DOI QR코드

DOI QR Code

Effects of Ovarian Parasite Marteilioides chungmuensis on the Reproduction of the Pacific Oyster Crassostrea gigas Assessed by Histology and Enzyme-Linked Immunosorbent Assay (ELISA)

  • Yanin, Limpanont (Department of Social and Environmental Medicine, Faculty of Tropical Medicine, Mahidol University) ;
  • Hyun-Sil, Kang (Tidal Flat Research Center, National Institute of Fisheries and Science) ;
  • Young-Ghan, Cho (Department of Marine Life Science and Marine Science Institue (BK21 FOUR), Jeju National University) ;
  • Jong-Seop, Shin (Department of Marine Life Science and Marine Science Institue (BK21 FOUR), Jeju National University) ;
  • Nobuhisa, Kajino (Department of Marine Life Science and Marine Science Institue (BK21 FOUR), Jeju National University) ;
  • Jeong-Hwa, Kim (Department of Marine Life Science and Marine Science Institue (BK21 FOUR), Jeju National University) ;
  • Hyun-Ki, Hong (Department of Marine Life Science and Marine Science Institue (BK21 FOUR), Jeju National University) ;
  • Kwang-Sik, Choi (Department of Marine Life Science and Marine Science Institue (BK21 FOUR), Jeju National University)
  • Received : 2022.09.14
  • Accepted : 2022.10.18
  • Published : 2022.12.30

Abstract

The paramyxean parasite Marteilioides chungmuensis infects the cytoplasm of the eggs of Pacific oysters Crassostrea gigas , resulting in spawning failure of the infected females. Such infected eggs appear as bump-like nodules on the body in late fall when most of the uninfected females complete spawning. In this study, we estimated the quantity of the infected eggs using an enzyme-linked immunosorbent assay (ELISA), which is destroyed by M. chungmuensis parasitism. In December, the infected oysters collected from Tongyoung on the south coast exhibited numerous yellowish bump-like nodules as signs of infection. In histology, the infected oysters exhibited mature eggs in the follicle, which were heavily infiltrated by hemocytes. ELISA indicated that the infected egg mass accounted for 7.52±5.50 percent of the body weight, suggesting the ovarian parasite causes substantial reproductive loss. Histology also indicated that the infected oysters are in a poor nutritional condition, as the digestive gland atrophy (DGA) level is comparatively higher than the uninfected oyster. The total carbohydrate contents in the infected oysters (108.68±44.41 mg/g dry wt) were significantly lower than in uninfected oysters (269.76±50.97 mg/g dry wt), suggesting that M. chungmuensis parasitism also affected the energy storage capacity of the host during the resting stage.

Keywords

Acknowledgement

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science and ICT (2021R1C1C2004304), and global research grant of Jeju National University 2022.

References

  1. Bayne BL, Salkeld PN, Worral CM (1983) Reproductive effort and value in different populations of marine mussel, Mytilus edulis L. Oecologia 59:18-26 https://doi.org/10.1007/BF00388067
  2. Berthe FRJ, Le Roux F, Adlard RD, Figueras A (2004) Marteiliosis in molluscs: a review. Aquat Living Resour 17:433-448 https://doi.org/10.1051/alr:2004051
  3. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911-917 https://doi.org/10.1139/y59-099
  4. Carrasco N, Green T, Itoh N (2015) Marteilia spp. parasites in bivalves: a revision of recent studies. J Invetebr Pathol 131:43-57 https://doi.org/10.1016/j.jip.2015.07.016
  5. Choi HJ, Hwang JY, Choi DL, Huh MD, Hur YB, Lee NS, Seo JS, Kwon MK, Choi HS, Park MA (2011) Nonspecific defensive factors of the Pacific oyster Crassostrea gigas against infection with Martellioides chungmuensis: a flow-cytometric study. Korean J Parasitol 49:229-234 https://doi.org/10.3347/kjp.2011.49.3.229
  6. Choi KS (2008) Oyster capture-based aquaculture in the Republic of Korea. In: Lovatelli A, Holthus PF (eds) Capture-based aquaculture. Global review. FAO Fisheries Technical Paper. No. 508. FAO, Rome, pp 271-286
  7. Chun SK (1972) Preliminary studies on the sporozoan parasites in oysters on the souther coast of Korea. Bull Korean Fish Soc 5:1-7
  8. Clark A (1987) Temperature, latitude and reproductive effort. Mar Ecol-Prog Ser 38:89-99 https://doi.org/10.3354/meps038089
  9. Comps M (1987) Fine structure of Marteilioides chungmuensis ng, n. sp., parasite of the oocytes of the oyster Crassostrea gigas. Aquaculture 67:264-265 https://doi.org/10.1016/0044-8486(87)90052-4
  10. Comps M, Park MS, Desportes I (1986) Etude ultrastructural de Marteilioides chungmuensis n.g., n. sp. parasite des ovocytes de l'huitre Crassostrea gigas TH. Protistologica 22:279-285
  11. Degremont L, Carcia C, Allen SK (2015) Genetic improvement for disease resistance in oysters: a review. J Invertebr Pathol 131:226-241 https://doi.org/10.1016/j.jip.2015.05.010
  12. Donaghy L, Hong HK, Lee HJ, Jun JC, Park YJ, Choi KS (2010) Hemocyte parameters of the Pacific oyster Crassostrea gigas a year after the Hebei Spirit oil spill off the west coast of Korea. Helgol Mar Res 64:349-355 https://doi.org/10.1007/s10152-010-0190-7
  13. Donaghy L, Kim BK, Hong HK, Park HS, Choi KS (2009) Flow cytometry studies on the populations and immune parameters of the hemocytes of the Suminoe oyster, Crassostrea ariakensis. Fish Shellfish Immunol 27:296-301 https://doi.org/10.1016/j.fsi.2009.05.010
  14. Dubois M, Gilles KA, Hamilton JK, Robers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350-356 https://doi.org/10.1021/ac60111a017
  15. Hirshfield MF, Tinkle DW (1975) Natural selection and the evolution of reproductive effort. Proc Nat Acad Sci USA 72:2227-2231 https://doi.org/10.1073/pnas.72.6.2227
  16. Hong HK, Jeung HD, Kang HS, Choi KS (2020) Seasonal variations in the hemocytes parameters, gonad development, energy storage and utilization of the giant honeycomb oyster Hyotissa hyotis (Linnaeus 1758) in Jeju Island off the south coast of Korea. Aquac Rep 17:100299. doi:10.1016/j.aqrep.2020.100299
  17. Hong HK, Kang HS, Le TC, Choi KS (2013) Comparative study on the hemocytes of subtropical oysters Saccostrea kegaki (Torigoe & Inaba, 1981), Ostrea circumpicta (Pilsbry, 1904), and Hyotissa hyotis (Linnaeus, 1758) in Jeju Island, Korea: morphology and functional aspects. Fish Shellfish Immunol 35:2020-2025 https://doi.org/10.1016/j.fsi.2013.09.022
  18. Hong HK, Park HS, Choi KS (2022) Growth and reproduction of the Pacific oyster Crassostrea gigas cultured on tidal flat in Hebei Spirit oil spill area on the west coast of Korea four years after the accident. Front Mar Sci 9:880210. doi:10.3389/fmars.2022.880210
  19. Imanaka S, Itoh N, Ogawa, K, Wakabayashi H (2001) Seasonal fluctuations in the occurrence of abnormal enlargement of the ovary of Pacific oyster Crassostrea gigas at Gokasho Bay, Mie, Japan. Fish Pathol 36:83-91 https://doi.org/10.3147/jsfp.36.83
  20. Itoh N, Komiyama, H, Ueki N, Ogawa K (2004) Early developmental stages of a protozoan parasite, Marteilioides chungmuensis (Paramyxea), the causative agent of the ovary enlargement disease in the Pacific oyster, Crassostrea gigas. Int J Parasitol 34:1129-1135 https://doi.org/10.1016/j.ijpara.2004.06.001
  21. Itoh N, Oda T, Ogawa K, Wakabayashi H (2002) Identification and development of a paramyxean ovarian parasite in the Pacific oyster Crassostrea gigas. Fish Pathol 37:23-28 https://doi.org/10.3147/jsfp.37.23
  22. Kang DH, Chu FL, Yang HS, Lee CH, Koh HB, Choi KS (2010) Growth, reproductive condition, and digestive tubule atrophy of Pacific oyster, Crassostrea gigas, in Gamakman Bay off the southern coast of Korea. J Shellfish Res 29:839-845 https://doi.org/10.2983/035.029.0418
  23. Kang DH, Kim SJ, Choi KS (2004) Microscopic observations of larval Ostrea circumpicta (Bivalve: Ostreidae) in brood c hambers. J Shellfish Res 23:411-415
  24. Kang SG, Choi KS, Bulgakov AA, Kim Y, Kim SY (2003) Enzyme-linked immunosorbent assay (ELISA) used in quantification of reproductive output in the pacific oyster, Crassostrea gigas, in Korea. J Exp Mar Biol Ecol 282:1-21 https://doi.org/10.1016/S0022-0981(02)00444-6
  25. Keeling PJ, del Campo J (2017) Marine protists are not just big bacteria. Curr Biol 27:R541-R849 https://doi.org/10.1016/j.cub.2017.03.075
  26. Kim BK, Choi KS (2012) Development of an immunological  probe to quantify reproductive effort in the Suminoe oyster, Crassostrea ariakensis (Gould 1861). J Shellfish Res 31:1033-1041 https://doi.org/10.2983/035.031.0415
  27. Kim JH, Lee HM, Cho YG, Shin JS, You JW, Choi KS, Hong HK (2020) Flow cytometric characterization of the hemocytes of blood cockles Anadara broughtonii (Schrenck, 1867), Anadara kagoshimensis (Lischke, 1869), and Tegillarca granosa (Linnaeus, 1758) as a biomarker for coastal environmental monitoring. Mar Poll Bull 160:111654. doi:10.1016/j.marpolbul.2020.111654
  28. Lee HM, Yang HS, Choi KS (2019) Reproductive condition and fecundity of female Suminoe oyster Crassostrea ariakensis (Fujita, 1913) from Seomin River estuary on the south coast of Korea during post-spawning period. Korea J Malacol 35:81-86
  29. Limpanont Y, Kang HS, Hong HK, Jeung HD, Kim BK, Le Cuong T, Kim YO, Choi, KS (2013) Molecular and histological identification of Marteilioides infection in Suminoe oyster Crassostrea ariakensis, Manila clam Ruditapes philippinarum and Pacific oyster Crassostrea gigas on the south coast of Korea. J Invertebr Pathol 114:277-284 https://doi.org/10.1016/j.jip.2013.08.008
  30. Lowry OH, Rosebrough NJ, Lewis FA, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275 https://doi.org/10.1016/S0021-9258(19)52451-6
  31. Matsusato T, Masumura K (1981) Abnormal enlargement of the ovary of oyster, Crassostrea gigas (THUNBERG) by an unidentified parasite. Fish Pathol 15:207-212 https://doi.org/10.3147/jsfp.15.207
  32. Mondol MR, Kim CW, Kang CK, Park SR, Noseworthy RG, Choi KS (2016) Growth and reproduction of early grow-out hardened juvenile Pacific oysters, Crassostrea gigas in Gamakman Bay, off the south c oast of Korea. Aquaculture 463:224-233 https://doi.org/10.1016/j.aquaculture.2016.05.047
  33. Mondol MR, Kim CW, Kim BK, Kang CK, Choi KS (2012) Early growth and reproduction of hatchery-produced Pacific oyster Crassostrea gigas in Gamakman Bay off the southern coast of Korea. Fish Sci 78:1285-1292 https://doi.org/10.1007/s12562-012-0553-x
  34. Ngo TTT, Kang SG, Choi KS (2002) Seasonal changes in reproductive condition of the Pacific oysters, Crassostrea gigas (Thunberg) from suspended culture in Gosung Bay, Korea. Korean J Environ Biol 3:268-275
  35. Ngo TTT, Kang SG, Kang DH, Sorgeloos P, Choi KS (2006) Effect of culture depth on the proximate composition and reduction of the Pacific oyster, Crassostrea gigas from Gosung Bay, Korea. Aquaculture 253:712-720 https://doi.org/10.1016/j.aquaculture.2005.09.009
  36. Ngo, TTT, Berthe FCJ, Choi KS (2003) Prevalence and infection intensity of the ovarian parasite Marteilioides chungmuensis during an annual reproductive cycle of the oyster Crassostrea gigas. Dis Aquat Org 56:259-267 https://doi.org/10.3354/dao056259
  37. Park KI, Choi KS (2004) Application of enzyme-linked immunosorbent assay for studying of reproduction in the Manila clam Ruditapes philippinarum (Mollusca: Bivalvia) I. quantifying eggs. Aquaculture 241:667-687 https://doi.org/10.1016/S0044-8486(04)00476-4
  38. Park MS, Chun SK (1989) Study on Marteilioides chungmuensis (Comps et al., 1986) parasite of the Pacific oyster, Crassostrea gigas Thunberg. J Fish Pathol 2:53-70
  39. Park MS, Kang CK, Choi DL, Jee BY (2003) Appearance and pathogenicity of ovarian parasite Marteilioides chungmuensis in the farmed Pacific oysters, Crassostrea gigas, in Korea. J Shellfish Res 22:475-479
  40. Park MS, Lyu HY, Lee TS (1999) Investigation on the cause of bad natural seed collection of the Pacific oyster, Crassostrea gigas: relationships between the conditions of mother shell and the viability of the released eggs and larvae based on the pathological and embryological survey. J Korean Fish Soc 32:62-67
  41. Pianka ER (1972) r and k selection or b and d selection? Am Nat 106:581-588
  42. Seki H (1934) On the abnormal growth of ovary of oysters collected from Hiroshima area (in Japanese). Report Nippon Gakujyutsu Kyokai 9:375-381
  43. Tun KL, Itoh N, Shimizu Y, Yamanoi H, Yoshinaga T, Ogawa K (2008) Seasonality in the infection and invasion of Marteilioides chungmuensis in the Pacific oyster Crassostrea gigas. Dis Aquat Org 80:157-165 https://doi.org/10.3354/dao01924
  44. Tun KL, Itoh N, Ueki N, Yoshinaga T, Ogawa K (2007) Relationship between Marteilioides chungmuensis infection and reproduction in the Pacific oyster, Crassostrea gigas. J Invertbr Pathol 96:205-212 https://doi.org/10.1016/j.jip.2007.06.001
  45. Uddin MJ, Park KI, Kang DH, Park YJ, Choi KS (2007) Comparative reproductive biology of Yezo scallop, Pantionpecten yessoensis, under two different culture systems on the east coast of Korea. Aquaculture 265:139-247 https://doi.org/10.1016/j.aquaculture.2007.01.047
  46. Winstead JT (1995) Digestive tubule atrophy in Eastern oysters, Crassostrea virginica (Gmelin, 1791), exposed to salinity and starvation stress. J Shellfish Res 14:105-111