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Hyperspora aquatica n.gn., n.sp. (Microsporidia), hyperparasitic in Marteilia cochillia (Paramyxida), is closely related to crustacean-infecting microspordian taxa

Published online by Cambridge University Press:  17 October 2016

G. D. STENTIFORD ,
A. RAMILO ,
E. ABOLLO ,
R. KERR ,
K. S. BATEMAN ,
S. W. FEIST ,
D. BASS  and
A. VILLALBA
G. D. STENTIFORD*
Affiliation:
European Union Reference Laboratory for Crustacean Diseases, Centre for Environment, Fisheries and Aquaculture Science (Cefas), Barrack Road, Weymouth, Dorset DT4 8UB, UK Pathology and Molecular Systematics Team, Weymouth Laboratory, Centre for Environment, Fisheries and Aquaculture Science (Cefas), Dorset DT4 8UB, UK
A. RAMILO
Affiliation:
Centro de Investigacións Mariñas (CIMA), Consellería do Mar, Xunta de Galicia, Aptdo.13, 36620 Vilanova de Arousa, Spain
E. ABOLLO
Affiliation:
Centro Tecnológico del Mar, Fundación CETMAR, Eduardo Cabello s/n, 36208 Vigo, Spain
R. KERR
Affiliation:
Pathology and Molecular Systematics Team, Weymouth Laboratory, Centre for Environment, Fisheries and Aquaculture Science (Cefas), Dorset DT4 8UB, UK
K. S. BATEMAN
Affiliation:
European Union Reference Laboratory for Crustacean Diseases, Centre for Environment, Fisheries and Aquaculture Science (Cefas), Barrack Road, Weymouth, Dorset DT4 8UB, UK Pathology and Molecular Systematics Team, Weymouth Laboratory, Centre for Environment, Fisheries and Aquaculture Science (Cefas), Dorset DT4 8UB, UK
S. W. FEIST
Affiliation:
Pathology and Molecular Systematics Team, Weymouth Laboratory, Centre for Environment, Fisheries and Aquaculture Science (Cefas), Dorset DT4 8UB, UK
D. BASS
Affiliation:
Pathology and Molecular Systematics Team, Weymouth Laboratory, Centre for Environment, Fisheries and Aquaculture Science (Cefas), Dorset DT4 8UB, UK Department of Life Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
A. VILLALBA
Affiliation:
Centro de Investigacións Mariñas (CIMA), Consellería do Mar, Xunta de Galicia, Aptdo.13, 36620 Vilanova de Arousa, Spain Honorary Professor of the Department of Life Sciences, University of Alcalá, Aptdo. 20, 28805 Alcalá de Henares, Spain
*
*Corresponding author: European Union Reference Laboratory for Crustacean Diseases, Centre for Environment, Fisheries and Aquaculture Science (Cefas), Barrack Road, Weymouth, Dorset DT4 8UB, UK. E-mail: grant.stentiford@cefas.co.uk
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Summary

The Paramyxida, closely related to haplosporidians, paradinids, and mikrocytids, is an obscure order of parasitic protists within the class Ascetosporea. All characterized ascetosporeans are parasites of invertebrate hosts, including molluscs, crustaceans and polychaetes. Representatives of the genus Marteilia are the best studied paramyxids, largely due to their impact on cultured oyster stocks, and their listing in international legislative frameworks. Although several examples of microsporidian hyperparasitism of paramyxids have been reported, phylogenetic data for these taxa are lacking. Recently, a microsporidian parasite was described infecting the paramyxid Marteilia cochillia, a serious pathogen of European cockles. In the current study, we investigated the phylogeny of the microsporidian hyperparasite infecting M. cochillia in cockles and, a further hyperparasite, Unikaryon legeri infecting the digenean Meiogymnophallus minutus, also in cockles. We show that rather than representing basally branching taxa in the increasingly replete Cryptomycota/Rozellomycota outgroup (containing taxa such as Mitosporidium and Paramicrosoridium), these hyperparasites instead group with other known microsporidian parasites infecting aquatic crustaceans. In doing so, we erect a new genus and species (Hyperspora aquatica n. gn., n.sp.) to contain the hyperparasite of M. cochillia and clarify the phylogenetic position of U. legeri. We propose that in both cases, hyperparasitism may provide a strategy for the vectoring of microsporidians between hosts of different trophic status (e.g. molluscs to crustaceans) within aquatic systems. In particular, we propose that the paramyxid hyperparasite H. aquatica may eventually be detected as a parasite of marine crustaceans. The potential route of transmission of the microsporidian between the paramyxid (in its host cockle) to crustaceans, and, the ‘hitch-hiking’ strategy employed by H. aquatica is discussed.

Keywords

MarteiliaParamyxeaCercozoaDigeneaPhylogenyFungiCryptomycota
Type
Research Article
Information
Parasitology , Volume 144 , Issue 2 , February 2017 , pp. 186 - 199
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Arzul, I., Chollet, B., Boyer, S., Bonnet, D., Gaillard, J., Baldi, Y., Robert, M., Joly, Y., Garcia, J. P. and Bouchoucha, M. (2014). Contribution to the understanding of the cycle of the protozoan parasite Marteilia refringens . Parasitology 141, 227–240.Google Scholar
Audemard, C., Le, R. F., Barnaud, A., Collins, C., Sautour, B., Sauria, P. G., de, M. X., Coustau, C., Combes, C. and Berthe, F. (2002). Needle in a haystack: involvement of the copepod Paracartia grani in the life-cycle of the oyster pathogen Marteilia refringens . Parasitology 124, 315–323.Google Scholar
Ba, C. T., Toguebaye, B. S. and Marchand, B. (2007). Ultrastructure of Nosema sp., microsporidia hyperparasite of Bothriocephalus clavipes (Cestoda, Bothriocephalidae) parasite of intestine of Anguilla anguilla (Pisces, Teleostei) from Corse, France. Journal of Eukaryotic Microbiology 54, 24S.Google Scholar
Bass, D., Chao, E. E. Y., Nikolaev, S., Yabuki, A., Ishida, K-I., Berney, C., Pakzad, U., Wylezich, C. and Cavalier-Smith, T. (2009). Phylogeny of novel naked filose and reticulose Cercozoa: Granofilosea cl. n. and Proteomyxidea revised. Protist 160, 75–109.Google Scholar
Boyer, S., Chollet, B., Bonnet, D. and Arzul, I. (2013). New evidence for the involvement of Paracartia grani (Copepoda, Calanoida) in the life cycle of Marteilia refringens (Paramyxea). International Journal for Parasitology 43, 1089–1099.Google Scholar
Burki, F., Corradi, N., Sierra, R., Pawlowski, J., Meyer, G. R., Abbott, C. L. and Keeling, P. J. (2013). Phylogenomics of the intracellular parasite Mikrocytos mackini reveals evidence for a mitosome in Rhizaria. Current Biology 23, 1541–1547.CrossRefGoogle ScholarPubMed
Cable, J. and Tinsley, R. C. (1992). Microsporidian hyperparasites and bacteria associated with Pseudodiplorchis americanus (Monogenea, Polystomatidae). Canadian Journal of Zoology 70, 523–529.Google Scholar
Canning, E. U. and Nicholas, J. P. (1974). Light and electron microscopy observations on Unikaryon legeri (Microsporida, Nosematidae), a parasite of the metacercaria of Meigymnophallus minutus in Cardium edule . Journal of Invertebrate Pathology 23, 92–100.CrossRefGoogle Scholar
Canning, E. U., Lai, P. F. and Lie, K. J. (1974). Microsporidian parasite of trematode larvae from aquatic snails in West Malaya. Journal of Protozoology 21, 19–25.Google Scholar
Capella-Gutiérrez, S., Marcet-Houben, M., Gabaldón, T. (2012). Phylogenomics supports microsporidia as the earliest diverging clade of sequenced fungi. BMC Biology 10, 47.Google Scholar
Carrasco, N., López-Flores, I., Alcaraz, M., Furones, M. D., Berthe, F. C. J. and Arzul, I. (2007). First record of a Marteilia parasite (Paramyxea) in zooplankton populations from a natural estuarine environment. Aquaculture 269, 63–70.CrossRefGoogle Scholar
Carrasco, N., Arzul, I., Berthe, F. C. J. and Furones, M. D. (2008). In situ hybridization detection of initial infective stages of Marteilia refringens (Paramyxea) in its host Mytilus galloprovincialis . Journal of Fish Diseases 31, 153–157.Google Scholar
Carrasco, N., Hine, M., Durfort, M., Andree, K. B., Malchus, N., Lacuesta, B., González, M., Roque, A., Rodgers, C. and Furones, M. D. (2013). Marteilia cochillia sp. nov., a new Marteilia species affecting the edible cockle Cerastoderma edule in European waters. Aquaculture 413–414, 223–230.Google Scholar
Caullery, M. and Mesnil, F. (1897). Sur un type nouveau (Metchnikovella n.g.) d'organismes parasites des grégarines. Comptes Rendus de Seances de la Societe de Biologie, Paris 49, 960–962.Google Scholar
Caullery, M. and Mesnil, F. (1914). Sur les Metchnikovellidae et autre protistes des grégarines d'annélides. Comptes Rendus de Seances de la Societe de Biologie, Paris 77, 527–532.Google Scholar
Chatton, E. (1911). Sur une Cnidosporidie sans cnidoblaste (Paramyxa paradoxa, n.g., n.sp.). Comptes Rendus de Seances de la Societe de Biologie, Paris 152, 631–633.Google Scholar
Comps, M., Grizel, H., Tigé, G. and Duthoit, J. L. (1975). Parasites nouveaux de la glande digestive des mollusques marins Mytilus edulis L. et Cardium edule . Comptes Rendus de Seances de la Societe de Biologie, Paris 281, 179–181.Google Scholar
Comps, M., Pichot, Y. and Deltreil, Y-P. (1979). Mise en evidence d'une microsporidie parasite de Marteilia refringens agent de la maladie de La glande digestive de Ostrea edulis L. Rev. Trav. Inst. Pèches marit. 43, 409–412.Google Scholar
Corsaro, D., Walochnik, J., Venditti, D., Steinmann, J., Müller, K-D. and Michel, R. (2014). Microsporidia-like parasites of amoebae belong to the early fungal lineage Rozellomycota. Parasitology Research 113, 1909–1918.Google Scholar
Czaker, R. (1997). Wittmannia antarctica n.g., n.sp. (Nosematidae), a new hyperparasite in the Antarctic dicyemid mesozoan Kantharella antarctica . Journal of Eukaryotic Microbiology 44, 438–446.Google Scholar
de Buron, I., Loubès, C. and Maurand, J. (1990). Infection and pathological alterations within the acanthocephalan Acanthocephaloides propinquus attributable to the microsporidian hyperparasite Microsporidium acanthocephali . Transactions of the American Microscopical Society 109, 91–97.Google Scholar
Diamant, A. and Paperna, I. (1985). The development and ultrastructure of Nosema ceratomyxae sp. nov., a microsporidian hyperparasite of the myxosporean Ceratomyxa sp. from Red Sea rabbitfish (Siganidae). Protistologica 21, 249–258.Google Scholar
Feist, S. W., Hine, P. M., Bateman, K. S., Stentiford, G. D. and Longshaw, M. (2009). Paramarteilia canceri sp. n. (Cercozoa) in the European edible crab (Cancer pagurus) with a proposal for the revision of the order Paramyxida Chatton, 1911. Folia Parasitologia 56, 73–85.Google Scholar
Foissner, I. and Foissner, W. (1995). Ciliatosporidium platyophryae nov. gen., nov. spec. (Microspora, Encephalitozoonidae), a parasite of Platyophrya terricola (Ciliophora, Colpodea). European Journal of Protistology 31, 248–259.CrossRefGoogle Scholar
Fokin, S. I., Di Giuseppe, G., Erra, F. and Dini, F. (2008). Euplotespora binucleata n. gen., n. sp. (Protozoa: Microsporidia), a parasite infecting the hypotrichous ciliate Euplotes woodruffi, with observations on microsporidian infections in ciliophora. Journal of Eukaryotic Microbiology 55, 214–228.Google Scholar
Freeman, M. A., Bell, A. S. and Sommerville, C. (2003). A hyperparasitic microsporidian infecting the salmon louse, Lepeophtheirus salmonis: an rDNA-based molecular phylogenetic study. Journal of Fish Diseases 26, 667–676.Google Scholar
Gatehouse, H. S. and Malone, L. A. (1998). The ribosomal RNA gene region of Nosema apis (Microspora): DNA sequence for small and large subunit rRNA genes and evidence of a large tandem repeat unit size. Journal of Invertebrate Pathology 71, 97–105.Google Scholar
Ginsburger-Vogel, T. (1991). Intersexuality in Orchestia mediterranea Costa, 1853, and Orchestia aestuarensis Wildish, 1987 (Amphipoda): a consequence of hybridization or parasitic infestation? Journal of Crustacean Biology 11, 530–539.Google Scholar
Ginsburger-Vogel, T. and Desportes, I. (1979). Structure and biology of Marteilia sp. in the amphipod Orchestia gammarellus . Marine Fisheries Review 41, 3–7.Google Scholar
Grizel, H., Comps, M., Bonami, J. R., Cousserans, F., Duthoit, J. L. and Le Pennec, M. A. (1974). Recherche sur l'agent de la maladie de la glande digestive de Ostrea edulis Linné. Sciences Pêche 240, 7–29.Google Scholar
Haag, K. L., James, T. Y., Pombert, J-F., Larsson, R., Schaer, T. M. M., Refardt, D. and Ebert, D. (2014). Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites. Proceedings of the National Academy of Sciences of the United States of America 111, 15480–15485.Google Scholar
Hartikainen, H., Ashford, O. S., Berney, C., Okamura, B., Feist, S. W., Baker-Austin, C., Stentiford, G. D. and Bass, D. (2014 a). Lineage-specific molecular probing reveals novel diversity and ecological partitioning of haplosporidians. ISME Journal 8, 177–186.CrossRefGoogle ScholarPubMed
Hartikainen, H., Stentiford, G. D., Bateman, K. S., Berney, C., Feist, S. W., Longshaw, M., Okamura, B., Stone, D., Ward, G., Wood, C. and Bass, D. (2014 b). Mikrocytids are a broadly distributed and divergent radiation of parasites in aquatic invertebrates. Current Biology 24, 807–812.Google Scholar
Haskin, H. H., Stauber, L. A. and Mackin, J. A. (1966). Minchinia nelsoni n. sp. (Haplosporida, Haplosporidiidae): causative agent of the Delaware Bay oyster epizootic. Science 153, 1414–1416.CrossRefGoogle Scholar
Hopwood, D. (1996). Theory and practice of histopathological techniques. In Fixation and Fixatives, 4th Edn (ed. Bamcroft, J. D. and Stevens, A.), pp. 23–46. Churchill Livingstone, Hong Kong.Google Scholar
James, T. Y., Pelin, A., Bonen, L., Ahrendt, S., Sain, D., Corradi, N. and Stajich, J. E. (2013). Shared signatures of parasitism and phylogenomics unite Cryptomycota and Microsporidia. Current Biology 23, 1548–1553.Google Scholar
Jones, M. D. M., Forn, I., Gadelha, C., Egan, M. J., Bass, D., Massana, R. and Richards, T. A. (2011 a). Discovery of novel intermediate forms redefines the fungal tree of life. Nature 474, 200–203.CrossRefGoogle ScholarPubMed
Jones, M. D., Richards, T. A., Hawksworth, D. L. and Bass, D. (2011 b). Validation and justification of the phylum name Cryptomycota phyl. nov. IMA Fungus 2, 173–175.CrossRefGoogle ScholarPubMed
Jones, S. R., Prosperi-Porta, G. and Kim, E. (2012). The diversity of Microsporidia in parasitic copepods (Caligidae: Siphonostomatoida) in the Northeast Pacific Ocean with description of Facilispora margolisi n. g., n. sp and a new family Facilisporidae n. fam. Journal of Eukaryotic Microbiology 59, 206–217.CrossRefGoogle Scholar
Karpov, S. A., Mikhailov, K. V., Mirzaeva, G. S., Mirabdullaev, I. M., Mamkaeva, K. A., Titova, N. N. and Aleoshin, V. V. (2013). Obligately phagotrophic aphelids turned out to branch with the earliest-diverging Fungi. Protist 164, 195–205.Google Scholar
Karpov, S. A., Mamkaeva, M. A., Aleoshin, V. V., Nassonova, E., Lilje, O. and Gleason, F. H. (2014). Morphology, phylogeny, and ecology of the aphelids (Aphelidea, Opisthokonta) and proposal for the new superphylum Opisthosporidia. Frontiers in Microbiology 5, 112.Google Scholar
Katoh, K. and Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.Google Scholar
Kleeman, S. N., Adlard, R. D. and Lester, R. J. G. (2002). Detection of the initial infective stages of the protozoan parasite Marteilia sydneyi in Saccostrea glomerata and their development through to sporogenesis. International Journal for Parasitology 32, 767–784.CrossRefGoogle ScholarPubMed
Larsson, J. I. R. (1987). On Haplosporidium gammari, a parasite of the amphipod Rivulogammarus pulex, and its relationships with the phylum Ascetospora. Journal of Invertebrate Pathology 49, 159–169.Google Scholar
Larsson, J. I. R. (2000). The hyperparasitic microsporidium Amphiacantha longa Caullery et Mesnil, 1914 (Microspora: Metchnikovellidae) – description of the cytology, redescription of the species, emended diagnosis of the genus Amphiacantha and establishment of the new family Amphiacanthidae. Folia Parasitologia 47, 241–256.Google Scholar
Larsson, J. I. R. and Koie, M. (2006). The ultrastructure and reproduction of Amphiamblys capitellides (Microspora, Metchnikovellidae), a parasite of the gregarine Ancora sagittata (Apicomplexa, Lecudinidae), with redescription of the species and comments on the taxonomy. European Journal of Protistology 42, 233–248.CrossRefGoogle ScholarPubMed
Lee, S. C., Corradi, N., Byrnes, E. J., Torres-Martinez, S., Dietrich, F. S., Keeling, P. J. and Heitmand, J. (2008). Microsporidia evolved from ancestral sexual fungi. Current Biology 18, 1675–1679.CrossRefGoogle ScholarPubMed
Lefèvre, T., Lebarbenchon, C., Gauthier-Clerc, M., Missé, D., Poulin, R. and Thomas, F. (2008) The ecological significance of manipulative parasites. Trends in Ecology and Evolution 24, 41–48.Google Scholar
Levron, C., Ternengo, S., Toguebaye, B. S. and Marchand, B. (2004). Ultrastructural description of the life cycle of Nosema diphterostomi sp. n., a microsporidia hyperparasite of Diphterostomum brusinae (Digenea: Zoogonidae), intestinal parasite of Diplodus annularis (Pisces: Teleostei). Acta Protozoologica 43, 329–336.Google Scholar
Levron, C., Ternengo, S., Toguebaye, B. S. and Marchand, B. (2005). Ultrastructural description of the life cycle of Nosema monorchis n. sp. (Microspora, Nosematidae), hyperparasite of Monorchis parvus (Digenea, Monorchiidae), intestinal parasite of Diplodus annularis (Pisces, Teleostei). European Journal of Protistology 41, 251–256.Google Scholar
Miller, M. A., Pfeiffer, W., and Schwartz, T. (2010). Creating the CIPRES science gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans, LA, pp. 1–8.Google Scholar
Morris, D. J. and Freeman, M. A. (2010). Hyperparasitism has wide-ranging implications for studies on the invertebrate phase of myxosporean (Myxozoa) life cycles. International Journal for Parasitology 40, 357–369.Google Scholar
Nylund, S., Andersen, L., Saevareid, I., Plarre, H., Watanabe, K., Arnesen, C. E., Karlsbakk, E. and Nylund, A. (2011). Diseases of farmed Atlantic salmon Salmo salar associated with infections by the microsporidian Paranucleospora theridion . Diseases of Aquatic Organisms 94, 41–57.Google Scholar
OIE (2014). Diagnostic Manual for Aquatic Animal Diseases. http://www.oie.int/international-standard-setting/aquatic-manual/access-online/.Google Scholar
Ramilo, A., Abollo, E. and Villalba, A. (2014). Species-specific oligonucleotide probe for detection of Bonamia exitiosa (Haplosporidia) using in situ hybridisation assay. Diseases of Aquatic Organisms 110, 81–91.CrossRefGoogle ScholarPubMed
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A. and Huelsenbeck, J. P. (2012). MrBayes 3·2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systems Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Rotari, Y. M., Paskerova, G. G. and Sokolova, Y. Y. (2015). Diversity of metchnikovellids (Metchnikovellidae, Rudimicrosporea), hyperparasites of bristle worms (Annelida, Polychaeta) from the White Sea. Protistology 9, 50–59.Google Scholar
Rozen, S. and Skaletsky, H. J. (2000). Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics Methods and Protocols: Methods in Molecular Biology (ed. Krawetz, S. and Misener, S.), pp. 365–386. Humana Press, Totowa, NJ.Google Scholar
Scheid, P. (2007). Mechanism of intrusion of a microspordian-like organism into the nucleus of host amoebae (Vannella sp.) isolated from a keratitis patient. Parasitology Research 101, 1097–1102.Google Scholar
Sene, A., Ba, C. T., Marchand, B. and Toguebaye, B. S. (1997). Ultrastructure of Unikaryon nomimoscolexi n. sp. (Microsporida, Unikaryonidae), a parasite of Nomimoscolex sp. (Cestoda, Proteocephalidea) from the gut of Clarotes laticeps (Pisces, Teleoste, Bagridae). Diseases of Aquatic Organisms 29, 35–40.Google Scholar
Short, S., Guler, Y., Yang, G., Kille, P. and Ford, A. T. (2012). Paramyxean microsporidian co-infection in amphipods: is the consensus that Microsporidia can feminise their hosts presumptive? International Journal for Parasitology 42, 683–691.Google Scholar
Simdianov, T., Yudina, V. and Aleoshin, V. (2009). First data on molecular phylogeny of microsporidian family Metchnikovellidae. In Proceedings of the XIII International Congress of Protistology, Armacao dos Buzios, Brasil, p. 144.Google Scholar
Sokolova, Y. Y., Paskerova, G. G., Rotari, Y. M., Nassonova, E. S. and Smirnov, A. V. (2013). Fine structure of Metchnikovella incurvata Caullery and Mesnil 1914 (microsporidia), a hyperparasite of gregarines Polyrhabdina sp. from the polychaete Pygospio elegans . Parasitology 140, 855–867.CrossRefGoogle ScholarPubMed
Sprague, V. (1977). Annotated list of species of microsporidia. In Comparative Pathobiology, Vol. 2 (ed. Bulla, L. E. and Cheng, T. C.), pp. 31–334. Plenum Press, New York and London.CrossRefGoogle Scholar
Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.Google Scholar
Stentiford, G. D. (2008). Diseases of the European edible crab (Cancer pagurus): a review. ICES Journal of Marine Science 65, 1578–1592.CrossRefGoogle Scholar
Stentiford, G. D., Bateman, K. S., Longshaw, M. and Feist, S. W. (2007). Enterospora canceri n. gen., n. sp., intranuclear within the hepatopancreatocytes of the European edible crab Cancer pagurus . Diseases of Aquatic Organisms 75, 61–72.CrossRefGoogle Scholar
Stentiford, G. D., Bateman, K. S., Small, H. J., Moss, J., Shields, J. D., Reece, K. S. and Tuck, I. (2010). Myospora metanephrops (n. g., n. sp.) from marine lobsters and a proposal for erection of a new order and family (Crustaceacida; Myosporidae) in the class Marinosporidia (Phylum Microsporidia). International Journal for Parasitology 40, 1433–1446.Google Scholar
Stentiford, G. D., Bateman, K. S., Dubuffett, A. and Stone, D. (2011). Hepatospora eriocheir (Wang and Chen, 2007) gen. et comb. nov infecting invasive Chinese mitten crabs (Eriocheir sinensis) in Europe. Journal of Invertebrate Pathology 108, 156–166.Google Scholar
Stentiford, G. D., Bateman, K. S., Feist, S. W., Stone, D. M. and Dunn, A. M. (2013). Microsporidia: diverse, dynamic and emergent pathogens in aquatic systems. Trends in Parasitology 29, 567–578.Google Scholar
Tanabe, Y., Watanabe, M. M. and Sugiyamaaff, J. (2002). Are Microsporidia really related to Fungi?: a reappraisal based on additional gene sequences from basal fungi. Mycology Research 106, 1380–1391.Google Scholar
Thomas, F., Renaud, F. and Poulin, R. (2008). Exploitation of manipulators: ‘hitch-hiking’ as a parasite transmission strategy. Animal Behaviour 56, 199–206.Google Scholar
Villalba, A., Mourelle, S. G., Carballal, M. J. and Lopez, C. (1997). Symbionts and diseases of farmed mussels Mytilus galloprovincialis throughout the culture process in the Rias of Galicia (NW Spain). Diseases of Aquatic Organisms 19, 127–139.Google Scholar
Villalba, A., Iglesias, D., Ramilo, A., Darriba, S., Parada, J. M., No, E., Abollo, E., Molares, J. and Carballal, M. J. (2014). Cockle Cerastoderma edule fishery collapse in the Ría de Arousa (Galicia, NW Spain) associated with the protistan parasite Marteilia cochillia . Diseases of Aquatic Organisms 109, 55–80.Google Scholar
Vinckier, D. (1975). Nosemoides gen. n., N. vivieri (Vinckier, Devauchelle & Prensier, 1970) comb. nov. (Microsporidie); etude de la différentiation sporoblastique et genèse des différentes structures de la spore. Journal of Protozoology 22, 170–184.Google Scholar
Vivier, E. (1965). Étude, au microscope électronique, de la spore de Metchnikovella hovassei n. sp.: appartenance des Metchnikovellidae aux Microsporidies. Comptes Rendus de Seances de la Societe de Biologie, Paris 260, 6982–6984.Google Scholar
Vossbrinck, C. R. and Debrunner-Vossbrinck, B. A. (2005) Molecular phylogeny of the Microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitologia 52, 131–142.Google Scholar
Wang, T. C., Nai, Y. S., Wang, C. Y., Solter, L. F., Hsu, H. C., Wang, C. H. and Lo, C. F. (2013). A new microsporidium, Triwangia caridinae gen. nov., sp. nov. parasitizing fresh water shrimp, Caridina formosae (Decapoda: Atyidae) in Taiwan. Journal of Invertebrate Pathology 112, 281–293.Google Scholar
Ward, G., Bennett, M., Bateman, K. S., Stentiford, G. D., Feist, S. W., Williams, S., Berney, C. and Bass, D. (2016). A new phylogeny and eDNA insight into paramyxids: an increasingly important but enigmatic clade of protistan parasites of marine invertebrates. International Journal for Parasitology 10, 605–619.Google Scholar
Weiss, L. M., Zhu, X., Cali, A., Tanowitz, H. B. and Wittner, M. (1994). Utility of microsporidian rRNA in diagnosis and phylogeny: a review. Folia Parasitologia 41, 81–90.Google Scholar
Yang, G., Short, S., Kille, P. and Ford, A. T. (2011). Microsporidia infections in the amphipod, Echinogammarus marinus (Leach): suggestions of varying causal mechanisms to intersexuality. Marine Biology 158, 461–470.Google Scholar