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Effect of Salinity on the Oxidoreductase Activity in Tissues of the Ark Clam Anadara kagoshimensis (Tokunaga, 1906), a Black Sea Invader

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Abstract

The effect of salinity on the activity of malate dehydrogenase (MDH, 1.1.1.37), lactate dehydrogenase (LDH, 1.1.1.27), and catalase (1.11.1.6) enzymes involved in the energy metabolism and antioxidant protection has been studied in tissues of Anadara kagoshimensis. Four groups of adult molluscs with the shell length of 37.0–55.5 mm were exposed for two days to different salinity levels (15, 25, 35, and 45‰) at a water temperature of 21°C and constant aeration (6.5 ± 0.3 mg O2/L). The MDH activity reached its maximum level in the foot and hepatopancreas tissues at a salinity level of 35‰ native for this invader; in both cases, the level of this activity exceeded 1.7-fold (p < 0.05) the values obtained for the salinity level of 15 and 25‰. The activity of this enzyme in gills remained stable. A trend toward an increase in the LDH activity by 24–48% in the foot and gill tissues under salinity of 25–35‰ was revealed, while activity of the enzyme in the hepatopancreas remained extremely low in all experiments. A negative correlation (r) between the MDH/LDH index and LDH activity (from −0.66 to −0.82, p < 0.05) was revealed for the foot and gill tissues. The maximum catalase activity in the foot, gill, and hepatopancreas tissues was registered within the salinity range of 25–35‰. In the case of gills, a significant correlation was revealed between the catalase and LDH activities at 25‰ (r = 0.72, p < 0.05) and 35‰ (r = 0.96, p < 0.05) as well as between the catalase and MDH activities (r = 0.71–0.89, p < 0.05) over the whole studied salinity range. A synchronous decrease in the activity of oxidoreductases beyond the optimal salinity range (25–35‰) may be one of the reasons for the growth retardation of the mollusc in water bodies with nonoptimal salinity.

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REFERENCES

  1. Acarli, S., Lok, A., and Yigitkurt, S., Growth and Survival of Anadara inaequivalvis (Bruguiere, 1789) in Sufa Lagoon, Izmir, Turkey, Isr. J. Aquacult.—Bamidgeh, 2012, vol. 64, pp. 2–7. http://hdl.handle.net/10524/23598.

    Google Scholar 

  2. Amira, A., Sifi, K., and Soltani, N., Measure of environmental stress biomarkers in Donax trunculus (Mollusca, Bivalvia) from the gulf of Annaba (Algeria), Eur. J. Exp. Biol., 2011, vol. 1, no. 2, pp. 7–16. http://www.pelagiaresearchlibrary.com.

  3. Anistratenko, V.V. and Khaliman, I.A., Bivalve mollusc Anadara inaequivalvis (Bivalvia, Arcidae) in the northern part of the Sea of Azov: Completion of colonization of the Azov–Black Sea basin, Vestn. Zool., 2006, vol. 40, no. 6, pp. 505–511.

    Google Scholar 

  4. Berger, V.J. and Kharazova, A.D., Mechanisms of salinity adaptations in marine molluscs, Hydrobiologia, 1997, vol. 355, pp. 115–126.

    Article  CAS  Google Scholar 

  5. Bishop, R.E. and Iliffe, T.M., Ecological physiology of the anchialine shrimp Barbouria cubensis: A comparison of epigean and hypogean populations, Mar. Biodiversity, 2012, vol. 42, no. 3, pp. 303–310. https://doi.org/10.1007/s12526-012-0113-8

    Article  Google Scholar 

  6. Boltacheva, N.A., Revkov, N.K., Nadol’nyi, A.A., and Anninskaya, I.N., Benthic fauna of the southwestern Sea of Azov. Macrozoobenthos taxonomic composition and its biocoenotic structure in 2016–2017, Morsk. Biol. Zh., 2022, vol. 7, no. 2, pp. 3–22. https://doi.org/10.21072/mbj.2022.07.2.01

    Article  Google Scholar 

  7. Carregosa, V., Figueira, E., Gil, A.M., Pereira, S., Pinto, J., Soares, A.M., and Freitas, R., Tolerance of Venerupis philippinarum to salinity: Osmotic and metabolic aspects, Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol., 2014, vol. 171, pp. 36–43. https://doi.org/10.1016/j.cbpa.2014.02.009

    Article  CAS  Google Scholar 

  8. Dahlhoff, E.P., Stillman, J.H., and Menge, B.A., Physiological community ecology: Variation in metabolic activity of ecologically important rocky intertidal invertebrates along environmental gradients, Integr. Comp. Biol., 2002, vol. 42, no. 4, pp. 862–871. https://doi.org/10.1093/icb/42.4.862

    Article  PubMed  Google Scholar 

  9. Dmitrieva, N.I., Ferraris, J.D., Norenburg, J.L., and Burg, M.B., The saltiness of the sea breaks DNA in marine invertebrates: Possible implications for animal evolution, Cell Cycle, 2006, vol. 5, pp. 1320–1323. https://doi.org/10.4161/cc.5.12.2867

    Article  CAS  PubMed  Google Scholar 

  10. Dong, Y., Liao, M., Meng, X., and Somero, G.N., Structural flexibility and protein adaptation to temperature: Molecular dynamics analysis of malate dehydrogenases of marine molluscs, Proc. Natl. Acad. Sci., U. S. A. 2018, vol. 115, no. 6, pp. 1274–1279. https://doi.org/10.1073/pnas.1718910115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Gagné, F., André, C., Blaise, C., Pellerin, J., Sherry, J., and Talbot, A., An investigation on the disruptive effect of pollution in cold-and warm-adapted clam populations, Invertebr. Survival J., 2009, vol. 6, no. 2, pp. 144–153.

    Google Scholar 

  12. Gainey, L.F., Jr. and Greenberg, M.J., Hydrogen sulfide is synthesized in the gills of the clam Mercenaria mercenaria and acts seasonally to modulate branchial muscle contraction, Biol. Bull., 2005, vol. 209, no. 1, pp. 11–20. https://doi.org/10.2307/3593138

    Article  CAS  PubMed  Google Scholar 

  13. Gietl, C., Malate dehydrogenase isoenzymes: Cellular locations and role in the flow of metabolites between the cytoplasm and cell organelles, Biochim. Biophys. Acta, Bioenerg., 1992, vol. 1100, no. 3, pp. 217–234. https://doi.org/10.1016/0167-4838(92)90476-T

    Article  CAS  Google Scholar 

  14. Girin, S.V., Modification of the method for determining catalase activity in biological substrates, Lab. Diagn., 1999, no. 4, pp. 45–46.

  15. Golovina, I.V., Resistance to negative effects and the ratio of energy metabolism enzyme activity in tissues of the Black Sea molluscs Mytilus galloprovincialis Lamarck, 1819 and Anadara kagoshimensis (Tokunaga, 1906), Morsk. Biol. Zh., 2019, vol. 4, no. 3, pp. 37–47. https://doi.org/10.21072/mbj.2019.04.3.04

    Article  Google Scholar 

  16. Golovina, I.V., Gostyukhina, O.L., and Andreyenko, T.I., Specific metabolic features in tissues of the ark clam Anadara kagoshimensis Tokunaga, 1906 (Bivalvia: Arcidae), a Black Sea invader, Russ. J. Biol. Invasions, 2016, vol. 7, no. 2, pp. 137–145. https://doi.org/10.1134/S2075111716020065

    Article  Google Scholar 

  17. Goromosova, S.A., and Shapiro, A.Z., Osnovnye cherty biokhimii energeticheskogo obmena midii (The Main Features of the Biochemistry of Mussel Energy Metabolism), Moscow: Legk. Pishch. Prom-st’, 1984.

  18. Gostyukhina, O.L., Soldatov, A.A., Golovina, I.V., and Borodina, A.V., Content of carotenoids and the state of tissue antioxidant enzymatic complex in bivalve mollusc Anadara inaequivalvis Br., J. Evol. Biochem. Physiol., 2013, vol. 49, no. 3, pp. 309–315. https://doi.org/10.1134/S0022093013030055

    Article  CAS  Google Scholar 

  19. Haider, F., Sokolov, E.P., Timm, S., Hagemann, M., Rayon, E.B., Marigomez, I., Izagirre, U., and Sokolova, I.M., Interactive effects of osmotic stress and burrowing activity on protein metabolism and muscle capacity in the soft shell clam Mya arenaria, Comp. Biochem. Physiol., 2019, vol. 228, pp. 81–93. https://doi.org/10.1016/j.cbpa.2018.10.022

    Article  CAS  Google Scholar 

  20. Hermes-Lima, M. and Zenteno-Savin, T., Animal response to drastic changes in oxygen availability and physiological oxidative stress, Comp. Biochem. Physiol., Part C: Toxicol. Pharmacol., 2002, vol. 133, no. 4, pp. 537–556.

    Google Scholar 

  21. Kiseleva, M.I., Comparative characteristics of benthic communities off the coast of the Caucasus, in Mnogoletnie izmeneniya zoobentosa Chernogo morya (Long-Term Changes in the Zoobenthos of the Black Sea), Kyiv: Naukova Dumka, 1992, pp. 84–99.

  22. Kladchenko, E.S., Andreyeva, A.Yu., Kukhareva, T.A., Rychkova, V.N., Soldatov, A.A., and Mindukshev, I.V., Impact of low salinity on hemocytes morphology and functional aspects in alien clam Anadara kagoshimensis (Tokunaga, 1906), Russ. J. Biol. Invasions, 2021, vol. 12, no. 2, pp. 203–212. https://doi.org/10.1134/S2075111721020089

    Article  Google Scholar 

  23. Kolyuchkina, G.A., Syomin, V.L., Spiridonov, V.A., Zalota, A.K., Biryukova, S.V., Basin, A.B., Simakova, U.V., and Nabozhenko, M.V., The resilience of macrozoobenthos of boreal coastal lagoons to non-indigenous species invasion: A case study of Taman Bay (the Sea of Azov), Reg. Stud. Mar. Sci., 2019, vol. 28, p. 100573. https://doi.org/10.1016/j.rsma.2019.100573

    Article  Google Scholar 

  24. Krapal, A.-M., Popa, O.P., Levarda, A.F., Iorgu, E.I., Costache, M., Crocetta, F., and Popa, L.O., Molecular confirmation on the presence of Anadara kagoshimensis (Tokunaga, 1906) (Mollusca: Bivalvia: Arcidae) in the Black Sea, Trav. Mus. Natl. Hist. Nat. “Grigore Antipa,” 2014, vol. 57, no. 1, pp. 9–12. https://doi.org/10.2478/travmu-2014-0001

    Article  Google Scholar 

  25. Mil’man, L.S., Yurovetskii, Yu.G., and Ermolaeva, L.P., Determination of the activity of the most important enzymes of carbohydrate metabolism, in Metody biologii razvitiya (Methods of Developmental Biology), Moscow, 1974, pp. 346–364.

  26. Miroshnichenko, O.S., Biogenesis, physiological role, and properties of catalase, Biopolym. Cell, 1992, vol. 8, no. 6, pp. 3–25. https://doi.org/10.7124/bc.00033C

    Article  CAS  Google Scholar 

  27. Nie, H., Jahan, K., Zhang, W., Huo, Z., and Yan, X., Physiological and biochemical responses of different shell color strains of Manila clam to low salinity challenges, Aquacult. Rep., 2020, vol. 16, p. 100260. https://doi.org/10.1016/j.aqrep.2019.100260

    Article  Google Scholar 

  28. Paganini, A., Kimmerer, W.J., and Stillman, J.H., Metabolic responses to environmental salinity in the invasive clam Corbula amurensis, Aquat. Biol., 2010, vol. 11, pp. 139–147. https://doi.org/10.3354/ab00304

    Article  Google Scholar 

  29. Rinaldi, E., Rapana venosa (Valenciennes) spiaggiata in notevole quantità sulla spiaggia di Rimini (Fo), Boll. Malacol., 1985, vol. 16, pp. 9–17.

    Google Scholar 

  30. Sarà, G., Romano, C., Widdows, J., and Staff, F.J., Effect of salinity and temperature on feeding physiology and scope for growth of an invasive species (Brachidontes pharaonis—Mollusca: Bivalvia) within the Mediterranean Sea, J. Exp. Mar. Biol. Ecol., 2008, vol. 363, nos. 1–2, pp. 130–136. https://doi.org/10.1016/j.jembe.2008.06.030

    Article  Google Scholar 

  31. Shin, Y.K., Lee, W.C., Jun, R.H., Kim, S.Y., and Park, J.J., Survival of the ark shell Scapharca subcrenata and physiological and histological changes at decreasing salinity, Fish. Aquat. Sci., 2009, vol. 12, no. 3, pp. 209–218. https://doi.org/10.5657/fas.2009.12

    Article  Google Scholar 

  32. Shurova, N.M., Strukturno-funktsional’naya organizatsiya populyatsii midii Mytilus galloprovincialis Chernogo morya (Structural and Functional Organization of the Mussel Population Mytilus galloprovincialis in the Black Sea), Kyiv: Naukova Dumka, 2013.

  33. Sokolova, I.M., Sukhotin, A.A., and Lannig, G., Stress effects on metabolism and energy budgets in molluscs, in Oxidative Stress in Aquatic Ecosystems, Part IV, Abele, D., Vazquez-Medina, J.P., Zenteno-Savín, T., Eds., New York: Blackwell, 2012, pp. 263–280. https://doi.org/10.1002/9781444345988.ch19.

  34. Sokołowski, A., Świeżak, J., Hallmann, A., Olsen, A.J., Ziółkowska, M., Øverjordet, I.B., Nordtug, T., Altin, D., Krause, D.F., Salaberria, I., and Smolarz, K., Cellular level response of the bivalve Limecola balthica to seawater acidification due to potential CO2 leakage from a sub-seabed storage site in the southern Baltic Sea: TiTank experiment at representative hydrostatic pressure, Sci. Total Environ., 2021, vol. 794, p. 148593. https://doi.org/10.1016/j.scitotenv.2021.148593

    Article  CAS  PubMed  Google Scholar 

  35. Soldatov, A.A., Andreenko, T.I., Golovina, I.V., and Stolbov, A.Y., Peculiarities of organization of tissue metabolism in molluscs with different tolerance to external hypoxia, J. Evol. Biochem. Physiol., 2010, vol. 46, no. 4, pp. 341–349. https://doi.org/10.1134/S0022093010040022

    Article  CAS  Google Scholar 

  36. Somero, G.N., The physiology of climate change: How potentials for acclimatization and genetic adaptation will determine “winners” and “losers,” J. Exp. Biol., 2010, vol. 213, pp. 912–920. https://doi.org/10.1242/jeb.037473

    Article  CAS  PubMed  Google Scholar 

  37. Somero, G.N., Lockwood, B.L., and Tomanek, L., Biochemical Adaptation: Response to Environmental Challenges from Life’s Origins to the Anthropocene, Sunderland: Sinauer Associates, 2017, p. 572.

    Google Scholar 

  38. Steed, J.W. and Atwood, J.L., Supramolecular Chemistry, Chichester: Wiley, Ltd., 2000.

    Google Scholar 

  39. Strafella, P., Ferrari, A., Fabi, G., Salvalaggio, V., Punzo, E., Cuicchi, C., Santelli, A., Cariani, A., Tinti, F., Tassetti, A.N., and Scarcella, G., Anadara kagoshimensis (Mollusca: Bivalvia: Arcidae) in Adriatic Sea: Morphological analysis, molecular taxonomy, spatial distribution, and prediction, Mediterr. Mar. Sci., 2017, vol. 18, no. 3, pp. 443–453. https://doi.org/10.12681/mms.1933

    Article  Google Scholar 

  40. Suzuki, H., Yamaguchi, K., and Seto, K., Effect of hypoxia and low salinity on growth and survival of the ark shell Scapharca kagoshimensis through the field experiment in Lake Nakaumi, Southwest Japan, Aquacult. Sci., 2012, vol. 60, no. 2, pp. 261–268. https://doi.org/10.11233/aquaculturesci.60.261

    Article  Google Scholar 

  41. Taylor, A.M., Maher, W.A., and Ubrihien, R.P., Mortality, condition index and cellular responses of Anadara trapezia to combined salinity and temperature stress, J. Exp. Mar. Biol. Ecol., 2017, vol. 497, pp. 172–179. https://doi.org/10.1016/j.jembe.2017.09.023

    Article  CAS  Google Scholar 

  42. Velez, C., Figueira, E., Soares, A.M., and Freitas, R., Native and introduced clams biochemical responses to salinity and pH changes, Sci. Total Environ., 2016, vol. 566, pp. 260–268. https://doi.org/10.1016/j.scitotenv.2016.05.019

    Article  CAS  PubMed  Google Scholar 

  43. Vysotskaya, R.U., Lomaeva, T.A., Taksheev, S.A., Amelina, V.S., and Bakhmet, I.N., Activity of lysosomal and some other enzymes in mussel tissues at different levels of salinity, in Problemy izucheniya, ratsional’nogo ispol’zovaniya i okhrany resursov Belogo morya (Problems of Study, Rational Use and Protection of the White Sea Resources), Petrozavodsk: PIN, 2005, pp. 72–75.

  44. Wang, Q., Xie, X., Zhang, M., Teng, W., Liang, M., Kong, N., Wang, C., and Zhou, Z., Effects of temperature and salinity on survival and growth of juvenile ark shell Anadara broughtonii, Fish. Sci., 2017, vol. 83, pp. 619–624. https://doi.org/10.1007/s12562-017-1095-z

    Article  CAS  Google Scholar 

  45. Yancey, P.H. and Siebenaller, J.F., Co-evolution of proteins and solutions: Protein adaptation versus cytoprotective micromolecules and their roles in marine organisms, J. Exp. Biol., 2015, vol. 218, no. 12, pp. 1880–1896. https://doi.org/10.1242/jeb.114355

    Article  PubMed  Google Scholar 

  46. Yancey, P.H., Clark, M.E., Hand, S.C., Bowlus, R.D., and Somero, G.N., Living with water stress: Evolution of osmolyte systems, Science, 1982, vol. 217, no. 4566, pp. 1214–1222. https://doi.org/10.1126/science.7112124

    Article  CAS  PubMed  Google Scholar 

  47. Yusseppone, M.S., Rocchetta, I., Sabatini, S.E., Luquet, C.M., Ríos de Molina, M.D.C., Held, C., and Abele, D., Inducing the alternative oxidase forms part of the molecular strategy of anoxic survival in freshwater bivalves, Front. Physiol., 2018, vol. 9, pp. 100–112. https://doi.org/10.3389/fphys.2018.00100

    Article  PubMed  PubMed Central  Google Scholar 

  48. Zhang, M., Li, L., Liu, Y., and Gao, X., Effects of a sudden drop in salinity on immune response mechanisms of Anadara kagoshimensis, Int. J. Mol. Sci., 2019, vol. 20, no. 18, pp. 4365–4384. https://doi.org/10.3390/ijms20184365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Zhivoglyadova, L.A., Revkov, N.K., Frolenko, L.N., and Afanasyev, D.F., The expansion of the bivalve mollusc Anadara kagoshimensis (Tokunaga, 1906) in the Sea of Azov, Russ. J. Biol. Invasions, 2021, vol. 12, no. 2, pp. 192–202. https://doi.org/10.1134/S2075111721020120

    Article  Google Scholar 

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ACKNOWLEDGMENTS

The author is grateful to Oksana Yurievna Vyalova, a senior researcher of the Animal Physiology and Biochemistry Department of the Federal Research Center Institute of Biology of the Southern Seas, for the organization of a sample collection under field conditions and transportation of collected molluscs to the laboratory.

Funding

The study was carried out within the framework of the State Assignment of the Federal Research Center Institute of Biology of the Southern Seas “Functional, Metabolic, and Toxicological Aspects of the Occurrence of Hydrobionts and Their Populations in Biotopes Differing in Their Physicochemical Regimes” (theme no. 121041400077-1).

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  1. Kovalevsky Institute of Biology of the Southern Seas, Russian Academy of Sciences, 299011, Sevastopol, Russia

    I. V. Golovina

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Conflict of interest. The author declares that she has no conflicts of interest.Statement of the welfare of animals. All experimental protocols were performed in accordance with the EU guidelines on the use of animals for experimental and other scientific purposes (86/609/CEE) and in compliance with the rules approved by the Order of the Presidium of the USSR Academy of Sciences no. 12000-496 (April 2, 1980) and the Order of the USSR Ministry of Higher Education no. 22 (September 13, 1984). All efforts were made to use the minimum number of animals required to obtain reliable scientific data.

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Golovina, I.V. Effect of Salinity on the Oxidoreductase Activity in Tissues of the Ark Clam Anadara kagoshimensis (Tokunaga, 1906), a Black Sea Invader. Russ J Biol Invasions 14, 299–307 (2023). https://doi.org/10.1134/S2075111723030074

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