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Haplosporosomes, sporoplasmosomes and their putative taxonomic relationships in rhizarians and myxozoans

Published online by Cambridge University Press:  18 September 2020

P.M. Hine ,
D.J. Morris ,
C. Azevedo ,
S.W. Feist  and
G. Casal Open the ORCID record for G. Casal [Opens in a new window]
P.M. Hine*
Affiliation:
73 rue de la Fée au Bois, Fouras, 17450, France
D.J. Morris
Affiliation:
Marine Scotland Science, Salmon and Freshwater Fisheries Laboratory, Faskally, Pitlochry, Perthshire, PH16 5LB, Scotland
C. Azevedo
Affiliation:
Laboratory of Animal Pathology, Interdisciplinary Centre for Marine and Environmental Research (CIIMAR), Matosinhos, Portugal Laboratory of Cell Biology, Institute of Biomedical Sciences (ICBAS/UP), University of Porto, 4050-313Porto, Portugal
S.W. Feist
Affiliation:
CEFAS Weymouth Laboratory, Barrack Road, The Nothe, Weymouth, Dorset, DT4 8UB, England
G. Casal
Affiliation:
Laboratory of Cell Biology, Institute of Biomedical Sciences (ICBAS/UP), University of Porto, 4050-313Porto, Portugal University Institute of Health Sciences & Institute of Research and Advanced Training in Health Sciences and Technologies, CESPU, 4585-116Gandra, Portugal
*
Author for correspondence: P.M. Hine, E-mail: vinet.hine@orange.fr
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Abstract

This paper reviews current knowledge of the structure, genesis, cytochemistry and putative functions of the haplosporosomes of haplosporidians (Urosporidium, Haplosporidium, Bonamia, Minchinia) and paramyxids (Paramyxa, Paramyxoides, Marteilia, Marteilioides, Paramarteilia), and the sporoplasmosomes of myxozoans (Myxozoa – Malacosporea, Myxosporea). In all 3 groups, these bodies occur in plasmodial trophic stages, disappear at the onset of sporogony, and reappear in the spore. Some haplosporidian haplosporosomes lack the internal membrane regarded as characteristic of these bodies and that phylum. Haplosporidian haplosporogenesis is through the Golgi (spherulosome in the spore), either to form haplosporosomes at the trans-Golgi network, or for the Golgi to produce formative bodies from which membranous vesicles bud, thus acquiring the external membrane. The former method also forms sporoplasmosomes in malacosporeans, while the latter is the common method of haplosporogenesis in paramyxids. Sporoplasmogenesis in myxosporeans is largely unknown. The haplosporosomes of Haplosporidium nelsoni and sporoplasmosomes of malacosporeans are similar in arraying themselves beneath the plasmodial plasma membrane with their internal membranes pointing to the exterior, possibly to secrete their contents to lyse host cells or repel haemocytes. It is concluded that these bodies are probably multifunctional within and between groups, their internal membranes separating different functional compartments, and their origin may be from common ancestors in the Neoproterozoic.

Keywords

Functionshaplosporidianshaplosporosomesmyxozoansparamyxidssporoplasmosomestaxonomic relationshipsultrastructure
Type
Review Article
Information
Parasitology , Volume 147 , Issue 14 , December 2020 , pp. 1614 - 1628
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Anderson, TJ and Lester, RGJ (1992) Sporulation of Marteilioides branchialis n. sp. (Paramyxea) in the Sydney rock oyster, Saccostrea commercialis: an electron microscope study. Journal of Protozoology 39, 502–508.10.1111/j.1550-7408.1992.tb04839.xCrossRefGoogle Scholar
Anderson, TJ, Newman, LJ and Lester, RJG (1993) Light and electron microscopic study of Urosporidium cannoni n. sp. haplosporidian parasite of the polyclad turbellarian Stylochus sp. Journal of Eukaryotic Microbiology 40, 162–168.CrossRefGoogle Scholar
Anderson, CL, Canning, EU and Okamura, B (1999) Molecular data implicate bryozoans as hosts for PKX (Phylum Myxozoa) and identify a clade of bryozoan parasites within the Myxozoa. Parasitology 199, 555–561.10.1017/S003118209900520XCrossRefGoogle Scholar
Auffret, M and Poder, M (1983 [1985]) Recherches sur Marteilia maurini, parasite de Mytilus edulis sur les côtes de Bretagne nord. Revue des Travaux de l’ Institut pêches maritimes 47, 105–109.Google Scholar
Azevedo, C (1984) Ultrastructure of the spore of Haplosporidium lusitanicum sp. n. (Haplosporida, Haplosporidiidae), parasite of a marine mollusc. Journal of Parasitology 70, 358–371.CrossRefGoogle Scholar
Azevedo, C (2001) Ultrastructural description of the spore maturation stages of the clam parasite Minchinia tapetis (Vilela, 1951) (Haplosporida: Haplosporidiidae). Systematic Parasitology 49, 189–194.10.1023/A:1010620721138CrossRefGoogle Scholar
Azevedo, C and Corral, L (1985) Cytochemical analysis of the haplosporosomes and vesicle-like droplets of Haplosporidium lusitanicum (Haplosporida, Haplosporidiidae), parasite of Helcion pellucidus (Prosobranchia). Journal of Invertebrate Pathology 46, 281–288.10.1016/0022-2011(85)90070-9CrossRefGoogle Scholar
Azevedo, C and Corral, L (1987) Fine structure, development and cytochemistry of the spherulosome of Haplosporidium lusitanicum (Haplosporida). European Journal of Protistology 23, 89–94.10.1016/S0932-4739(87)80011-1CrossRefGoogle Scholar
Azevedo, C and Corral, L (1989) Fine structural observations of the natural spore excystment of Minchinia sp. (Haplosporida). European Journal of Protistology 24, 168–173.10.1016/S0932-4739(89)80046-XCrossRefGoogle Scholar
Azevedo, C, Lom, J and Corral, L (1989) Ultrastructural aspects of Myxidium giardi (Myxozoa, Myxosporea), parasite of the European eel Anguilla anguilla. Diseases of Aquatic Organisms 6, 55–61.10.3354/dao006055CrossRefGoogle Scholar
Azevedo, C, Balseiro, P, Casal, G, Gestal, C, Aranguren, R, Stokes, N, Carnegie, R, Novoa, B, Burreson, E and Figueras, A (2006) Ultrastructural and molecular characterization of Haplosporidium montforti n. sp., parasite of the European abalone Haliotis tuberculata. Journal of Invertebrate Pathology 92, 23–32.Google ScholarPubMed
Azevedo, C, Casal, G and Montes, J (2008a) Ultrastructural developmental cycle of Haplosporidium montforti (Phylum Haplosporidia) in its farmed abalone host, Haliotis tuberculata (Gastropoda). Journal of Parasitology 94, 137–142. doi: 10.1645/GE-1177.1.CrossRefGoogle Scholar
Azevedo, C, Casal, G, Matos, P and Matos, E (2008b) A new species of Myxozoa, Henneguya rondoni n. sp. (Myxozoa), from the peripheral nervous system of the Amazonian fish, Gymnorhamphicthys rondoni (Teleostei). Journal of Eukaryotic Microbiology 55, 229–234. doi: 10.1111/j.1550-7408.2008.00317.x.CrossRefGoogle Scholar
Azevedo, C, Casal, G, Matos, P, Alves, Â and Matos, E (2011) Henneguya torpedo sp. nov. (Myxozoa), a parasite from the nervous system of the Amazonian teleost Brachyhypopomus pinnicaudatus. Diseases of Aquatic. Organisms 93, 235–242. doi: 10.3354/dao02292.CrossRefGoogle Scholar
Azevedo, C, Carmona De São Clemente, S, Casal, G, Matos, P, Oliveira, E, Al-Quraishy, S and Matos, ER (2013) Ultrastructure of the plasmodial development of Myxobolus insignis (Myxozoa), infecting the Amazonian fish Semaprochilodus insignis (Prochilodontidae). Acta Protozoologica 52, 91–97. doi: 10.4467/16890027AP.13.009.1088.Google Scholar
Ball, SJ (1980) Fine structure of the spores of Minchinia chitonis (Lankester, 1885) Labbé, 1896 (Sporozoa: Haplosporida), a parasite of the chiton, Lepidochitona cinereus. Parasitology 81, 169–176.10.1017/S003118200005513XCrossRefGoogle Scholar
Bartošová-Sojková, P, Hrabcová, M, Pecková, H, Patra, S, Kodádkova, A, Jurajda, P, Tyml, T and Holzer, AS (2014) Hidden diversity and evolutionary trends in malacosporean parasites (Cnidaria: Myxozoa) identified using molecular phylogenetics. International Journal of Parasitology 44, 565–577.10.1016/j.ijpara.2014.04.005CrossRefGoogle ScholarPubMed
Bass, D, Chao, EEY, 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. doi: 10.1016/j.protis.2008.07.002.CrossRefGoogle Scholar
Bearham, D, Spiers, Z, Raidal, S, Jones, JB and Nicholls, PK (2008a) Spore ornamentation of Minchinia occulta n. sp. (Haplosporidia) in rock oysters Saccostrea cuccullata (Born, 1778). Parasitology 135, 1271–1280. doi: 10.1017/S0031182008004897.CrossRefGoogle Scholar
Bearham, D, Spiers, Z, Raidal, S, Jones, JB and Burreson, EM (2008b) Spore ornamentation of Haplosporidium hinei n. sp. (Haplosporidia) in pearl oysters Pinctada maxima (Jameson, 1901). Parasitology 135, 521–527. doi: 10.1017/S0031182008004149.Google Scholar
Berthe, FCJ, Le Roux, F, Adlard, RD and Figueras, A (2004) Marteiliosis in molluscs: a review. Aquatic Living Resources 17, 433–448. doi: 10.1051/alr.2004051.CrossRefGoogle Scholar
Bower, SM and Meyer, GR (2002) Morphology and ultrastructure of a protistan pathogen in the haemolymph of shrimp (Pandalus spp.) in the northeastern Pacific Ocean. Canadian Journal of Zoology 80, 1055–1068. doi: 10.1139/Z02-080.CrossRefGoogle Scholar
Burreson, EM (2001) Spore ornamentation of Haplosporidium pickfordi Barrow, 1961 (Haplosporidia), a parasite of freshwater snails in Michigan, USA. Journal of Eukaryotic Microbiology 48, 622–626.10.1111/j.1550-7408.2001.tb00201.xCrossRefGoogle Scholar
Burreson, EM and Ford, SE (2004) A review of recent information on the Haplosporidia, with special reference to Haplosporidium nelsoni (MSX disease). Aquatic Living Resources 17, 499–517. doi: 10.1051/alr.2004056.CrossRefGoogle Scholar
Canning, EU, Curry, A, Feist, SW, Longshaw, M and Okamura, B (1999) Tetracapsula bryosalmonae n.sp. for PKX organism the cause of PKD in salmonid fish. Bulletin of the European Association of Fish Pathologists 19, 203–206.Google Scholar
Canning, EU, Curry, A, Feist, SW, Longshaw, M and Okamura, B (2000) A new class and order of myxozoans to accomodate parasites of bryozoans with ultrastructural observations on Tetracapsula bryosalmonae (PKX organism). Journal of Eukaryotic Microbiology 47, 456–568.10.1111/j.1550-7408.2000.tb00075.xCrossRefGoogle Scholar
Canning, EU, Curry, A, Hill, SL and Okamura, B (2007) Ultrastructure of Buddenbrockia allmani n. sp. (Myxozoa, Malacosporea), a parasite of Lophopus crystallinus (Bryozoa, Phylactolaemata). Journal of Eukaryotic Microbiology 54, 247–262.10.1111/j.1550-7408.2007.00261.xCrossRefGoogle Scholar
Canning, EU, Curry, A and Okamura, B (2008) Early development of the myxozoan Buddenbrockia plumatellae in the bryozoans Hyalinella punctata and Plumatella fungosa, With comments on taxonomy and systematics of the Myxozoa. Folia Parasitologica 55, 241–255.10.14411/fp.2008.032CrossRefGoogle ScholarPubMed
Carballal, MJ, Diaz, S and Villalba, A (2005) Urosporidium sp. hyperparasite of the turbellarian Paravortex cardii in the cockle Cerastoderma edule. Journal of Invertebrate Pathology 90, 104–107.10.1016/j.jip.2005.08.003CrossRefGoogle ScholarPubMed
Carnegie, RB, Burreson, EM, Hine, PM, Stokes, NA, Audemard, C, Bishop, MJ and Peterson, PH (2006) Bonamia perspora n. sp. (Haplosporidia), a parasite of the oyster Ostreola equestris, is the first Bonamia species known to produce spores. Journal of Eukaryotic Microbiology 53, 232–245.10.1111/j.1550-7408.2006.00100.xCrossRefGoogle Scholar
Carrasco, N, Hine, PM, Durfort, M, Andree, KB, Malchus, N, Lacuesta, B, González, M, Roque, A, Rodgers, C and Furones, MD (2013) Marteilia cochillia sp. nov., a new Marteilia species affecting the edible cockle Cerastoderma edule in European waters. Aquaculture 412–413, 223–230. doi: 10.1016/j.aquaculture.2013.07.027.CrossRefGoogle Scholar
Casal, G, Matos, E and Azevedo, C (2003) Light and electron microscopic study of the myxosporean, Henneguya friderici N. sp. from the Amazonian teleostean fish, Leporinus friderici. Parasitology 126, 313–319.10.1017/S0031182003002944CrossRefGoogle ScholarPubMed
Casal, G, Matos, E and Azevedo, C (2006) A new myxozoan parasite from the Amazonian fish Metynnis argenteus (Teleostei, Characidae): light and electron microscope observations. Journal of Parasitology 92, 817–821.10.1645/GE-750R.1CrossRefGoogle ScholarPubMed
Casal, G, Costa, G and Azevedo, C (2007) Ultrastructural description of Ceratomyxa tenuispora (Myxozoa), a parasite of the marine fish Aphanopus carbo (Trichiuridae), from the Atlantic coast of Madeira Island (Portugal). Folia Parasitologica 54, 165–171.10.14411/fp.2007.023CrossRefGoogle Scholar
Catanese, G, Grau, A, Valencia, JM, Garcia-March, JR, Vazquez-Luis, M, Alvarez, E, Deudero, S, Darriba, S, Carballal, MJ and Villalba, A (2018) Haplosporidium pinnae sp.nov., a haplosporidian parasite associated with mass mortalities of the fan mussel, Pinna nobilis, in the Western Mediterranean Sea. Journal of Invertebrate Pathology 157, 9–24. doi: 10.1016/j.jip.2018.07.006.CrossRefGoogle Scholar
Cavalier-Smith, T, Chao, EE and Lewis, R (2018) Multi-gene phylogeny and cell evolution of chromist infra-kingdom Rhizaria: contrasting cell organization of sister phyla Cercozoa and Retaria. Protoplasma 255, 1517–1574. doi: 10.1007/s00709-018-1241-1.CrossRefGoogle Scholar
Chang, ES, Neuhof, M, Rubinstein, ND, Diamant, A, Philippe, H, Huchon, D and Cartwright, P (2015) Genomic insights into the evolutionary origin of Myxozoa within Cnidaria. Proceedings of the National Academy of Sciences 112, 14912–14917. doi: 10.1073/pnas.1511468112.CrossRefGoogle ScholarPubMed
Ciancio, A, Srippa, S and Izzo, C (1999) Ultrastructure of vegetative and sporulation stages of Haplosporidium ascidiarium from the ascidian Ciona intestinalis L. European Journal of Protistology 35, 175–182.10.1016/S0932-4739(99)80035-2CrossRefGoogle Scholar
Comps, M (1983 [1985]) Étude morphologique de Marteilia christenseni sp. n. parasite du lavignon Scrobicularia piperata P. (Mollusque Pélécypode). Revue des Travaux de l’ Institut pêches maritimes 47, 99–104.Google Scholar
Comps, M and Pichot, Y (1991) Fine spore structure of a haplosporidan parasitizing Crassostrea gigas: taxonomic implications. Diseases of Aquatic Organisms 11, 73–77.CrossRefGoogle Scholar
Comps, M and Tigé, G (1997) Fine structure of Minchinia sp., a haplosporidan infecting the mussel Mytilus galloprovincialis. Systematic Parasitology 38, 45–50.10.1023/A:1005821424831CrossRefGoogle Scholar
Comps, M, Park, MS and Desportes, I (1986) Étude ultrastructurale de Marteilioides chungmuensis n.g. n.sp. parasite des ovocytes de l'Huître Crassostrea gigas Th. Protistologica 22, 279–285.Google Scholar
Desportes, I (1981) Étude ultrastructurale de la sporulation de Paramyxa paradoxa Chatton (Paramyxida) parasite de l'annelide polychète Poecilochaetus serpens. Protistologica 17, 365–386.Google Scholar
Desportes, I and Lom, J (1981) Affinités de Paramyxa paradoxa Chatton, 1911, parasite de Poecilochaetus serpens (Annélide, polychète) avec les Marteiliidae Sprague, parasites d'huîtres et du crustacé Orchestia gammarellus. Comptes Rendus de l'Académie des Sciences. Paris 292, 627–632.Google Scholar
Desportes, I and Nashed, NN (1983) Ultrastructure of sporulation in Minchinia dentali (Arvy), an haplosporean parasite of Dentalium entale (Scaphopoda, Mollusca); taxonomic implications. Protistologica 19, 435–460.Google Scholar
Diggles, BK, Nichol, J, Hine, PM, Wakefield, S, Cochennec-Laureau, N, Roberts, RD and Freidman, CS (2002) Pathology of cultured paua Haliotis iris infected with a novel haplosporidian parasite, with some observations on the course of disease. Diseases of Aquatic Organisms 50, 219–231.10.3354/dao050219CrossRefGoogle ScholarPubMed
Dyková, I, Lom, J and Fajer, E (1988) A new haplosporean infecting the hepatopancreas in the penaeid shrimp, Penaeus vannamei. Journal of Fish Diseases 11, 15–22.10.1111/j.1365-2761.1988.tb00519.xCrossRefGoogle Scholar
Evans, NM, Holder, MT, Barbeitos, MS, Okamura, B and Cartwright, P (2010) The phylogenetic position of Myxozoa: exploring conflicting signals in phylogenomic and ribosomal data sets. Molecular Biology and Evolution 27, 2733–2746.CrossRefGoogle ScholarPubMed
Feist, SW and Bucke, D (1987) Ultrastructural aspects of PKX, the causative agent of proliferative kidney disease in rainbow trout, Salmo gairdneri Richardson. Journal of Fish Diseases 10, 323–327.CrossRefGoogle Scholar
Feist, SW, Hine, PM, Bateman, KS, Stentiford, GD 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 Parasitologica 56, 73–85.CrossRefGoogle Scholar
Ferguson, HW and Needham, EA (1978) Proliferative kidney disease in rainbow trout Salmo gairdneri Richardson. Journal of Fish Diseases 1, 91–108.10.1111/j.1365-2761.1978.tb00008.xCrossRefGoogle Scholar
Foox, J and Siddall, ME (2015) The road to Cnidaria: history of phylogeny of the Myxozoa. Journal of Parasitology 101, 269–274. doi: 10.1645/14-671.1.CrossRefGoogle ScholarPubMed
Ford, SE and Ashton-Alcox, KA (1998) Altered response of oyster hemocytes to Haplosporidium nelsoni (MSX) plasmodia treated with enzymes or metabolic inhibitors. Journal of Invertebrate Pathology 72, 160–166.10.1006/jipa.1998.4775CrossRefGoogle ScholarPubMed
Ford, SE, Ashton-Alcox, KA and Kanaley, SA (1993) In vitro interactions between bivalve hemocytes and the oyster pathogen Haplosporidium nelsoni. Journal of Parasitology 79, 255–265.10.2307/3283516CrossRefGoogle Scholar
Ginsburger-Vogel, T and Desportes, I (1979a) Étude ultrastructurale de la sporulation de Paramarteilia orchestiae gen. n., sp. n., parasite de l'amphipode Orchestia gammarellus (Pallas). Journal of Protozoology 26, 390–403.10.1111/j.1550-7408.1979.tb04642.xCrossRefGoogle Scholar
Ginsburger-Vogel, T and Desportes, I (1979b) Structure and biology of Marteilia sp. in the amphipod. Orchestia gammarellus. Marine Fisheries Review 41, 3–7.Google Scholar
Grabner, DS and El-Matbouli, M (2010a) Experimental transmission of malacosporean parasites from bryozoans to common carp (Cyprinus carpio) and minnow (Phoxinus phoxinus). Parasitology 137, 629–639. doi: 10.1017/S0031182009991429.CrossRefGoogle Scholar
Grabner, DS and El-Matbouli, M (2010b) Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) portal of entry into the fish host. Diseases of Aquatic Organisms 90, 197–206. doi: 10.3354/dao02236.CrossRefGoogle Scholar
Hartikainen, H, Ashford, OS, Berney, C, Okamura, B, Feist, SW, Baker-Austin, C, Stentiford, GD and Bass, D (2014a) Lineage-specific molecular probing reveals novel diversity and ecological partitioning of haplosporidians. ISME Journal 8, 177–186. doi: 10.1038/ismej.2013.136.CrossRefGoogle Scholar
Hartikainen, H, Stentiford, GD, Bateman, KS, Berney, C, Feist, SW, Longshaw, M, Okamura, B, Stone, D, Ward, G, Wood, C and Bass, D (2014b) Mikrocytids are a broadly distributed and divergent radiation of parasites in aquatic invertebrates. Current Biology 24, 807–812. doi: 10.1016/j.cub.2014.02.003.CrossRefGoogle Scholar
Hervio, D, Chagot, D, Godin, P, Grizel, H and Mialhe, E (1991) Localization and characterization of acid phosphatase activity in Bonamia ostreae (Ascetospora), an intrahemocytic protozoan parasite of the flat oyster Ostrea edulis (Bivalvia). Diseases of Aquatic Organisms 12, 67–70.CrossRefGoogle Scholar
Hillman, RE, Ford, SE and Haskin, HH (1990) Minchinia teredinis n.sp. (Balanosporida, Haplosporidiidae), a parasite of teredinid shipworms. Journal of Protozoology 37, 364–368.CrossRefGoogle Scholar
Hine, PM (1991) Ultrastructural observations on the annual infection pattern of Bonamia sp. in flat oysters Tiostrea chilensis. Diseases of Aquatic Organisms 11, 163–171.CrossRefGoogle Scholar
Hine, PM (1992) Ultrastructural and enzyme cytochemical observations on Bonamia sp. in oysters (Tiostrea chilensis), with a consideration of organelle function. Aquaculture 107, 175–183. doi: 10.1016/0044-8486(92)90064-R.CrossRefGoogle Scholar
Hine, PM (2020) Haplosporidian host:parasite interactions. Fish and Shellfish Immunology 103, 190–199. doi: 10.1016/j.fsi.2020.05.004.CrossRefGoogle ScholarPubMed
Hine, PM and Thorne, T (1998) Haplosporidium sp. (Haplosporidia) in hatchery-reared pearl oysters, Pinctada maxima (Jameson, 1901), in north Western Australia. Journal of Invertebrate Pathology 71, 48–52.10.1006/jipa.1997.4705CrossRefGoogle Scholar
Hine, PM and Thorne, T (2002) Haplosporidium sp. (Alveolata: Haplosporidia) associated with mortalities among rock oysters (Saccostrea cuccullata Born, 1778) in north Western Australia. Diseases of Aquatic Organisms 51, 123–133.10.3354/dao051123CrossRefGoogle Scholar
Hine, PM and Wesney, B (1992) Interrelationships of cytoplasmic structures in Bonamia sp. (Haplosporidia) infecting oysters Tiostrea chilensis: an interpretation. Diseases of Aquatic Organisms 14, 59–68.CrossRefGoogle Scholar
Hine, PM and Wesney, B (1994a) The functional cytology of Bonamia sp. (Haplosporidia) infecting oysters (Tiostrea chilensis): an ultracytochemical study. Diseases of Aquatic Organisms 20, 207–217.10.3354/dao020207CrossRefGoogle Scholar
Hine, PM and Wesney, B (1994b) Interaction of phagocytosed Bonamia sp. (Haplosporidia) with haemocytes of oysters (Tiostrea chilensis). Diseases of Aquatic Organisms 20, 219–229.10.3354/dao020219CrossRefGoogle Scholar
Hine, PM, Bower, SM, Meyer, GR, Cochennec-Laureau, N and Berthe, FCJ (2001a) The ultrastructure of Mikrocytos mackini, The cause of Denman Island disease in oysters Crassostrea spp. and Ostrea spp. in British Columbia, Canada. Diseases of Aquatic Organisms 45, 215–227.10.3354/dao045215CrossRefGoogle Scholar
Hine, PM, Cochennec-Laureau, N and Berthe, FCJ (2001b) Bonamia exitiosus n. sp. (Haplosporidia) infecting flat oysters Ostrea chilensis in New Zealand. Diseases of Aquatic Organisms 47, 63–72.10.3354/dao047063CrossRefGoogle Scholar
Hine, PM, Wakefield, S, Diggles, BK, Webb, VL and Maas, EW (2002) The ultrastructure of a haplosporidian containing Rickettsiae, associated with mortalities among cultured paua Haliotis iris. Diseases of Aquatic Organisms 49, 207–219.10.3354/dao049207CrossRefGoogle ScholarPubMed
Hine, PM, Engelsma, MY and Wakefield, SJ (2007) Ultrastructure of sporulation in Haplosporidium armoricanum. Diseases of Aquatic Organisms 77, 225–233. doi: 10.3354/dao01822.CrossRefGoogle ScholarPubMed
Hine, PM, Carnegie, RB, Burreson, EM and Engelsma, MY (2009) Inter-relationships of haplosporidians, deduced from ultrastructural studies. Diseases of Aquatic Organisms 83, 247–256. doi: 10.3354/dao02016.CrossRefGoogle ScholarPubMed
Holzer, A, Bartošová-Sojková, P, Born-Torrijos, A, Lövy, A, Hartigan, A and Fiala, I (2018) The joint evolution of the Myxozoa and their alternate hosts: a cnidarian recipe for success and vast biodiversity. Molecular Ecology 27, 1651–1666. doi: 10.1111/mec.14558.CrossRefGoogle ScholarPubMed
Itoh, N, Yamamoto, T, Kang, H-S, Choi, K-S, Green, TJ, Carrasco, N, Awaji, M and Chow, S (2014) A novel paramyxean parasite, Marteilia granula sp. nov. (Cercozoa), from the digestive gland of Manila clam Ruditapes philippinarum in Japan. Fish Pathology 49, 181–193. doi: 10.3147/jsfp.49.181.CrossRefGoogle Scholar
Ituarte, C, Bagnato, E, Siddall, M and Cremonte, F (2014) A new species of Haplosporidium Caullery & Mesnil, 1899 in the marine false limpet Siphonaria lessoni (Gastropoda: Siphonariidae) from Patagonia. Systematic Parasitology 88, 63–73.10.1007/s11230-014-9480-9CrossRefGoogle Scholar
Jiménez-Guri, E, Philippe, H, Okamura, B and Holland, PWH (2007) Buddenbrockia is a cnidarian worm. Science 317, 116–118. doi: 10.1126/science.1142024.CrossRefGoogle ScholarPubMed
Kent, ML and Hedrick, RP (1985) PKX, the causative agent of Proliferative Kidney Disease (PKD) in Pacific salmonid fishes and its affinities with the Myxozoa. Journal of Parasitology 32, 254–260.Google ScholarPubMed
Kleeman, SN, Adlard, RD and Lester, RJG (2002) Detection of the initial infective stages of the protozoan parasite Marteilia sydneyi in Saccostrea glomerata and their development through to sporogenesis. International Journal of Parasitology 32, 767–784.10.1016/S0020-7519(02)00025-5CrossRefGoogle ScholarPubMed
Kodádková, A, Bartošová-Sojková, P, Holzer, AS and Fiala, I (2015) Bipteria vetusta n. sp. – an old parasite in an old host: tracing the origin of myxosporean parasitism in vertebrates. International Journal of Parasitology 45, 269–276. doi: 10.1016/j.ijpara.2014.12.004.CrossRefGoogle Scholar
La Haye, CA, Holland, ND and McLean, N (1984) Electron microscopic study of Haplosporidium comatulae n. sp. (Phylum Ascetospora: Class Stellatosporea), a haplosporidian endoparasite of an Australian crinoid, Oligometra serripinna (Phylum Echinodermata). Protistologica 20, 507–515.Google Scholar
Larsson, JIR (1987) On Haplosporidium gammari, a parasite of the amphipod Rivulogammarus pulex, and its relationship with the phylum Ascetospora. Journal of Invertebrate Pathology 49, 159–169.10.1016/0022-2011(87)90156-XCrossRefGoogle Scholar
Larsson, JIR and Køie, M (2005) Ultrastructural study and description of Paramyxoides nephthys gen. n., sp. n. a parasite of Nephthys caeca (Fabricius, 1780) (Polychaeta: Nephthyidae). Acta Protozoologica 44, 175–187.Google Scholar
Lom, J and de Puytorac, P (1965) Studies on the myxosporidian ultrastructure and polar capsule development. Protistologica 1, 53–65.Google Scholar
Lom, J and Dyková, I (1988) Sporogenesis and spore structure in Kudoa lunata (Myxosporea, Multivalvulida). Parasitology Research 74, 521–530.CrossRefGoogle Scholar
Lom, J and Dyková, I (1997) Ultrastructural features of the actinosporean phase of Myxosporea (phylum Myxozoa): a comparative study. Acta Protozoologica 36, 83–103.Google Scholar
Lom, J and Dyková, I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica 53, 1–36.CrossRefGoogle ScholarPubMed
Lom, J, Molnár, K and Dyková, I (1986) Hoferellus gilsoni (Debaisieux, 1925) comb. n. (Myxozoa, Myxosporea): redescription and mode of attachment to the epithelium of the urinary bladder of its host, the European eel. Protistologica XXII, 405–413.Google Scholar
Lom, J, Feist, SW, Dyková, I and Kepr, T (1989) Brain myxoboliasis of bullhead, Cottus gobio L., due to Myxobolus jiroveci sp. nov.: light and electron microscope observations. Journal of Fish Diseases 12, 15–27.10.1111/j.1365-2761.1989.tb01235.xCrossRefGoogle Scholar
Longshaw, M, Feist, SW, Matthews, RA and Figueras, A (2001) Ultrastructural characterisation of Marteilia species (Paramyxea) from Ostrea edulis, Mytilus edulis and Mytilus galloprovincialis in Europe. Diseases Aquatic Organisms 44, 137–142.10.3354/dao044137CrossRefGoogle Scholar
Marchand, J and Sprague, V (1979) Ultrastructure de Minchinia cadomensis sp.n. (Haplosporida) parasite du décapode Rhithropanopeus harrisii tridentatus Maitland dans le canal de Caen à la mer. Journal of Protozoology 26, 179–185.10.1111/j.1550-7408.1979.tb02758.xCrossRefGoogle Scholar
McGovern, ER and Burreson, EM (1990) Ultrastructure of Minchinia sp. spores from shipworms (Teredo spp.) in the western north Atlantic, with a discussion of taxonomy of the Haplosporidiidae. Journal of Protozoology 37, 212–218.10.1111/j.1550-7408.1990.tb01130.xCrossRefGoogle Scholar
Meyers, TR, Lightner, DV and Redman, RM (1994) A dinoflagellate-like parasite in Alaskan spot shrimp Pandalus platyceros and pink shrimp P. borealis. Diseases of Aquatic Organisms 18, 71–76.CrossRefGoogle Scholar
Morris, DJ (2012) A new model for myxosporean (Myxozoa) development explains the endogenous budding phenomenon, the nature of cell within cell life stages and evolution of parasitism from a cnidarian ancestor. International Journal of Parasitology 42, 829–840. doi: 10.1016/j.ijpara.2012.06.001.CrossRefGoogle ScholarPubMed
Morris, DJ and Adams, A (2006) Proliferative presaccular stages of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) within the invertbrate host Fredericella sultana (Bryozoa: Phylactolaemata). Journal of Parasitology 92, 984–989. doi: 10.1645/GE-868R.1.CrossRefGoogle Scholar
Morris, DJ and Adams, A (2007) Sacculogenesis of Buddenbrockia plumatellae (Myxozoa) within the invertebrate host Plumatella repens (Bryozoa) with comments on the evolutionary relationships of the Myxozoa. International Journal of Parasitology 37, 1163–1171. doi: 10.1016/j.ijpara.2007.03.001.CrossRefGoogle ScholarPubMed
Morris, DJ and Adams, A (2008) Sporogony of Tetracapsuloides bryosalmonae in the brown trout Salmo trutta and the role of the tertiary cell during the vertebrate phase of myxozoan life cycles. Parasitology 135, 1075–1092. doi: 10.1017/S0031182008004605.CrossRefGoogle ScholarPubMed
Morris, DJ and Freeman, MA (2010) Hyperparasitism has wide-ranging implications for studies on the invertebrate phase of myxosporean (Myxozoa) life cycles. International Journal of Parasitology 40, 357–369. doi: 10.1016/j.ijpara.2009.08.014.CrossRefGoogle ScholarPubMed
Morris, DJ, Adams, A and Richards, RH (1997) Studies of the PKX parasite in rainbow trout via immunohistochemistry and immunogold electron microscopy. Journal of Aquatic Animal Health 9, 265–273. doi: 10.1577/1548-8667(1997)009<0265:SOTPPI>2.3.CO;2.2.3.CO;2>CrossRefGoogle Scholar
Morris, DJ, Adams, A and Richards, RH (2000) Observations on the electron-dense bodies of the PKX parasite, agent of proliferative kidney disease in salmonids. Diseases of Aquatic Organisms 39, 201–209.CrossRefGoogle ScholarPubMed
Morrison, CM, Martell, DJ, Leggiadro, C and O'Neil, D (1996) Ceratomyxa drepanopsettae in the gallbladder of the Atlantic halibut, Hippoglossus hippoglossus, From the northwest Atlantic Ocean. Folia Parasitologica. (Praha) 43, 20–36.Google Scholar
Newman, MW, Johnson, CA and Pauley, GB (1976) A Minchinia-like haplosporidan parasitizing blue crabs, Callinectes sapidus. Journal of Invertebrate Pathology 27, 311–315.CrossRefGoogle ScholarPubMed
Okamura, B, Hartigan, A and Naldoni, J (2018) Extensive uncharted biodiversity: the parasite dimension. Integrative and Comparative Biodiversity 58, 1132–1145. doi: 10.1093/icb/icy039.Google ScholarPubMed
Ormières, R (1980) Haplosporidium parisi n. sp. haplosporidie parasite de Serpula vermicularis L. étude ultrastructurale de la spore. Protistologica 16, 467–474.Google Scholar
Ormières, R, Sprague, V and Bartoli, P (1973) Light and electron microscope study of a new species of Urosporidium (Haplosporida), hyperparasite of trematode sporocysts in the clam Abra ovata. Journal of Invertebrate Pathology 21, 71–86.10.1016/0022-2011(73)90115-8CrossRefGoogle Scholar
Perkins, FO (1968) Fine structure of the oyster pathogen Minchinia nelsoni (Haplosporida, Haplosporidiidae). Journal of Invertebrate Pathology 10, 287–307.CrossRefGoogle Scholar
Perkins, FO (1969) Electron microscope studies of sporulation in the oyster pathogen, Minchinia costalis (Sporozoa: Haplosporida). Journal of Parasitology 55, 897–920.10.2307/3277152CrossRefGoogle Scholar
Perkins, FO (1971) Sporulation in the trematode hyperparasite Urosporidium crescens de Turk, 1940 (Haplosporida: Haplosporidiidae) – an electron microscope study. Journal of Parasitology 57, 9–23.CrossRefGoogle Scholar
Perkins, FO (1975) Fine structure of Minchinia sp. (Haplosporida) sporulation in the mud crab, Panopeus herbstii. Marine Fisheries Review 37, 46–60.Google Scholar
Perkins, FO (1976) Ultrastructure of sporulation in the European flat oyster pathogen, Marteilia refringens-taxonomic implications. Journal of Protozoology 23, 64–74.10.1111/j.1550-7408.1976.tb05247.xCrossRefGoogle Scholar
Perkins, FO (1979) Cell structure of shellfish pathogens and hyperparasites in the genera Minchinia, Urosporidium, Haplosporidium and Marteilia – taxonomic implications. Marine Fisheries Review January-February, 25–37.Google Scholar
Perkins, FO and Wolf, PH (1976) Fine structure of Marteilia sydneyi sp. n. – haplosporidan pathogen of Australian oysters. Journal of Parasitology 62, 528–538.CrossRefGoogle Scholar
Pichot, Y, Comps, M, Tigé, G, Grizel, H and Rabouin, M-A (1979) Recherches sur Bonamia ostreae gen. n., sp. n., parasite nouveau de l'huître plate Ostrea edulis. Revue des Travaux de l’ Institut pêches Maritimes 43, 131–140.Google Scholar
Rangel, LF, Azevedo, C, Casal, G and Santos, MJ (2012) Ultrastructural aspects of Ellipsomyxa mugilis (Myxozoa: Ceratomyxidae) spores and developmental stages in Nereis diversicolor (Polychaeta: Nereidae). Journal of Parasitology 98, 513–519. doi: 10.1645/GE-3005.1.CrossRefGoogle Scholar
Reece, KS and Stokes, NA (2003) Molecular analysis of a haplosporidian parasite from cultured New Zealand abalone Haliotis iris. Diseases of Aquatic Organisms 53, 61–66.CrossRefGoogle ScholarPubMed
Reece, KS, Siddall, ME, Stokes, NA and Burreson, EM (2004) Molecular phylogeny of the Haplosporidia based on two independent gene sequences. Journal of Parasitology 90, 1111–1122.CrossRefGoogle ScholarPubMed
Renault, T, Stokes, NA, Chollet, B, Cochennec, N, Berthe, F, Gérard, A and Burreson, EM (2000) Haplosporidiosis in the Pacific oyster Crassostrea gigas from the French Atlantic coast. Diseases of Aquatic Organisms 42, 207–214.10.3354/dao042207CrossRefGoogle ScholarPubMed
Ruiz, M, López, C, Lee, R-S, Rodríguez, R and Darriba, S (2016) A novel paramyxean parasite, Marteilia octospora n. sp. (Cercozoa) infecting the grooved razor shell clam Solen marginatus from Galicia (NW Spain). Journal of Invertebrate Pathology 135, 34–42.CrossRefGoogle Scholar
Scro, RA and Ford, SE (1990) An electron microscope study of disease progression in the oyster, Crassostrea virginica, infected with the protozoan parasite, Haplosporidium nelsoni (MSX). In Perkins, FO and Cheng, TC (eds), Pathology in Marine Science. New York: Academic Press, pp. 229–254.Google Scholar
Seagrave, CP, Bucke, D and Alderman, DJ (1980) Ultrastructure of a Haplosporean-like organism: the possible causative agent of proliferative kidney disease in rainbow trout. Journal of Fish Biology 16, 453–459.10.1111/j.1095-8649.1980.tb03724.xCrossRefGoogle Scholar
Siddall, ME, Martin, DS, Bridge, D, Desser, SS and Cone, DK (1995) The demise of a phylum of protists: phylogeny of myxozoan and other parasitic Cnidaria. Journal of Parasitology 81, 961–967.CrossRefGoogle ScholarPubMed
Skovgaard, A and Daugbjerg, N (2008) Identity and systematic position of Paradinium poucheti and other Paradinium-like parasites of marine copepods based on morphology and nuclear-encoded SSU rDNA. Protist 159, 401–413. doi: 10.1016/j.protis.2008.02.003.CrossRefGoogle ScholarPubMed
Smith, CE, Morrison, JK, Ramsey, HW and Ferguson, HW (1984) Proliferative kidney disease: first reported outbreak in North America. Journal of Fish Diseases 7, 207–216.10.1111/j.1365-2761.1984.tb00925.xCrossRefGoogle Scholar
Stentiford, GD, Feist, SW, Bateman, KS and Hine, PM (2004) A haemolymph parasite of the shore crab Carcinus maenas: pathology, ultrastructure and observations on crustacean haplosporidians. Diseases of Aquatic Organisms 59, 57–68.CrossRefGoogle ScholarPubMed
Stentiford, GD, Bateman, KS, Stokes, NA and Carnegie, RB (2013) Haplosporidium littoralis sp. nov.: a crustacean pathogen within the Haplosporidia (Cercozoa, Ascetospora). Diseases of Aquatic Organisms 105, 243–252. doi: 10.3354/dao02619.CrossRefGoogle Scholar
Urrutia, A, Bass, D, Ward, G, Ross, S, Bojko, J, Marigomez, I and Feist, SW (2019) Ultrastructure, phylogeny and histopathology of two novel haplosporidians parasitizing amphipods, and importance of crustaceans as hosts. Diseases of Aquatic Organisms 136, 89–105. doi: 10.3354/dao03417.CrossRefGoogle Scholar
Van Iten, H, Marques, AC, de Moraes Leme, J, Forancelli Pacheco, MLA and Guimaraes Simões, M (2014) Origin and early diversification of the phylum Cnidaria Verrill: major developments in the analysis of the taxon's Proterozoic-Cambrian history. Palaeontology 57, 677–690. doi: 10.1111/pala.12116.CrossRefGoogle Scholar
Villalba, A, Iglesias, D, Ramilo, A, Darriba, S, Parada, JM, No, E, Abollo, E, Molares, J and Carballal, MJ (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. doi: 10.3354/dao02723.CrossRefGoogle ScholarPubMed
Vita, P, Corral, L, Matos, E and Azevedo, C (2003) Ultrastructural aspects of the myxosporean Henneguya astyanax n. sp. (Myxozoa: Myxobolidae), a parasite of the Amazonian teleost Astyanax keithi (Characidae). Diseases of Aquatic Organisms 53, 55–60.CrossRefGoogle Scholar
Voronin, VN (1993) PKX-like organism in common carp during swim bladder inflammation: further evidence of an association with the myxosporean Sphaerospora renicola. Bulletin of the European Association of Fish Pathologists 13, 127–129.Google Scholar
Voronin, VN and Chernysheva, NB (1993) An intracellular gill parasite as the possible causative agent of mortality during swim-bladder inflammation in common carp, Cyprinus carpio L. Journal of Fish Diseases 16, 609–611. doi: 10.1111/j.1365-2761.1993.tb00899.x.CrossRefGoogle Scholar
Ward, GM, Bennett, M, Bateman, KS, Stentiford, GD, Kerr, R, Feist, SW, Williams, ST, Berney, C and Bass, D (2016) A new phylogeny and environmental DNA insight in to paramyxids: an increasingly important but enigmatic clade of protistan parasites of marine invertebrates. International Journal of Parasitology 46, 605–619. doi: 10.1016/j.ijpara.2016.04.010.CrossRefGoogle ScholarPubMed
Ward, GM, Neuhauser, S, Groben, R, Ciaghi, S, Berney, C, Romac, S and Bass, D (2018) Environmental sequencing fills the gap between parasitic haplosporidians and giant amoebae. Journal of Eukaryotic Microbiology 65, 574–586. doi: 10.1111/jeu.12501.CrossRefGoogle Scholar
Winters, AD and Faisal, M (2014) Molecular and ultrastructural characterization of Haplosporidium diporeiae n. sp., a parasite of Diporeia sp. (Amphipoda, Gammaridea) in the Laurentian Great Lakes (USA). Parasite Vectors 7, 343. doi: 10.1186/1756-3305-7-343.CrossRefGoogle Scholar