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Evidence for trophic transfer of Inodosporus octospora and Ovipleistophora arlo n. sp. (Microsporidia) between crustacean and fish hosts

Published online by Cambridge University Press:  18 December 2017

G.D. Stentiford ,
S. Ross ,
D. Minardi ,
S.W. Feist ,
K.S. Bateman ,
P.A. Gainey ,
C. Troman  and
D. Bass
G.D. Stentiford*
Affiliation:
Pathology and Microbial Systematics Theme, Cefas Weymouth Laboratory, Weymouth, Dorset DT4 8UB, UK European Union Reference Laboratory for Crustacean Diseases, Cefas Weymouth Laboratory, Weymouth, Dorset DT4 8UB, UK
S. Ross
Affiliation:
Pathology and Microbial Systematics Theme, Cefas Weymouth Laboratory, Weymouth, Dorset DT4 8UB, UK European Union Reference Laboratory for Crustacean Diseases, Cefas Weymouth Laboratory, Weymouth, Dorset DT4 8UB, UK
D. Minardi
Affiliation:
Pathology and Microbial Systematics Theme, Cefas Weymouth Laboratory, Weymouth, Dorset DT4 8UB, UK European Union Reference Laboratory for Crustacean Diseases, Cefas Weymouth Laboratory, Weymouth, Dorset DT4 8UB, UK
S.W. Feist
Affiliation:
Pathology and Microbial Systematics Theme, Cefas Weymouth Laboratory, Weymouth, Dorset DT4 8UB, UK
K.S. Bateman
Affiliation:
Pathology and Microbial Systematics Theme, Cefas Weymouth Laboratory, Weymouth, Dorset DT4 8UB, UK European Union Reference Laboratory for Crustacean Diseases, Cefas Weymouth Laboratory, Weymouth, Dorset DT4 8UB, UK
P.A. Gainey
Affiliation:
Polwithen Road, Penryn TR10 8QT, Cornwall, UK
C. Troman
Affiliation:
Department of Life Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
D. Bass
Affiliation:
Pathology and Microbial Systematics Theme, Cefas Weymouth Laboratory, Weymouth, Dorset DT4 8UB, UK European Union Reference Laboratory for Crustacean Diseases, Cefas Weymouth Laboratory, Weymouth, Dorset DT4 8UB, UK Department of Life Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
*
Author for correspondence: G.D. Stentiford, E-mail: grant.stentiford@cefas.co.uk
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Abstract

Within aquatic habitats, the hyper-abundant Order Crustacea appear to be the predominant host group for members of the Phylum Microsporidia. The musculature, a common site of infection, provides access to biochemical (carbohydrate-rich) and physiological (mitochondria-rich) conditions conducive to prolific parasite replication and maturation. The significant proportion of body plan devoted to skeletal musculature in Crustacea provides the location for a highly efficient intracellular parasite factory. In this study, we utilize histological, ultrastructural and phylogenetic evidence to describe a previously known (Inodosporus octospora) and novel (Ovipleistophora arlo n. sp.) microsporidian parasites infecting the musculature of the common prawn (Palaemon serratus) from the same site, at the same time of year. Despite similar clinical signs of infection, both parasites are otherwise distinct in terms of pathogenesis, morphology and phylogeny. Based upon partial subunit ribosomal RNA (SSU rDNA) sequence, we show that that I. octospora may be identical to a Kabatana sp. previously described infecting two-spot goby (Gobiusculus flavescens) in Europe, or at least that Inodosporus and Kabatana genera are synonyms. In addition, SSU rDNA sequence for O. arlo places it within a distinct clade containing Ovipleistophora mirandellae and Ovipleistophora ovariae, both infecting the oocytes of freshwater fish in Europe. Taken together, our data provide strong evidence for trophic-transfer between crustacean and fish hosts for two different microsporidians within clade 5 of the phylum. Furthermore, it demonstrates that morphologically and phylogenetically distinct microsporidians can infect the same tissues of the same host species to impart clinical signs which mimic infection with the other.

Keywords

CrustaceaMicrosporidiamusclehistopathologyphylogenyultrastructure
Type
Research Article
Information
Parasitology , Volume 145 , Issue 8 , July 2018 , pp. 1105 - 1117
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Copyright
Copyright © Cambridge University Press 2017 

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References

Appeltans, W, Ahyong, ST, Anderson, G, Angel, MV, Artois, T, Bailly, N, Bamber, R, Barber, A, Bartsch, I, Berta, A, Błażewicz-Paszkowycz, M, Bock, P, Boxshall, G, Boyko, CB, Brandão, SN, Bray, RA, Bruce, NL, Cairns, SD, Chan, T-Y, Cheng, L, Collins, AG, Cribb, T, Curini-Galletti, M, Dahdouh-Guebas, F, Davie, PJF, Dawson, MN, De Clerck, O, Decock, W, De Grave, S, de Voogd, NJ, Domning, DP, Emig, CC, Erséus, C, Eschmeyer, W, Fauchald, K, Fautin, DG, Feist, SW, Fransen, CHJM, Furuya, H, Garcia-Alvarez, O, Gerken, S, Gibson, D, Gittenberger, A, Gofas, S, Gómez-Daglio, L, Gordon, DP, Guiry, MD, Hernandez, F, Hoeksema, BW, Hopcroft, RR, Jaume, D, Kirk, P, Koedam, N, Koenemann, S, Kolb, JB, Kristensen, RM, Kroh, A, Lambert, G, Lazarus, DB, Lemaitre, R, Longshaw, M, Lowry, J, Macpherson, E, Madin, LP, Mah, C, Mapstone, G, McLaughlin, PA, Mees, J, Meland, K, Messing, CG, Mills, CE, Molodtsova, TN, Mooi, R, Neuhaus, B, Ng, PKL, Nielsen, C, Norenburg, J, Opresko, DM, Osawa, M, Paulay, G, Perrin, W, Pilger, JF, Poore, GCB, Pugh, P, Read, GB, Reimer, JD, Rius, M, Rocha, RM, Saiz-Salinas, JI, Scarabino, V, Schierwater, B, Schmidt-Rhaesa, A, Schnabel, KE, Schotte, M, Schuchert, P, Schwabe, E, Segers, H, Self-Sullivan, C, Shenkar, N, Siegel, V, Sterrer, W, Stöhr, S, Swalla, B, Tasker, ML, Thuesen, EV, Timm, T, Todaro, MA, Turon, X, Tyler, S, Uetz, P, van der Land, J, Vanhoorne, B, van Ofwegen, LP, van Soest, RWM, Vanaverbeke, J, Walker-Smith, G, Walter, TC, Warren, A, Williams, GC, Wilson, SP, Costello, MJ (2012) The Magnitude of Global Marine Species Diversity. Current Biology 22, 2189–2202.CrossRefGoogle ScholarPubMed
Atkinson, A, Siegel, V, Pakhomov, EA, Jessopp, MJ and Loeb, V (2009) A re-appraisal of the total biomass and annual production of Antarctic krill. Deep Sea Research I 56, 727–740.Google Scholar
Azevedo, C, Corral, L and Vivares, CP (2000) Ultrastructure of the microsporidian Inodosporus octospora (Thelohaniidae), a parasite of the shrimp Palaemon serratus (Crustacea, Decapoda). Diseases of Aquatic Organisms 41, 151–158.Google Scholar
Balbiani, EG (1882) Sur les microsporidies ou psorospermies des Articulés. Comptes Rendus de l'Académie des Sciences Paris Series D 95, 1168–1171.Google Scholar
Barber, I, Davies, AJ, Ironside, JE, Forsgren, E and Amundsen, T (2009) First record of a Kabatana sp. microsporidium infecting fish in the Atlantic Ocean. Diseases of Aquatic Organisms 83, 145–152.Google Scholar
Barrento, S, Marques, A, Teixeira, B, Carvalho, ML, Vaz-Pires, P and Nunes, ML (2009) Influence of season and sex on the contents of minerals and trace elements in brown crab (Cancer pagurus, Linnaeus, 1758). Journal of Agriculture and Food Chemistry 57, 3253–3260.Google Scholar
Brown, WP, Selgeby, JH and Collins, HL (1998) Reproduction and early life history of ruffe (Gymnocephalus cernuus) in the St. Louis River, a Lake Superior tributary. Journal of Great Lakes Research 24, 217–227.Google Scholar
Casal, G, Matos, E, Rocha, S, Sindeaux-Neto, J, Al-Quraishy, S and Azevedo, C (2016) Ultrastructure and Phylogeny of Pleistophora beebei sp. nov. (Microsporidia) Infecting the Amazonian Teleostean Brachyhypopomus beebei (fam. Hypopomidae). Acta Protozoologica 55, 259–268.Google Scholar
Codreanu, R (1966) On the occurrence of spore or sporont appendages in the microsporidia and their taxonomic significance. In Corradetti, A (ed.). Proc. 1st International Congress of Parasitology, Roma. New York, Pergamon Press, pp. 602–603.Google Scholar
Codreanu, R, Codreanu-Balcescu, D and Porchet-Hennerb, E (1974) Caracteres ultrastructuraux dans la sporogenese d'une Microsporidie de type thelohanien parasite musculaire de la crevette Palaemon serratus des cotes de France. Comptes Rendus de l'Académie des Sciences 279, 2047–2049.Google Scholar
Collins, SP (1981) Littoral and Benthic Investigations on the West Coast of Ireland: XIII. The Biology of Gobiusculus flavescens (Fabricius) on the Connemara coast. Proceedings of the Royal Irish Academy B 81, 63–87.Google Scholar
Crawford, DL (1980) Meat yield and shell removal functions of shrimp processing. Oregon State University Extension, Marine Advisory Program. Special Report No. 597, 6p.Google Scholar
Fitt, BD, Huang, YJ, van den Bosch, F and West, JS (2006) Coexistence of related pathogen species on arable crops in space and time. Annual Reviews in Phytopathology 44, 163–182.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, 95–98.Google Scholar
Hamelin, FM, Bisson, A, Desprez-Loustau, ML, Fabre, F and Mailleret, L (2016) Temporal niche differentiation of parasites sharing the same plant host: oak powdery mildew as a case study. Ecosphere 7, 1–13.Google Scholar
Hardin, G (1960) The competitive exclusion principle. Science 131, 1292–1297.Google Scholar
Helfman, GS, Colette, BB and Facey, DE (1997) Fishes as Social Animals. Ch. 21: The Diversity of Fishes. UK: Blackwell. ISBN 0-86542-256-7.Google Scholar
Henneguy, F and Thelohan, P (1892) Myxosporidies parasites des muscles chez quelques crustaces decapodes. Annals of Micrographics 4, 617–641.Google Scholar
Hoese, DF (1998) Gobiidae. In Paxton, JR, Eschmeyer, WN (eds). Encyclopedia of Fishes. San Diego: Academic Press. pp. 218–222. ISBN 0-12-547665-5.Google Scholar
Katoh, K and Standley, DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.Google Scholar
Lodé, T (2012) ‘Oviparity or viviparity? That is the question…’. Reproductive Biology 12, 259–264.Google Scholar
Lom, J, Dyková, I and Tonguthai, K (2000) Kabatana gen. n., new name for the microsporidian genus Kabataia Lom, Dyková et Tonguthai, 1999. Folia Parasitologica 47, 78.CrossRefGoogle Scholar
Lom, J and Nilsen, F (2003) Fish microsporidia: fine structural diversity and phylogeny. International Journal for Parasitology 33, 107–127.Google Scholar
Lovy, J and Friend, SE (2017) Phylogeny and morphology of Ovipleistophora diplostomuri n. sp. (Microsporidia) with a unique dual-host tropism for bluegill sunfish and the digenean parasite Posthodiplostomum minimum (Strigeatida). Parasitology 144, 1898–1911.CrossRefGoogle Scholar
McGourty, KR, Kinziger, AP, Hendrickson, GL, Goldsmith, GH, Casal, G and Azevedo, C (2007) A new microsporidian infecting the musculature of the endangered tidewater goby (Gobiidae). Journal of Parasitology 93, 655–660.CrossRefGoogle ScholarPubMed
Miller, MA, 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 Nov. 2010,New Orleans, LA, pp 1–8.Google Scholar
Mills, CA (1981) The spawning of roach Rutilus rutilus (L.) in a chalk stream. Aquacultural Research 12, 49–54.CrossRefGoogle Scholar
Nylund, S, Nylund, A, Watanabe, K, Arnesen, CE and Karlsbank, E (2009) Paranucleospora theridion n. gen., n.sp. (Microsporidia, Enterocytozoonidae) with a life cycle in the salmon louse (Lepeophtheirus salmonis, Copepoda) and Atlantic salmon (Salmo salar). Journal of Eukaryotic Microbiology 57, 95–114.Google Scholar
Ødegaard, F (2000) How many species of arthropods? Erwin's estimate revised. Biological Journal of the Linnean Society 71, 583–597.Google Scholar
Olson, RE, Tiekotter, KL and Reno, PW (1994) Nadelspora canceri N. G., N. Sp., an unusual microsporidian parasite of the Dungeness crab, cancer magister. Journal of Eukaryotic Microbiology 41, 349–359.Google Scholar
Overstreet, RM and Weidner, EZF (1974) Differentiation of microsporidian spore-tails in Inodosporus spraguei gen. et sp. n. Parasitenkunde 44, 169.Google Scholar
Patzner, RA, Van Tassell, JL, Kovačiĉ, M and Kapoor, BG (eds) (2011) The biology of gobies. CRC Press Taylor and Francis Group & Science Publishers, Enfield.Google Scholar
Pekkarinen, M, Lom, J and Nilsen, F (2002) Ovipleistophora gen. n., a new genus for Pleistophora mirandellae-like microsporidia. Diseases of Aquatic Organisms 48, 133–142.Google Scholar
Pixell-Goodrich, HLM (1920) The spore of Thelohania. Archives of Zoology 59, 17–19.Google Scholar
Potts, G, Edwards, J and Costello, M (1990) The diet of the two-spot goby, Gobiusculus flavescens (Pisces). Journal of the Marine Biological Association, UK 70, 329–342.Google Scholar
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DL, Darling, A, Hohna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) Mrbayes 3·2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.Google Scholar
Sanders, JL, Lawrence, C, Nichols, DK, Brubaker, JF, Peterson, TS, Murray, KN and Kent, ML (2010) Pleistophora hyphessobryconis (Microsporidia) infecting zebrafish Danio rerio in research facilities. Diseases of Aquatic Organisms 91, 47–56.Google Scholar
Shao, B (1997) Nest association of pumpkinseed, Lepomis gibbosus, and golden shiner, Notemigonus crysoleucas. Environmental Biology and Fisheries 50, 41–48.Google Scholar
Small, HJ, Meyer, GR, Stentiford, GD, Dunham, JS, Bateman, KS and Shields, JD (2014) Ameson metacarcini n. sp. (Cryptomycota: Microsporidia) infecting the musculature of Dungeness crabs (Metacarcinus magister). Journal of Invertebrate Pathology 110, 213–225.Google 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, GD, Bateman, KS, Small, HJ, Moss, J, Shields, JD, Reece, KS and Tuck, I (2010) Myospora metanephrops (n. gn., 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, GD, Bateman, KS, Feist, SW, Stone, DM and Dunn, AM (2013a) Microsporidia: diverse, dynamic and emergent pathogens in aquatic systems. Trends in Parasitology 29, 567–578.Google Scholar
Stentiford, GD, Bateman, KB, Feist, SW, Chambers, E and Stone, DM (2013b) Plastic parasites: extreme dimorphism creates a taxonomic conundrum in the phylum Microsporidia. International Journal for Parasitology 43, 339–352.Google Scholar
Stentiford, GD, Feist, SW, Stone, DM, Peeler, EJ and Bass, D (2014) Policy, phylogeny and the parasite. Trends in Parasitology 30, 274–281.Google Scholar
Stentiford, GD, Ross, S and Kerr, R (2015) Paradoxium irvingi n.gn., n.sp. (Cryptomycota: Microsporidia) infecting the musculature of pink shrimp Pandalus montagui. Journal for Invertebrate Pathology 130, 1–8.Google Scholar
Stentiford, GD, Becnel, J, Weiss, L, Keeling, P, Didier, E, Williams, B, Bjornson, S, Kent, M, Freeman, MA, Brown, MJF, Troemel, E, Roesel, K, Sokolova, Y, Snowden, KF and Solter, L (2016a) Microsporidia – emergent pathogens in the global food chain. Trends in Parasitology 32, 336–348.Google Scholar
Stentiford, GD, Kerr, R, Bateman, KS, Feist, SW, Bass, D, Abollo Rodriguez, E, Ramilo, A and Villalba, A (2016b) Hyperspora aquatica n.gn., n. sp. (Microsporidia), hyperparasitic in Marteilia cochillia (Paramyxida), is closely related to crustacean-infecting microsporidian taxa. Parasitology 144, 186–199.Google Scholar
Summerfelt, RC (1964) A new microsporidian parasite from the golden shiner, Notemigonus crysoleucus. Transactions of the American Fisheries Society 93, 6–10.Google Scholar
Thompson, JN (1994) The Coevolutionary Process, University of Chicago Press, p. 9, ISBN 0-226-79760-0CrossRefGoogle Scholar
Turner, JT (2004) The importance of small planktonic copepods and their roles in pelagic marine food webs. Zoological Studies 43, 255–266.Google Scholar
Vaney, C and Conte, A (1901) Sur une nouvelle microsporidie, Pleistophora mirandellae, parasite de l’ovaire d’Alburnus mirandella Blanch. Comptes Rendus de l'Académie des Sciences Paris 133, 644–646.Google Scholar
Vávra, J and Lukeš, J (2013) Microsporidia and ‘the art of living together’. Advances in Parasitology 82, 253–319.Google Scholar
Vossbrinck, CR, Debrunner-Vossbrinck, BA and Weiss, LM (2014) Phylogeny of the microsporidia. In Weiss, LM and Becnel, JJ (eds). Microsporidia: Pathogens of Opportunity, 1st edn. Chichester, UK: John Wiley & Sons, Inc. doi: 10.1002/9781118395264.ch6Google Scholar
Zhang, ZQ (2011) Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness – Phylum Arthropoda von Siebold, 1848. Zootaxa 4138, 99–103.Google Scholar