Skip to main content

Ceratomyxa gracillima n. sp. (Cnidaria: Myxosporea) provides evidence of panmixia and ceratomyxid radiation in the Amazon basin

  • Suellen A. Zatti (a1), Stephen D. Atkinson (a2), Antônio A. M. Maia (a3), Jerri L. Bartholomew (a2) and Edson A. Adriano (a1) (a4)...

We describe a new freshwater myxosporean species Ceratomyxa gracillima n. sp. from the gall bladder of the Amazonian catfish Brachyplatystoma rousseauxii; the first myxozoan recorded in this host. The new Ceratomyxa was described on the basis of its host, myxospore morphometry, ssrDNA and internal transcribed spacer region (ITS-1) sequences. Infected fish were sampled from geographically distant localities: the Tapajós River, Pará State, the Amazon River, Amapá State and the Solimões River, Amazonas State. Immature and mature plasmodia were slender, tapered at both ends, and exhibited vermiform motility. The ribosomal sequences from parasite isolates from the three localities were identical, and distinct from all other Ceratomyxa sequences. No population-level genetic variation was observed, even in the typically more variable ITS-1 region. This absence of genetic variation in widely separated parasite samples suggests high gene flow as a result of panmixia in the parasite populations. Maximum likelihood and maximum parsimony analyses placed C. gracillima n. sp. sister to Ceratomyxa vermiformis in a subclade together with Ceratomyxa brasiliensis and Ceratomyxa amazonensis, all of which have Amazonian hosts. This subclade, together with other Ceratomyxa from freshwater hosts, formed an apparently early diverging lineage. The Amazonian freshwater Ceratomyxa species may represent a radiation that originated during marine incursions into the Amazon basin that introduced an ancestral lineage in the late Oligocene or early Miocene.

Corresponding author
Author for correspondence: Edson A. Adriano, E-mail:
Hide All
Adriano EA and Okamura B (2017) Motility, morphology and phylogeny of the plasmodial worm, Ceratomyxa vermiformis n. sp. (Cnidaria: Myxozoa: Myxosporea). Parasitology 144, 158168.
Adriano EA and Oliveira OMP (2017). Myxosporea in Catálogo Taxonômico da Fauna do Brasil. PNUD. (Accessed May 2017).
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W and Lipman DJ (1997) Gapped BLASTn and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 338933902.
Atkinson SD and Bartholomew JL (2010a) Disparate infection patterns of Ceratomyxa shasta (Myxozoa) in rainbow trout Oncorhynchus mykiss and Chinook salmon Oncorhynchus tshawytscha correlate with ITS-1 sequence variation in the parasite. International Journal for Parasitology 40, 599604.
Atkinson SD and Bartholomew JL (2010b) Spatial, temporal and host factors structure the Ceratomyxa shasta (Myxozoa) population in the Klamath River basin. Infection, Genetics and Evolution 10, 10191026.
Azevedo C, Ribeiro M, Clemente SCS, Casal G, Lopes L, Matos P, Al-Quraishy AS and Matos E (2011) Light and ultrastructural description of Meglitschia mylei n. sp. (Myxozoa) from Myleus rubripinnis (Teleostei: Serrasalmidae) in the Amazon River system. Journal of Eukaryotic Microbiology 58, 525528.
Azevedo C, Rocha S, Casal G, São Clemente SC, Matos P, Al-Quraishy S and Matos E (2013) Ultrastructural description of Ceratomyxa microlepis n. sp. (Phylum Myxozoa): a parasite infecting the gall bladder of Hemiodus microlepis, a freshwater teleost from the Amazon River. Memórias do Instituto Oswaldo Cruz 108, 150154.
Barthem RB and Goulding M (1997). Os bagres balizadores: ecologia, migração e conservação de peixes amazônicos. Brasília: Sociedade Civil Mamirauá; CNPq.
Barthem RB, Goulding M, Leite RG, Cañas C, Forsberg B, Venticinque E, Petry P, Ribeiro MLB, Chuctaya J and Mercado A (2017) Goliash catfish spawing in the far western Amazon confirmed by the distribution of mature adults, drifting larvae and migrating juveniles. Scientific Reports 7, 41784.
Batista JS and Alves-Gomes JA (2006) Phylogeography of Brachyplatystoma rousseauxii (Siluriformes – Pimelodidae) in the Amazon Basin offers preliminary evidence for the first case of ‘homing’ for an Amazonian migratory catfish. Genetics and Molecular Research 5, 723740.
Ben-David J, Atkinson SD, Pollak Y, Yossifon G, Shavit U, Bartholomew JL and Lotan T (2016) Myxozoan polar tubules display structural and functional variation. Parasites & Vectors 9, 549.
Bloom DD and Lovejoy NR (2017) On the origins of marine-derived freshwater fishes in South America. Journal of Biogeography, 44, 19271938.
Boeger WA and Kritsky DC (2003) Parasites, fossils and ecologic history: historical biogeography of the South American freshwater croakers, Plagioscion spp. (Teleostei, Sciaenidae). Zoologica Scripta, 32, 311.
Carriero MM, Adriano EA, Silva MRM, Ceccarelli PS and Maia AAM (2013) Molecular phylogeny of the Myxobolus and Henneguya genera with several new South American species. PLoS ONE 8, e73713.
Carvajal-Vallejos FM, Duponchelle F, Desmarais E, Cerqueira F, Querouil S, Nunez J, Garcia C and Renno JF (2014) Genetic structure in the Amazonian catfish Brachyplatystoma rousseauxii: influence of life history strategies. Genetica 142, 323336.
Cooke GM, Chao NL and Beheregary LB (2011) Marine incursions, cryptic species and ecological diversification in Amazonia: the biogeographic history of the croaker genus Plagioscion (Sciaenidae). Journal of Biogeography 39, 724738.
Eiras JC (2006) Synopsis of the species of Ceratomyxa Thélohan, 1892 (Myxozoa: Myxosporea: Ceratomyxiidae). Systematic Parasitology 65, 4971.
Ferguson JA, Atkinson SD, Whipps CM and Kent ML (2008) Molecular and morphological analysis of Myxobolus spp. of salmonid fishes with the description of a new Myxobolus species. Journal of Parasitology 94, 13221334.
Fiala I, Hlavnicková M, Kodádková A, Freeman MA, Bartosová-Sojková P and Atkinson SD (2015) Evolutionary origin of Ceratonova shasta and phylogeny of the marine myxosporean lineage. Molecular Phylogenetic and Evolution 86, 7589.
Froese R and Pauly D (eds) (2013) FishBase. World Wide Web electronic publication. (Accessed November 2017).
Gasser RB, Chilton NB, Hoste H and Beveridge I (1993) Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Research 21, 25252526.
Gruhl A and Okamura B (2012) Development and myogenesis of the vermiform Buddenbrockia (Myxozoa) and implications for cnidarian body plan evolution. EvoDevo 3, 10.
Guindon S and Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696704.
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W and Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307321.
Gunter NL, Whipps CM and Adlard RD (2009) Ceratomyxa (Myxozoa: Bivalvulida): robust taxon or genus of convenience? International Journal for Parasitology 39, 13951405.
Gunter NL and Adlard RD (2010) The demise of Leptotheca Thélohan, 1895 (Myxozoa: Myxosporea: Ceratomyxidae) and assignment of its species to Ceratomyxa Thélohan, 1892 (Myxosporea: Ceratomyxidae), Ellipsomyxa Køie, 2003 (Myxosporea: Ceratomyxidae), Myxobolus Bütschli, 1882 and Sphaerospora Thélohan, 1892 (Myxosporea: Sphaerosporidae). Systematic Parasitology 75, 81104.
Hall TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.
Hallett SL and 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. Diseases of Aquatic Organisms 46, 197212.
Hallett SL, Atkinson SD and El-Matbouli M (2002) Molecular characterization of two aurantiactinomyxon (Myxozoa) phenotypes reveals one genotype. Journal of Fish Diseases 25, 627631.
Hillis DM and Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. The Quarterly Review of Biology 66, 411453.
Holland JW, Okamura B, Hartikainen H and Secombes CJ (2011) A novel minicollagen gene links cnidarians and myxozoans. Proceedings of the Royal Society B: Biological Sciences 278, 546553.
Hoorn C, Wesselingh FP, Steege H, Bermudez MA, Mora A, Sevink J, Sanmartin I, Sanchez-Meseguer A, Anderson CL, Figueiredo JP, Jaramillo C, Riff D, Negri FR, Hooghiemstra H, Lundberg J, Stadler T, Sarkinen T and Antonelli A (2010) Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science, 330, 927931.
Jiménez-Guri E, Philippe H, Okamura B and Holland PWH (2007) Buddenbrockia is a cnidarian worm. Science 317, 116118.
Kent ML, Andree KB, Bartholomew JL, El-Matbouli M, Desser SS, Devlin RH, Feist SW, Hedrick RP, Hoffmann RW, Khattra J, Hallett SL, Lester RJG, Palenzeula O, Siddall ME and Xiao C (2001) Recent advances in our knowledge of the Myxozoa. Journal of Eukaryotic Microbiology 48, 395413.
Kumar S, Stecher G and Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0. Molecular Biology and Evolution 33, 18701874.
Lom J and Arthur JR (1989) A guideline for the preparation of species descriptions in Myxosporea. Journal of Fish Diseases 12, 151156.
Lom J and Dyková I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica 53, 136.
Lovejoy NR, Albert JS and Crampton WGR (2006) Miocene marine incursions and marine/freshwater transitions: evidence from Neotropical fishes. Journal of South American Earth Sciences 21, 513.
Mathews PD, Naldoni J, Maia AAM and Adriano EA (2016) Morphology and small subunit rDNA-based phylogeny of Ceratomyxa amazonensis n. sp. parasite of Symphysodon discus, an ornamental freshwater fish from Amazon. Parasitology Research 115, 40214025.
Meglitsch PA (1960) Some Coelozoic Myxosporidia from New Zealand fishes – general, and family Ceratomyxidae. Transactions of the Royal Society of New Zealand 88, 265356.
Nelson JS, Grande TC and Wilson MVH (2016). Fishes of the World. 5rd edn. NY, USA: John Wiley & Sons Inc.
Nesnidal MP, Helmkampf M, Bruchhaus I, El-Matbouli M and Hausdorf B (2013) Agent of whirling disease meets orphan worm: phylogenomic analyses firmly place Myxozoa in Cnidaria. PLoS ONE 8, 6.
Okamura B, Gruhl A and Bartholomew JL (2015) An introduction to Myxozoan evolution, ecology and development. In Okamura B, Gruhl A and Bartholomew JL (eds). Myxozoan Evolution, Ecology and Development. Switzerland: Springer International Publishing, pp. 120.
Posada D (2008) Jmodeltest: phylogenetic model averaging. Molecular Biology and Evolution 25, 12531256.
Rambaut A (2008) FigTree v1.1.1: Tree figure drawing tool. (Accessed 6 April 2017).
Siddal ME, Martin DS, Bridge D, Desser SS and Cone DK (1995) The demise of a phylum of protists: phylogeny of Myxozoa and other parasitic Cnidaria. The Journal of Parasitology 81, 961967.
Swofford DL (2002). Paup*. Phylogenetic Studies Using Parsimony (* and other Methods). Version 4. Sunderland, Massachusetts: Sinauer Associates.
Takeuchi F, Sekizuka T, Ogasawara Y, Yokoyama H, Kamikawa R, Nozaki T, Konishi-Sugita Y, Ohnish T and Kuroda M (2015) The mitochondrial genomes of a myxozoan genus Kudoa are extremely divergent in Metazoa. PLoS ONE 10.
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F and Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 48764882.
Whipps CM and Kent M (2006) Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea). Journal of Eukaryotic Microbiology 53, 364373.
Whipps CM, Adlard RD, Bryant MS and Kent ML (2003) Two unusual myxozoans, Kudoa quadricornis n. sp. (Multivalvulida) from the muscle of godspotted trevally (Carangoides fulvoguttatus) and Kudoa permulticapsula n. sp. (Multivalvulida) from the muscle of Spanish mackerel (Scomberomorus commersoni) from the Great Barrier Reef, Australia. Journal of Parasitology 89, 168173.
Zatti SA, Atkinson SD, Bartholomew JL, Maia AAM and Adriano EA (2017) Amazonian waters harbour an ancient freshwater Ceratomyxa lineage (Cnidaria: Myxosporea). Acta Tropica 169, 100106.
Zhang ZQ (2011) Animal biodiversity: an introduction to higher-level classification and taxonomic richness. Zootaxa 3148, 712.
Zhao YJ, Zhou Y, Kent ML and Whipps CM (2008) Replacement of the preoccupied name Davisia Laird 1953 and description of a new myxozoan species (Myxosporea: Sinuolineidae) from Sebastiscus marmoratus (Cuvier, 1829) in the East China Sea. Journal of Parasitology 94, 269279.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 8
Total number of PDF views: 29 *
Loading metrics...

Abstract views

Total abstract views: 115 *
Loading metrics...

* Views captured on Cambridge Core between 17th January 2018 - 21st February 2018. This data will be updated every 24 hours.