Biomarkers of stress in common coastal amphipods and bivalves under salinity gradient and pollution influence (the White Sea)

Мұқаба

Дәйексөз келтіру

Толық мәтін

Ашық рұқсат Ашық рұқсат
Рұқсат жабық Рұқсат берілді
Рұқсат жабық Тек жазылушылар үшін

Аннотация

Studies of the biochemical parameters of aquatic organisms are important for understanding the mechanisms of their adaptive reactions in response to the influence of environmental factors. They are also used in a comprehensive assessment of the quality of the aquatic environment under the influence of anthropogenic pollution. The purpose of the work is a comparative study of the biochemical parameters of marine invertebrates, showing neurotoxic effects, the process of antioxidant protection, and the functioning of the biotransformation system. These indicators are considered “biomarkers of stress” in aquatic organisms. Widespread White Sea species were chosen as model species: Gammarus oceanicus (Amphipoda: Malacostraca), Mytilus edulis (Mytilida: Bivalvia), and Mya arenaria (Myoida: Bivalvia). At the end of August 2015–2016, these invertebrates were collected from several locations of the littoral zone of the Kandalaksha Bay of the White Sea: the wild littoral in the absence of visible anthropogenic influence, and with different levels of local pollution (far from an urban settlement (Maly Pitkul Bay), on a wild beach near the confluence of the Niva River, near the port of Kandalaksha at the boat pier, and at the Kartesh biological station). In addition, a comparison was made between molluscs (M. edulis) living in the intertidal and subtidal zones (as part of mussel rope aquaculture). The highest levels of enzyme activity (catalase, glutathione-S-transferase) and increased levels of lipid peroxidation, indicating the state of oxidative stress in the amphipods and molluscs, were determined for animals living at the mouth of the Niva River and local pollution with oil products in the port of Kandalaksha. For each indicator, interspecies differences in response to impacts of one nature or another were found. Principal component analysis revealed two factors that explained 81.08% of the variability of the variables. The main influencing factors were the river reducing the salinity of the water and introducing pollutants into the sea, increasing the levels of metals (copper, zinc, and lead) in the water. The second important impact factor was local pollution of habitats with oil products (motor boats), and it was this second factor that was associated with changes in a large number of biochemical parameters of molluscs and amphipods, indicating the state of stress in organisms. The results of this study confirm the usefulness of using biochemical indicators of marine invertebrates to assess their condition under the influence of environmental stress factors, including pollution, and the high indicator significance of the applied biomarkers.

Толық мәтін

Рұқсат жабық

Авторлар туралы

N. Berezina

Zoological Institute, RAS

Хат алмасуға жауапты Автор.
Email: nadezhda.berezina@zin.ru
Ресей, Universitetskaya Embankment, 1, St. Petersburg, 199034

Әдебиет тізімі

  1. Бергер В.Я., 1986. Адаптации морских моллюсков к изменениям солености среды. Л.: Наука. 218 с.
  2. Кабдрахманова Г.Б., Утепкалиева А.П., 2018. О роли экотоксикантов в развитии нейротоксикозов // West Kazakhstan Med. J. № 57 (1). С. 29–36.
  3. Ковыршина Т., Руднева И., 2014. Холинэстеразы рыб как биомаркеры загрязнения морской среды пестицидами // Междунар. сельскохоз. журн. № 3. С. 38–42.
  4. Немова Н.Н., Высоцкая Р.У., 2004. Биохимическая индикация состояния рыб. М.: Наука. 316 с.
  5. Немова Н.Н., Мещерякова О.В., Лысенко Л.А., Фокина Н.Н., 2014. Оценка состояния водных организмов по биохимическому статусу // Тр. КарНЦ РАН. № 5. С. 18–29.
  6. Сухаренко Е.В., Недзвецкий В.С., Кириченко С.В., 2017. Биомаркеры нарушений метаболизма двустворчатых моллюсков в условиях загрязнения среды обитания продуктами переработки нефти // Biosyst. Divers. V. 25. № 2. P. 113–118. https://doi.org/10.15421/011717
  7. Филатов Н., Тержевик А., Дружинин П., 2011. Беломорье – регион решения арктических задач // Aрктика: экология и экономика. № 2. С. 90–101.
  8. Фокина Н.Н., Нефедова З.А., Немова Н.Н., 2011. Биохимические адаптации морских двустворчатых моллюсков к аноксии (обзор) // Тр. КарНЦ РАН. № 3. С. 121–130.
  9. Хочачка П., Сомеро Дж., 1988. Стратегия биохимической адаптации. М.: Мир. 586 с.
  10. Чуйко Г.М., 2017. Биомаркеры в системе оценки токсического воздействия на гидробионтов и в экологическом мониторинге водных экосистем // Вода Magazine. № 7 (119). С. 26–29.
  11. Amer N.R., Lawler S.P., Zohdy N.M., Younes A., ElSayed W.M., et al., 2022. Copper exposure affects anti-predatory behaviour and acetylcholinesterase levels in Culex pipiens (Diptera, Culicidae) // Insects. V. 13. № 12. Art. 1151. https://doi.org/10.3390/insects13121151
  12. Berezina N.A., 2023. Energy metabolism of crustaceans (Amphipoda) from the northern populations (White Sea Basin) // Russ. J. Ecol. V. 54. P. 62–69. https://doi.org/10.1134/S1067413623010022
  13. Berezina N.A., Lehtonen K.K., Ahvo A., 2019. Coupled application of antioxidant defense response and embryo development in amphipod crustaceans in the assessment of sediment toxicity // Environ. Toxicol. Chem. V. 38. № 9. P. 2020–2031. http//doi.org/10.1002/etc.4516
  14. Beyer J., Green N.W., Brooks S., Allan I.J., Ruus A., et al., 2017. Blue mussels (Mytilus edulis spp.) as sentinel organisms in coastal pollution monitoring: A review // Mar. Environ. Res. V. 130. P. 338–365. http//doi.org/10.1016/j.marenvres.2017.07.024
  15. Binelli A., Ricciardi F., Riva C., Provini A., 2006. New evidences for old biomarkers: Effects of several xenobiotics on EROD and AChE activities in zebra mussel (Dreissena polymopha) // Chemosphere. V. 62. P. 510–519. https://doi.org/10.1016/j.chemosphere.2005.06.033
  16. Bradford M.M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding // Ann. Biochem. V. 72. P. 248–254. http//doi.org/10.1006/abio.1976.9999
  17. Cajaraville M.P., Bebianno M.J., Blasco J., Porte C., Sarasquete C., Viarengo A., 2000. The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: A practical approach // Sci. Total Environ. V. 247. P. 295–311. https://doi.org/10.1016/s0048-9697(99)00499-4
  18. Camus L., Birkely S.R., Jones M.B., Børseth J.F., Grøsvik B.E., et al., 2003. Biomarker responses and PAH uptake in Mya truncate following exposure to oil-contaminated sediment in an Arctic fjord (Svalbard) // Sci. Total Environ. V. 308. P. 221–234. https://doi.org/10.1016/S0048-9697(02)00616-2
  19. Chevin L.-M., Lande R., Mace G.M., 2010. Adaptation, plasticity, and extinction in a changing environment: Towards a predictive theory // PLoS Biol. V. 8. № 4. Art. e1000357. https://doi.org/10.1371/journal.pbio.1000357
  20. Claiborne A., 1985. Catalase activity // CRC Handbook of Methods for Oxygen Radical Research / Ed. Greenwald R.A. Boca Raton: CRC Press. P. 283–284.
  21. Cobelo-García A., Millward G.E., Prego R., Lukashin V., 2006. Metal concentrations in Kandalaksha Bay, White Sea (Russia) following the spring snowmelt // Environ. Pollut. V. 143. P. 89–99. https://doi.org/10.1016/j.envpol.2005.11.006
  22. Dietz R., Letcher R.J., Desforges J.-P. et al., 2019. Current state of knowledge on biological effects from contaminants on arctic wildlife and fish // Sci. Total Environ. V. 696. Art. 133792. https://doi.org/10.1016/j.scitotenv.2019.133792
  23. Ellman G.L., Courtney K.D., Andres V., Featherstone R.M., 1961. A new and rapid colorimetric determination of acetylcholinesterase activity // Biochem. Pharmacol. V. 7. P. 88–95. https://doi.org/10.1016/10.1016/0006-2952(61)90145-9
  24. Fokina N.N., Bakhmet I.N., Shklyarevich G.A., Nemova N.N., 2014. Effect of seawater desalination and oil pollution on the lipid composition of blue mussels Mytilus edulis L. from the White Sea // Ecotoxicol. Environ. Saf. V. 110. P. 103–109. https://doi.org/10.1016/j.ecoenv.2014.08.010
  25. Frasco M.F., Fournier D., Carvalho F., Guilhermino L., 2005. Do metals inhibit acetylcholinesterase (AchE)? Implementation of assay conditions for the use of AchE activity as a biomarker of metal toxicity // Biomarkers. V. 10. P. 360–375. https://doi.org/10.1080/13547500500264660
  26. Freitas R., Costa E., Velez C., Santos J., Lima A., et al., 2012. 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. Saf. V. 75. № 1. P. 109–118. https://doi.org/10.1016/j.ecoenv.2011.08.019
  27. Golovanova I.L., Golovanov V.K., Chuiko G.M., Podgornaya V.A., Aminov A.I., 2019. Effects of roundup herbicide at low concentration and of thermal stress on physiological and biochemical parameters in Amur Sleeper Perccottus glenii Dybowski juveniles // Inland Water Biol. V. 12. № 4. P. 462–469. https://doi.org/10.1134/S1995082919040059
  28. Gostyukhina O.L., Kladchenko E.S., Chelebieva E.S., Tkachuk A.A., Lavrichenko D.S., Andreyeva A.Y., 2023. Short-time salinity fluctuations are strong activators of oxidative stress in Mediterranean mussel (Mytilus galloprovincialis) // Ecol. Montenegrina. V. 63. P. 46–58. https://doi.org/10.37828/em.2023.63.5
  29. Gray J.S., Elliott M., 2009. Ecology of Marine Sediments: From Science to Management. 2nd ed. Oxford: Oxford Univ. Press. 225 р.
  30. Habig W.H., Pabst M.J., Jakoby W.B., 1974. Glutathione S-transferases. The first step in mercapturic acid formation // J. Biol. Chem. V. 249. P. 7130–7139.
  31. Havelková M., Randak T., Blahová J., Slatinská I., Svobodová Z., 2008. Biochemical markers for the assessment of aquatic environment contamination // Interdiscip. Toxicol. V. 1. P. 169–181. https://doi.org/10.2478/v10102-010-0034-y
  32. Huang Y., Tang H., Jin J., Fan M., Chang A.K., Ying X., 2020. Effects of waterborne cadmium exposure on its internal distribution in Meretrix meretrix and detoxification by metallothionein and antioxidant enzymes // Front. Mar. Sci. V. 7. Art. 502. https://doi.org/10.3389/fmars.2020.00502
  33. Kim Y.H., Lee S.H., 2018. Invertebrate acetylcholinesterases: Insights into their evolution and non-classical functions // J. Asia Pac. Entomol. V. 21. P. 186–195. https://doi.org/10.1016/j.aspen.2017.11.017
  34. Klimova Y.S., Chuiko G.M., Gapeeva M.V., Pesnya D.S., Ivanova E.I., 2019. The use of oxidative stress parameters of bivalve mollusks Dreissena polymorpha (Pallas, 1771) as biomarkers for ecotoxicological assessment of environment // Inland Water Biol. V. 12. № S2. P. 88–95. https://doi.org/10.1134/S1995082919060063
  35. Kwok C.-T., Van de Merwe J., Chiu J., Wu R., 2012. Antioxidant responses and lipid peroxidation in gills and hepatopancreas of the mussel Perna viridis upon exposure to the red-tide organism Chattonella marina and hydrogen peroxide // Harmful Algae. V. 13. P. 40–46. https://doi.org/10.1016/j.hal.2011.10.001
  36. Lehtonen K.K., Leiniö S., Schneider R., Leivuori M., 2006. Biomarkers of pollution effects in the bivalves Mytilus edulis and Macoma balthica collected from the southern coast of Finland (Baltic Sea) // Mar. Ecol. Prog. Ser. V. 322. P. 155–168. https://doi.org/10.3354/meps322155
  37. Leiniö S., Lehtonen K.K., 2005. Seasonal variability in biomarkers in the bivalves Mytilus edulis and Macoma balthica from the northern Baltic Sea // Comp. Biochem. Physiol. C. Toxicol. Pharmacol. V. 140. P. 408–421. https://doi.org/10.1016/j.cca.2005.04.005
  38. Lushchak V.I., 2011. Environmentally induced oxidative stress in aquatic animals // Aquat. Toxicol. V. 101. P. 13–30. https://doi.org/10.1016/j.aquatox.2010.10.006
  39. Lysenko L., Kantserova N., Käiväräinen E., Krupnova M., Shklyarevich G., Nemova N., 2014. Biochemical markers of pollutant responses in macrozoobenthos from the White Sea: Intracellular proteolysis // Mar. Environ. Res. V. 96. P. 38–44. https://doi.org/10.1016/j.marenvres.2014.01.005
  40. Mennillo E., Casu V., Tardelli F., De Marchi L., Freitas R., Pretti C., 2017. Suitability of cholinesterase of polychaete Diopatra neapolitana as biomarker of exposure to pesticides: In vitro characterization // Comp. Biochem. Physiol. C. Toxicol. Pharmacol. V. 191. P. 152–159. https://doi.org/10.1016/j.cbpc.2016.10.007
  41. Nunes B., 2011. The use of cholinesterases in ecotoxicology // Rev. Environ. Contam. Toxicol. V. 212. P. 29–59. https://doi.org/10.1007/978-1-4419-8453-1_2
  42. Nunes B.S., Travasso R., Gonçalves F., Castro B.B., 2015. Biochemical and physiological modifications in tissues of Sardina pilchardus: Spatial and temporal patterns as a baseline for biomonitoring studies // Front. Environ. Sci. V. 3. Art. 7. https://doi.org/10.3389/fenvs.2015.00007
  43. Ohkawa H., Ohishi N., Yagi K., 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction // Ann. Biochem. V. 95. P. 351–358. https://doi.org/10.1016/0003-2697(79)90738-3
  44. Regoli F., 1998. Trace metals and antioxidant enzymes in gills and digestive gland of the Mediterranean mussel Mytilus galloprovincialis // Arch. Environ. Contam. Toxicol. V. 34. P. 48–63. https://doi.org/10.1007/s002449900285
  45. Seen S., 2021. Chronic liver disease and oxidative stress – a narrative review // Expert Rev. Gastroenterol. Hepatol. V. 15. P. 1021–1035. https://doi.org/10.1080/17474124.2021.1949289
  46. Timbrell J.A., 1998. Biomarkers in toxicology // Toxicology. V. 129. P. 1–12. https://doi.org/10.1016/S0300-483X(98)00058-4
  47. Timofeyev M.A., 2006. Antioxidant enzyme activity in endemic Baikalean versus Palaearctic amphipods: tagma- and size-related changes // Comp. Biochem. Physiol. B. Biochem. Mol. Biol. V. 143. № 3. P. 302–308. https://doi.org/10.1016/j.cbpb.2005.12.001
  48. Turja R., Sanni S., Stankevičiūtė M., Butrimavičienė L., Devier M-H., et al., 2020. Biomarker responses and accumulation of polycyclic aromatic hydrocarbons in Mytilus trossulus and Gammarus oceanicus during exposure to crude oil // Environ. Sci. Pollut. Res. V. 27. P. 15498–15514. https://doi.org/10.1007/s11356-020-07946-7
  49. Viarengo А., 1991. Seasonal variations in the antioxidant defence systems and lipid peroxidation of the digestive gland of mussels // Comp. Biochem. Physiol. C. Comp. Pharmacol. V. 100. № 1–2. P. 187–190. https://doi.org/10.1016/0742-8413(91)90151-i
  50. Won E.J., Rhee J.S., Kim R.O., Ra K., Kim K.T., et al., 2012. Susceptibility to oxidative stress and modulated expression of antioxidant genes in the copper-exposed polychaete Perinereis nuntia // Comp. Biochem. Physiol. C. Toxicol. Pharmacol. V. 155. № 2. P. 344–351. https://doi.org/10.1016/j.cbpc.2011.10.002

Қосымша файлдар

Қосымша файлдар
Әрекет
1. JATS XML
Жүктеу
2. Fig. 1. Schematic map of the study area indicating the sampling locations.

Жүктеу (352KB)
Метадеректер
3. Fig. 2. Catalase activity (CAT, μmol/min protein) in three studied species (M. edulis, M. arenaria, and G. oceanicus) at the Kartesh biostation (1 and 2) in September 2015 and in Kandalaksha Bay in early August 2016 (3–6). Statistical differences between sites are shown in Table 2 at p < 0.05.

Жүктеу (97KB)
Метадеректер
4. Fig. 3. Glutathione-S-transferase (GST) activity, nmol/min protein in three studied species (M. edulis, M. arenaria, and G. oceanicus) at the Kartesh biostation (1 and 2) in September 2015 and in Kandalaksha Bay in early August 2016 (3–6). Statistical differences between sites are shown in Table 2 at p < 0.05.

Жүктеу (100KB)
Метадеректер
5. Fig. 4. Lipid peroxidation activity (LPO, nmol TBAR/g wet weight) in three studied species (M. edulis, M. arenaria, and G. oceanicus) at the Kartesh Biostation (1 and 2) in September 2015 and in Kandalaksha Bay in early August 2016 (3–6). Statistical differences between sites are shown in Table 2 at p < 0.05.

Жүктеу (86KB)
Метадеректер
6. Fig. 5. AChE activity (nmol/min mg protein) in three studied species (M. edulis, M. arenaria, and G. oceanicus) at the Kartesh Biostation (1 and 2) in September 2015 and in Kandalaksha Bay in early August 2016 (3–6). Statistical differences between sites are shown in Table 2 at p < 0.05.

Жүктеу (88KB)
Метадеректер
7. Fig. 6. Principal component analysis and association of variables for two main factors. 1 – CAT G.o., 2 – CAT M.e., 3 – CAT M.a., 4 – GST G.o., 5 – GST M.e., 6 – GST M.a., 7 – POL G.o., 8 – POL M.e., 9 – POL M.a., 10 – AChE G.o., 11 – AChE M.e., 12 – AChE M.a., 13 – water salinity, 14 – oil products, 15 – Cu, 16 – Zn, 17 – Cd, 18 – Pb. Designations for species: G.o. – Gammarus oceanicus, M.e. – Mytilus edulis, M.a. – Mya arenaria. Variables: Active – active, Suppl. – additional.

Жүктеу (139KB)
Метадеректер

© Russian Academy of Sciences, 2024