How Does the Dinoflagellate Parasite Outsmart the Immune System of Its Crustacean Hosts?

1. Chatton É, Poisson R. Sur l’existence dans le sang des crabs, de péridiniens parasites: Hematodinium perezi n. g., n. sp. (Syndinidae). C R Séances Soc Biol. 1931;105 : 553–557. doi: 10.1039/c4sm01112k 25115726

2. Meyers TR, Koeneman TM, Botelho C, Short S. Bitter crab disease: a fatal dinoflagellate infection and marketing problem for Alaskan Tanner crabs Chionoecetes bairdi. Dis Aquat Org. 1987;3 : 195–216.

3. Messick GA. Hematodinium perezi infections in adult and juvenile blue crabs Callinectes sapidus from coastal bays of Maryland and Virginia, USA. Dis Aquat Org. 1994;19 : 77–82.

4. Latrouite D, Morizur T, Nöel P, Chagot D, Wilhelm G. Mortalite du tourteau Cancer pagurus provoquee par le dinoflagellate parasite: Hematodinium sp. Conseil Int. pour L’Exploration de la Mer. CM. 1988/K:32.

5. Field RH, Chapman CJ, Taylor AC, Neil DM, Vickerman K. Infection of the Norway lobster Nephrops norvegicus by a Hematodinium-like species of dinofiagellate on the west coast of Scotland. Dis Aquat Org. 1992;13 : 1–15.

6. Stentiford GD, Green M, Bateman K, Small HJ, Neil DM, Feist SW. Infection by a Hematodinium-like parasitic dinoflagellate causes Pink Crab Disease (PCD) in the edible crab Cancer pagurus. J Invertebr Pathol. 2002;79 : 179–191. 12133707

7. Smith AL, Hirschle L, Vogan C., Rowley AF. Parasitisation of juvenile edible crabs (Cancer pagurus) by the dinoflagellate, Hematodinium sp.: pathobiology, seasonality and its potential effects on commercial fisheries. Parasitology 2015; 142 : 428–438. doi: 10.1017/S0031182014001255 25118672

8. Hudson DA, Shields JD. Hematodinium australis n. sp., a parasitic dinoflagellate of the sand crab Portunus pelagicus from Moreton Bay, Australia. Dis Aquat Org. 1994;19 : 109–119.

9. Xu WJ, Shi H, Xu HX, Small HJ. Preliminary study on the Hematodinium infection in cultured Portunus triberculatus. Acta Hydrobiol Sin. 2007;31 : 640–647.

10. Stentiford GD, Shields JD. A review of the parasitic dinoflagellates Hematodinium species and Hematodinium-like infections in marine crustaceans. Dis Aquat Org. 2005;66 : 47–70. 16175968

11. Small HJ. Advances in our understanding of the global diversity and distribution of Hematodinium spp.—significant pathogens of commercially exploited crustaceans. J Invertebr Pathol. 2012;110 : 234–246. doi: 10.1016/j.jip.2012.03.012 22433998

12. Lee RF, Frischer ME. The decline of the blue crab. Amer Scientist 2004;92 : 548–553.

13. Wilhelm G, Mialhe E. Dinoflagellate infection associated with the decline of Necora puber crab populations in France. Dis Aquat Org. 1996;26 : 213–219.

14. Xu WJ, Xie J, Shi H, Li C. Hematodinium infections in cultured ridgetail white prawns, Exopalaemon carinicauda, in eastern China. Aquaculture 2010;300 : 25–31.

15. Li C, Song S, Liu Y, Chen T. Hematodinium infections in cultured Chinese swimming crab, Portunus trituberculatus in northern China. Aquaculture 2013;396–399 : 59–65.

16. Pagenkopp Lohan KM, Small HJ, Shields JD, Place AR, Reece K. Conservation of the first internal transcribed spacer (ITS1) region of Hematodinium perezi (genotype III) from Callinectes sapidus. Dis Aquat Org. 2013;103 : 65–75. doi: 10.3354/dao02559 23482386

17. Small HJ, Shields JD, Reece KS, Bateman K, Stentiford GD. Morphological and molecular characterization of Hematodinium perezi (Dinophyceae: Syndininiales), a dinoflagellete parasite of the harbour crab, Liocarcinus depurator. J Eukaryot Microbiol. 2012;59 : 54–66. doi: 10.1111/j.1550-7408.2011.00592.x 22092696

18. Shields JD, Taylor DM, Sutton SG, O’Keefe PG, Ings D, Pardy AL. Epidemiology of bitter crab disease (Hematodinium sp.) in snow crabs Chionoecetes opilio from Newfoundland, Canada. Dis Aquat Org. 2005;64 : 253–264. 15997824

19. Shields JD, Taylor DM, O’Keefe PG, Colbourne E, Hynick E. Epidemiological determinants in outbreaks of bitter crab disease (Hematodinium sp.) in snow crabs Chionoecetes opilio from Conception Bay, Newfoundland, Canada. Dis Aquat Org. 2007;77 : 61–72. 17933398

20. Shields JD, Squyars CM. Mortality and hematology of blue crabs, Callinectes sapidus, experimentally infected with the parasitic dinoflagellate Hematodinium perezi. Fish Bull. 2000;98 : 139–152.

21. Stentiford GD, Neil DM. A rapid onset, post-capture muscle necrosis in Norway lobster, Nephrops norvegicus (L.) from the west coast of Scotland, United Kingdom. J Fish Dis. 2000;23 : 251–264.

22. Shields JD, Scanlon C, Volety A. Aspects of the pathophysiology of blue crabs, Callinectes sapidus, infected with the parasitic dinoflagellate Hematodinium perezi. Bull Mar Sci. 2003;72 : 519–535.

23. Coates C, Nairn J. Diverse immune functions of hemocyanins. Dev Comp Immunol, 2014;45 : 43–55. doi: 10.1016/j.dci.2014.01.021 24486681

24. Butler MJ IV, Tiggelaar JM II, Shields JD, Butler MJ V. Effects of the parasitic dinoflagellate Hematodinium perezi on blue crab (Callinectes sapidus) behavior and predation. J Exp Mar Biol Ecol. 2014;461 : 381–388.

25. Stentiford GD, Neil DM, Albalat A, Milligan RJ, Bailey N. The effect of parasitic infection by Hematodinium sp. on escape swimming and subsequent recovery in the Norway lobster, Nephrops norvegicus (L.). J Crust Biol. 2015 (in press)

26. Cerenius L, Jiravanichpaisal P, Liu H-p, Söderhäll I. Crustacean Immunity In: Söderhäll K, editor. Invertebrate Immunity, Landes Bioscience; 2010. pp. 239–259.

27. Rowley AF, Powell A. Invertebrate immune systems: specific, quasi-specific or nonspecific? J Immunol. 2007;179 : 7209–7214. 18025161

28. Stentiford GD, Evans M, Bateman K, Feist SW. Co-infection by a yeast-like organism in Hematodinium-infected European edible crabs Cancer pagurus and velvet swimming crabs Necora puber from the English Channel. Dis Aquat Org. 2003;54 : 195–202. 12803383

29. Stentiford GD. Diseases of the European edible crab (Cancer pagurus): a review. ICES J Mar Sci. 2008;65 : 1578–1592.

30. Smith AL, Whitten MMA, Hirschle L, Pope EC, Wootton EC, Vogan CL, et al. Bacterial septicaemia in prerecruit edible crabs, Cancer pagurus L. J Fish Dis. 2014;37 : 729–737. doi: 10.1111/jfd.12163 23962351

31. Wheeler K, Shields JD, Taylor DM. Pathology of Hematodinium infections in snow crabs (Chionoecetes opilio) from Newfoundland, Canada. J Invertebr Pathol. 2007;95 : 93–100. 17336326

32. Field RH, Appleton PL. A Hematodinium-like dinoflagellate infection of the Norway lobster Nephrops norvegicus: observations on pathology and progression of infection. Dis Aquat Org. 1995;22 : 115–128.

33. Smith AL, Hamilton KM, Hirschle L, Wootton EC, Vogan CL, Pope EC, et al. Characterization and molecular epidemiology of a fungal infection of edible crabs (Cancer pagurus) and interaction of the fungus with the dinoflagellate parasite Hematodinium. Appl Env Microbiol. 2013;79 : 783–793.

34. Li M, Li C, Wang J, Song S. Immune response and gene expression in hemocytes of Portunus trituberculatus inoculated with the parasitic dinoflagellate Hematodinium. Mol Immunol. 2015;65 : 113–122. doi: 10.1016/j.molimm.2015.01.002 25659082

35. Marois E. The multifaceted mosquito anti-Plasmodium response. Curr Opin Microbiol. 2011;14 : 429–435. doi: 10.1016/j.mib.2011.07.016 21802348

36. Molina-Cruz A, Garver LS, Alabaster A, Bangiolo L. Haile A, Winikor J, et al. The human malaria parasite Pfs47 gene mediates evasion of the mosquito immune system. Science 2013;340 : 984–987. doi: 10.1126/science.1235264 23661646

37. Yoshino TP, Wu X-J, Gonzale L.A, Hooke CH. Circulating Biomphalaria glabrata hemocyte subpopulations possess shared schistosome glycans and receptors capable of binding larval glycoconjugates. Exp Parasitol. 2013;133 : 28–36. doi: 10.1016/j.exppara.2012.10.002 23085445

38. Yoshino TP, Wu X-J, Liu H, Gonzalez LA, Deelder AM, Hokke CH. Glycotope sharing between snail hemolymph and larval schistosomes: larval transformation products alter shared glycan patterns of plasma proteins. PLoS Negl Trop Dis. 2012;6: e1569. doi: 10.1371/journal.pntd.0001569 22448293

39. Kawasaki M, Delamare-Deboutteville J, Dang C, Barnes AC. Hemiuroid trematode sporocysts are undetected by hemocytes of the intermediate host, the ark cockle Anadara trapezia: potential role of surface carbohydrates in successful parasitism. Fish Shellfish Immunol. 2013;35 : 1937–1947. doi: 10.1016/j.fsi.2013.09.040 24161777

40. Hoppes JH. Effects of the dinoflagellate parasite Hematodinium sp. on the immune response of its crustacean hosts. PhD thesis, University of Southampton, U.K., 2011.

41. Small HJ, Shields JD, Neil DM, Taylor AC, Coombs GH. Differences in enzyme activities between two species of Hematodinium, parasitic dinoflagellates of crustaceans. J Invertebr Pathol. 2007;94 : 175–183. 17156792

42. Shumway SE. A review of the effects of algal blooms on shellfish and aquaculture. J World Aquac Soc. 1990;21 : 65–104.

43. Mello DF, de Oliveira ES, Vieira RC, Simoes E, Trevisan R, Liuz Dafre A, et al. Cellular and transcriptional responses of Crassostrea gigas hemocytes exposed in vitro to bevetoxin (PbTx-2). Mar Drugs 2012;10 : 583–597. doi: 10.3390/md10030583 22611355