Long-term monitoring of a coastal marine ecosystem after landfill remediation using oxidative stress biomarkers and heavy metal analysis in mussels

Abstract

Gornostay Bay, located near the city of Vladivostok (Far East of Russia), has long served as a site for the placement and operation of a solid domestic waste landfill. The functioning of the landfill resulted in extensive and complex pollution of the coastal water area. Remediation and closure measures in 2010 were expected to improve the ecological condition of the bay. This study demonstrates the application of biochemical markers of oxidative stress as indicators of metabolic recovery processes in marine invertebrates, using bivalves as a model group. The results demonstrated a time-dependent decrease in the concentrations of potentially toxic elements in mussel tissues and a reduction in oxidative lipid degradation to control levels. These findings indicate an improvement in the quality of the marine environment in the years following the 2010 landfill remediation activities. Based on molecular indicators of oxidative stress and the content of heavy metals in the digestive gland and gills of Crenomytilus grayanus from polluted Gornostay Bay, the study concludes that a gradual restoration of the marine environment has occurred.

Keywords

Biomonitoring / Potentially toxic elements / Landfill / Marine environmental remediation / Mussels / Oxidative stress

Funding

This research was supported by the V.I. Il’ichev Pacific Oceanological Institute, Far Eastern Branch of the Russian Academy of Sciences, through the research project “Ecological and Biogeochemical Processes in Ecosystems of the Far Eastern Seas”(project number 124022100077-0).

Conflict of interest

The authors declare no conflicts of interest.

References

[1] Nicholson, S, Lam, PK. Pollution monitoring in Southeast Asia using biomarkers in the mytilid mussel Perna viridis (Mytilidae: Bivalvia). Environ Int. 2005: 31(1):121-132. doi: 10.1016/j.envint.2004.05.007

[2] Valavanidis, A, Vlahogianni, T, Dassenakis, M, Scoullos, M. Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol Environ Saf. 2006: 64(2):178-189. doi: 10.1016/j.ecoenv.2005.03.013

[3] Belcheva, NN, Zakhartsev, MV, Dovzhenco, NV, Zhukovskaya, AF, Kavun, VY, Chelomin, VP. Anthropogenic pollution stimulates oxidative stress in soft tissues of mussel Crenomytilus grayanus. Ocean Sci. J. 2011; 46:85-94. doi: 10.1007/s12601-011-0008-9

[4] Emmanouil, C, Smart, DJ, Hodges, NJ, Chipman, JK.Oxidative damage produced by Cr(VI) and repair in mussel (Mytilus edulis L.) gill. Mar Environ Res. 2006; 62:292-296. doi: 10.1016/j.marenvres.2006.04.024

[5] Sedova, LG, Sokolenko, DA. State of settlements, resources and fishery of Gray mussel Crenomytilus grayanus at the coast of Primorsky Region (Japan Sea). Izv. TINRO. 2019; 198(3):33-45. doi: 10.26428/1606-9919-2019-198-33-45

[6] Kovekovdova, LT, Simokon, MV. Tendencies of change in the chemoecological situation in coastal area of Primorye. Toxic elements in bottom sediments and aquatic organisms. Izv. TINRO. 2004; 137:310-320.

[7] Shulkin, VM. Metally v Ekosistemakh Morskikh Melkovodii (PTEs in Marine Shallow-Water Ecosystems). Russian: Dalnauka, Vladivostok; 2004.

[8] Tkalin, AV, Lishavskaya, TS, Shulkin, VM. Radionuclides and trace metals in mussels and bottom sediments around Vladivostok, Russia. Mar Pollut Bull. 1998; 36(7):511-554. doi: 10.1016/S0025-326X(98)00030-7

[9] Khristoforova, NK, Gnetetskiy, AV. The contents of PTEs in long-lived mytilids from Ussuriisky bay. Russ J Mar Biol. 2022; 48:26-32. doi: 10.1134/S1063074022010060

[10] Ramu, K, Kajiwara, N, Isobe, T, et al. Spatial distribution and accumulation of brominated flame retardants, polychlorinated biphenyls and organochlorine pesticides in blue mussels (Mytilus edulis) from coastal waters of Korea. Environ Pollut. 2007; 148(2):562-569. doi: 10.1016/j.envpol.2006.11.034

[11] Tkalin, A, Lishavskaya, TS, Hills, JW. Persistent organic pollutants in mussels and bottom sediments from peter the great bay near vladivostok. Ocean Res. 1997; 19(2):115-119.

[12] Anikiev, VV, Kosenkova, ST, Savel’eva, NI, Voloshin, GY, Dudarev, OV.Statistical zoning of the spatial distribution of trace elements in the bottom sediments of the peter the great gulf, the Sea of Japan. Geochem Int. 2000; 38(6):603-614.

[13] Yatsuk, AV, Obzhirov, AI, Gresov, AI, Korovitskaya, EV. Gas geochemical research and geoecology of the dump of Vladivostok city. In: Current Ecological State of Peter the Great Bay, Sea of Japan. Vladivostok: Far Eastern Federal University Press; 2012. p. 426-437.

[14] Tkalin, AV, Samsonov, DP, Lishavskaya, TS, Chernik, GV. New data on organochlorine distributions in the marine environment near Vladivosto. Mar Poll Bull. 2000; 40(10):879-881. doi: 10.1016/S0025-326X(00)00091-6

[15] Di Giulio, RT, Washburn, PC, Wenning, RJ, Winston, GW, Jewell, CS. Biochemical responses in aquatic animals: A review of determinants of oxidative stress. Environ Toxicol Chem. 1989; 8(12):1103-1123. doi: 10.1002/etc.5620081203

[16] Livingstone, DR. Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Poll Bull. 2001; 42(8):656-666. doi: 10.1016/s0025-326x(01)00060-1

[17] Viarengo, A, Canesi, L, Pertica, M, Poli, G, Moore, MN, Orunesu, M. Heavy metal effects on lipid peroxidation in the tissues of Mytilus galloprovincialis Lam. Comp Biochem Physiol C. 1990; 97(1):37-42. doi: 10.1016/0742-8413(90)90168-9

[18] Dovzhenko, NV, Kurilenko, AV, Belcheva, NN, Chelomin, VP. Cadmium-induced oxidative stress in the bivalve mollusk Modiolus modiolus. Russ J Mar Biol. 2005; 31:309-313. doi: 10.1007/s11179-005-0093-7

[19] Koukouzika, N, Raftopoulou, EK, Dimitriadis, VK. Seasonal differences of lisosomal, lipid and lipofuscin parameters in the digestive gland of the mussel Mutilus galloprovincialis. J. Molluscan Stud. 2009; 75(3):261-267. doi: 10.1093/mollus/eyp022

[20] Dovzhenko, NV, Belcheva, NN, Kavun, VY, Chelomin, V. Using of biochemical markers in active monitoring of contaminated marine environment. Biol Commun. 2012; 3:12-24.

[21] Kavun, VY, Shulkin, VM. Changes in the microelement composition in organs and tissues of the bivalve Crenomytilus grayanus acclimatized in a biotope with long-term heavy metal contamination. Russ J Mar Biol. 2005; 31:109-114. doi: 10.1007/s11179-005-0051-4

[22] Podorvanova, NF, Ivashinnikova, TS, Petrenko, VS, Khomichuk, LS. Osnovnye Cherty Gidrokhimii Zaligva Petra Velikogo, Yaponskoe More (The Main Hydrochemical Features of Peter the Great Bay, Sea of Japan). Russian, Vladivostok: Far East Branch of the Russian Academy of Sciences; 1989.

[23] Shulkin, VM. Metals in Shallow Marine Ecosystems. Vladivostok: Dalnauka; 2004.

[24] Sevastyanov, AV, Lishavskaya, TS, Chatkina, TV. Monitoring of Self-Purification of Seawater and Bottom Sediment of Ussuriysky Bay in the Area of the Former Municipal Dumping Site (Gornostay Bay), Trudy DVNIGMI (Transactions of Far Eastern Regional Hydrometeorological Research Institute). Vol. 155. Vladivostok: Dalnauka, Press; 2014. p. 160-175.

[25] Brooks, SJ, Farmen, E, Heier, LS, Blanco-Rayón, E, Izagirre, U. Differences in copper bioaccumulation and biological responses in three Mytilus species. Aquat Toxicol. 2015; 160:1-12. doi: 10.1016/j.aquatox.2014.12.018

[26] Benali, I, Boutiba, Z, Merabet, A, Chèvre, N. Integrated use of biomarkers and condition indices in mussels (Mytilus galloprovincialis) for monitoring pollution and development of biomarker index to assess the potential toxic of coastal sites. Mar Pollut Bull. 2015; 95(1):385-394. doi: 10.1016/j.marpolbul.2015.03.041

[27] Paoletti, F, Aldinuccio, D, Mocali, A, Carparrini, AA. A sensitive spectrophotometric method for the determination of superoxide dismutase activity in tissue extracts. Anal Biochem. 1989: 154(2):536-541.doi: 10.1016/0003-2697(86)90026-6

[28] Regoli, F, Principato, G. Glutathione, glutathione-dependent and antioxidant enzymes in mussel, Mytilis galloprovincialis, exposed to metals under field and laboratory conditions: Implications for the use of biochemical biomarkers. Aquat Toxicol. 1995; 31(2):143-164. doi: 10.1016/0166-445X(94)00064-W

[29] Lawrence, RA, Burk, RF. Glutathione peroxidase activity in selenium deficient rat liver. Biochem Biophys Res Commun. 1976; 71(4):952-958. doi: 10.1016/0006-291X(76)90747-6

[30] Moron, MS, Depierre, JW, Mannervik, B. Levels of glutathione, glutathione reductase and glutathione S-transferase activities in rat lung and liver. Biochim Biophys Acta. 1979; 582(1):67-78. doi: 10.1016/0304-4165(79)90289-7

[31] Buege, JA, Aust, SD.Microsomal lipid peroxidation. Methods Enzymol. 1978; 52:302-310. doi: 10.1016/S0076-6879(78)52032-6

[32] Corongiu, FP, Banni, S. Detection of conjugated dienes by second derivative ultraviolet spectrophotometry. Methods Enzymol. 1994; 233:303-310. doi: 10.1016/S0076-6879(94)33033-6

[33] Folch, J, Lees, M, Stanley, J. A simple method for isolation and purification of total lipids from animal tissues. J Biol Chem. 1957; 226(1):497-509. doi: 10.1016/S0021-9258(18)64849-5

[34] Dillard, CJ, Tappel, AL. Fluorescent damage products of lipid peroxidation. Methods Enzymol. 1984; 105: 337-341. doi: 10.1016/S0076-6879(84)05044-8

[35] Markwell, MA, Haas, SM, Bieber, LL, Tolbert, N. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem. 1978; 87(1):206-210. doi: 10.1016/0003-2697(78)90586-9

[36] Bartosz, G, Janaszewska, A, Ertel, D, Bartosz, M. Simple determination of peroxyl radical-trapping capacity. Biochem Mol Biol Int. 1998; 46(3):519-528. doi: 10.1080/15216549800204042

[37] Zolotarev, VN. Sklerokhronologiya Morskikh Dvustvorchatykh Mollyuskov (Sklerochronology of Marine Bivalves). Kiev, Russian: Naukova Dumka; 1989.

[38] Istomina, A, Mazur, A, Chelomin, V, Kukla, S, Slobodskova, V, Zvyagintsev, A, Fedorets, Y. The different biomarkers in the assessment of the marine environmental quality using the representative species Mytilus trossulus. Water Air Soil Pollut. 2020; 231(8):403. doi: 10.1007/s11270-020-04782-w

[39] Shulkin, VM, Kavun, VY. Long-term monitoring of pollution of the coastal water area of Ussuri Bay with metals: A case study of “green” oysters Magallana gigas (Crassostrea gigas) (Thunberg, 1793). Russ J Mar Biol. 2023; 49(2):97-105. doi: 10.1134/S1063074023020074

[40] Sevastyanov, AV, Lishavskaya, TS, Chatkina, TV. Monitoring of self-purification of seawater and bottom sediment of Ussuriysky Bay in the area of the former municipal waste site (Gornostay Bay). In: Hydrometeorological applications for Russian Far East region. Russian, Vladivostok: Dalnauka Press; 2015. p. 144-155.

[41] Kozhenkova, SI, Khristoforova, NK, Chernova, EN, Kobzar, AD. Long-term biomonitoring of heavy metal pollution of Ussuri Bay, Sea of Japan. Russ J Mar Biol. 2021; 47(4):256-264. doi: 10.1134/S106307402104009X

[42] Moshchenko, AV, Belan, TA, Lishavskaya, TS, Sevastianov, AV, Borisov, BM. Longterm dynamics of prior pollutants concentration and total level of chemical contamination in the coastal areas at Vladivostok (Peter the Great Bay, Japan Sea). Izvestiya TINRO. 2020; 200(2):377-400. doi: 10.26428/1606-9919-2020-200-377-400

[43] Belcheva, N, Istomina, A, Dovzhenko, N, Lishavskaya, T, Chelomin, V. Using heavy metal content and lipid peroxidation indicators in the tissues of the mussel Crenomytilus grayanus for pollution assessment after marine environmental remediation. Bull Environ Contam Toxicol. 2015; 95(4):481-487. doi: 10.1007/s00128-015-1624-3

[44] Fokina, NN, Vasil’eva, OB, Ruokolainen, TR, Nemova, NN. Changes in lipid composition and lipid peroxidation products content in the freshwater mussel Anodonta cygnea L. under cadmium effect. Limnol Freshwater Biol. 2019; 5:286-296. doi: 10.31951/2658-3518-2019-A-5-286

[45] Giuliani, ME, Accoroni, S, Mezzelani, M, et al. Biological effects of the azaspiracid-producing dinoflagellate Azadinium dexteroporum in Mytilus galloprovincialis from the Mediterranean Sea. Marine Drugs. 2019; 17(10):595. doi: 10.3390/md17100595

[46] Copeto, S, Ganço, S, Ferreira, IJ, Silva, M, Motta, C, Diniz, M. The effects of tetrabromobisphenol A (TBBPA) on the Mussel Mytilus galloprovincialis: A multi-biomarker approach. Oceans. 2024; 5(2):181-195. doi: 10.3390/oceans5020011

[47] Halliwell, BH, Gutteridge, JMC. Free Radicals in Biology and Medicine. 5th ed. Oxford: Oxford University Press; 2015. doi: 10.1093/acprof:oso/9780198717478.001.0001

[48] Hayes, JD, Flanagan, JU, Jowsey, IR. Glutathione, transferases. Annu Rev Pharmacol Toxicol. 2005; 45:51-88. doi: 10.1146/annurev.pharmtox.45.120403.095857

[49] Torres, MA, Testa, СP, Gaspari, C, et al. Oxidative stress in the mussel Mytella guyanensis from polluted mangroves on Santa Catarina Island, Brazil. Mar Poll Bull. 2002; 44:923-932. doi: 10.1016/S0025-326X(02)00142-X

[50] Lushchak, VI. Free radicals, reactive oxygen species, oxidative stress and its classification. Chem Biol Inter. 2014; 224:164-175. doi: 10.1016/j.cbi.2014.10.016

[51] Costantini, D. The Role of Organismal Oxidative Stress in the Ecology and Life-History Evolution of Animals. Berlin: Springer Nature Switzerland AG; 2024. doi: 10.1007/978-3-031-65183-0