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

Published online by Cambridge University Press:  17 January 2018

Suellen A. Zatti
Affiliation:
Department of Animal Biology, Institute of Biology, University of Campinas, Caixa Postal 6109, CEP 13083-970, Campinas, SP, Brazil
Stephen D. Atkinson
Affiliation:
Department of Microbiology, Oregon State University, Corvallis, Oregon, USA
Antônio A. M. Maia
Affiliation:
Department of Veterinary Medicine, Faculty of Animal Science and Food Engineering, São Paulo University, Avenida Duque de Caxias Norte, 225, CEP 13635-900, Pirassununga, SP, Brazil
Jerri L. Bartholomew
Affiliation:
Department of Microbiology, Oregon State University, Corvallis, Oregon, USA
Edson A. Adriano*
Affiliation:
Department of Animal Biology, Institute of Biology, University of Campinas, Caixa Postal 6109, CEP 13083-970, Campinas, SP, Brazil Department of Ecology and Evolutionary Biology, Federal University of São Paulo, Rua Professor Arthur Riedel, 275, Jardim Eldorado, CEP 09972-270, Diadema, SP, Brazil
*
Author for correspondence: Edson A. Adriano, E-mail: [email protected]

Abstract

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.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

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References

Adriano, EA and Okamura, B (2017) Motility, morphology and phylogeny of the plasmodial worm, Ceratomyxa vermiformis n. sp. (Cnidaria: Myxozoa: Myxosporea). Parasitology 144, 158168.Google Scholar
Adriano, EA and Oliveira, OMP (2017). Myxosporea in Catálogo Taxonômico da Fauna do Brasil. PNUD. http://fauna.jbrj.gov.br/fauna/faunadobrasil/152799 (Accessed May 2017).Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Barthem, RB and Goulding, M (1997). Os bagres balizadores: ecologia, migração e conservação de peixes amazônicos. Brasília: Sociedade Civil Mamirauá; CNPq.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Bloom, DD and Lovejoy, NR (2017) On the origins of marine-derived freshwater fishes in South America. Journal of Biogeography, 44, 19271938.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Eiras, JC (2006) Synopsis of the species of Ceratomyxa Thélohan, 1892 (Myxozoa: Myxosporea: Ceratomyxiidae). Systematic Parasitology 65, 4971.Google Scholar
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.Google Scholar
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.Google Scholar
Froese, R and Pauly, D (eds) (2013) FishBase. World Wide Web electronic publication. www.fishbase.org (Accessed November 2017).Google Scholar
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.Google Scholar
Gruhl, A and Okamura, B (2012) Development and myogenesis of the vermiform Buddenbrockia (Myxozoa) and implications for cnidarian body plan evolution. EvoDevo 3, 10.Google Scholar
Guindon, S and Gascuel, O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696704.Google Scholar
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.Google Scholar
Gunter, NL, Whipps, CM and Adlard, RD (2009) Ceratomyxa (Myxozoa: Bivalvulida): robust taxon or genus of convenience? International Journal for Parasitology 39, 13951405.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Hillis, DM and Dixon, MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. The Quarterly Review of Biology 66, 411453.Google Scholar
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.Google Scholar
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.Google Scholar
Jiménez-Guri, E, Philippe, H, Okamura, B and Holland, PWH (2007) Buddenbrockia is a cnidarian worm. Science 317, 116118.Google Scholar
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.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0. Molecular Biology and Evolution 33, 18701874.Google Scholar
Lom, J and Arthur, JR (1989) A guideline for the preparation of species descriptions in Myxosporea. Journal of Fish Diseases 12, 151156.Google Scholar
Lom, J and Dyková, I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica 53, 136.Google Scholar
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.Google Scholar
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.Google Scholar
Meglitsch, PA (1960) Some Coelozoic Myxosporidia from New Zealand fishes – general, and family Ceratomyxidae. Transactions of the Royal Society of New Zealand 88, 265356.Google Scholar
Nelson, JS, Grande, TC and Wilson, MVH (2016). Fishes of the World. 5rd edn. NY, USA: John Wiley & Sons Inc.Google Scholar
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.Google Scholar
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.Google Scholar
Posada, D (2008) Jmodeltest: phylogenetic model averaging. Molecular Biology and Evolution 25, 12531256.Google Scholar
Rambaut, A (2008) FigTree v1.1.1: Tree figure drawing tool. http://tree.bio.ed.ac.uk/software/figtree/ (Accessed 6 April 2017).Google Scholar
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.Google Scholar
Swofford, DL (2002). Paup*. Phylogenetic Studies Using Parsimony (* and other Methods). Version 4. Sunderland, Massachusetts: Sinauer Associates.Google Scholar
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.Google Scholar
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.Google Scholar
Whipps, CM and Kent, M (2006) Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea). Journal of Eukaryotic Microbiology 53, 364373.Google Scholar
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.Google Scholar
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.Google Scholar
Zhang, ZQ (2011) Animal biodiversity: an introduction to higher-level classification and taxonomic richness. Zootaxa 3148, 712.Google Scholar
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.Google Scholar