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Effect of Hydrogen Sulfide Loading on the Activity of Energy Metabolism Enzymes and the Adenylate System in Tissues of the Anadara kagoshimensis Clam

  • ECOLOGICAL PHYSIOLOGY AND BIOCHEMISTRY OF HYDROBIONTS
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Abstract

Species with a high resistance to hypoxia are usually characterized by an increased H2S tolerance of hydrogen sulfide; however, high anaerobic potential cannot be the only explanation for survival in an environment with elevated concentrations of sulfides. The activity of oxidoreductases, as well as parameters of adenylate system were studied in the tissues of hypoxia/anoxia-tolerant clam Anadara kagoshimensis (Tokunaga, 1906) under conditions of experimental H2S loading (HSL). Adult specimens with a shell height of 26–38 mm are used. The control group of clams is kept in an aquarium with an oxygen concentration of 7.0–7.1 mg/L (normoxia). The experimental group is exposed to the effect of HSL created by dissolving sodium sulfide (H2S donor) in water to a final concentration of 6 mg S2–/L; exposure time is 24 h. After the first day of the experiment, the level of O2 in water is 1.8 mg/L and there is no hydrogen sulfide. Some of the clams are exposed to repeated hydrogen sulfide loading (second day of the experiment), and Na2S is introduced to a final concentration of 9 mg S2–/L; by the end of the second day, 1.9 mg S2–/L and trace concentration of O2 (0.03 mg/L) are registered. In the first days of HSL, a high activity of malate dehydrogenase (MDH) against the background of a significant suppression of the activity of lactate dehydrogenase (LDH) and an increase in the values of MDH/LDG index persists; this reflects a strengthening of anaerobic processes in the tissues of anadara with relatively high concentrations of О2 in water (1.8 mg/L). After the second day of HSL, the activity of oxidoreductases in the clam tissues does not change when compared with the first day; however, the value of adenylate energy charge (AEC) persists against the background of a relative decrease in [ATP]. The retention of AEC indicates the ability of the anadara to exist under conditions of hydrogen sulfide contamination and acute forms of hypoxia/anoxia.

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REFERENCES

  1. Arp, A.J. and Childress, J.J., Blood function in the hydrothermal vent vestimentiferan tube worm, Science, 1981, vol. 213, pp. 342–344. https://doi.org/10.1126/science.213.4505.342

    Article  CAS  PubMed  Google Scholar 

  2. Arp, A.J. and Childress, J.J., Sulfide binding by the blood of the hydrothermal vent tube worm Riftia pachyptila, Science, 1983, vol. 219, pp. 295–297. https://doi.org/10.1126/science.219.4582.295

    Article  CAS  PubMed  Google Scholar 

  3. Atkinson, D.E., Energy charge of the adenylate pools as a regulatory parameter. Interaction with feedback modifiers, Biochemistry, 1968, vol. 7, no. 11, pp. 4030–4034. https://doi.org/10.1021/bi00851a033

    Article  CAS  PubMed  Google Scholar 

  4. Bacchiocchi, S. and Principato, G., Mitochondrial contribution to metabolic changes in the digestive gland of Mytilus galloprovincialis during anaerobiosis, J. Exp. Zool., 2000, vol. 286, pp. 107–113. https://doi.org/10.1002/(sici)1097-010x(20000201)286:2<107::aid-jez1>3.0.co;2-8

    Article  CAS  PubMed  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. Buck, L.T., Succinate and alanine as anaerobic end-products in the diving turtle (Chrysemys picta bellii), Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2000, vol. 126, no. 3, pp. 409–413. https://doi.org/10.1016/s0305-0491(00)00215-7

    Article  CAS  Google Scholar 

  7. Cadenas, S., Mitochondrial uncoupling, ROS generation and cardioprotection, Biochim. Biophys. Acta, Bioenerg., 2018, vol. 1859, no. 9, pp. 940–950. https://doi.org/10.1016/j.bbabio.2018.05.019

    Article  CAS  Google Scholar 

  8. Cao, Y., Wang, H.G., Cao, Y.Y., et al., Inhibition effects of protein-conjugated amorphous zinc sulfide nanoparticles on tumor cells growth, J. Nanopart. Res., 2011, vol. 13, pp. 2759–2767. https://doi.org/10.1007/s11051-010-0163-4

    Article  CAS  Google Scholar 

  9. Chew, S.F., Gan, J., and Ip, Y.K., Nitrogen metabolism and excretion in the swamp eel, Monopterus albus, during 6 or 40 days of estivation in mud, Physiol. Biochem. Zool., 2005, vol. 78, no. 4, pp. 620. https://doi.org/10.1086/430233

    Article  CAS  PubMed  Google Scholar 

  10. Cortesi, P., Cattani, O., and Vitali, G., Physiological and biochemical responses of the bivalve Scapharca inaequivalvis to hypoxia and cadmium exposure: erythrocytes versus other tissues, Proceedings of an International Conference Marine Coastal Eutrophication, Bologna, 1992, p. 1041. https://doi.org/10.1016/B978-0-444-89990-3.50090-0

  11. De Zwaan, A., Cortesi, P., Thillart, G., et al., Differential sensitivities to hypoxia by two anoxia-tolerant marine molluscs: A biochemical analysis, Mar. Biol., 1991, vol. 111, no. 3, pp. 343–351.

    Article  Google Scholar 

  12. Doeller, J.E., Kraus, D.W., Colacino, J.M., and Wittenberg, J.B., Gill hemoglobin may deliver sulfide to bacterial symbionts of Solemya velum (Bivalvia, Mollusca), Biol. Bull., 1988, vol. 175, no. 3, pp. 388–396.

    Article  CAS  Google Scholar 

  13. Gäde, G., Energy production during anoxia and recovery in the adductor muscle of the file shell, Lima hians, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 1983, vol. 76, no. 1, pp. 73–77. https://doi.org/10.1016/0305-0491(83)90173-6

    Article  Google Scholar 

  14. 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 

  15. Grieshaber, M.K. and Völkel, S., Animal adaptations for tolerance and exploitation of poisonous sulfide, Annu. Rev. Physiol., 1998, vol. 60, pp. 33–53. https://doi.org/10.1146/annurev.physiol.60.1.33

    Article  CAS  PubMed  Google Scholar 

  16. Grivennikova, V.G. and Vinogradov, A.D., Mitochondrial production of reactive oxygen species, Biochemistry (Moscow), 2013, vol. 78, no. 13, pp. 1490–1511. https://doi.org/10.1134/S0006297913130087

    Article  CAS  PubMed  Google Scholar 

  17. Hand, S.C. and Somero, G.N., Energy metabolism pathways of hydrothermal vent animals: adaptations to a food-rich and sulfide-rich deep-sea environment, Biol. Bull., 1983, vol. 165, pp. 167–181.

    Article  CAS  Google Scholar 

  18. Hochachka, P.W. and Somero, G.N., Biochemical Adaptation: Mechanism and Process in Physiological Evolution, New York: Oxford Univ. Press, 2002.

    Google Scholar 

  19. Holm-Hansen, O. and Booth, C.R., The measurement of adenosine triphosphate in the Ocean and its ecological significance, Limnol. Oceanogr., 1966, vol. 11, no. 4, pp. 510–519. https://doi.org/10.4319/lo.1966.11.4.0510

    Article  CAS  Google Scholar 

  20. Isani, G., Cattani, O., and Tacconi, S., Energy metabolism during anaerobiosis and recovery in the posterior adductor muscle of Scapharca inaequivalvis (Bruguière), Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 1989, vol. 93, no. 1, pp. 193–200.

    Article  Google Scholar 

  21. Kolesnikova, E.E. and Golovina, I.V., Oxidoreductase activities in oxyphilic tissues of the black sea ruff Scorpaena porcus under short-term hydrogen sulfide loading, J. Evol. Biochem. Physiol., 2020, vol. 56, no. 5, pp. 459–470. https://doi.org/10.1134/S0022093020050099

    Article  CAS  Google Scholar 

  22. Kraus, D.W., Heme proteins in sulfide-oxidizing bacteria/mollusc symbioses, Am. Zool., 1995, vol. 35, no. 2, pp. 112–120. https://doi.org/10.1093/icb/35.2.112

    Article  CAS  Google Scholar 

  23. Larade, K. and Storey, K.B., A profile of the metabolic responses to anoxia in marine invertebrates, Cell and Molecular Responses to Stress, Vol. 3: Sensing, Signaling and Cell Adaptation, Amsterdam: Elsevier Sci. B, 2002a.

    Google Scholar 

  24. Larade, K. and Storey, K.B., Reversible suppression of protein synthesis in concert with polysome disaggregation during anoxia exposure in Littorina littorea, Mol. Cell. Biochem., 2002b, vol. 232, nos. 1–2, pp. 121–127.https://doi.org/10.1023/a:1014811017753

    Article  CAS  PubMed  Google Scholar 

  25. Luk’yanova, O.N., ATP-ases as nonspecific molecular biomarkers of the state of aquatic organisms under anthropogenic pollution, Tezisy Dokladov II Mezhdunarodnoi nauchnoi konferentsii “Biotekhnologiya – okhrane okruzhayushchei sredy” (Proc. II Int. Sci. Conf. “Biotechnology in Environmental Protection”), Moscow: Mosk. Gos. Univ., 2004.

  26. Miyamoto, Y. and Iwanaga, C., Effects of sulphide on anoxia-driven mortality and anaerobic metabolism in the ark shell Anadara kagoshimensi, J. Mar. Biology. Assoc. U. K., 2017, vol. 97, no. 2, pp. 329. https://doi.org/10.1017/S0025315416000412

    Article  CAS  Google Scholar 

  27. Nakano, T., Yamada, K., and Okamura, K., Duration rather than frequency of hypoxia causes mass mortality in ark shells (Anadara kagoshimensis), Mar. Pollut. Bull., 2017, vol. 125, nos. 1–2, pp. 86–91. https://doi.org/10.1016/j.marpolbul.2017.07.073

    Article  CAS  PubMed  Google Scholar 

  28. Oeschger, R. and Storey, K.B., Regulation of glycolytic enzymes in the marine invertebrate Halicryptus spinulosus (Priapulida) during environmental anoxia and exposure to hydrogen sulfide, Mar. Biol., 1990, vol. 106, pp. 261–266.

    Article  CAS  Google Scholar 

  29. Orekhova, N.A. and Konovalov, S.K., Oxygen and sulfides in bottom sediments of the coastal Sevastopol Region of Crimea, Oceanology, 2018, vol. 58, no. 5, pp. 679–688.https://doi.org/10.1134/S0001437018050107

    Article  CAS  Google Scholar 

  30. Owen, T.G. and Hochachka, P.W., Purification and properties of dolphin muscle aspartate and alanine transaminases and their possible roles in the energy metabolism of diving mammals, Biochem. J., 1974, vol. 143, no. 3, pp. 541–553. https://doi.org/10.1042/bj1430541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Powell, M.A. and Arp, A.J., Hydrogen sulfide oxidation by abundant nonhemoglobin heme compounds in marine invertebrates from sulfide-rich habitats, J. Exp. Zool., 1989, vol. 249, no. 2, pp. 121–132. https://doi.org/10.1002/jez.1402490202

    Article  CAS  Google Scholar 

  32. Revkov, N.K., Colonization’s features of the Black sea basin by recent invader Anadara kagoshimensis (Bivalvia: Arcidae), Morsk. Biol. Zh., 2016, vol. 1, no. 2, pp. 3–17. https://doi.org/10.21072/mbj.2016.01.2.01

    Article  Google Scholar 

  33. Rosenberg, R., Nilsson, H.C., and Diaz, R.J., Response of benthic fauna and changing sediment redox profiles over a hypoxic gradient, Estuarine, Coastal Shelf Sci., 2001, vol. 53, no. 3, pp. 343–350. https://doi.org/10.1006/ecss.2001.0810

    Article  CAS  Google Scholar 

  34. Sahin, C., Erbay, M., Kalayci, F., et al., Life-history traits of the Black Scorpionfish (Scorpaena porcus) in southeastern Black Sea, Turk. J. Fish. Aquat. Sci., 2019, vol. 19, no. 7, pp. 571–584. https://doi.org/10.4194/1303-2712-v19_7_04

    Article  Google Scholar 

  35. Savina, M.V., Mekhanizmy adaptatsii tkanevogo dykhaniya v evolyutsii pozvonochnykh (Adaptation Mechanisms of Tissue Respiration in Vertebrate Evolution), St. Petersburg: Nauka, 1992.

  36. Soldatov, A.A., Andreenko, T.I., Sysoeva, I.V., and Sysoev, A.A., Tissue specificity of metabolism in the bivalve mollusc Anadara inaequivalvis Br. under conditions of experimental anoxia, J. Evol. Biochem. Physiol., 2009, vol. 45, no. 3, pp. 349–355. https://doi.org/10.1134/S002209300903003X

    Article  CAS  Google Scholar 

  37. Soldatov, A.A., Andreenko, T.I., Golovina, I.V., and Stolbov, A.Ya., Peculiarities of organization of tissue metabolism in mollusks 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 

  38. Soldatov, A.A., Kukhareva, T.A., Andreeva, A.Y., and Efremova, E.S., Erythroid elements of hemolymph in Anadara kagoshimensis (Tokunaga, 1906) under conditions of the combined action of hypoxia and hydrogen sulfide contamination, Rus. J. Mar. Biol., 2018, vol. 44, no. 6, pp. 452–457. https://doi.org/10.1134/S1063074018060111

    Article  CAS  Google Scholar 

  39. 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, no. 6, pp. 912–920. https://doi.org/10.1242/jeb.037473

    Article  CAS  PubMed  Google Scholar 

  40. Stewart, F.J. and Cavanaugh, C.M., Bacterial endosymbioses in Solemya (Mollusca: Bivalvia) —Model systems for studies of symbiont–host adaptation, Antonie Leeuwenhoek, 2006, vol. 90, pp. 343–360. https://doi.org/10.1007/s10482-006-9086-6

    Article  PubMed  Google Scholar 

  41. van Hellemond, J.J., van der Klei, A., van Weelden, S.W., and Tielens, A.G., Biochemical and evolutionary aspects of anaerobically fuctioning mitochondria, Philos. Trans. R. Soc., B, 2003, vol. 358, no. 1429. https://doi.org/10.1098/rstb.2002.1182

  42. Vismann, B., Hematin and sulfide removal in hemolymph of the hemoglobin-containing bivalve Scapharca inaequivalvis, Mar. Ecol. Prog. Ser., 1993, vol. 98, pp. 115–122.

    Article  CAS  Google Scholar 

  43. Völkel, S., Berenbrink, M., Heisler, N., and Nikinmaa, M., Effect of sulfide on K+ flux pathways in red blood cells of crusian carp and rainbow trout, Fish Physiol. Biochem., 2001, vol. 24, pp. 213–223. https://doi.org/10.1023/A:1014050001585

    Article  Google Scholar 

  44. Washizu, T., Nakamura, M., Izawa, N., et al., The activity ratio of the cytosolic MDH/LDH and the isoenzyme pattern of LDH in the peripheral leukocytes of dogs, cats and rabbits, Vet. Res. Commun., 2002, vol. 26, no. 5, pp. 341–346. https://doi.org/10.1023/a:1016278409138

    Article  CAS  PubMed  Google Scholar 

  45. Watanabe, T., Effects of hypoxic and osmotic stress on the free D-aspartate level in the muscle of blood shell Scapharca broughtonii, Amino Acids, 2005, vol. 28, no. 3, pp. 291–296. https://doi.org/10.1007/s00726-005-0188-7

    Article  CAS  PubMed  Google Scholar 

  46. Wijsman, T.C.M., Adenosine phosphates and energy charge in different tissues of Mytilus edulis under aerobic and anaerobic conditions, J. Comp. Physiol., 1976, vol. 107, no. 1, pp. 129–140.

    Article  CAS  Google Scholar 

  47. Yusseppone, M.S., Rocchetta, I., Sabatini, S.E., et al., Inducing the alternative oxidase forms part of the molecular strategy of anoxic survival in freshwater bivalves, Front. Physiol., 2018, vol. 9, art. ID 100. https://doi.org/10.3389/fphys.2018.00100

    Article  PubMed  PubMed Central  Google Scholar 

  48. Zaika, V.E., Konovalov, S.K., and Sergeeva, N.G., The events of local and seasonal hypoxia at the bottom of the Sevastopol bays and their influence on macro-benthos, Morsk. Biol. Zh., 2011, vol. 10, no. 3, p. 15.

    Google Scholar 

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Funding

This work was supported by State Task no. 121041400077-1 and the Russian Foundation for Basic Research, project no. 20-04-00037.

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

    A. A. Soldatov, I. V. Golovina, E. E. Kolesnikova, I. V. Sysoeva & A. A. Sysoev

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Translated by A. Barkhash

Abbreviations: AEC, adenylate energy charge; LDH, lactate dehydrogenase; MDH, malate dehydrogenase; AP, adenylate pool; ATP, triphosphate, ADP, diphosphate, and AMP, adenosine 5-monophosphate; HSL, H2S loading.

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Soldatov, A.A., Golovina, I.V., Kolesnikova, E.E. et al. Effect of Hydrogen Sulfide Loading on the Activity of Energy Metabolism Enzymes and the Adenylate System in Tissues of the Anadara kagoshimensis Clam. Inland Water Biol 15, 632–640 (2022). https://doi.org/10.1134/S1995082922050194

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