Marteilioides chungmuensis of Oysters
Category 1 (Not Reported in Canada)
Common, generally accepted names of the organism or disease agent
Marteilioides of oocytes.
Scientific name or taxonomic affiliation
Marteilioides chungmuensis (Comps et al. 1987) in the phylum Paramyxea as proposed by Desportes and Perkins (1990) and supported by Berthe et al. (2000). The genus was defined by Anderson and Lester (1992) who indicated that the vegetative stages had amoeboid primary cell that cleaved internally to form secondary cells (sporonts) and sporulation consisted of sporonts that produce a single pluricellular spore, then degenerate such that the spore was enveloped by a cytoplasmic residuum and the plasmalemma of the sporont. Some of the infections described as "oyster egg diseases" may be attributed to M. chungmuensis.
Korea and Japan.
Crassostrea gigas. Also in Crassostrea nippona transplanted to an enzootic area (Itoh et al. 2004a). A similar looking parasite was reported from the ova of Crassostrea echinata from Northern Territory, Australia (Wolf 1977) and Western Australia (Hine and Thorne 2000). A Marteilioides -like parasite has also been reported at low prevalence (1.6%) from the oocytes of Manila clams, Venerupis (=Tapes ) philippinarum, in coastal areas of Korea (Lee et al. 2001).
Impact on the host
Abnormal egg-masses with a nodular appearance (like multiple tumors) among cultured Crassastrea gigas in Hiroshima Prefecture, Japan were first reported in the 1930s. Surveys in Matsushima Bay, Japan in the early 1960s revealed prevalences up to 46.2% but the intensity of infection was usually low (Imai et al. 1968). In 1974, Matsuzato et al. (1977) detected a parasite in the ova of abnormal oysters from Hiroshima Prefecture where 0 to 12% of the oysters were found affected. In Korea, M. chungmuensis was reported for the first time in 1970. Chun (1979) who called the parasite an enigmatic amoeba reported an infection prevalence of 13.3% in the Hansan area of Korea in 1978 and 1979. Park and Chun (1986) who identified the parasite as Marteilia sp. detected low prevalence (0.6%) in two oyster farms but did not detect the parasite in two others during a survey of 30 oysters from each farm per month for 1 year. Elston (1993) reported prevalences of infection up to 8.3% in the late 1980s. Apparently, the prevalence of infection in Korea has continued to increase and M. chungmuensis has been implicated as a cause of poor seed collection and high mortalities among cultured oysters since 1990 (Park 2005). Also, occurrence has extended from the spawning season (late summer-early fall) to year round with highest prevalence during spawning (from June to August) and during the gonadal regeneration period (from September to October) (Park 2002, 2005; Park et al. 2003). Tun et al. (2007) found that infected female oysters produced oocytes continuously and spawned repeatedly from October to March, during which period healthy oysters were reproductively inactive and concluded that M. chungmuensis extends the reproductive period of infected oysters for its own reproductive benefit. This prolonged spawning activity of infected oysters resulted in nutritional wasting and mortality of infected oysters, causing a decline in prevalence of infection within the epizootic area in autumn and the continued decrease in prevalence during the winter was attributed to recovery from infection (Tun et al. 2008a).
Marteilioides chungmuensis infects the cytoplasm of oocytes and can affect large areas of the reproductive follicles causing irregular enlargement of the infected gonadal tissues. Histological observations suggested that M. chungmuensis invades immature ova which move to the center of the follicle and the growth of the parasite was highly correlated with the growth and maturation of host gonadal cells (Itoh et al. 2002a). Infected eggs may be liberated via the genital canal or retained in the ovarian follicle and this parasite can have a significant effect on the reproductive output of an infected female oyster. Infection can also cause spawning failure by delaying spawning and destroying ripe oyster oocytes (Ngo et al. 2003). Infection also significantly reduced glycogen levels and serum protein concentrations affecting metabolic recovery after spawning (Park et al. 2003, Park 2005). Infected oysters lose their marketability due to the unaesthetic appearance and thus causes a serious economical impact.
Basic biological information pertaining to the complete life cycle of this parasite, including the method of transmission, remains unknown (Itoh et al. 2002b). However, Itoh et al. (2004b) used parasite-specific DNA probes and electron microscopy to reveal the route of infection and to identify early infective and multiplication stages in the oyster (Fig A1). Briefly, the parasite invaded the oyster through the epithelial tissues of the gills, mantle and labial palps. Extrasporogonic multiplication of the primary cell repeatedly occurred outside of host cells in the connective tissue by binary fission. In addition, internal cleavage within the primary cell resulted in the production of secondary cells which in turn occasionally contained a tertiary cell. Apparently, the secondary cell released from the primary cell migrates through the epithelium of the gonad and invades an immature oocyte where it forms the stem cell of the sporogonic stage. Sporogonic stages were observed only inside the oocytes of the host (as described below). Crassostrea gigas placed into an area enzootic for M. chungmuensis (Okayama Prefecture, Japan) in August developed gross signs of the disease within a month (Itoh et al. 2004b). In this area, Tun et al. (2008b) reported that the prevalence of infection detected by polymerase chain reaction (PCR, see below) was 70% or higher from August to October, but declined sharply in November and reached 7% or lower from February to April. However, transferring the oysters to warm seawater (from 8 to 10°C at the enzootic location to 24°C in M. chungmuensis -free experimental tanks) increased the prevalence of infection from about 7% to 87% within 3 weeks indicating that the low prevalence in winter was due to insufficient replication of M. chungmuensis at low seawater temperatures, resulting in levels not detectable by nested PCR, and not to the absence of invasion (Tun et al. 2008b).
Itoh et al. (2004b) identified extrasporogic stages in male C. gigas but sporulation in male oysters was not confirmed. Although the prevalence of infection detected by PCR after 4 weeks of exposure in an enzootic area was similar in both male and female oysters (about 60%), the prevalence in males declined in the subsequent 3 weekly samples (down to 24%) while that of the females remained consistently high (above 60%). Itoh et al. (2004b) suggested that M. chungmuensis may be excluded from male oysters without initiating sporulation.
Gross: Tumour-like distensions of the mantle tissues of heavily infected oysters.
Smears: Dried smears of the nodules (infected gonad) stained with Wright, Wright-Giemsa or equivalent stain (e.g. Hemacolor, Merck; Diff-QuiK, Baxter) enables the rapid detection of developmental stages within and liberated from the ova. The usual form of M. chungmuensis in mature oyster oocytes is two sporonts (secondary cells), each containing one developing spore, within each degenerate stem cell. However, stem cells containing from three to six sporonts (each containing one developing spore) have been observed but are rare (Imanaka et al. 2001).
Histology:Stem cells containing one to three (usually two) sporonts (secondary cells), resulting from exogenous budding, within the cytoplasm of infected oocytes and ova. Within each sporont, one tertiary cell forms by endogenous budding. The tertiary cell develops into a tricellular spore by internal cleavage. A related species, Marteilioides branchialis, from the gills of Saccostrea glomerata (=commercialis) has from two to six and rarely up to 12 sporonts in each primary cell and each spore is bicellular (two cells, one within the other, in each spore).
Electron microscopy: Examination of the ultrastructure is required to identify the tricellular nature of the spore (Comps et al. 1987).
DNA Probes: A partial sequence of the 18s small subunit ribosomal DNA (ca. 1200 base pairs listed in GenBank accession number AB089819) was identified from sporonts isolated from infected oysters using a freeze-thaw procedure and differential centrifugation in discontinuous sucrose and Percoll gradients (Itoh et al. 2003a). The sequence was used to design three M. chungmuensis specific probes. The probes detected parasite cells by in situ hybridisation and were used to elucidate the life cycle of M. chungmuensis (Itoh et al. 2004b). The identified sequence for this parasite will also be used to determine the phylogenetic position of this parasite (Itoh et al. 2002b, 2003a). Two sets of specific primers were developed into a nested-polymerase chain reaction (PCR) that had a far greater sensitivity for detecting M. chungmuensis than traditional histological techniques and gross observations (Itoh et al. 2003b).
Methods of control
No known methods of prevention. Infected oysters should not be transported into areas known to be free of the disease. In Japan, the prevalence of infection increased during the summer suggesting that active multiplication of the parasite occurs in the warm water months (Imanaka et al. 2001). Tun et al. (2006) indicated that a lower prevalence of infection was detected in oysters from the intertidal zone (with a daily average of 6 hours in seawater). However, they determined that the decrease in prevalence in the intertidal oysters was not due to short-term exposure to parasitic invasion, but to factors that decreased the female population, because spore formation of M. chungmuensis (and associated pathology) occurs only in female oysters (Tun et al. 2006). The National Fisheries Research and Development Institute (NFRDI) in Korea has recommend that the oyster culture industry in affected areas grow triploid oysters which are not susceptible to infection by the parasite (Park 2005).
Anderson, T.J. and R.J.G. Lester. 1992. Sporulation of Marteilioides branchialis n.sp. (Paramyxea) in the Sydney rock oyster, Saccostrea commercialis: an electron microscope study. Journal of Protozoology 39: 502-508.
Berthe, F.C.J., F. Le Roux, E. Peyretaillade, P. Peyret, D. Rodriguez, M. Gouy and C.P. Vivares. 2000. Phylogenetic analysis of the small subunit ribosomal RNA of Marteilia refringens validates the existence of Phylum Paramyxea (Desportes and Perkins, 1990). The Journal of Eukaryotic Microbiology 47: 288-293.
Bondad-Reantaso, M.G., S.E. McGladdery, I. East and R.P. Subasinghe (eds). 2001. Asia Diagnostic Guide to Aquatic Animal Diseases. FAO Fisheries Technical Paper 402 Supplement 2. Food and Agriculture Organisation of the United Nations and Network of Aquaculture Centres in Asia-Pacific, Rome. Pg. 144-146.
Chun, S.-K. 1979. Amoeba infection in oyster (Crassostrea gigas). Bulletin of the Korean Fisheries Society 12: 281-285.
Comps, M., M.S. Park and I. Desportes. 1986. Etude ultrastructurale de Marteilioides chungmuensis n.g. n.sp., parasite des ovocytes de l'huître Crassostrea gigas Th. Protistologica 22: 279-285.
Comps, M., M.S. Park and I. Desportes. 1987. Fine structure of Marteilioides chungmuensis n.g. n.sp., parasite of the oocytes of the oyster Crassostrea gigas. Aquaculture 67: 264-265.
Desportes, I. and F.O. Perkins. 1990. Phylum Paramyxea. In: Margulis, L., J.O. Corliss, M. Melkonian and D.J. Chapman (eds), Handbook of Protoctista. Jones and Bartlett Publishers, Boston, MA. Pg. 30-35.
Elston, R.A. 1993. Infectious diseases of the Pacific oyster Crassostrea gigas. Annual Review of Fish Diseases 3: 259-276.
Hine, P.M. and T. Thorne. 2000. A survey of some parasites and diseases of several species of bivalve mollusc in northern Western Australia. Diseases of Aquatic Organisms 40: 67-78.
Imai, T., K. Mori, Y. Sugawara, H. Tamate, J. Oizumi and O. Itakawa. 1968. Studies on the mass mortality of oysters in Matsushima Bay VII. Pathogenetic investigation. Tohoku Journal of Agricultural Research 19: 250-265.
Imanaka, S., N. Itoh, K. Ogawa and H. Wakabayashi. 2001. Seasonal fluctuations in the occurrence of abnormal enlargement of the ovary of Pacific oyster Crassostrea gigas at Gokasho Bay, Mie, Japan. Fish Pathology (Tokyo) 36: 83-91.
Itoh, N., T. Oda, K. Ogawa and H. Wakabayashi. 2002a. Identification and development of a paramyxean ovarian parasite in the Pacific oyster Crassostrea gigas. Fish Pathology (Tokyo) 37: 23-28.
Itoh, N., T. Oda and K. Ogawa 2002b. Marteilioides chungmuensis (Paramyxea), an intracellular parasite of the ovocyte of Pacific oyster Crassostrea gigas: isolation and sequencing of small subunit ribosomal DNA. Handbook and Abstracts, Fifth Symposium on Diseases in Asian Aquaculture, Queensland, Australia, 24-28 November 2002. Pg. 97.
Itoh, N., T. Oda, T. Yoshinaga and K. Ogawa. 2003a. Isolation and 18S ribosomal DNA gene sequence of Marteilioides chungmuensis (Paramyxea), an ovarian parasite of the Pacific oyster Crassostrea gigas. Diseases of Aquatic Organisms 54: 163-169.
Itoh, N., T. Oda, T. Yoshinaga and K. Ogawa. 2003b. DNA probes for detection of Marteilioides chungmuensis from the ovary of Pacific oyster Crassostrea gigas. Fish Pathology (Tokyo) 38: 163-169.
Itoh, N., K.L. Tun, H. Komiyama, N. Ueki and K. Ogawa. 2004a. An ovarian infection in the Iwagaki oyster, Crassostrea nippona, with the protozoan parasite Marteilioides chungmuensis. Journal of Fish Diseases 27: 311-314.
Itoh, N., H. Komiyama, N. Ueki and K. Orawa. 2004b. Early developmental stages of a protozoan parasite, Marteilioides chungmuensis (Paramyxea), the causative agent of the ovary enlargement disease in the Pacific oyster, Crassostrea gigas. International Journal for Parasitology 34: 1129-1135.
Lee, M.-K., B.-Y. Cho, S.-J. Lee, J.-Y. Kang, H.D. Jeong, S.H. Huh and M.-D. Huh. 2001. Histopathologucal lesions of Manila clam, Tapes philippinarum, from Hadong and Namhae coastal areas of Korea. Aquaculture 201: 199-209.
Matsusato, T. and K. Masumura. 1981. Abnormal enlargement of the ovary of oyster, Crassostrea gigas (Thunberg) by an unidentified parasite. Fish Pathology (Tokyo) 15: 207-212.
Matsuzato, T., T. Hoshina, K.Y. Arakawa and K. Masumura. 1977. Studies on the so-called abnormal egg-mass of Japanese oyster, Crassostrea gigas (Thunberg) - I. Distribution of the oyster collected in the coast of Hiroshime Pref., and parasite in the egg-cell. Bulletin of the Hiroshima Fisheries Experimental Station 8: 9-25.
Mortensen, S., I. Arzul, L. Miossec, C. Paillard, S. Feist, G. Stentiford, T. Renault, D. Saulnier and A. Gregory. 2007. Molluscs and crustaceans. In: Raynard, R., T. Wahli, I. Vatsos, S. Mortensen (eds.). Review of disease interactions and pathogen exchange between farmed and wild finfish and shellfish in Europe. VESO on behalf of DIPNET, Oslo. Chapter 5.3.17, pp. 385-388. For electronic version see www.dipnet.info under "Documents" subgroup "Reports and project deliverables".
Ngo, T.T.T., F.C.J. Berthe and K.-S. Choi. 2003. Prevalence and infection intensity of the ovarian parasite Marteilioides chungmuensis during an annual reproductive cycle of the oyster Crassostrea gigas. Diseases of Aquatic Organisms 56: 259-267.
Park, M.S. 2002. Survey on the ovarian parasite, Marteilioides chungmuensis in the cultured Pacific oysters Crassostrea gigas in Korea. Handbook and Abstracts, Fifth Symposium on Diseases in Asian Aquaculture, Queensland, Australia, 24-28 November 2002. Pg. 96.
Park, M.S. 2005. Survey on the ovarian parasite, Marteilioides chungmuensis in the culture Pacific oyster, Crassostrea gigas in Korea. In: Walker, P.J., R.G. Lester, M.G. Bondad-Reantaso (eds.) Diseases in Asian Aquaculture V. Proceedings of the 5th Symposium on Diseases in Asian Aquaculture. Fish Health Section, Asian Fisheries Society, Manila. pp. 311-320.
Park, M.S. and S.K. Chun. 1986. On the Marteilia sp. infection in the oyster, Crassostrea gigas (Thunberg). Bulletin of Fisheries Research and Development Agency 39: 105-109.
Park, M.S., C.-K. Kang, D.-L. Choi and B.-Y. Jee. 2003. Appearance and pathogenicity of ovarian parasite Marteilioides chungmuensis in the farmed Pacific oysters, Crassostrea gigas, in Korea. Journal of Shellfish Research 22: 475-479.
Tun, K.L., N. Itoh, H. Komiyama, N. Ueki, T. Yoshinaga and K. Ogawa. 2006. Comparison of Marteilioides chungmuensis infection in the Pacific oyster Crassostrea gigas cultured in different conditions. Aquaculture 253: 91-97.
Tun, K.L., N. Itoh, N. Ueki, T. Yoshinaga and K. Ogawa. 2007. Relationship between Marteilioides chungmuensis infection and reproduction in the Pacific oyster, Crassostrea gigas. Journal of Invertebrate Pathology 96: 205-212.
Tun, K.L., N. Itoh, Y. Shimizu, H. Yamanoi, T. Yoshinaga and K. Ogawa. 2008a. Pathogenicity of the protozoan parasite Marteilioides chungmuensis in the Pacific oyster Crassostrea gigas. International Journal for Parasitology 38: 211-217.
Tun, K.L., Y. Shimizu, H. Yamanoi, T. Yoshinaga and K. Ogawa. 2008b. Seasonality in the infection and invasion of Marteilioides chungmuensis in the Pacific oyster Crassostrea gigas. Diseases of Aquatic Organisms 80: 157-165.
Wolf, P.H. 1977. An unidentified protistan parasite in the ova of the blacklipped oyster, Crassostrea echinata, from northern Australia. Journal of Invertebrate Pathology 29: 244-246.
Bower, S.M., Itoh, N., Choi, D.-L., Park, M.S. (2011): Synopsis of Infectious Diseases and Parasites of Commercially Exploited Shellfish: Marteilioides chungmuensis of Oysters.
Contact information for co-authors:
Naoki Itoh, Graduate School of Agricultural Science, Tohoku University, 1-1 Amamiya-machi, Tsutsumidori, Aoba-ku, Sendai 981-8555, Miyagi Japan. E-mail: email@example.com
Dong-Lim Choi and Mi Seon Park, Pathology Division, National Fisheries Research and Development Institute (NFRDI), 408-1, Silang-ri, Kitang-up, Kitang-gum, Pusan 619-900, Republic of Korea. E-mail: firstname.lastname@example.org
Date last revised: June 2011
Comments to Susan Bower
- Date modified: