Integrative biomarker approach to decode seasonal variation in biomarker responses of Scylla serrata and Penaeus monodon from Sundarbans estuarine system

Baag, Sritama; Mandal, Sumit

doi:10.5697/IVQW7412

Artykuł - szczegóły

Tytuł artykułu

Integrative biomarker approach to decode seasonal variation in biomarker responses of Scylla serrata and Penaeus monodon from Sundarbans estuarine system

Autorzy

Baag Sritama , Mandal Sumit

Wybrane pełne teksty z tego czasopisma

Identyfikatory

DOI

10.5697/IVQW7412

Warianty tytułu

Języki publikacji

Abstrakty

Sundarbans Estuarine System is a highly productive estuary and is considered the most important spawning and nursery ground for various commercial fish and shellfish species. Estuarine organisms are frequently exposed to a wide variety of pollutants due to their vicinity to human habitation. Marine organisms residing in this area are also exposed to extensive fluctuations of environmental factors which vary with season. In the present study, effects of seasonal variation on oxidative stress biomarkers such as superoxide dismutase, catalase, glutathione-S-transferase, and lipid peroxidation in the hepatopancreas of mud crab Scylla serrata and shrimp Penaeus monodon, were studied during monsoon, winter, spring and summer seasons. The integrated biomarker response (IBR) was assessed with the biomarker scores for all four seasons in both species. Our results suggested seasonal discrepancies as the governing factor behind biomarkers’ variability. The breeding period of the animals also seems to play a significant role in their oxidative stress physiology. The IBR results indicated that moderately high temperatures and low salinity in the monsoon season are the most stressful for crabs. This stress might also be ascribed to the breeding period of these crabs which exacerbates the stress level during this season. However, in the case of shrimps, the highest IBR value was observed in the winter season due to impaired ROS elimination at low temperatures. This study also offers baseline values in various seasons that would be beneficial to be considered in environmental monitoring programs to avoid the misinterpretation of environmental factors, which change seasonally.

Słowa kluczowe

seasonal variation biomarkers antioxidant enzymes estuary integrated biomarker approach

Wydawca

Polish Academy of Sciences, Institute of Oceanology
Elsevier

Czasopismo

Oceanologia

Rocznik

2025

Tom

No. 67 (1)

Strony

Art. no. 67108

Opis fizyczny

Bibliogr. 67 poz., rys., tab., wykr.

Twórcy

autor

Baag Sritama

Marine Ecology Laboratory, Department of Life Sciences, Presidency University, 86/1, College Street, Kolkata – 700073, India

autor

Mandal Sumit

sumit.dbs@presiuniv.ac.in

Marine Ecology Laboratory, Department of Life Sciences, Presidency University, 86/1, College Street, Kolkata – 700073, India

Bibliografia

1. Aebi, H., 1984. Catalase in vitro. Methods Enzymol. 105, 121-126. https://doi.org/10.1016/s0076-6879(84)05016-3
2. Alves, A.S., Caetano, A., Costa, J.L., Costa, M.J., Marques, J.C., 2015. Estuarine intertidal meiofauna and nematode communities as indicators of ecosystem’s recovery following mitigation measures. Ecol. Indic. 54, 184-196. https://doi.org/10.1016/j.ecolind.2015.02.013
3. Amaral, A.M.B., de Moura, L.K., de Pellegrin, D., Guerra, L.J., Cerezer, F.O., Saibt, N., Prestes, O.D., Zanella, R., Loro, V.L., Clasen, B., 2020. Seasonal factors driving biochemical biomarkers in two fish species from a subtropical reservoir in southern Brazil: An integrated approach. Environ. Pollut. 266, 115168. https://doi.org/10.1016/j.envpol.2020.115168
4. Anderson, D., Yu, T.W., Phillips, B.J., Schmezer, P., 1994. The effect of various antioxidants and other modifying agents on oxygen radicals generated DNA damage in human lymphocytes in the Comet assay. Mutat. Res. Fund Mol. Mech. Mutagen 307, 261-271. https://doi.org/10.1016/0027-5107(94)90300-X
5. Attri, S.D., Tyagi, A., 2010. Climate Profile of India, Met. Monograph., Environment Meteorology – 01/2010. India Meteorol. Depart., Ministry of Earth Sciences, Government of India, 129 pp.
6. Baag, S., Mahapatra, S., Mandal, S., 2021. An Integrated and Multibiomarker approach to delineate oxidative stress status of Bellamya bengalensis under the interactions of elevated temperature and chlorpyrifos contamination. Chemosphere, 264, 128512. https://doi.org/10.1016/j.chemosphere.2020.128512
7. Baag, S., Mandal, S., 2023a. Do global environmental drivers’ ocean acidification and warming exacerbate the effects of oil pollution on the physiological energetics of Scylla serrata? Environ. Sci. Pollut. Res. 30, 23213-23224. https://doi.org/10.1007/s11356-022-23849-1
8. Baag, S., Mandal, S., 2023b. The influence of ocean acidification and warming on responses of Scylla serrata to oil pollution: an integrated biomarker approach. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 266, 110847. https://doi.org/10.1016/j.cbpb.2023.110847
9. Beliaeff, B., Burgeot, T., 2002. Integrated biomarker response: a useful tool for ecological risk assessment. Environ. Toxicol. Chem. 21, 1316-1322. https://doi.org/10.1002/etc.5620210629
10. Bhagat, J., Sarkar A., Ingole, B.S., 2016. DNA Damage and Oxidative Stress in Marine Gastropod Morula granulata Exposed to Phenanthrene. Water Air Soil Pollut. 227, 114. https://doi.org/10.1007/s11270-016-2815-1
11. Bhowmik, M., Mandal, S., 2021. Do seasonal dynamics influence traits and composition of macrobenthic assemblages of Sundarbans Estuarine System, India? Oceanologia 63(1), 80-98. https://doi.org/10.1016/j.oceano.2020.10.002
12. Bradford, M.M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254. https://doi.org/10.1006/abio.1976.9999
13. Brooks, S., Harman, C., Zaldibar, B., Izagirre, U., Glette, T., Marigomez, I., 2011. Integrated biomarker assessment of the effects exerted by treated produced water from an onshore natural gas processing plant in the North Sea on the mussel Mytilus edulis. Mar. Pollut. Bull. 62, 327-339.
14. Brooks, S., Lyons, B., Goodsir, F., Bignell, J., Thain, J., 2009. Biomarker responses in mussels, an integrated approach to biological effects measurements. J. Toxicol. Environ. Health Pt. A 72, 196-208.
15. Cailleaud, K., Maillet, G., Budzinski, H., Souissi, S., Forget Leray, J., 2007. Effects of salinity and temperature on the expression of enzymatic biomarkers in Eurytemora affinis (Calanoida, Copepoda). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 147, 841-849.
16. Catarina, V., Madeira, D., Mendonça, V., Madeira, C., Diniz, M.S., 2021. Warming in shallow waters: Seasonal response of stress biomarkers in a tide pool fish. Estuar. Coast. Shelf Sci. 251, 107187. https://doi.org/10.1016/j.ecss.2021.107187
17. Chen, J.C., Chia, P.G., 1997. Osmotic and ionic concentrations of Scylla serrata (Forskal) subjected to different salinity levels. Compar. Biochem. Physiol. A 227, 239-244. https://doi.org/10.1016/S0300-9629(96)00237-X
18. Clarke, K.R., Gorley, R.N., 2006. PRIMER V6: User Manual/Tutorial. PRIMER-E, Plymouth. Clarke, K.R., Somerfield, P.J., Chapman, M.G., 2008. Testing of null hypotheses in explanatory community analyses: similarity profiles and biota-environment linkage. J. Exp. Mar Biol. 366, 56-69.
19. CMFRI, 2020. Annual Report 2019. Central Marine Fisheries Research Institute, Kochi. 284 pp.
20. Costanza, R., d’Arge, R., de Groot, R., Farber, S., Grasso, M., Hannon, B., Limburg, K., Naeem, S., O’Neill, R.V., Paruelo, J., Raskin, R.G., Sutton, P., 1997. The value of the world’s ecosystem services and natural capital. Nature, 387, 253-260. https://doi.org/10.1038/387253a0
21. Dagnino, A., Allen, J.I., Moore, M.N., Broeg, K., Canesi, L., Viarengo, A., 2007. Development of an expert system for the integration of biomarker responses in mussels into an animal health index. Biomarkers, 12, 155-172. https://doi.org/10.1080/13547500601037171
22. Devin, S., Burgeot, T., Giamberini, L., Minguez, L., Pain Devin, S., 2014. The integrated biomarker response revisited: optimization to avoid misuse. Environ. Sci. Pollut. Res. 21, 2448-2454. https://doi.org/10.1007/s11356-013-2169-9
23. dos Santos, C.C.M., da Costa, J.F.M., Dos Santos, C.R.M., Amado, L.L., 2019. Influence of seasonality on the natural modulation of oxidative stress biomarkers in mangrove crab Ucides cordatus (Brachyura, Ucididae). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 227, 146-153. https://doi.org/10.1016/j.cbpa.2018.10.001
24. Ern, R., Huong, D.T.T., Nguyen, V.C., Wang, T., Bayley, M., 2012. Effects of salinity on standard metabolic rate and critical oxygen tension in the giant freshwater prawn (Macrobrachium rosenbergii). Aquacul. Res. 44, 1-7. https://doi.org/10.1111/j.1365-2109.2012.03129.x
25. Feidantsis, K., Michaelidis, B., Raitsos, D.E., Vafidis, D., 2021. Seasonal metabolic and oxidative stress responses of commercially important invertebrate species—correlation with their habitat. Mar. Ecol. Prog. Ser. 658, 27-46. https://doi.org/10.3354/meps13565
26. Ghosh, M., Mandal, S., Chatterjee, M., 2018. Impact of unusual monsoonal rainfall in structuring meiobenthic assemblages at Sundarban estuarine system, India. Ecol. Indic. 94, 139-150. https://doi.org/10.1016/j.ecolind.2018.06.067
27. Ghosh, M., Mandal, S., 2019. Does vertical distribution of meiobenthic community structure differ among various mangrove habitats of Sundarban Estuarine System? Reg. Stud. Mar. Sci. 31, 1—11. https://doi.org/10.1016/j.rsma.2019.100778
28. Grasshoff, K., Kremling, K., Ehrhardt, M., 1999. Methods of seawater analysis. Verlag Chemie, Weinheim Germany, 634 pp.
29. Grilo, T.F., Cardoso, P.G., Dolbeth, M., Bordalo, M.D., Pardal, M.A., 2011. Effects of extreme climate events on the macrobenthic communities’ structure and functioning of a temperate estuary. Mar. Pollut. Bull. 62, 303-311. https://doi.org/10.1016/j.marpolbul.2010.10.010
30. Gutteridge, J.M.C., Halliwell, B., 2018. Mini-review: oxidative stress, redox stress or redox success? Biochem. Biophys. Res. Commun. 502, 183-186. https://doi.org/10.1016/j.bbrc.2018.05.045
31. Habig, W.H., Pabst, M.J., Jakoby, W.B., 1974. Glutathione S transferases the first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249, 7130-7139.
32. Halliwell, B., Gutteridge, J.M.C., 2007. Free Radicals in Biology and Medicine. Oxford Univ. Press, Oxford.
33. Hu, M., Li, L., Sui, Y., Li, J., Wang, Y., Lu, W., Dupont, S., 2015. Effect of pH and temperature on antioxidant responses of the thick shell mussel Mytilus coruscus. Fish Shellfish Immunol. 46(2), 573-583. https://doi.org/10.1016/j.fsi.2015.07.025
34. Jackson, C.J., Burford, M.A., 2003. The effects of temperature and salinity on growth and survival of larval shrimp Penaeus Semisulcatus (Decapoda: Penaeoidea). J. Crustacean Biol. 23 (4), 819-826. https://doi.org/10.1651/C-2379
35. Kannan, D., Jagadeesan, K., Shettu, N., Thirunavukkarasu, P., 2014. Maturation and Spawning of Commercially Important Penaeid Shrimp Penaeus monodon Fabricus at Pazhayar Tamil Nadu (South East Coast of India). J. Fish. Aquat. Sci. 9, 170-175. https://doi.org/10.3923/jfas.2014.170.175
36. Kennish, M.J., 2002. Environmental threats and environmental future of estuaries. Environ. Conserv. 29, 78-107. https://doi.org/10.3923/jfas.2014.170.175
37. Kong, X., Wang, G., Li, S., 2008. Seasonal variations of AT-Pase activity and antioxidant defenses in gills of the mudcrab Scylla serrata (Crustacea, Decapoda). Mar. Biol. 154, 269-276. https://doi.org/10.1007/s00227-008-0920-4
38. Lushchak, V.I., 2011. Environmentally induced oxidative stress in aquatic animals. Aquat. Toxicol. 101, 13-30. https://doi.org/10.1016/j.aquatox.2010.10.006
39. Luvizotto-Santos, R., Lee, J.T., Branco, Z.P., Bianchini, A., Nery, L.E.M., 2003. Lipids as energy source during salinity acclimation in the euryhaline crab Chasmagnathus granulata Dana, 1851 (crustacea-grapsidae). J. Exp. Zool. Part A. 295, 200-205. https://doi.org/10.1002/jez.a.10219
40. Madeira, C., Leal, M.C., Diniz, M.S., Cabral, H.N., Vinagre, C., 2018. Thermal stress and energy metabolism in two circumtropical decapod crustaceans: Responses to acute temperature events. Mar. Environ. Res. 141, 148-158. https://doi.org/10.1016/j.marenvres.2018.08.015
41. Madeira, D., Mendonça, V., Dias, M., Roma, J., Costa, P.M., Larguinho, M., Vinagre, C., Diniz, M.S., 2015. Physiological, cellular and biochemical thermal stress response of intertidal shrimps with different vertical distributions: Palaemon elegans and Palaemon serratus. Comp. Biochem. Physiol. A 183, 107-115. https://doi.org/10.1016/j.cbpa.2014.12.039
42. Madeira, D., Mendonça, V., Vinagre, C., Diniz, M.S., 2016. Is the stress response affected by season? Clues from an insitu study with a key intertidal shrimp. Mar. Biol. 163, art. no. 41. https://doi.org/10.1007/s00227-015-2803-9
43. Malanga, G., Estevez, M.S., Calvo, J., Abele, D., Puntarulo, S., 2007. The effect of seasonality on oxidative metabolism in Nacella (Patinigera) magellanica. Comp. Biochem. Physiol. A 146, 551-558. https://doi.org/10.1016/j.cbpa.2006.01.029
44. Marques, J.A., Abrantes, D.P., Marangoni, L.F., Bianchini, A., 2020. Ecotoxicological responses of a reef calcifier exposed to copper, acidification and warming: A multiple biomarker approach. Environ. Pollut. 257, 113572. https://doi.org/10.1016/j.envpol.2019.113572
45. Martin, Jr., J.P., Dailey, M., Sugarman, E., 1987. Negative and positive assays of superoxide dismutase based on hematoxylin autoxidation. Arch. Biochem. Biophys. 255, 329-336. https://doi.org/10.1016/0003-9861(87)90400-0
46. Na, J., Song, J., Achar, C., Jung, J., 2021. Synergistic effect of microplastic fragments and benzophenone-3 additives on lethal and sublethal Daphnia magna toxicity. J. Hazard. Mater. 402, 123845. https://doi.org/10.1016/j.jhazmat.2020.123845
47. Nandy, T., Baag, S., Mandal, S., 2021. Impact of elevated temperature on physiological energetics of Penaeus monodon post larvae: A mesocosm study. J. Therm. Biol. 97, 102829. https://doi.org/10.1016/j.jtherbio.2020.102829
48. Nandy, T., Mandal, S., 2020. Unravelling the spatio-temporal variation of zooplankton community from the river Matla in the Sundarbans Estuarine System, India. Oceanologia 62 (3), 326-346. https://doi.org/10.1016/j.oceano.2020.03.005
49. Nandy, T., Mandal, S., Chatterjee, M., 2018. Intra-monsoonal variation of zooplankton population in the Sundarbans Estuarine System, India. Environ. Monit. Assess. 190, 1-20. https://doi.org/10.1007/s10661-018-6969-8
50. Ohkawa, H., Ohishi, N., Yagi, K., 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95, 351-358. https://doi.org/10.1016/0003-2697(79)90738-3
51. Paital, B., Chainy, G.B., 2013. Seasonal variability of antioxidant biomarkers in mud crabs (Scylla serrata). Ecotoxicol. Environ. Saf. 87, 33-41. https://doi.org/10.1016/j.ecoenv.2012.10.006
52. Paital, B., Chainy, G.B.N., 2010. Antioxidant defenses and oxidative stress parameters in tissues of mud crab (Scylla serrata) with reference to changing salinity. Compar. Biochem. Physiol. C 151, 142-151. https://doi.org/10.1016/j.cbpc.2009.09.007
53. Paschke, K., Cumillaf, J.P., Loyola, S., Gebauer, P., Urbina, M., Chinal, M.E., Pascual, C., 2010. Effect of dissolved oxygen level on respiratory metabolism, nutritional physiology, and immune condition of southern king crab Lithodes santolla (Molina, 1782) (Decapoda, Lithodidae). Mar. Biol. 157, 7-18. https://doi.org/10.1007/s00227-009-1291-1
54. Prandle, D., 2009. Estuaries: Dynamics, Mixing, Sedimentation and Morphology. Cambridge University Press, UK.
55. Qiu, J., Wang, W.N., Wang, L.J., Liu, Y.F., Wang, A.L., 2011. Oxidative stress, DNA damage and osmolality in the Pacific white shrimp, Litopenaeus vannamei exposed to acute low temperature stress. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 154, 36-41. https://doi.org/10.1016/j.cbpc.2011.02.007
56. Ragunathan, M.G., 2017. Vicissitudes of oxidative stress biomarkers in the estuarine crab Scylla serrata with reference to dry and wet weather conditions in Ennore estuary, Tamil Nadu, India. Mar. Pollut. Bull. 116, 113-120. https://doi.org/10.1016/j.marpolbul.2016.12.069
57. Rahi, M.L., Azad, K.N., Tabassum, M., Irin, H.H., Hossain, K.S., Aziz, D., Moshtaghi, A., Hurwood, D.A., 2021. Effects of Salinity on Physiological, Biochemical and Gene Expression Parameters of Black Tiger Shrimp (Penaeus monodon): Potential for Farming in Low-Salinity Environments. Biology (Basel). 10, 1220. https://doi.org/10.3390/biology10121220
58. Regoli, F., Giuliani, M.E., 2014. Oxidative pathways of chemical toxicity and oxidative stress biomarkers in marine organisms. Mar. Environ. Res. 93, 106-117. https://doi.org/10.1016/j.marenvres.2013.07.006
59. Romero, M.C., Tapella, F., Sotelano, M.P., Ansaldo, M., Lovrich, G.A., 2011. Oxidative stress in the subantarctic false king crab Paralomis granulosa during air exposure and subsequent re-submersion. Aquaculture 319, 205-210. https://doi.org/10.1016/j.aquaculture.2011.06.041
60. Samanta, P., Im, H., Na, J., Jung, J., 2018. Ecological risk assessment of a contaminated stream using multi-level integrated biomarker response in Carassius auratus. Environ. Pollut. 233, 429-438. https://doi.org/10.1016/j.envpol.2017.10.061
61. Sardi, A.E., Sandrini-Neto, L., da Cunha Lana, P., Camus, L., 2020. Seasonal variation of oxidative biomarkers in gills and digestive glands of the clam Anomalocardia flexuosa and the mangrove oyster Crassostrea rhizophorae. Mar. Pollut. Bull. 156, 111193. https://doi.org/10.1016/j.marpolbul.2020.111193
62. Schvezov, N., Lovrich, G.A., Florentı́n, O., Romero, M.C., 2015. Baseline defense system of commercial male king crab Lithodes santolla from the Beagle Channel. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 181, 18-26. https://doi.org/10.1016/j.cbpa.2014.11.016
63. Semprucci, F., Balsamo, M., Frontalini, F., 2014. The nematode assemblage of a coastal lagoon (Lake Varano, Southern Italy): ecology and biodiversity patterns. Sci. Mar. 78, 579-588. https://doi.org/10.3989/scimar.04018.02A
64. Stoliar, O.B., Lushchak, V.I., 2012. Environmental pollution and oxidative stress in fish. [in:] Lushchak, V.I. (Ed.), Oxidative Stress: Environmental Induction and Dietary Antioxidants. InTech Open, Rijeka, Croatia, 131-166. https://doi.org/10.5772/38094
65. Van Der Oost, R., Beyer, J., Vermeulen, N.P.E., 2003. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ. Toxicol. Pharmacol. 13, 57-149. https://doi.org/10.1016/S1382-6689(02)00126-6
66. Wang, W.N., Wang, A.L., Liu, Y., Xiu, J., Liu, Z.B., Sun, R.Y., 2006. Effects of temperature on growth, adenosine phosphates, ATPase and cellular defense response of juvenile shrimp Macrobrachium nipponense. Aquaculture, 256, 624-630. https://doi.org/10.1016/j.aquaculture.2006.02.009
67. Zheng, J., Cao, J., Yong, M., Su, Y., Wang, J., 2019. Effects of thermal stress on oxidative stress and antioxidant response, heat shock proteins expression profiles and histological changes in Marsupenaeus japonicus. Ecol. Indicat. 101, 780-791. https://doi.org/10.1016/j.ecolind.2018.11.044

Typ dokumentu

Bibliografia

Identyfikator YADDA

bwmeta1.element.baztech-bf8f27e1-bdab-4f34-83f7-b627b4b2998c