Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-10T12:49:34.642Z Has data issue: false hasContentIssue false
  • English
  • Français

Motility, morphology and phylogeny of the plasmodial worm, Ceratomyxa vermiformis n. sp. (Cnidaria: Myxozoa: Myxosporea)

Published online by Cambridge University Press:  08 November 2016

E. A. ADRIANO  and
B. OKAMURA
E. A. ADRIANO*
Affiliation:
Departamento de Ciências Biológicas, Universidade Federal de São Paulo (UNIFESP), Diadema, SP, Brazil Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK
B. OKAMURA
Affiliation:
Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK
*
*Corresponding author: Departamento de Ciências Biológicas, Universidade Federal de São Paulo (UNIFESP), Rua Professor Artur Riedel, 275, Jardim Eldorado, 09972-270 Diadema, SP, Brazil. E-mail: edapadriano@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

The Myxozoa demonstrate extensive morphological simplification and miniaturization relative to their free-living cnidarian ancestors. This is particularly pronounced in the highly derived myxosporeans, which develop as plasmodia and pseudoplasmodia. To date, motility in these stages has been linked with membrane deformation (e.g. as pseudopodia and mobile folds). Here we illustrate a motile, elongate plasmodium that undergoes coordinated undulatory locomotion, revealing remarkable convergence to a functional worm at the cellular level. Ultrastructural and confocal analyses of these plasmodia identify a highly differentiated external layer containing an actin-rich network, long tubular mitochondria, abundant microtubules, a secreted glycocalyx layer, and an internal region where sporogony occurs and which contains homogeneously distributed granular/fibrillar material. We consider how some of these features may support motility. We also describe the species based on spore morphology and SSU rDNA sequence data, undertake molecular phylogenetic analysis to place it within an early-diverging clade of the ceratomyxids, and evaluate the resultant implications for classification (validity of the genus Meglitschia) and for inferring early host environments (freshwater) of ceratomyxids.

Keywords

ultrastructuremitochondrial distributionvermiform morphologySSU rDNAconfocal microscopyfreshwater fish hostsAmazonia
Type
Research Article
Information
Parasitology , Volume 144 , Issue 2 , February 2017 , pp. 158 - 168
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alama-Bermejo, G., Bron, J. E., Raga, J. A. and Holzer, A. S. (2012). 3D Morphology, ultrastructure and development of Ceratomyxa puntazzi stages: first insights into the mechanisms of motility and budding in the Myxozoa. PLoS ONE 7, e32679.Google Scholar
Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J. H., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.Google Scholar
Anderson, F. E. and Swofford, D. L. (2004). Should we be worried about long-branch attraction in real data sets? Investigations using metazoan 18S rDNA. Molecular Phylogenetics and Evolution 33, 440–451.Google Scholar
Anesti, V. and Scorrano, L. (2006). The relationship between mitochondrial shape and function and the cytoskeleton. Biochimica et Biophysica Acta 1757, 692–699.CrossRefGoogle ScholarPubMed
Atkinson, S. D., Foott, J. S. and Bartholomew, J. L. (2014). Erection of Ceratonova n. gen. (Myxosporea: Ceratomyxidae) to encompass freshwater species C. gasterostea n. sp. from threespine stickleback (Gasterosteus aculeatus) and C. shasta n. comb. from salmonid fishes. Journal of Parasitology 100, 640–645.Google Scholar
Azevedo, C., Ribeiro, M., Clemente, S. C. S., Casal, G., Lopes, L., Matos, P., Al-Quraishy, A. S. 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, 525–528.Google Scholar
Azevedo, C., Clemente, S. C. S., Casal, G., Matos, P., Oliveira, E., Al-Quraishy, A. S. and Matos, E. (2013). Ultrastructure of the plasmodial development of Myxobolus insignis (Myxozoa), infecting the amazonian fish Semaprochilodus insignis (Prochilodontidae). Acta Protozoologica 52, 91–97.Google Scholar
Barta, J. R., Martin, D. S., Liberator, P. A., Dashkevicz, M., Anderson, J. W., Feighner, S. D., Elbrecht, A., Perkins-Barrow, A., Jenkins, M. C., Danforth, H. D., Ruff, M. D. and Profous-Juchelka, H. (1997). Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. Journal of Parasitology 83, 262–271.Google Scholar
Canning, E. U. and Okamura, B. (2004). Biodiversity and evolution of the Myxozoa. Advances in Parasitology 56, 43–131.Google Scholar
Cho, J. B., Kwon, S. R., Kim, S. K., Nam, Y. K. and Kim, K. H. (2004). Ultrastructure and development of Ceratomyxa protopsettae Fujita, 1923 (Myxosporea) in the gallbladder of cultured olive flounder, Paralichthys olivaceus . Acta Protozoologica 43, 241–250.Google Scholar
Cooper, G. M. (2003). The Cell, A Molecular Approach, 3rd Edn. Sinauer Associates Inc., U.S.Google Scholar
Costa, L. R. F., Barthem, R. B., and Bittencourt, M. M. (2001). A Pesca do tambaqui, Colossoma macropomum, com enfoque na área do médio Solimões, Amazonas, Brasil. Acta Amazonica 31, 449–468.Google Scholar
Diamant, A., Whipps, C. M. and Kent, M. L. (2004). A new species of Sphaeromyxa (Myxosporea: Sphaeromyxina: Sphaeromyxidae) in devil firefish, Pterois miles (Scorpaenidae), from the northern Red Sea: morphology, ultrastructure, and phylogeny. Journal of Parasitology 90, 1434–1442.Google Scholar
Feist, S. W., Morris, D. J., Alama-Bermejo, G. and Holzer, A. S. (2015). Cellular processes in myxozoans. In Myxozoan Evolution, Ecology and Development (ed. Okamura, B., Gruhl, A. and Bartholomew, J. L.), pp. 139–154. Springer International Publishing, Switzerland.Google Scholar
Fiala, I., Bartošová-Sojková, P. and Whipps, C. M. (2015 a). Classification and phylogenetics of Myxozoa. In Myxozoan Evolution, Ecology and Development (ed. Okamura, B., Gruhl, A. and Bartholomew, J. L.), pp. 85–110. Springer International Publishing, Switzerland.Google Scholar
Fiala, I., Hlavničková, M., Kodádková, A., Freeman, M. A., Bartošová-Sojková, P. and Atkinson, S. D. (2015 b). Evolutionary origin of Ceratonova shasta and phylogeny of the marine myxosporean lineage. Molecular Phylogenetics and Evolution 86, 75–89.Google Scholar
Froese, R. and Pauly, D. (2009). FishBase. World Wide Web Electronic Publication. Version (03/2009). www.fishbase.org (Accessed on 25/03/2016).Google Scholar
Goudinho, M. and Carvalho, M. L. (1982). Life history and management of the tambaqui (Colossoma macropomum, Characidae): an important Amazonian food fish. Revista Brasileira de Zoologia 1, 107–133.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.CrossRefGoogle ScholarPubMed
Gruhl, A. and Okamura, B. (2015). Tissue Characteristics and Development in Myxozoa. In Myxozoan Evolution, Ecology and Development (ed. Okamura, B., Gruhl, A. and Bartholomew, J. L.), pp. 155–174. Springer International Publishing Switzerland.CrossRefGoogle Scholar
Guindon, S., Dufayard, J. F., 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, 307–321.Google Scholar
Gunter, N. L., Whipps, C. M. and Adlard, R. D. (2009). Ceratomyxa (Myxozoa: Bivalvulida): robust taxon or genus of convenience? International Journal for Parasitology 39, 1395–1405.Google Scholar
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hausmann, K., Hülsmann, N. and Radek, R. (2003). Protistology. 3rd completely revised edition. E. Schweizerbart´sche Verlagsbuchhandlung (Nägele u. Obermiller). Stuttgart.Google Scholar
Korbie, D. J. and Mattick, J. S. (2008). Touchdown PCR for increased specificity and sensitivity in PCR amplification. Nature Protocols 3, 1452–1456.Google Scholar
Kovaleva, A. A. (1988). Suborder Sphaeromyxina (Myxosporea, Bivalvulida) its structure and place in myxosporidian classification. Zoologicheskii Zhurnal 67, 1616–1620.Google Scholar
Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.Google Scholar
Lom, J. and Arthur, J. R. (1989). A guideline for the preparation of species descriptions in Myxosporea. Journal Fish Diseases 12, 151–156.Google Scholar
Lom, J., Dyková, I. and Pavlásková, M. (1983). “Unidentified” mobile protozoans from the blood of carp and some unsolved problems of myxosporean life cycles. Journal of Protozoology 30, 497–508.Google Scholar
Mathews, P. D., Naldoni, J., Maia, A. A. M. and Adriano, E. A. (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, 4021–4025.Google Scholar
Meglitsch, P. A. (1960). Some coelozoic Myxosporidia from New Zealand fishes. I. General and family Ceratomyxidae. Transactions and Proceeding of the Royal Society of New Zealand 88, 265–365.Google Scholar
MPA–Ministério da Pesca e Aquicultura (2012). Boletim Estatístico da Pesca e Aquicultura. Brasília, Brasil.Google Scholar
Naldoni, J., Arana, S., Maia, A. A. M., Ceccarelli, P. S., Tavares, L. E. R., Borges, F. A., Pozo, C. F. and Adriano, E. A. (2009). Henneguya pseudoplatystoma n. sp. causing reduction in epithelial area of gills in the farmed pintado, a South American catfish: histopathology and ultrastructure. Veterinary Parasitology 166, 52–59.Google Scholar
Okamura, B., Gruhl, A. and Bartholomew, J. L. (2015). An introduction to myxozoan evolution, ecology and development. In Myxozoan Evolution, Ecology and Development (ed. Okamura, B., Gruhl, A. and Bartholomew, J. L.), pp. 1–22. Springer International Publishing, Switzerland.Google Scholar
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmoungin, F. and Higgins, D. G. (1997). The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.Google Scholar
Zhao, Y. J., Zhou, Y., Kent, M. L. and Whipps, C. M. (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, 269–279.Google Scholar
Supplementary material: File

Adriano and Okamura supplementary material

Supplementary Figures

Download Adriano and Okamura supplementary material(File)
File 56.9 MB