Abstract
The genus Myxobolus Bütschli, 1882 is the largest group within the class Myxosporea and includes 905 nominal species, 18 of which have been found to infect fish belonging to the family Salmonidae. In the present study, microscopic analysis enabled detection of myxospores in 43 of 613 (7.0%) gastrointestinal tracts from brown trout (Salmo trutta) captured in several rivers in the northwest of the Iberian Peninsula. Measurement of the whole myxospores, polar capsules and other morphological characteristics, together with identification of the site of infection, has led us to propose a novel salmonid-myxobolid species, Myxobolus compostellanus n. sp. Molecular analysis of the small subunit ribosomal RNA (SSU-rRNA) gene yielded the same consensus sequence of 2039 bp in 14 fish specimens. A BLAST search indicated 97.6% similarity to Myxobolus neurobius. Phylogenetic analysis revealed that M. compostellanus n. sp. is clustered with other salmonid-infecting myxobolids. The present findings contribute to the existing knowledge about the genus Myxobolus, providing both morphological and molecular data on a novel species of Myxobolus found to infect the gastrointestinal tract of salmonids, M. compostellanus n. sp. in the brown trout (S. trutta).
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Akhmerov AK (1960) Myxosporidia of fishes of the Amur River Basin. Rybn Khozyaistvo Vnutrikh Vodemov Latv SSR 5:239–308 (In Russian)
Almodóvar A, Nicola GG (2004) Angling impact on conservation of Spanish stream-dwelling brown trout Salmo trutta. Fish Manag Ecol 11:173–182. https://doi.org/10.1111/j.1365-2400.2004.00402.x
Arsan EL, Atkinson SD, Hallett SL, Meyers T, Bartholomew JL (2007) Expanded geographical distribution of Myxobolus cerebralis: first detections from Alaska. J Fish Dis 30:483–491. https://doi.org/10.1111/j.1365-2761.2007.00834.x
Atkinson SD, Bartošová-Sojková P, Whipps CM, Bartholomew JL (2015) Approaches for characterising myxozoan species. In: Okamura B, Gruhl A, Bartholomew JL (eds) Myxozoan evolution, ecology and development. Springer International Publishing, Cham, pp 111–123
Canning EU, Okamura B (2004) Biodiversity and evolution of the Myxozoa. Adv Parasitol 56:43–131. https://doi.org/10.1016/s0065-308x(03)56002-x
Carriero MM, Adriano EA, Silva MRM, Ceccarelli PS, Maia AAM (2013) Molecular phylogeny of the Myxobolus and Henneguya genera with several new South American species. PLoS ONE 8:e73713. https://doi.org/10.1371/journal.pone.0073713
Chang ES, Neuhof M, Rubinstein ND, Diamant A, Philippe H, Huchon D, Cartwright P (2015) Genomic insights into the evolutionary origin of Myxozoa within Cnidaria. Proc Natl Acad Sci U S A 112:14912–14917. https://doi.org/10.1073/pnas.1511468112
Cobo F, Vieira R, Barca S, Sánchez J, Silva S, Nachón D, Gómez P, Morquecho C, Lago L, Couto MT, Servia MJ, Cobo MC (2015) La trucha en la pesca con mosca. Sekotia S. L., Madrid
Couso-Pérez S, Ares-Mazás E, Gómez-Couso H (2019) First report of Cryptosporidium molnari-like genotype and Cryptosporidium parvum zoonotic subtypes (IIaA15G2R1 and IIaA18G3R1) in brown trout (Salmo trutta). J Parasitol 105:170–179. https://doi.org/10.1645/18-83
Doadrio I (2002) Atlas y libro rojo de los peces continentales de España, 2nd edn. Ministerio de Medio Ambiente, Madrid
Donec ZS, Vartanyan LK, Mkrtchyan ZA (1973) A new species of myxosporidia (Myxosporidia: Cnidosporidia) from the muscles of the trout. Biol Zhurnal Armen 26:84–87
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
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
Ferguson JA, Atkinson SD, Whipps CM, Kent ML (2008) Molecular and morphological analysis of Myxobolus spp. of salmonid fishes with the description of a new Myxobolus species. J Parasitol 94:1322–1334. https://doi.org/10.1645/ge-1606.1
Fiala I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol 36:1521–1534. https://doi.org/10.1016/j.ijpara.2006.06.016
González-Lanza C, Álvarez-Pellitero P (1984) Myxobolus farionis n. sp. and M. ibericus n. sp. of Salmo trutta f. fario from the Duero basin (NW Spain). Description and population dynamics. Angew Parasitol 25:181–189
Gurley MD (1893) On the classification of the Myxosporidia, a group of protozoa parasites infecting fishes. Bull U S Fish Comm 11:407–420
Hallett S, 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
Hillis D, Dixon M (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411–453. https://doi.org/10.1086/417338
Hogge CI, Campbell MR, Johnson KA (2008a) Redescription and molecular characterization of Myxobolus kisutchi Yasutake & Wood, 1957. J Fish Dis 31:707–712. https://doi.org/10.1111/j.1365-2761.2008.00936.x
Hogge CI, Campbell MR, Johnson KA (2008b) A new species of myxozoan (Myxosporea) from the brain and spinal cord of rainbow trout (Oncorhynchus mykiss) from Idaho. J Parasitol 94:218–222
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. https://doi.org/10.1016/j.ijpara.2004.06.002
Holzer AS, Sommerville C, Wootten R (2006) Molecular studies on the seasonal occurrence and development of five myxozoans in farmed Salmo trutta L. Parasitology 132:193–205. https://doi.org/10.1017/S0031182005008917
Holzer AS, Bartošová-Sojková P, Born-Torrijos A, Lövy 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 27:1651–1666. https://doi.org/10.1111/mec.14558
Hoshina T (1949) On a new myxosporidian parasite of the genus Myxosoma, M. salmonis n. sp., infecting on the scales of the dog salmon. Seibutsu 4:106–109
Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36:W5–W9. https://doi.org/10.1093/nar/gkn201
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Ksepka SP, Rash JM, Whelan N, Bullard SA (2019) A new species of Myxobolus (Myxozoa: Bivalvulida) infecting the medulla oblongata and nerve cord of brook trout Salvelinus fontinalis in southern Appalachia (New River, NC, USA). Parasitol Res 118:3241–3252. https://doi.org/10.1007/s00436-019-06472-x
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
Lom J, Dyková I (1992) Protozoan parasites of fishes, 1st edn. Elsevier, Amsterdam
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
Lom J, Hoffman GL (1971) Morphology of the spores of Myxosoma cerebralis (Hofer, 1903) and M. cartilaginis (Hoffman, Putz, and Dunbar, 1965). J Parasitol 57:1302–1308. https://doi.org/10.1645/0022-3395(2003)089[0653:MOTSOM]2.0.CO;2
MacCrimmon HR, Marshall TL (1968) World distribution of brown trout, Salmo trutta. J Fish Res Board Canada 25:2527–2548. https://doi.org/10.1139/f68-225
Molnár K, Eszterbauer E (2015) Specificity of infection sites in vertebrate hosts. In: Okamura B, Gruhl A, Bartholomew JL (eds) Myxozoan evolution, ecology and development. Springer International Publishing, Cham, pp 295–313
Okamura B, Gruhl A, Bartholomew JL (2015) An introduction to Myxozoan evolution, ecology and development. In: Okamura B, Gruhl A, Bartholomew JL (eds) Myxozoan evolution, ecology and development. Springer International Publishing, Cham, pp 1–20
Polley TM, Atkinson SD, Jones GR, Bartholomew JL (2013) Supplemental description of Myxobolus squamalis (Myxozoa). J Parasitol 99:725–728. https://doi.org/10.1645/12-109.1
Rocha S, Azevedo C, Alves Â, Antunes C, Casal G (2019a) Morphological and molecular characterization of myxobolids (Cnidaria, Myxozoa) infecting cypriniforms (Actinopterygii, Teleostei) endemic to the Iberian Peninsula. Parasite 26:48. https://doi.org/10.1051/PARASITE/2019049
Rocha S, Casal G, Alves Â, Antunes C, Rodrigues P, Azevedo C (2019b) Myxozoan biodiversity in mullets (Teleostei, Mugilidae) unravels hyperdiversification of Myxobolus (Cnidaria, Myxosporea). Parasitol Res 118:3279–3305. https://doi.org/10.1007/s00436-019-06476-7
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 61:539–542. https://doi.org/10.1093/sysbio/sys029
Sánchez-Hernández J, Servia MJ, Vieira R, Barca-Bravo S, Cobo F (2012) References data on the growth and population parameters of brown trout in siliceous rivers of Galicia (NW Spain). Limnetica 31:273–288. https://doi.org/10.23818/limn.31.24
Sayers EW, Cavanaugh M, Clark K, Ostell J, Pruitt KD, Karsch-Mizrachi I (2019) GenBank. Nucleic Acids Res 47:D94–D99. https://doi.org/10.1093/nar/gky989
Sayers EW, Beck J, Brister JR, Bolton EE, Canese K, Comeau DC, Funk K, Ketter A, Kim S, Kimchi A, Kitts PA, Kuznetsov A, Lathrop S, Lu Z, Mcgarvey K, Madden TL, Murphy TD, O’leary N, Phan L, Schneider VA, Oise Thibaud-Nissen F, Trawick BW, Pruitt KD, Ostell J (2020) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 48:D9–D16. https://doi.org/10.1093/nar/gkz899
Schuberg A, Schröder O (1905) Myxosporidien aus dem Neversystem und der Haut der Bachforelle (Myxobolus neurobius n. sp. u. Henneguya nüsslini n. sp.). Arch Protistenkd 6:47–70
Urawa S, Lida Y, Freeman MA, Yanagida T, Karlsbakk E, Yokoyama H (2009) Morphological and molecular comparisons of Myxobolus spp. in the nerve tissues of salmonid fishes with the description of Myxobolus murakamii n. sp., the causative agent of myxosporean sleeping disease. Fish Pathol 44:72–80. https://doi.org/10.3147/jsfp.44.72
Whipps CM, Adlard RD, Bryant MS, Lester RJG, 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 50:215–219. https://doi.org/10.1111/j.1550-7408.2003.tb00120.x
Zhang B, Gu Z, Liu Y (2018) Morphological, histological and molecular characterization of three Myxobolus species (Cnidaria: Myxosporea) from silver carp Hypophthalmichthys molitrix Valenciennes and bighead carp Hypophthalmichthys nobilis Richardson in China. Parasitol Int 67:509–516. https://doi.org/10.1016/j.parint.2018.04.011
Acknowledgements
The authors thank all the local anglers for their helpful collaboration and Dr. Concepción Cabrillana for the assistance. S C-P also acknowledges the IACOBUS Program of the European Grouping of Territorial Cooperation Galicia—North Portugal (GNP, AECT) for the economic support for a research stay at the Laboratory of Animal Pathology, Department of Biology, Faculty of Sciences, University of Porto.
Funding
The study was funded by the Autonomous Government of Galicia (grants GPC2014/069 and ED431C 2017/31) and partially supported by FCT—Foundation for Science and Technology within the scope of UIDB/04423/2020 and UIDP/04423/2020.
Author information
Authors and Affiliations
Corresponding author
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.
Supplementary Information
Table S1
Prevalence of Myxobolus compostellanus n. sp. in brown trout (Salmo trutta) from Galicia (NW Spain) in relation to the watershed and river where the fish specimens were captured. Data from rivers with positive trout are highlighted in bold. (DOCX 19 kb)
Rights and permissions
About this article
Cite this article
Couso-Pérez, S., Rangel, L.F., Santos, M.J. et al. Morphological and molecular characterization of a novel Myxobolus species from the gastrointestinal tract of brown trout (Salmo trutta) in Spain. Parasitol Res 120, 2469–2478 (2021). https://doi.org/10.1007/s00436-021-07201-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-021-07201-z