Microsporidia in a Woodland Pool I. Lanatospora costata sp. n. (Opisthosporidia, Microsporidia), Parasite of Megacyclops viridis (Crustacea, Copepoda): Fine Structure and Molecular Phylogeny.

Jiří Vávra; Miroslav Hyliš; Ivan Fiala; Dominik Refardt; J. I. Ronny Larsson

Microsporidia in a Woodland Pool I. Lanatospora costata sp. n. (Opisthosporidia, Microsporidia), Parasite of Megacyclops viridis (Crustacea, Copepoda): Fine Structure and Molecular Phylogeny.

Publication date: 19.12.2016

Acta Protozoologica, 2016, Volume 55, Issue 4, pp. 269 - 280

https://doi.org/10.4467/16890027AP.16.023.6010

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Microsporidia in a Woodland Pool I. Lanatospora costata sp. n. (Opisthosporidia, Microsporidia), Parasite of Megacyclops viridis (Crustacea, Copepoda): Fine Structure and Molecular Phylogeny.

Abstract

Lanatospora costatasp. n., a new microsporidian parasite of the adipose and connective tissue cells of Megacyclops viridis (Jurine, 1820) (Copepoda: Cyclopidae) is described. It was isolated from a woodland pool with a rich and diverse fauna of microsporidia-infected small crustaceans and insect larvae. The parasite is structurally similar to the genus Lanatospora Voronin, 1989, characterized by a complex decorated exospore. In the described species the exospore is armoured by a conspicuous layer of interwoven ribs forming labyrinth on the spore surface. SSU rRNA phylogeny places the organism in the “aquatic outgroup” of microsporidia (Vossbrinck et al. 2004), which includes a number of microsporidia from aquatic microcrustacea of the classes Copepoda and Cladocera. The increasing number of available SSU rRNA gene sequences of these microsporidia allows a more detailed interpretation of their developmental histories.

Keywords

Lower fungi, phylogeny, utrastructure, spore, exospore

References

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Ardila-Garcia A. M., Raghuram N., Sihota P., Fast N. M. (2013) Microsporidian diversity in soil, sand, and compost of the pacific Northwest. J. Eukaryot. Microbiol. 60: 601–608

Becnel J. J. (2012) Complementary techniques: preparations of entomopathogens and diseased specimens for more detailed study using microscopy. In: Manual of Techniques in Invertebrate Pathology, Sec. Ed. (Ed. L. A. Lacey), Academic Press, 451–466

Becnel J. J., Takvorian P. M., Cali A. (2014) Checklist of available generic names for Microsporidia with type species and type hosts. In: Microsporidia, Pathogens of Opportunity (Eds. L. M. Weiss, J. J. Becnel) Wiley Blackwell, 671–686

Bjørnson S., Oi D. (2014) Microsporidia biological control agents and pathogens of beneficial insects. In: Microsporidia, Pathogens of Opportunity, (Eds. L. M. Weiss, J. J. Becnel) Wiley Blackwell, 635–670

Bronnvall A. M., Larsson J. I. R. (1995) Description of Lanatospora tubulifera sp. n. (Microspora, Tuzetiidae) with emended diagnosis and new systematic position for the genus Lanatospora. Arch. Protistenkd. 146: 69–78

Bronnvall A. M., Larsson J. I. R. (2001) Ultrastructure and light microscopic cytology of Agglomerata lacrima sp. n. (Microspora, Duboscqiidae), a microsporidian parasite of Acanthocyclops vernalis (Copepoda, Cyclopidae). Europ. J. Protistol. 37: 89–101

Cali A., Takvorian P. M. (2014) Developmental morphology and life cycles of Microsporidia. In: Microsporidia, Pathogens of Opportunity, (Eds. L. M. Weiss, J. J. Becnel), Wiley Blackwell, 71–133

Galtier N., Gouy M., Gautier C. (1996) SEAVIEW and PHYLO_WIN: Two graphic tools for sequence alignment and molecular phylogeny. Computer Applications in the Biosciences 12: 543–548

Haag K. L., James T. Y., Pombert J.-F., Larsson R., Schaer T. M. M., Refardt D., Ebert D. (2014) Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites. PNAS 111: 15480–15485

Hesse E. (1935) Sur quelques Microsporidies parasites de Megacyclops viridis, Jurine. Arch. Zool. Exp. Gén. 75: 651–661

Issi I. V., Tokarev Y. S., Voronin V. N., Seliverstova E. V., Pavlova O. A., Dolgikh V. V. (2010) Ultrastructure and molecular phylogeny of Mrazekia macrocyclopis sp. n. (Microsporidia, Mrazekiidae), a microsporidian parasite of Macrocyclops albidus (Jur.) (Crustacea, Copepoda). Acta Protozool. 49: 75–84

Jírovec O. (1936) Studien über Microsporidien. Mem. Soc. Zool. Tchécoslovaque de Prague 4: 1–75

Jones S. R. M., Prosperi-Porta G., Kim E. (2012) The diversity of microsporidia in parasitic copepods (Caligidae: Siphonostomatoida) in the northeast pacific ocean with description of Facilispora margolisi n. g., sp. n. and a new family Facilisporidae n. fam. J. Eukaryot. Microbiol. 59: 206–217

Karpov S. A., Mamkaeva M. A., Aleoshin V. V., Nassonova E., Lilje O., Gleason F. H. (2014) Morphology, phylogeny, and ecology of the aphelids (Aphelidea, Opisthokonta) and proposal for the new superphylum Opisthosporidia. Front. Microbiol. 5: art. 112

Katoh K., Kuma K., Toh H., Miyata T. (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucl. Acids Res. 33: 511–518

Kudo R. (1921) Microsporidia parasitic in copepods. J. Parasitol. 7: 137–143

Larsson R. A. (1983) Revisionary study of the taxon Tuzetia Maurand, Fize, Fenwick and Michel, 1971, and related forms (Microspora,Tuzetiidae). Protistologica 19: 323–355

Larsson J. I. R., Voronin V. N. (2000) Light and electron microscopic study of Agglomerata volgensae n. sp. (Microspora: Dubosqiidae), a new microsporidian parasite of Daphnia magna (Crustacea: Daphniidae). Europ. J. Protistol. 36: 89–99

Lom J., Vávra J. (1963) Mucous envelopes of spores of the subphyllum Cnidospora (Doflein, 1901). Acta Soc. Zool. Bohemoslov. 27: 4–6

Loubès C. (1979) Ultrastructure, sexualité, dimorphisme sporogonique des Microsporidies (Protozoaires). Incidences taxonomiques et biologiques. Thèse. Université des Sciences et Techniques du Languedoc, Montpellier.

Maurand J., Fize A., Fenwick B., Michel R. (1971) Etude au microscope électronique de Nosema infirmum Kudo 1921. Microsporidie parasite d’un Copépode Cyclopoide, création du genre nouveau Tuzetia a propos de cette espèce. Protistologica 7: 221–225

Ralphs J. R., Matthews R. A. (1986) Hepatic microsporidiosis of juvenile gray mullet Chelon labrosus (Risso), due to Microgemma hepaticus gen. nov., sp. nov. J. Fish Diseases 9: 225–245

Rambaut A., Drummond A. J. (2007) Tracer v1.4, Available from http://beast.bio.ed.ac.uk/Tracer

Refardt D., Decaestecker E., Johnson P. T. J., Vávra J. (2008) Morphology, molecular phylogeny, and ecology of Binucleata daphniae, n. g., n. sp. (Fungi: Microsporidia), a parasite of Daphnia magna Straus, 1820 (Crustacea: Branchiopoda). J. Eukaryot. Microbiol. 55: 393–408

Ronquist F., Huelsenbeck J. P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19: 1572–1574

Simakova A. V., Lukiantsev V. V., Vossbrinck C. R., Andreadis T. G. (2011) Identification of mosquito-parasitic microsporidia, Amblyospora rugosa and Trichoctosporea pygopellita (Microsporidia: Amblysporidae), from Acanthocyclops venustus and Acanthocyclops reductus (Copepoda: Cyclopidae), based on small subunit rDNA analysis. Parazitologiya 45:

Sokolova Y. Y., Senderskiy I. V., Tokarev Y. S. (2016) Microsporidia Alfvenia sibirica sp. n. and Agglomerata cladocera (Pfeiffer) 1895, from Siberian microcrustaceans and phylogenetic relationships within the “Aquatic outgroup” lineage of fresh water microsporidia J. Invertebr. Pathol. 136: 81–91

Sprague V. (1977) Systematics of the Microsporidia. In: Comparative Pathobiology, Vol. 2. (Eds. A. Bulla, Jr., T. C. Cheng), Plenum Press, N.Y., 1–510

Sprague V., Becnel J. J., Hazard E. I. (1992) Taxonomy of the phylum Microspora. Crit. Rev. Microbiol. 18: 285–395

Stamatakis A. (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.

Stentiford G. D., Feist S. W., Stone D. M., Bateman K. S., Dunn A. M. (2013) Microsporidia: Diverse, dynamic, and emergent pathogens in aquatic systems. Trends in Parasitology 29: 567–578

Swofford D. L., Waddell P. J., Huelsenbeck J. P., Foster P. G., Lewis P. O. Rogers J. S. (2001) Bias in phylogenetic estimation and its relevance to the choice between parsimony and likelihood methods. Systematic Biology 50: 525–539

Vávra J., Hyliš M., Oborník M., Vossbrinck C. R. (2005) Microsporidia in aquatic microcrustacea: the copepod microsporidium Marssoniella elegans Lemmermann, 1900 revisited. Folia Parasitologica 52: 163–172

Vávra J., Larsson J. I. R. (2014) Structure of Microsporidia. In: Microsporidia, Pathogens of Opportunity, (Eds. L. M. Weiss, J. J. Becnel), Wiley Blackwell, 1–70

Vávra J., Larsson J. I. R., Baker M. D. (1997) Light and electron microscopic cytology of Trichotuzetia guttata gen. et sp. n. (Microspora, Tuzetiidae), a microsporidian parasite of Cyclops vicinus Uljanin, 1875 (Crustacea, Copepoda). Arch. Protistenkd. 147: 293–306

Vávra J., Lukeš J. (2013) Microsporidia and ‘the art of living together’. Advances in parasitology 82: 253–319

Vávra J., Maddox J. V. (1976). Methods in microsporidiology. In: Comparative Pathobiology, Vol. 1. (Eds. A. Bulla, Jr., T. C. Cheng), Plenum Press, N.Y., 281–319

Voronin V. N. (1986) The microsporidia of crustaceans. Protozoology (Leningrad) 10: 137–165

Voronin V. N. (1989) The ultrastructure of Lanatospora macrocyclopis (Protozoa, Microsporida) from the Cyclope Macrocyclops albidus (Jur.) (Crustacea, Copepoda). Arch. Protistenkd. 137: 357–366

Voronin V. N. (1990) The effect of methods of the host preparation on the microsporidian extrasporal coat (Microsporidia). Parazitologyia 3: 242–244

Voronin V. N. (1995) On the possibility of using highly specific parasites (Microsporidia, Protozoa) for the analysis of systematic relationships within Cladocera (in Russian). Zool. Zhurnal 74: 17–21

Voronin V. N. (1999) The microsporidia of freshwater invertebrates and fish of Russia. The thesis of doctoral dissertation, Saint-Petersburg, 47 (in Russian)

Vossbrinck C. R., Debrunner-Vossbrinck B. A. (2005) Molecular phylogeny of the Microsporidia: Ecological, ultrastructural and taxonomic considerations. Folia Parasitologica, 52: 131–142

Vossbrinck C. R., Andreadis T. G., Vávra, J., Becnel J. J. (2004) Molecular phylogeny and evolution of mosquito parasitic microsporidia (Microsporidia: Amblyosporidae). J. Eukaryot. Microbiol. 51: 88–95

Weiser J. (1945) Příspěvek ke znalosti Mikrosporidií perlooček a buchanek (Contribution to the knowledge of Microsporidia of cladocera and copepods. In Czech, no English summary). Acta Societatis Scientiarum Naturalium Moravicae 17: 1–10

Yang D., Pan G., Dang X. et al. (2015) Interaction and assembly of two novel proteins in the spore wall of the microsporidian species Nosema bombycis and their roles in adherence to and infection of host cells. Infect. Immun. 83: 1715–1731

Information

Information: Acta Protozoologica, 2016, Volume 55, Issue 4, pp. 269 - 280

DOI: https://doi.org/10.4467/16890027AP.16.023.6010

Article type: Original article

Authors

Jiří Vávra

Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic

Miroslav Hyliš

Laboratory of Electron Microscopy, Faculty of Science, Charles University in Prague, Czech Republic

Ivan Fiala

Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic

Dominik Refardt

Institute of Natural Resource Sciences, Zurich University of Applied Sciences, 8820 Wädenswil, Switzerland

J. I. Ronny Larsson

Department of Biology, Lund University, Lund, Sweden

Published at: 19.12.2016

Article status: Open

Licence: None

Percentage share of authors:

Jiří Vávra (Author) - 20%

Miroslav Hyliš (Author) - 20%

Ivan Fiala (Author) - 20%

Dominik Refardt (Author) - 20%

J. I. Ronny Larsson (Author) - 20%

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Microsporidia in a Woodland Pool I. Lanatospora costata sp. n. (Opisthosporidia, Microsporidia), Parasite of Megacyclops viridis (Crustacea, Copepoda): Fine Structure and Molecular Phylogeny.

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