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Seasonal Changes in Hemolymph Parameters of the Bivalve Modiolus kurilensis Bernard, 1983 from Vostok Bay, Sea of Japan

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Abstract

Hemolymph is one of the main tissues providing invertebrates’ immunity and homeostasis. Earlier, we showed that some of the hemolymph immune parameters of the common Far Eastern mollusk Modiolus kurilensis are sensitive to bacterial and anthropogenic challenges. In this work, a number of cellular parameters such as total hemocyte count (THC), hemocyte phagocytic activity (PA), and reactive oxygen species (ROS) and humoral parameters such as hemagglutination (HA) and hemolytic (HL) activity of plasma, as well as its protein concentration (CP) and profiling in M. kurilensis were studied depending on the season and environmental indicators (temperature, salinity, and oxygen concentration). The total hemocyte count was weakly correlated with water oxygen concentration (R = –0.25) and temperature (R = 0.27), and the 36 kDa plasma protein was weakly correlated with temperature (R = –0.33). Also, there was a correlation (R = 0.38) between hemagglutination activity and the 19 kDa protein fraction. The minimum values for a number of parameters were noted in January (THC, PA, ROS, HA, HL), while the maximum values were observed in late spring (THC, PA, ROS, HA, HL). At the same time, in other months, these and most other parameters had metastable values. Thus, the indicators that were identified in previous studies (THC, PA, ROS, HA, HL, CP, protein fractions 55 and 124 kDa) are suitable for assessing the physiological state of M. kurilensis during most of the year.

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REFERENCES

  1. Carballal, M.J., López, C., Azevedo, C., et al., Enzymes involved in defense functions of hemocytes of Mussel Mytilus galloprovincialis, J. Invertebr. Pathol., 1997, vol. 70, pp. 96–105. https://doi.org/10.1006/jipa.1997.4670

    Article  CAS  PubMed  Google Scholar 

  2. Carballal, M.J., Villalba, A., and López, C., Seasonal variation and effects of age, food availability, size, gonadal development, and parasitism on the hemogram of Mytilus galloprovincialis, J. Invertebr. Pathol., 1998, vol. 72, pp. 304–312. https://doi.org/10.1006/jipa.1998.4779

    Article  CAS  PubMed  Google Scholar 

  3. Malagoli, D., Casarini, L., and Ottaviani, E., Monitoring of the immune efficiency of Mytilus galloprovincialis in Adriatic sea mussel farms in 2006: Regular changes of cytotoxicity during the year, Invertebr. Survival J., 2007, vol. 4, pp. 10–12.

    Google Scholar 

  4. Novas, A., Barcia, R., and Ramos-Martínez, J.I., Nitric oxide production by haemocytes from Mytilus galloprovincialis shows seasonal variations, Fish Shellfish Immunol., 2007, vol. 23, pp. 886–891. https://doi.org/10.1016/j.fsi.2007.04.007

    Article  CAS  PubMed  Google Scholar 

  5. Schmidt, W., Power, E., and Quinn, B., Seasonal variations of biomarker responses in the marine blue mussel (Mytilus spp.), Mar. Pollut. Bull., 2013, vol. 74, pp. 50–55. https://doi.org/10.1016/j.marpolbul.2013.07.033

    Article  CAS  PubMed  Google Scholar 

  6. Soudant, P., Paillard, C., Choquet, G., et al., Impact of season and rearing site on the physiological and immunological parameters of the Manila clam Venerupis (=Tapes, =Ruditapes) philippinarum, Aquaculture, 2004, vol. 229, pp. 401–418. https://doi.org/10.1016/S0044-8486(03)00352-1

    Article  Google Scholar 

  7. Mitta, G., Vandenbulcke, F., and Roch, P., Original involvement of antimicrobial peptides in mussel innate immunity, FEBS Lett., 2000, vol. 486, pp. 185–190. https://doi.org/10.1016/S0014-5793(00)02192-X

    Article  CAS  PubMed  Google Scholar 

  8. Montes, J.F., Durfort, M., and García-Valero, J., Cellular defence mechanism of the clam Tapes semidecussatus against infection by the protozoan Perkinsus sp., Cell Tissue Res., 1995, vol. 279, pp. 529–538. https://doi.org/10.1007/BF00318165

    Article  CAS  Google Scholar 

  9. Cheng, T.C., Bivalves, in Invertebrate Blood Cells, Ratcliffe, N.A. and Rowley, A.F., Eds., London: Academic Press, 1981, pp. 233–300.

    Google Scholar 

  10. Ottaviani, E., Franchini, A., Barbieri, D., et al., Comparative and morphofunctional studies on Mytilus galloprovincialis hemocytes: Presence of two aging-related hemocyte stages, Ital. J. Zool., 1998, vol. 65, pp. 349–354. https://doi.org/10.1080/11250009809386772

    Article  Google Scholar 

  11. Wootton, E.C., Dyrynda, E.A., and Ratcliffe, N.A., Bivalve immunity: Comparisons between the marine mussel (Mytilus edulis), the edible cockle (Cerastoderma edule) and the razor-shell (Ensis siliqua), Fish Shellfish Immunol., 2003, vol. 15, pp. 195–210. https://doi.org/10.1016/S1050-4648(02)00161-4

    Article  CAS  PubMed  Google Scholar 

  12. Ottaviani, E., Molluscan immunorecognition, Invertebr. Survival J., 2006, vol. 15, pp. 50–63.

    Google Scholar 

  13. Luna-Acosta, A., Bustamante, P., Budzinski, H., et al., Persistent organic pollutants in a marine bivalve on the Marennes–Oléron Bay and the Gironde Estuary (French Atlantic Coast)-Part 2: Potential biological effects, Sci. Total Environ., 2015, vol. 514, pp. 511–522. https://doi.org/10.1016/j.scitotenv.2014.10.050

    Article  CAS  PubMed  Google Scholar 

  14. Espinosa Ruiz, C., Morghese, M., Renda, G., et al., Effects of BDE-47 exposure on immune-related parameters of Mytilus galloprovincialis, Aquat. Toxicol., 2019, vol. 215. https://doi.org/10.1016/j.aquatox.2019.105266

  15. Matozzo, V., Da Ros, L., Ballarin, L., et al., Functional responses of haemocytes in the clam Tapes philippinarum from the Lagoon of Venice: Fishing impact and seasonal variations, Can. J. Fish. Aquat. Sci., 2003, vol. 60, pp. 949–958. https://doi.org/10.1139/f03-084

    Article  Google Scholar 

  16. Donaghy, L. and Volety, A.K., Functional and metabolic characterization of hemocytes of the green mussel, Perna viridis: In vitro impacts of temperature, Fish Shellfish Immunol., 2011, vol. 31, pp. 808–814. https://doi.org/10.1016/j.fsi.2011.07.018

    Article  CAS  PubMed  Google Scholar 

  17. Franco-Martínez, L., Martínez-Subiela, S., Escribano, D., et al., Alterations in haemolymph proteome of Mytilus galloprovincialis mussel after an induced injury, Fish Shellfish Immunol., 2018, vol. 75, pp. 41–47. https://doi.org/10.1016/j.fsi.2018.01.038

    Article  CAS  PubMed  Google Scholar 

  18. Wang, Y., Hu, M., Cheung, S.G., et al., Chronic hypoxia and low salinity impair anti-predatory responses of the green-lipped mussel Perna viridis, Mar. Environ. Res., 2012, vol. 77, pp. 84–89. https://doi.org/10.1016/j.marenvres.2012.02.006

    Article  CAS  PubMed  Google Scholar 

  19. Wang, Y., Hu, M., Cheung, S.G., et al., Immune parameter changes of hemocytes in green-lipped mussel Perna viridis exposure to hypoxia and hyposalinity, Aquaculture, 2012, vols. 356–357, pp. 22–29. https://doi.org/10.1016/j.aquaculture.2012.06.001

    Article  Google Scholar 

  20. Duchemin, M.B., Fournier, M., and Auffret, M., Seasonal variations of immune parameters in diploid and triploid Pacific oysters, Crassostrea gigas (Thunberg), Aquaculture, 2007, vol. 264, pp. 73–81. https://doi.org/10.1016/j.aquaculture.2006.12.030

    Article  Google Scholar 

  21. Kumeiko, V.V., Sokolnikova, Y.N., Grinchenko, A.V., et al., Immune state correlates with histopathological level and reveals molluscan health in populations of Modiolus kurilensis by integral health index (IHI), J. Invertebr. Pathol., 2018, vol. 154, pp. 42–57. https://doi.org/10.1016/j.jip.2018.03.014

    Article  PubMed  Google Scholar 

  22. Sokolnikova, Y.N., Trubetskaya, E.V., Beleneva, I.A., Grinchenko, A.V., and Kumeiko, V.V., Fluorescent in vitro phagocytosis assay differentiates hemocyte activity of the bivalve molluscs Modiolus kurilensis (Bernard, 1983) inhabiting impacted and non-impacted water areas, Russ. J. Mar. Biol., 2015, vol. 154, pp. 118–126. https://doi.org/10.1134/S106307401502011X

    Article  CAS  Google Scholar 

  23. Grinchenko, A.V., Sokolnikova, Y.N., Korneiko, D.D., et al., Dynamics of the immune response of the horse mussel Modiolus kurilensis (Bernard, 1983) following challenge with heat-inactivated bacteria, J. Shellfish Res., 2015, vol. 34, pp. 909–917. https://doi.org/10.2983/035.034.0321

    Article  Google Scholar 

  24. Ishikawa, H., Takahashi, G., and Katsuyoshi, M., Annual changes in maturation of the gonad and phagocytic activity in hemocytes of the pacific oyster, Crassostrea gigas, in Onagawa Bay, Miyagi prefecture, Aquacult. Sci., 1999, vol. 47, pp. 519–525.

    Google Scholar 

  25. Flye-Sainte-Marie, J., Soudant, P., Lambert, C., et al., Variability of the hemocyte parameters of Ruditapes philippinarum in the field during an annual cycle, J. Exp. Mar. Bio. Ecol., 2009, vol. 377, pp. 1–11. https://doi.org/10.1016/j.jembe.2009.06.003

    Article  Google Scholar 

  26. Vaschenko, M.A., Kovaleva, A.L., Syasina, I.G., et al., Reproduction-related effects of green alga Coccomyxa sp. infestation in the horse mussel Modiolus modiolus, J. Invertebr. Pathol., 2013, vol. 113, pp. 86–95. https://doi.org/10.1016/j.jip.2013.02.003

    Article  CAS  PubMed  Google Scholar 

  27. Rodovets, A.V. and Khristoforova, N.K., Density dynamics of commercial bivalves larvae in plankton of the Minonosok Bight and Vostok Bay (Japan Sea), Izv. Tikhookean. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 2008, vol. 153, pp. 201–214.

    Google Scholar 

  28. Gajbhiye, D.S. and Khandeparker, L., Immunoecology of the short neck clam Paphia malabarica (Chemnitz, 1782) in a tropical monsoon-influenced estuary, Mar. Environ. Res., 2019, vol. 143, pp. 60–70. https://doi.org/10.1016/j.marenvres.2018.11.004

    Article  CAS  PubMed  Google Scholar 

  29. Carballal, M.J., Villalba, A., and López, C., Seasonal variation and effects of age, food availability, size, gonadal development, and parasitism on the hemogram of Mytilus galloprovincialis, J. Invertebr. Pathol., 1998, vol. 72, pp. 304–312. https://doi.org/10.1006/jipa.1998.4779

    Article  CAS  PubMed  Google Scholar 

  30. Duchemin, M.B., Fournier, M., and Auffret, M., Seasonal variations of immune parameters in diploid and triploid Pacific oysters, Crassostrea gigas (Thunberg), Aquaculture, 2007, vol. 264, pp. 73–81. https://doi.org/10.1016/j.aquaculture.2006.12.030

    Article  Google Scholar 

  31. Bussell, J.A., Gidman, E.A., Causton, D.R., et al., Changes in the immune response and metabolic fingerprint of the mussel, Mytilus edulis (Linnaeus) in response to lowered salinity and physical stress, J. Exp. Mar. Biol. Ecol., 2008, vol. 358, pp. 78–85. https://doi.org/10.1016/j.jembe.2008.01.018

    Article  Google Scholar 

  32. Hauton, C., Hawkins, L.E., and Hutchinson, S., The effects of salinity on the interaction between a pathogen (Listonella anguillarum) and components of a host (Ostrea edulis) immune system, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2000, vol. 127, pp. 203–212. https://doi.org/10.1016/S0305-0491(00)00251-0

    Article  CAS  Google Scholar 

  33. Yu, J., Choi, M., Park, K., et al., Effects of anoxia on immune functions in the surf clam Mactra veneriformis, Zool. Stud., 2010, vol. 49, pp. 94–101.

    Google Scholar 

  34. Chen, M., Yang, H., Delaporte, M., et al., Immune condition of Chlamys farreri in response to acute temperature challenge, Aquaculture, 2007, vol. 271, pp. 479–487. https://doi.org/10.1016/j.aquaculture.2007.04.051

    Article  Google Scholar 

  35. Mosca, F., Narcisi, V., Calzetta, A., et al., Effects of high temperature and exposure to air on mussel (Mytilus galloprovincialis, Lmk 1819) hemocyte phagocytosis: Modulation of spreading and oxidative response, Tissue Cell, 2013, vol. 45, pp. 198–203. https://doi.org/10.1016/j.tice.2012.12.002

    Article  CAS  PubMed  Google Scholar 

  36. Rahman, M.A., Henderson, S., Miller-Ezzy, P., et al., Immune response to temperature stress in three bivalve species: Pacific oyster Crassostrea gigas, Mediterranean mussel Mytilus galloprovincialis and mud cockle Katelysia rhytiphora, Fish Shellfish Immunol., 2019, vol. 86, pp. 868–874. https://doi.org/10.1016/j.fsi.2018.12.017

    Article  CAS  PubMed  Google Scholar 

  37. Bibby, R., Widdicombe, S., Parry, H., et al., Effects of ocean acidification on the immune response of the blue mussel Mytilus edulis, Aquat. Biol., 2008, vol. 2, pp. 67–74. https://doi.org/10.3354/ab00037

    Article  Google Scholar 

  38. Santarem, M.M., Robledo, J.A.F., and Figueras, A., Seasonal changes in hemocytes and serum defense factors in the blue mussel Mytilus galloprovincialis, Dis. Aquat. Organ., 1994, vol. 18, pp. 217–222. https://doi.org/10.3354/dao018217

    Article  CAS  Google Scholar 

  39. Wang, Q., Wang, C., Mu, C., et al., A novel C-type lysozyme from Mytilus galloprovincialis: Insight into innate immunity and molecular evolution of invertebrate C-type lysozymes, PLoS One, 2013, vol. 8. https://doi.org/10.1371/journal.pone.0067469

  40. Zhao, J., Qiu, L., Ning, X., et al., Cloning and characterization of an invertebrate type lysozyme from Venerupis philippinarum, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2010, vol. 156. pp. 56–60. https://doi.org/10.1016/j.cbpb.2010.02.001

    Article  CAS  Google Scholar 

  41. Xue, Q.G., Itoh, N., Schey, K.L., et al., A new lysozyme from the eastern oyster (Crassostrea virginica) indicates adaptive evolution of i-type lysozymes, Cell Mol. Life Sci., 2007, vol. 64, pp. 82–95. https://doi.org/10.1007/s00018-006-6386-y

    Article  CAS  PubMed  Google Scholar 

  42. Itoh, N., Xue, Q.G., Li, Y., et al., cDNA cloning and tissue expression of plasma lysozyme in the eastern oyster, Crassostrea virginica, Fish Shellfish Immunol., 2007, vol. 23, pp. 957–968. https://doi.org/10.1016/j.fsi.2007.03.006

    Article  CAS  PubMed  Google Scholar 

  43. Dai, W., Wu, D., Zhang, M., et al., Molecular cloning and functional characterization of a novel i-type lysozyme in the freshwater mussel Cristaria plicata, Microbiol. Immunol., 2015, vol. 59, pp. 744–755. https://doi.org/10.1111/1348-0421.12341

    Article  CAS  PubMed  Google Scholar 

  44. Yue, X., Liu, B., and Xue, Q., An i-type lysozyme from the Asiatic hard clam Meretrix meretrix potentially functioning in host immunity, Fish Shellfish Immunol., 2011, vol. 30, pp. 550–558. https://doi.org/10.1016/j.fsi.2010.11.022

    Article  CAS  PubMed  Google Scholar 

  45. Liu, S., Jiang, X., Hu, X., et al., Effects of temperature on non-specific immune parameters in two scallop species: Argopecten irradians (Lamarck 1819) and Chlamys farreri (Jones & Preston 1904), Aquacult. Res., 2004, vol. 35, pp. 678–682. https://doi.org/10.1111/j.1365-2109.2004.01065.x

    Article  Google Scholar 

  46. Kim, H.J., Lee, J.H., Hur, Y.B., et al., Marine antifreeze proteins: Structure, function, and application to cryopreservation as a potential cryoprotectant, Mar. Drugs, 2017, vol. 15. https://doi.org/10.3390/md15020027

  47. Graham, L.A., Boddington, M.E., Holmstrup, M., et al., Antifreeze protein complements cryoprotective dehydration in the freeze-avoiding springtail Megaphorura arctica, Sci Rep., 2020, vol. 10. https://doi.org/10.1038/s41598-020-60060-z

  48. Ciacci, C., Fabbri, R., Betti, M., et al., Seasonal changes in functional parameters of the hemolymph of Mytilus galloprovincialis, Invertebr. Survival J., 2009, vol. 6, pp. 44–48.

    Google Scholar 

  49. Lacroix, C., Duvieilbourg, E., Guillou, N., et al., Seasonal monitoring of blue mussel (Mytilus spp.) populations in a harbor area: A focus on responses to environmental factors and chronic contamination, Mar. Environ. Res., 2017, vol. 129, pp. 24–35. https://doi.org/10.1016/j.marenvres.2017.04.008

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was supported by the Ministry of Science and Higher Education of the Russian Federation (project no. 0657-2020-0004).

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Authors and Affiliations

  1. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, 690041, Vladivostok, Russia

    A. V. Grinchenko, Y. N. Sokolnikova & V. V. Kumeiko

  2. Far Eastern Federal University, 690950, Vladivostok, Russia

    D. V. Ilyaskina & V. V. Kumeiko

  3. Vrije Universiteit, 1081 HV, Amsterdam, The Netherlands

    D. V. Ilyaskina

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  1. A. V. Grinchenko
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  2. Y. N. Sokolnikova
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Correspondence to A. V. Grinchenko.

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Grinchenko, A.V., Sokolnikova, Y.N., Ilyaskina, D.V. et al. Seasonal Changes in Hemolymph Parameters of the Bivalve Modiolus kurilensis Bernard, 1983 from Vostok Bay, Sea of Japan. Russ J Mar Biol 47, 300–311 (2021). https://doi.org/10.1134/S1063074021040052

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