1016/j.aquaculture.2012.06.033

    Article  Google Scholar 

  • Videira M, Velasco M, Matos P, São Clemente SC, Sanches O, Matos E (2014) Hepatic steatosis associated with microsporidiosis in teleost fishes from Marajó Island. Brazil an Acad Bras Ciênc 86(3):1347–1350. https://doi.org/10.1590/0001-3765201420130147

    Article  PubMed  Google Scholar 

  • Videira M, Velasco M, Sanches O, Matos P , Santos PS, Matos E (2020) First report of Kudoa sp. in the palate and pharyngeal musculature of Gobioides grahamae Palmer and Wheeler, 1955 (Perciformes, Gobiidae) from Marajó Island, Brazil. Arq. Bras Med Vet. Zootec 72(2):517–522. https://doi.org/10.1590/1678-4162-11081

  • Violante-González J, García-Varela M, Rojas-Herrera A, Guerrero SG (2009) Diplostomiasis in cultured and wild tilapia Oreochromis niloticus in Guerrero State, Mexico. Parasitol Res 105:803–807. https://doi.org/10.1007/s00436-009-1458-1

    Article  PubMed  Google Scholar 

  • Zatti SA, Atkinson SD, Bartholomew JL, Maia AAM, Adriano EA (2017) Amazonian waters harbour an ancient freshwater Ceratomyxa lineage (Cnidaria: Myxosporea). Acta Trop 169:100–106. https://doi.org/10.1016/j.actatropica.2017.02.006

    Article  PubMed  Google Scholar 

  • Whipps CM, Adlard RD, Bryant MS, Lester RJG, Findlay 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. https://doi.org/10.1111/j.1550-7408.2003.tb00120.x

  • Whipps CM, Font WF (2013) Interaction of two myxozoan parasites from naked goby Gobiosoma bosc, in Lake Pontchartrain, Louisiana. J Parasitol 99(3): 441–447.https://doi.org/10.1645/12-49.1

  • Whipps CM (2015 Oct) Zhao Y (2015) Synopsis of the species of the genus Sphaeromyxa Thélohan, 1892 (Myxosporea: Bivalvulida: Variisporina: Sphaeromyxidae). Syst Parasitol 92(2):81–99. https://doi.org/10.1007/s11230-015-9591-y

    Article  PubMed  Google Scholar 

Download references

Funding

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001.

Author information

Authors and Affiliations

  1. Federal University of Pará (UFPa), Belém, Brazil

    Kelly Cristine Vilela Carreira & Diehgo Tuloza da Silva

  2. Universidade Santo Amaro - UNISA, São Paulo, Brazil

    Osimar de Carvalho Sanches

  3. Carlos Azevedo Research Laboratory, Federal Rural University of the Amazon (UFRA), Avenida Presidente Tancredo Neves, 2501, Montese, Belém, Pará, 66077-901, Brazil

    Edilson R. Matos

  4. Laboratory of Applied Genetics, Federal Rural University of Amazonia (UFRA), Belém, Pará, Brazil

    Igor Hamoy

Authors
  1. Kelly Cristine Vilela Carreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Diehgo Tuloza da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Osimar de Carvalho Sanches
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Edilson R. Matos
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Igor Hamoy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Edilson R. Matos.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Section Editor: Sascha L Hallett

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Carreira, K.C.V., da Silva, D.T., de Carvalho Sanches, O. et al. Sphaeromyxa azevedoi n. sp. (Myxozoa: Sphaeromyxidae) infecting the gall bladder of Gobioides grahamae (Perciformes: Gobiidae) in the Amazon region. Parasitol Res 121, 867–875 (2022). https://doi.org/10.1007/s00436-022-07443-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-022-07443-5

Keywords

Search

Navigation