Skip to main content
SpringerLink
Log in

Carotenoid Content and Antioxidant Status in Tissues of the Eurybiontic Bivalve Mollusk Cerastoderma glaucum (Cardiidae)

  • Comparative and Ontogenic Biochemistry
  • Published:
Journal of Evolutionary Biochemistry and Physiology Aims and scope Submit manuscript

Abstract

The relationship between the total carotenoid content and the state of the antioxidant (AO) complex was studied in tissues of the eurybiontic Black Sea bivalve mollusk Cerastoderma glaucum (Bruguière, 1789) from natural habitats, which has a high oxidative stress tolerance. In the hepatopancreas, gills and foot, the total carotenoid content, glutathione peroxidase (GP), glutathione reductase (GR), superoxide dismutase (SOD) and catalase activities, as well as the level of reduced glutathione (G-SH) and TBA-reactive products were determined. A direct correlation was established between the total carotenoid content and the GSH level (R 2 = 0.98) and GP activity (R 2 = 0.84). This correlation reflects a possible synergistic interaction between these systems when performing AO functions. An inverse relationship was found between the total carotenoid content and SOD and catalase activities (R 2 = 0.97 and 0.98, respectively), which may be due to a possible competitive interrelationship of these two systems. The revealed correlations reflect specific interrelationships between carotenoids and the AO complex in the clam C. glaucum, as well as their role in the formation of adaptive responses of the mollusk to oxidative stress. They can also serve a starting point for further research aimed at obtaining biologically active substances with antioxidant properties from mollusk tissues.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

Abbreviations

AO:

antioxidant

AGS:

antioxidant glutathione system

ROS:

reactive oxygen species

GSH:

reduced glutathione

GSSG:

oxidized glutathione

GP:

glutathione peroxidase

GR:

glutathione reductase

MDA:

malondialdehyde

OS:

oxidative stress

LPO:

lipid peroxidation

FRO:

free-radical oxidation

SOD:

superoxide dismutase

SOAR:

superoxide anion radical

TCC:

total carotenoid content

TBARS:

thiobarbituric acid-reactive substances

REFERENCES

  1. Matsuno, T., Aquatic animal carotenoids, Fish. Sci. (Tokyo, Japan), 2001, vol. 67(5), pp. 771–783.

  2. Leontarakis, P.K., Loukia, I., Xatzianastasiou, L.I., and Theodorou, J.A., Biological aspects of the lagoon cockle, Cerastoderma glaucum (Poiret, 1879), in a coastal lagoon in Keramoti, Greece in the Northeastern Mediterranean, J. Shellfish Res., 2008, vol. 27(5), pp. 1171–1175.

  3. Letendre, F., Leboulenger, J., and Durand, F., Oxidative challenge and redox sensing in molluscs: effects of natural and anthropic stressors, Oxidative Stress in Vertebrates and Invertebrates: Molecular Aspects of Oxidative Stress on Cell Signaling, Farooqui, T. and Farooqui, A.A., Eds., Hoboken, NJ, Wiley-Blackwell, 2011.

  4. Maoka, T., Carotenoids in marine animals, J. Agric. Food Chem., 2011, vol. 9, pp. 278–293.

  5. Woo, S., Denis, V., and Won, H., Expressions of oxidative stress-related genes and antioxidant enzyme activities in Mytilus galloprovincialis (Bivalvia, Mollusca) exposed to hypoxia, Zool. Stud., 2013, vol. 52(15), pp. 1–8.

  6. Soldatov, A.A., Gostyukhina, O.L., Borodina, A.V., and Golovina, I.V., Qualitative composition of carotenoids, catalase and superoxide dismutase activities in tissues of the bivalve mollusc Anadara inaequivalvis (Bruguiere, 1789), J. Evol. Biochem. Physiol., 2013, vol. 49(4), pp. 389–398.

  7. Soldatov, A.A., Gostyukhina, O.L., Borodina, A.V., and Golovina, I.V., Glutathione antioxidant complex and carotenoid composition in tissues of the bivalve mollusk Anadara kagoshimensis (Tokunaga, 1906), J. Evol. Biochem. Physiol., 2017, vol. 53(4), pp. 289–297.

  8. Gostyukhina, O.L. and Andreenko, T.I., Enzymatic and low-molecular-weight units of antioxidant complex in two species of the Black Sea mollusks with different resistance to oxidative stress: Mytilus galloprovincialis Lam. and Anadara kagoshimensis (Tokunaga, 1906), Zh. Obshchei Biol., 2018, vol. 79(6), pp. 483–493.

  9. Maria, V.L. and Bebianno, M.J., Antioxidant and lipid peroxidation responses in Mytilus galloprovincialis exposed to mixtures of benzo(a)pyrene and copper, Comp. Biochem. Physiol. Pt. C: Toxicol. Pharmacol., 2011, vol. 154(1), pp. 56–63.

  10. Soldatov, A.A., Gostyukhina, O.L., and Golovina, I.V., Functional states of antioxidant enzymatic complex of tissues of Mytillus galloprovincialis Lam. under conditions of oxidative stress, J. Evol. Biochem. Physiol., 2014, vol. 50(3), pp. 206–214.

  11. Woodall, A.A., Britton, G., and Jackson, M.J., Carotenoids and protection of phospholipids in solution or in liposomes against oxidation by peroxyl radicals: relationship between carotenoid structure and protective ability, Biochim. Biophys. Acta, 1997, vol. 1336, pp. 575–586.

  12. Carotenoids. Natural Functions, Britton, G., Liaaen-Jonsen, S., and Pfander, H., Eds., Basel, Switzerland, vol. 4, 2008, p. 370.

  13. Suhnel, S., Lagreze, F., and Ferreira, J.F., Carotenoid extraction from the gonad of the scallop Nodipecten nodosus (Linnaeus, 1758) (Bivalvia: Pectinidae), Brazil. J. Biol., 2009, vol. 69(1), pp. 209–215.

  14. Gostiukhina, 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(3), pp. 309–315.

  15. Freitas, R., Costa, E., and Velez, C., Looking for suitable biomarkers in benthic macroinvertebrates inhabiting coastal areas with low metal contamination: Comparison between the bivalve Cerastoderma edule and the polychaete Diopatra neapolitana, Ecotoxicol. Environ. Safety, 2012, vol. 75, pp. 109–118.

  16. Marques, A., Pilo, D., Araujo, O., Pereira, F., Guilherme, S., Carvalho, S., Santos, A.M., Pacheco, M., and Pereira, P., Propensity to metal accumulation and oxidative stress responses of two benthic species (Cerastoderma edule and Nephtys hombergii): are tolerance processes limiting their responsiveness? Ecotoxicol., 2016, vol. 25(4), pp. 664–676.

  17. Shashkina, M.Y., Shashkin, P.N., and Sergeev, A.V., Carotenoids as a base for development of cancer chemoprevention, Ross. Bioterapevt. Zh., 2009, vol. 8(4), pp. 91–98.

  18. Besednova, N.N., Sea hydrobionts—potential sources of drugs, Zdor. Med. Ekol. Nauka, 2014, vol. 3(57), pp. 4–10.

  19. Manduzio, H., Rocher, B., Durand, F., Galap, C., and Leboulenge, F., The point about oxidative stress in mollusks, a review, ISJ, 2005, vol. 2, pp. 91–104.

  20. Belcheva, N.N., Dovzhenko, N.V., Istomina, A.A., Zhukovskaya, A.F., and Kukla, S.P., The antioxidant system of the Gray’s mussel Crenomytilus grayanus (Dunker, 1853) and the Japanese scallop Mizuhopecten yessoensis (Jay, 1857) (Mollusca: Bivalvia), Biol. Morya, 2016, vol. 42(5), pp. 375–380.

  21. Gostyukhina, O.L. and Andreenko, T.I., Tissue metabolism and the state of the antioxidant complex in the Black Sea mollusks Anadara kagoshimensis (Tokunaga, 1906) and Mytilus galloprovincialis (Lamarck, 1819) with different tolerances to oxidative stress, Russ. J. Mar. Biol., 2019, vol. 45(3), pp. 211–220.

  22. Boyden, C.R., The behaviour, survival and respiration of the cockles Cerastoderma edule and C. glaucum in air, J. Mar. Biol. Ass. U.K., 1972, vol. 52(3), pp. 661–680.

  23. Welker, A.F., Moreira, D., Campos, E., and Hermes-Lima, M., Role of redox metabolism for adaptation of aquatic animals to drastic changes in oxygen availability, Comp. Biochem. Physiol. Pt. A: Mol. Integr. Physiol., 2013, vol. 165(4), pp. 384–404.

  24. Fokina, N.N., Nefеdova, Z.A., and Nemova, N.N., Biochemical adaptations of marine bivalves to anoxic conditions, a review, Trudy Karel’skogo Nauchnogo Tsentra RAN, 2011, vol. 3, pp. 121–130.

  25. Viarengo, A., Canesi, L., Garcia Martinez, P., Peters, L.D., and Livingston, D.R., Pro-oxidant processes and antioxidant defense systems in the tissues of the Antarctic scallop (Adamussium colbecki) compared with the Mediterranean scallop (Pecten jacobaeus), Comp. Biochem. Physiol. Pt. B: Biochem. Mol. Biol., 1995, vol. 111(1), pp. 119–126.

  26. Shashkina, M.Y., Shashkin, P.N., and Sergeev, A.V., Carotenoids in human health and prevention of diseases, Ross. Bioterapevt. Zh., 2010, vol. 9(1), pp. 77–86.

  27. Maoka, T. and Akimoto, N., Natural product chemistry in carotenoid some experimental techniques for structural elucidation and analysis of natural carotenoids, Carotenoid Sci., 2008, vol. 13, pp. 10–17.

  28. Karnaukhov, V.N., Biologicheskie funktsii karotinoidov (Biological Functions of Carotenoids), Moscow, 1998.

  29. Pereslegina, I.A., The activity of antioxidant enzymes in the saliva of healthy children, Lab. Delo, 1989, vol. 11, pp. 20–23.

  30. Nishikimi, M., Rao, N.A., and Yagi, K., Occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen, Biochem. Biophys. Res. Commun., 1972, vol. 46, pp. 849–854.

  31. Girin, S.V., Modification of method of determination of catalase activity in biological substrates, Lab. Diagnost., 1999, vol. 4, pp. 45–46.

  32. Putilina, F.E., Determination of reduced glutathione content in tissues, Metody biokhimicheskikh issledovanii (Methods of Biochemical Research), Leningrad, 1982.

  33. Ohkawa, H., Ohishi, N., and Yagi, K., Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction, Anal. Biochem., 1979, vol. 95(1), pp. 351–358.

  34. Yeum, K.J., Aldini, G., Russell, R.M., and Krinsky, N.I., Antioxidant/pro-oxidant actions of carotenoids, Carotenoids, Carotenoids, vol. 5, Britton, G., Pfander, H., and Liaaen-Jensen, S., Eds., Basel, 2009.

  35. Men’shchikova, E.B. and Zenkov, N.K., Antioxidants and inhibitors of radical oxidative processes, Usp. Sovr. Biol., 1993, vol. 113(4), pp. 442–455.

  36. Shimidzu, N., Goto, M., and Miki, W., Carotenoids as singlet oxygen quenchers in marine organisms, Fish. Sci. (Tokyo, Japan), 1996, vol. 62(1), pp. 134–137.

  37. Osipov, A.N., Azizova, O.A., and Vladimirov, Y.A., Rective oxygen species and their role in the organism, Usp. Biol. Khim., 1990, vol. 31, pp. 180–189.

  38. Polyakov, N.E. and Leshina, T.V., Certain aspects of the reactivity of carotenoids, redox processes and complexation, Russ. Chem. Rev., 2006, vol. 75(12), pp. 1049–1064.

  39. Men’shchikova, E.B., Lankin, V.Z., and Zenkov, N.K., Okislitel’nyi stress. Prooksidanty i antioksidanty (Oxidative Stress. Prooxidants and Antioxidants), Moscow, 2006.

  40. Lipinski, B., Hydroxyl radical and its scavengers in health and disease, Oxid. Med. Cell. Longevity, 2011, vol. 211, pp. 1–9.

  41. Vengerovsky, A.I., Pharmacological methods of regulation of liver functions, Byull. Sibir. Med., 2002, vol. 1, pp. 25–29.

  42. Trevisan, R., Mello, D., Delapedra, G., Silva, D., Arl, M., Danielli, N., and Dafre, A., Gills as a glutathione-dependent metabolic barrier in Pacific oysters Crassostrea gigas: absorption, metabolism and excretion of a model electrophile, Aquat. Toxicol., 2016, vol. 173, pp. 105–119.

  43. Broom, M.J., The biology and culture of marine bivalve mollusks of the genus Anadara, ICLARM Studies and Reviews 12, International Center for Living Aquatic Resources Management, Manila, Philippines, 1985.

  44. Soldatov, A.A., Aleksandrova, O.L., Golovina, I.V., and Stolbov, A.Ya. Enzyme system of antioxidant defense in the Black Sea mollusk Mytilus galloprovincialis Lam. with pigmented and depigmented tissue structures, Dokl. Nat. Akad. Nauk Ukr., 2003, vol. 5, pp. 162–170.

  45. Gostyukhina, O.L., Soldatov, A.A., and Golovina, I.V., Antioksidantnyi fermentny kompleks tkanei chernomorskikh dvustvorchatykh mollyuskov. Chernomorskie mollyuski: elementy sravnitelnoi i ekologicheskoi biokhimii (Antioxidant Enzyme Complex in Tissues of Black Sea Bbivalve Shellfish. Black Sea Clams: Elements of Comparative and Ecological Biochemistry), Sevastopol, 2014.

  46. Meng, Z., Zhang, B., Liu, B., Li, H., Fan, S., and Yu, D., High carotenoids content can enhance resistance of selected Pinctada fucata families to high temperature stress, Fish Shellfish Immunol., 2017, vol. 61, pp. 211–218.

  47. Rudneva, I.I., Antioxidant system of Black Sea animals in early development, Comp. Biochem. Physiol. Pt. C: Toxicol. Pharmacol., 1999, vol. 122(2), pp. 265–271.

Download references

Funding

This work was implemented within a state assignment to the A.O. Kovalevsky Institute of Biology of the Southern Seas, Russian Academy of Sciences (reg. no. АААА-А18-118021490093-4 of 14.02.2018).

Author information

Authors and Affiliations

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

    O. L. Gostyukhina & A. V. Borodina

Authors
  1. O. L. Gostyukhina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. V. Borodina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to O. L. Gostyukhina or A. V. Borodina.

Ethics declarations

All applicable international, national and institutional principles of handling and using experimental animals for scientific purposes were observed. This study did not involve human subjects as research objects.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gostyukhina, O.L., Borodina, A.V. Carotenoid Content and Antioxidant Status in Tissues of the Eurybiontic Bivalve Mollusk Cerastoderma glaucum (Cardiidae). J Evol Biochem Phys 56, 195–206 (2020). https://doi.org/10.1134/S0022093020030023

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0022093020030023

Keywords:

Search

Navigation