Hematodinium sp. and its bacteria-like endosymbiont in European brown shrimp (Crangon crangon)
Tóm tắt
Parasitic dinoflagellates of the genus Hematodinium are significant pathogens affecting the global decapod crustacean fishery. Despite this, considerable knowledge gaps exist regarding the life history of the pathogen in vivo, and the role of free living life stages in transmission to naïve hosts. In this study, we describe a novel disease in European brown shrimp (Crangon crangon) caused by infection with a parasitic dinoflagellate of the genus Hematodinium. This is the second example host within the Infraorder Caridea (shrimp) and significantly, the first description within the superfamily Crangonoidea. Based upon analysis of the rRNA gene (SSU) and spacers (ITS1), the parasite in C. crangon is the same as that previously described infecting Nephrops norvegicus and Cancer pagurus from European seas, and to the parasite infecting several other commercially important crab species in the Northern Hemisphere. The parasite is however distinct from the type species, H. perezi, found infecting type hosts (Carcinus maenas and Liocarcinus depurator) from nearby sites within Europe. Despite these similarities, the current study has also described for the first time, a bacteria-like endosymbiont within dinospore stages of the parasite infecting shrimp. The endosymbionts were either contained individually within electron lucent vacuoles within the parasite cell cytoplasm, or remained in direct contact with the parasite cytoplasm or in some cases, the nucleoplasm. In all of these cases, no apparent detrimental effects of colonization were observed within the parasite cell. The presence of bacteria-like endosymbionts within dinospore life stages presumes that the relationship between the dinoflagellate and the bacteria is extended beyond the period of liberation of spores from the infected host shrimp. In this context, a potential role of endosymbiosis in the survival of free-living stages of the parasite is possible. The finding offers a further intriguing insight into the life history of this enigmatic pathogen of marine crustacean hosts and highlights a potential for mixotrophy in the parasitic dinoflagellates contained within the genus Hematodinium.
Tài liệu tham khảo
Small HJ: Advances in our understanding of the global diversity and distribution of Hematodinium spp. – Significant pathogens of commercially exploited crustaceans. J Invert Pathol. 2012, 110: 234-246. 10.1016/j.jip.2012.03.012.
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.
Morado JF: Protistan diseases of commercially important crabs: A review. J Invertebr Pathol. 2011, 106: 27-53. 10.1016/j.jip.2010.09.014.
Xu W-J, Xie J, Shi H, Li C: Hematodinium infections in cultured ridgetail white prawns, Exopalaemon carinicauda, in eastern China. Aquaculture. 2010, 300: 25-31. 10.1016/j.aquaculture.2009.12.024.
Xu W-J, Shi H, Xu H-X, Small HJ: Preliminary study on the Hematodinium infection in cultured Portunus trituberculatus. Acta Hydrobiol Sin. 2007, 31: 640-647.
Li YY, Xia XA, Wu QY, Liu WH, Lin YS: Infection with Hematodinium sp. in mud crabs Scylla serrata cultured in low salinity water in southern China. Dis Aquat Org. 2008, 82: 145-150.
Eigemann F, Burmeister A, Skovgaard A: Hematodinium sp. (Alveolata, Syndinea) detected in marine decapod crustaceans from waters of Denmark and Greenland. Dis Aquat Org. 2010, 92: 59-68. 10.3354/dao02257.
Pagenkopp Lohan KM, Reece KS, Miller TL, Wheeler KN, Small HJ, Shields JD: The role of alternate hosts in the ecology and life history of Hematodinium sp. a parasitic dinoflagellate of the blue crab (Callinectes sapidus). J Parasitol. 2012, 98: 73-84. 10.1645/GE-2854.1.
Johnson PT: Parasites of benthic amphipods: dinoflagellates (Duboscquodinida: Syndinidae). Fish Bull. 1986, 84: 605-614.
Small HJ, Neil DM, Taylor AC, Atkinson RJA, Coombs GH: Molecular detection of Hematodinium spp. in Norway lobsters, Nephrops norvegicus, and other crustaceans. Dis Aquat Org. 2006, 69: 18-195.
Small HJ, Reece KS, Shields JD, Bateman K, Stentiford GD: Morphological and molecular characterization of Hematodinium perezi (Dinophyceae: Syndiniales), a dinoflagellate parasite of the harbour crab, Liocarcinus depurator. J Eukaryot Microbiol. 2012, 59: 54-66. 10.1111/j.1550-7408.2011.00592.x.
Hudson DA, Adlard RD: Nucleotide sequence determination of the partial SSU rDNA gene and ITS1 region of Hematodinium cf. perezi and Hematodinium-like dinoflagellates. Dis Aquat Org. 1996, 24: 55-60.
Jensen PC, Califf K, Lowe V, Hauser L, Morado JF: Molecular detection of Hematodinium sp. in Northeast Pacific Chionoecetes spp. and evidence of two species in the Northern Hemisphere. Dis Aquat Org. 2010, 89: 15-166.
Small HJ, Shields JD, Hudson KL, Reece KS: Molecular detection of Hematodinium sp. infecting the blue crab Callinectes sapidus. J Shellfish Res. 2007a, 26: 131-139. 10.2983/0730-8000(2007)26[131:MDOHSI]2.0.CO;2.
Field RH, Chapman CJ, Taylor AC, Neil DM, Vickerman K: Infection of the Norway lobster Nephrops norvegicus by a Hematodinium-like species of dinoflagellate on the West Coast of Scotland. Dis Aquat Org. 1992, 13: 1-15.
Latrouite D, Morizur Y, Noël P, Chagot D, Wilhelm G: Mortalite du tourteau Cancer pagurus provoquee par le dinoflagelle parasite: Hematodinium sp. Conseil International pour l’Exploration de la Mer, CM. 1988, 32:
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. 10.1016/S0022-2011(02)00028-9.
Stentiford GD, Bateman K, Feist SW: Pathology and ultrastructure of an intranuclear bacilliform virus (IBV) infecting brown shrimp Crangon crangon (Decapoda: Crangonidae). Dis Aquat Org. 2004, 58: 89-87.
Stentiford GD, Feist SW: A histopathological survey of shore crab (Carcinus maenas) and brown shrimp (Crangon crangon) from six estuaries in the United Kingdom. J Invertebr Pathol. 2005, 88: 136-146. 10.1016/j.jip.2005.01.006.
Small HJ, Shields JD, Moss JA, Reece KS: Conservation in the first internal transcribed spacer region (ITS1) in Hematodinium species infecting crustacean hosts found in the UK and Newfoundland. Dis Aquat Org. 2007, 75: 251-258.
Hamilton KM, Morritt D, Shaw PW: Genetic diversity of the crustacean parasite Hematodinium (Alveolata, Syndinea). Eur J Protistol. 2010, 46: 17-28. 10.1016/j.ejop.2009.10.002.
Stentiford GD, Neil DM, Peeler EJ, Shields JD, Small HJ, Flegel TW, Vlak JM, Jones B, Morado F, Moss S, Lotz J, Bartholomay L, Behringer DC, Hauton C, Lightner DV: Disease will limit future food supply from the global crustacean fishery and aquaculture sectors. J Invert Pathol. 2012, 110: 141-157. 10.1016/j.jip.2012.03.013.
Hamilton KM, Morritt D, Shaw PW: Molecular and histological identification of the crustacean parasite Hematodinium (Alveolata, Syndinea) in the shore crab Carcinus maenas. Acta Protozool. 2007, 46: 183-192.
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.
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.
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.
Stentiford GD, Neil DM: Diseases of Nephrops and Metanephrops: a review. J Invertebr Pathol. 2011, 106: 92-109. 10.1016/j.jip.2010.09.017.
Frischer ME, Lee RF, Sheppard MA, Mauer A, Rambow F, Neumann M, Brofft JE, Wizenmann T, Danforth JM: Evidence for a free-living life stage of the blue crab parasitic dinoflagellate, Hematodinium sp. Harmful Algae. 2006, 5: 548-557. 10.1016/j.hal.2005.11.002.
Nowack ECM, Melkonian M: Endosymbiotic associations within protists. Phil Trans R Soc B. 2010, 365: 699-712. 10.1098/rstb.2009.0188.
Tomas RN, Cox ER: Observations on the symbiosis of Perktinium balticum and its intracellular alga I. Ultrastructure. J. Phycol. 1973, 9: 304-323.
Wilcox LW, Wedemayer GJ: Gymnodinium acidotum Nygaard (Pyrrophyta), a dinoflagellate with an endosymbiotic cryptomonad. J. Phycol. 1984, 20: 236-242. 10.1111/j.0022-3646.1984.00236.x.
Wilcox LW: Prokaryotic endosymbionts in the chloroplast stroma of the dinoflagellate Woloszynskia pascheri. Protoplasma. 1986, 135: 71-79. 10.1007/BF01277000.
Silva ES: Endonuclear bacteria in two species of dinoflagellates. Protistologica. 1978, 14: 113-119.
Schweikert M, Meyer B: Characterization of intracellular bacteria in the freshwater dinoflagellate Peridinium cincture. Protoplasma. 2001, 217: 177-184. 10.1007/BF01283398.
Stoecker DK: Mixotrophy among dinoflagellates. J Eukary Microbiol. 1999, 46: 397-401. 10.1111/j.1550-7408.1999.tb04619.x.
Gachon CMM, Telesphore S-N, Strittmatter M, Chambouvet A, Kim GH: Algal diseases: spotlight on a black box. Trends Plant Sci. 2010, 15: 633-640. 10.1016/j.tplants.2010.08.005.
Kim D, Kim JF, Yim JH, Kwon SK, Lee CH, Lee HK: Red to red - the marine bacterium Hahella chejuensis and its product prodigiosin for mitigation of harmful algal blooms. J Microbiol Biotechnol. 2008, 18: 1621-1629.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol. 1990, 215: 403-410.