Abstract
A series of mass mortalities of the cultured blood clam, Tegillarca granosa, occurred in the Yueqing Bay of China from 2005 to 2009. An obligate intracellular prokaryote, designated as rickettsia-like organism (RLO), was frequently found in the moribund or dead blood clam sample during ultrastructural examination. These organisms were usually round, ellipsoid or occasionally dumbbell-shaped, ranged from approximately 0.28 to 0.71 µm in size and had a trilaminar cell wall. Two reproductive modes of organisms, transverse binary fission and budding, were observed. The organisms were able to form eosinophilic inclusions. Most inclusions were found within epithelial and connective tissues of the mantle, gills and digestive tube. The biological and morphological characteristics indicate that these organisms may belong to the family Rickettsiaceae. RLOs exhibited significant pathogenicity. Cytopathological examinations revealed extensive necrosis and destruction in the infected cell. The degree of tissue destruction was positively related to the number of RLO inclusions in the tissues, and the cytopathological effects were positively related to the number of intracellular RLO. RLOs and their inclusions were discovered throughout different disease areas and in different time periods. The infection intensity of the RLOs was positively correlated with the mortality rate of clams. Therefore, RLO infection might be associated with mass mortalities of cultured blood clams in the Yueqing Bay.
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Anderson I G, Shariff M, Nash G, et al. 1987. Mortalities of juvenile shrimp, Penaeus monodon, associated with Penaeus monodon baculovirus, cytoplasmic reo-like virus, and rickettsial and bacterial infections from Malaysian brackish water ponds. Asian Fisheries Science, 1: 47–64
Azevedo C, Mendonca I, Matos Edilson. 2005. Ultrastructural analysis of rickettsia-like organisms in the oyster Crassostrea rizophorae from the northeastern Atlantic coast of Brazil. Braz J Microphol Sci, 22: 5–8
Bower S M, Meyer G R, Boutillier J A. 1996. Stained prawn disease (SPD) of Pandalus platyceros in British Columbia, Canada, caused by a rickettsial infection. Dis Aquat Org, 24: 41–54
Carces L H, Larenas J J, Smith P A, et al. 1991. Infectivity of a rickettsia isolated from coho salmon Oncorhynchus kisutch. Dis Aquat Org, 11: 93–97
Chen S C, Wang P C, Tung M C, et al. 2000. A Piscirickettsia salmonis-like organism in grouper, Epinephelus melanostigma, in Taiwan. J Fish Dis, 23: 415–418
Elston R. 1986. Occurrence of branchial rickettsiales-like infections in two bivalve mollusks, Tapes japonica and Patinopecten yessoensis, with comments on their significance. J Fish Dis, 9: 69–71
Elston R, Peacock M G. 1984. A Rickettsiales-like infection in the Pacific razor clam, Siliqua patula. J Invertebr Pathol, 44: 84–86.
Federici B A, Hazard E I, Anthony D W. 1974. Rickettsialike organism causing disease in a crangonid amphipod from Florida. Appl Microbiol, 28: 885–886
Fries C R, Grant D M. 1991. Rickettsiae in gill epithelial cells of the hard clam, Mercenaria mercenaria. J Invertebr Pathol, 57: 166–171
Friedman C S, Andree K B, Beauchamp K A, et al. 2000. ’Candidatus xenohaliotis californiensis’, a newly described pathogen of abalone, Haliotis spp. along the west coast of North America. Int J Syst and Evol Bacteriol, 50: 847–855
Friedman C S, McDowell T, Groff J M, et al. 1989. Presence of Bonamia ostreae among populations of the European flat oyster, Ostrea edulis Linné, in California, USA. J Shellfish Res, 8: 133–137
Fryer J L, Lannan C N. 1994. Rickettsial and chlamydial infections of freshwater and marine fishes, bivalves, and crustaceans. Zool Stud, 33: 95–107
Fryer J L, Lannan C N, Giovannoni S J, et al. 1992. Piscirickettsia salmonid gen, the causative agent of an epizootic disease in samonid fishes. Int J Syst Bacteriol, 42: 120–126
Gardner G R, Harshbarger J C, Lake J L, et al. 1995. Association of prokaryotes with symptomatic appearance of withering syndrome in black abalone Haliotis cracherodii. J Invertebr Pathol, 66: 111–120
Gulka G, Chang P W. 1984. Pathogenicity and infectivity of a rickettsia-like organism in the sea scallop, Placopecten magellanicus. J Fish Dis, 8: 309–318
Gulka G, Chang P W, Marti K A. 1983. Prokaryotic infection associated with a mass mortality of the sea scallop, Placopecten magellanicus. J Fish Dis, 6: 355–364
Harshbarger J C, Chang S C, Otto S V. 1977. Chlamydia (with phages), mycoplasmas and rickettsiae in Chesapeake Bay bivalves. Science, 196: 666–668
Krol R M, Hawkins W E, Overstreet R M. 1991. Rickettsial and mollicute infections in hepatopancreatic cells of cultured Pacific white shrimp (Penaeus vannamei). J Invertebr Pathol, 57: 362–370
Legall G, Chagot D, Mialhe E. 1988. Branchial rickettsiales-like infection associated with a mass mortality of sea scallop, Pecten maximus. DisAquat Org, 4: 229–232
Meyers T R, Short S, Eaton W. 1990. Summer mortalities and incidental parasitism of cultured Pacific oysters in Alaska. Journal of Aquatic Animal Health, 2: 172–176
Meyers T R. 1981. Endemic disease of cultured shellfish of Long Island, New York: adult and juvenile American oysters (Crassostrea virginica) and hard clams (Mercenaria mercenaria). Aquaculture, 22: 305–330
Moore J D, Cherr G N, Friedman C S. 2001. Detection of ‘Candidatus xenohaliotis californiensis’ (Rickettsiales-like prokaryote) inclusions in tissue squashes of abalone (Haliotis spp.) gastrointestinal epithelium using a nucleic acid fluorochrome. Dis Aquat Org, 46(2): 147–152
Moore J D, Robbins T T, Friedman C S. 2000. The role of a Rickettsia-like prokaryote in withering syndrome in California red abalone, Haliotis rufescens. J Shellfish Res, 19(1): 525–526
Morrison C, Shum G. 1983. Rickettsias in the kidney of the bay scallop, Argopecten irradians (Lamarck). J Fish Dis, 6: 537–541
Norton J H, Shepherd M A, Abdon-Naguit M R, et al. 1993. Mortalities in the giant clam Hippopus hippopus associated with rickettsiales-like organisms. J Invertebr Pathol, 62: 207–209
Norton J H, Shepherd M A, Prior H C. 1993. Intracellular bacteria associated with winter mortality in juvenile giant clams, Tridacna gigas. J Invertebr Pathol 62: 204–206
Olsen A B, Melby H P, Speilberg L, et al. 1997. Piscirickettsia salmonis infection in Atlantic salmon Salmo salar in Norway-epidemiological, pathological and microbiological findings. Dis Aquat Org, 31: 35–48
Paperna I. 1977. Epitheliocystis disease in wild and cultured sea bream (Sparus aurata, Sparidae) and grey mullets (liza ramada, Mugilidae). Aquaculture, 10: 169–176
Renault T, Cochennec N. 1994. Rickettsia-like organisms in the cytoplasm of gill epithelial cells of the Pacific oyster Crassostrea gigas. J Invertebr Pathol, 64: 160–162
Romero X, Turnbull J F, Jimenez R. 2000. Ultrastructure and Cytopathology of a Rickettsia-like Organism (RLO) Causing Systemic Infection in the Redclaw crayfish Cherax quadricarinatus in Ecuador. J Invertebr Pathol, 76: 95–104
SAS Institute. 2000. SAS/STAT User’s Guide. Cary, NC: SAS Institute Inc
Sun Jingfeng, Wu Xinzhong. 2004. The histology, ultrastructure, and morphogenesis of the rickettsia-like organism hyperpatasited by phage particles from the oyster, Crassostres ariakensis Gould. J Invertebr Pathol, 86: 77–86
Van Blaricom G R, Ruediger J L, Friedman C S, et al. 1993. Discovery of withering syndrome among black abalone Haliotis cracherodii Leach 1814 populations at San Nicolas Island, California. J Shellfish Res, 12: 185–188
Villalba A, Carballal M J, Lopez C, et al. 1999. Branchial rickettsia-like infection associated with clam Venerupis rhomboids mortality. Dis Aquat Org, 36(1): 53–60
Wen Chiou-Ming, Kou Guang-Hsiung, Chen Shiu-Nan. 1994. Rickettsiaceae-like microorganisms in the gill and digestive gland of the hard clam, Meretrix lusoria Rooding. J Invertebr Pathol, 64: 138–142
Wu Xinzhong. 2003a. Rickettsiae infection in farmed abalone, Haliotis diversicolor Reeve (Mollusca, Gastropoda) from the Daya Bay, Guangdong in China. Proceedings of the third World Fisheries Congress. Bethesda: American Fisheries Society, 221
Wu Xinzhong. 2003b. Advances in the research of marine-cultured animal diseases in China. In: Lee C S, ed. Andria Ventura. Status of Aquaculture in China. Hawaii, USA in Honolulu: The Oceanic Institute, 29–54
Wu Xinzhong, Pan Jinpei. 1999a. Studies on rickettsialike organism disease of tropical marine peal oyster: I. The fine structure and morphogenesis of Pinctada maxima pathogen rickettsia-like organism. J Invertebr Pathol, 73: 162–172
Wu Xinzhong, Pan Jinpei. 1999b. Studies on rickettsialike organism disease of tropical marine peal oyster, Pinctada maxima and P. fucata: IV. On histocytopathology of RLO diseases. Acta Oceanologica Sinica, 21: 93–98
Wu Xinzhong, Pan Jinpei. 1999c. Studies on the Rickettsia-like organism disease of tropical marine pearl oyster: V. Ultrastructural pathology and pathogenesis of Rickettsia-like organism disease. Acta Oceanologica Sinica, 21: 113–120
Wu Xinzhong, Pan Jinpei. 2000. An intracellular prokaryotic microorganism associated with lesions in the oyster, Crassostrea ariakensis Gould. J Fish Dis, 23: 409–414
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Foundation item: Scientific Projects of Zhejiang Province, China under contract Nos 2004C23041 and 20080123.
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Zhu, Z., Xu, T., He, Z. et al. Rickettsia-like organism infection associated with mass mortalities of blood clam, Tegillarca granosa, in the Yueqing Bay in China. Acta Oceanol. Sin. 31, 106–115 (2012). https://doi.org/10.1007/s13131-012-0182-3
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DOI: https://doi.org/10.1007/s13131-012-0182-3