In the eastern Gulf of Mexico, off the coast of Florida, grey snapper, Lutjanus griseus was found to be infected with the myxozoan parasite Sphaerospora motemarini n. sp., with high prevalence (83%) and intensity of infection occuring in age-0 fish, and with parasite levels decreasing with age (age-1 snapper 40%; age-2 snapper 0%). The morphological, molecular and phylogenetic characterisation of the myxozoan showed that it is a member of the typically marine, polysporoplasmid Sphaerospora spp. which form a subclade within the Sphaerospora sensu stricto clade of myxozoans, which is characterised by large expansion segments in their SSU rDNA sequences. Presporogonic stages of S. motemarini n. sp. were detected in the blood, using PCR. Pseudoplasmodia and spores were found to develop in the renal corpuscles of the host, causing their massive expansion. Macroscopic and histopathological changes were observed in age-0 fish and show that S. motemarini n. sp. causes severe glomerulonephritis in L. griseus leading to a compromised host condition, which makes it more susceptible to stress (catch-and-release, predators, water quality) and can result in mortalities. These results are discussed in relation to the exploitation of grey snapper populations by commercial and recreational fisheries and with the observed increased mortalities with temperature along the coast of Florida. In the future, we would like to determine prevalence and intensity of infection with S. motemarini n. sp. in juvenile L. griseus in different areas of the Gulf of Mexico in order to be able to estimate the temperature dependence of S. motemarini n. sp. proliferation and to be able to predict its distribution and severity during climatic changes in the Gulf.

Institute of Parasitology Biology Centre of the Academy of Sciences of the Czech Republic Branišovská 31 37005 České Budějovice Czech Republic

Institute of Parasitology Biology Centre of the Academy of Sciences of the Czech Republic Branišovská 31 37005 České Budějovice Czech Republic ; Faculty of Science University of South Bohemia Branišovská 31 37005 České Budějovice Czech Republic

Mote Marine Laboratory 1600 Ken Thompson Parkway Sarasota FL 34236 USA

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Alama-Bermejo G., Cuadrado M., Raga J.A., Holzer A.S. Morphological and molecular re-description of the myxozoan Unicapsula pflugfelderi Schubert et al., 1975 from two teleost hosts in the Mediterranean. A review of the genus Unicapsula Davis, 1924. J. Fish Dis. 2009;32:335–350. PubMed

Allman J.A., Grimes C.B. Temporal and spatial dynamics of spawning, settlement, and growth of gray snapper (Lutjanus griseus) from the West Florida shelf as determined from otholith microstructures. Fish. Bull. 2002;100:391–403.

Arthur R., Lom J. A guideline for the preparation of species descriptions in Myxosporea. J. Fish Dis. 1989;12:151–156.

Asahida T., Kobayashi T., Saitoh K., Nakayama I. Tissue preservation and total DNA extraction from fish stored at ambient temperature using buffers containing high concentration of urea. Fish. Sci. 1996;62:727–730.

Ault, J.S., Smith, S.G., Mester, G.A., Lou, J., Bohnsack, J.A., Miller, S.L., 2002. Baseline multispecies coral reef fish stock assessment for Dry Tortugas. NOAA Technical Memorandum, NMFS-SEFSC-487. <http://bonefish.rsmas.miami.edu/femar/Publications/487techmemo_tortugas.pdf>.

Ault J.S., Smith S.G., Bohnsack J.A. Evaluation of average length as an estimator of exploitation status for the Florida coral-reef fish community. J. Mar. Sci. 2005;62:417–423.

Barta J.R., Martin D.S., Liberator P.A., Dashkevicz M., Anderson J.W., Feighner S.D., Elbrecht A., Perkins-Barrow A., Jenkins M.C., Danforth H.D., Ruff M.D., Profous-Juchelka H. Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. J. Parasitol. 1997;83:262–271. PubMed

Bartholomew A., Bohnsack J.A. A review of catch-and-release angling mortality with implications for no-take reserves. Rev. Fish Biol. Fish. 2005;15:129–154.

Bartošová, P., Fiala, I., Cinková, M., Jirků, M., Caffara, M., Fioravanti, M.L., Atkinson, S., Bartholomew, J., Holzer, A.S., Sphaerospora sensu stricto: taxonomy, diversity and evolution of a unique lineage of myxosporeans (Myxozoa). Mol. Phylogenet. Evol., in press. 10.1016/j.ympev.2013.02.026. PubMed DOI

Baska F., Molnár K. Blood stages of Sphaerospora spp. (Myxosporea) in cyprinid fishes. Dis. Aquat. Org. 1988;5:23–28.

Burton M.L. Age, growth, and mortality of gray snapper, Lutjanus griseus, from the east coast of Florida. Fish. Bull. 2001;99:254–365.

Coleman F.C., Koenig C.C., Eklund A.M., Gries C.B. Management and conservation of temperate reef fishes in the grouper–snapper complex of the southeastern United States. Am. Fish. Soc. Symp. 1999;23:233–242.

Diamant A., Whipps C.M., Kent M.L. A new species of Sphaeromyxa (Myxosporea: Sphaeromyxina: Sphaeromyxidae) in devil firefish, Pterois miles (Scorpaenidae), from the northern Red Sea: morphology, ultrastructure, and phylogeny. J. Parasitol. 2004;90:1434–1442. PubMed

Domeier M.L., Colin P.L. Tropical reef fish spawning aggregations: defined and reviewed. Bull. Mar. Sci. 1997;60:698–726.

Eszterbauer, E., Sipos, D., Forró, B., Bartošová, P., Holzer, A.S. in press. Molecular characterization of Sphaerospora molnari (Myxozoa), the agent of gill sphaerosporosis in common carp (Cyprinus carpio carpio). Dis. Aquat. Org. PubMed

Faunce C.H., Serafy J.E. Nearshore habitat use by gray snapper (Lutjanus griseus) and bluestriped grunt (Haemulon sciurus): environmental gradients and ontogenetic shifts. Bull. Mar. Sci. 2007;80:473–597.

Ferguson H.W. The effects of water temperature on the development of proliferative kidney disease in rainbow trout, Salmo gairdneri Richardson. J. Fish Dis. 1981;4:175–177.

Fischer A.J., Baker M.S., Jr., Wilson C.A., Nieland D.L. Age, growth, mortality, and radiometric age validation of gray snapper (Lutjanus griseus) from Louisiana. Fish. Bull. 2005;103:307–319.

Foott J.S., Hedrick R.P. Seasonal occurrence of the infectious stage of proliferative kidney disease (PKD) and resistance of rainbow trout, Salmo gairdneri Richardson, to reinfection. J. Fish. Biol. 1987;30:477–483.

Gold J.R., Saillant E., Ebelt N.D., Lem S. Conservation genetics of Gray Snapper (Lutjanus griseus) in U.S. waters of the Northern Gulf of Mexico and Western Atlantic Ocean. Copeia. 2009;2:277–286.

Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 1999;41:95–98.

Hallett S.L., Atkinson S.D., El-Matbouli M. Molecular characterisation of two aurantiactinomyxon (Myxozoa) phenotypes reveals one genotype. J. Fish Dis. 2002;25:627–631.

Holland J.W., Okamura B., Hartikainen H., Secombes C.J. A novel minicollagen gene links cnidarians and myxozoans. Proc. Royal Soc. B – Biol. Sci. 2011;278:546–553. PubMed PMC

Holzer A.S., Sommerville C., Wootten R. Molecular relationships and phylogeny in a community of myxosporeans and actinosporeans based on their 18S rDNA sequences. Int. J. Parasitol. 2004;34:1099–1111. PubMed

Jirků M., Fiala I., Modrý D. Tracing the genus Sphaerospora: rediscovery, redescription and phylogeny of Sphaerospora ranae (Morelle, 1929) n. comb. (Myxosporea, Sphaerosporidae), with emendation of the genus Sphaerospora. Parasitology. 2007;134:1727–1739. PubMed

Jones D.L., Walter J.F., Brooks E.N., Serafy J.E. Connectivity through ontogeny: fish population linkages among mangrove and coral reef habitats. Mar. Ecol. Prog. Ser. 2010;401:245–258.

Kent M.L., Khattra J., Hervio D.M.L., Devlin R.H. Ribosomal DNA sequence analysis of isolates of the PKX myxosporean and their relationship to members of the genus Sphaerospora. J. Aquat. Anim. Health. 1998;10:12–21.

Lom J., Dyková I. Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Fol. Parasitol. 2006;53:1–36. PubMed

Manooch C.S., III, Matheson R.H., III Age, growth and mortality of gray snapper collected from Florida waters. Proc. Southeast Ass. Fish Wildlife Ag. 1981;35:331–344.

McGeorge J., Sommerville C., Wootten R. Epizootiology of Sphaerospora truttae (Myxozoa: Myxosporea) infections in Atlantic salmon Salmo salar at freshwater smolt producing hatcheries in Scotland. Dis. Aquat. Org. 1996;26:33–41.

NMFS (National Marine Fisheries Service), 2012. Annual Commercial landings Query: Gray Snapper (1980–2010, Atlantic and Gulf by state). NOAA Fisheries: Office of Science and Technology. Online at: <http://www.st.nmfs.noa.gov/st1/commercial/>.

Odening K., Walter G., Bockhardt I. Zur jahreszeithchen Dynamik von Sphaerospora renicola (Myxosporidia) beim Karpfen (Osteichthyes) Angew. Parasitol. 1988;29:65–80. PubMed

Palenzuela O., Álvarez-Pellitero P., Sitjà-Bobadilla A. Glomerular disease associated with Polysporoplasma sparis (Myxozoa) infections in cultured gilthead sea bream, Sparus aurata L. (Pisces: Teleostei) Parasitology. 1999;118:245–256. PubMed

Rambaut, A., Drummond, A.J., 2007. Tracer v1.4, <http://beast.bio.ed.ac.uk/Tracer>.

Ray R.A., Holt R.A., Bartholomew J.L. Relationship between temperature and Ceratomyxa shasta-induced mortality in Klamath River salmonids. J. Parasitol. 2012;98:520–526. PubMed

Redondo M.J., Palenzuela O., Riaza A., Macias A., Alvarez-Pellitero P. Experimental transmission of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of turbot Scophthalmus maximus. J. Parasitol. 2002;88:482–488. PubMed

Robins C.R., Ray F.C., Douglas J., Freund R. Houghton Mifflin Company; Boston, MA: 1986. A Field Guide to Atlantic Coast Fishes. p. 345.

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

Sitjà-Bobadilla A., Álvarez-Pellitero P. Revised classification and key species of the genus Sphaerospora Davies, 1917 (Protozoa: Myxosporea) Res. Rev. Parasitol. 1994;54:67–80.

Sitjà-Bobadilla A., Álvarez-Pellitero P. Light and electron microscopic description of Polysporoplasma n. g. (Myxosporea: Bivalvulida), Polysporoplasma sparis n. sp. from Sparus aurata (L.), and Polysporoplasma mugilis n. sp. from Liza aurata L. Eur. J. Protistol. 1995;31:77–89.

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

Supamattaya K., Fischer-Scherl T., Hoffmann R.W., Boonyaratpalin S. Light and electron microscope observations on presporogonic and sporogonic stages of Sphaerospora epinepheli (Myxosporea) in grouper (Epinephelus malabaricus) J. Eukaryot. Microbiol. 1993;40:71–80. PubMed

Swofford, D.L., 2001. PAUP∗: Phylogenetic Analysis Using Parsimony (∗and other methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.

Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The ClustalX Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997;24:4876–4882. PubMed PMC

Tolan J.M., Fisher M. Biological response to changes in climate patterns: population increases of gray snapper (Lutjanus griseus) in Texas bays and estuaries. Fish. Bull. 2009;107:36–44.

Tops S., Lockwood W., Okamura B. Temperature-driven proliferation of Tetracapsuloides bryosalmonae in bryozoan hosts portends salmonid declines. Dis. Aquat. Org. 2006;70:227–236. PubMed

Whaley S.D., Burd J.J., Jr., Robertson B.A. Using estuarine landscape structure to model distribution patterns in nekton communities and in juveniles of fishery species. Mar. Ecol. Prog. Ser. 2007;330:83–99.

Yasuda H., Ooyama T., Iwata K., Tun T., Yokoyama H., Ogawa K. Fish-to-fish transmission of Myxidium spp. (Myxozoa) in cultured tiger puffer suffering from emaciation disease. Fish Pathol. 2002;37:29–33.

Biodiversity and host-parasite cophylogeny of Sphaerospora (sensu stricto) (Cnidaria: Myxozoa)