PERTANIKA JOURNAL OF TROPICAL AGRICULTURAL SCIENCE

 

e-ISSN 2231-8542
ISSN 1511-3701

Home / Regular Issue / JTAS Vol. 32 (4) Jul. 2024 / JST-4439-2023

 

Evaluation of Glutathione S-transferases Expression as Biomarkers by Heavy Metals in Geloina expansa from Sepang Besar River, Selangor, Malaysia

Sarini Ahmad Wakid, Nor Azwady Abd Aziz, Zazali Alias, Muskhazli Mustafa, Wan Mohd Syazwan and Syaizwan Zahmir Zulkifli

Pertanika Journal of Tropical Agricultural Science, Volume 32, Issue 4, July 2024

DOI: https://doi.org/10.47836/pjst.32.4.01

Keywords: Biomarker, bivalves, Geloina expansa, glutathione S-transferase, heavy metals, SDG 14

Published on: 25 July 2024

Glutathione S-transferases (GSTs) are enzymes involved in phase II of detoxification metabolism and could be used as biomarkers for water pollution. This study aims to determine heavy metal concentrations in the soft tissue of the mangrove clam Geloina expansa, as well as the expression of GSTs in the species. The acid digestion method was used to digest the samples, followed by a standard USEPA 6010B procedure using inductively coupled plasma optical emission spectrometry (ICP-OES) to measure the heavy metal contents in the samples. GST enzyme activity was measured using 1-chloro-2, 4-dinitrobenzene (CDNB) as substrate. One-way ANOVA was performed to compare the mean values of heavy metal concentration, protein concentration, enzyme activity, and specific activity. There was a significant difference (p<0.05) for Zn, total protein, and specific activity in G. expansa, but no significant difference in Pb, Cu and enzyme activity. GST enzyme activities were estimated at 0.16 ± 0.01 µmol/min, with a protein content of 1.24 ± 0.04 mg. The specific activity for GST was 0.13 ± 0.01 µmol/min/mg, calculated as the ratio of enzyme activity to the total protein. GST-specific activity positively correlates with Pb concentration in the soft tissue of G. expansa. Detailed studies on the effects of pollution on the expression of GST need to be further investigated for the future use of this species as an efficient biomarker model.

  • Amira, A., Merad, I., Almeida, C. M. R., Guimarães, L., & Soltani, N. (2018). Seasonal variation in biomarker responses of Donax trunculus from the Gulf of Annaba (Algeria): Implication of metal accumulation in sediments. Comptes Rendus - Geoscience, 350(4), 173-179. https://doi.org/10.1016/j.crte.2018.02.002

  • Aouini, F., Trombini, C., Volland, M., Elcafsi, M., & Blasco, J. (2018). Assessing lead toxicity in the clam Ruditapes philippinarum: Bioaccumulation and biochemical responses. Ecotoxicology and Environmental Safety, 158, 193-203. https://doi.org/10.1016/j.ecoenv.2018.04.033

  • Azevedo, C. C., Guzmán-Guillén, R., Martins, J. C., Osório, H., Vasconcelos, V., da Fonseca, R. R., & Campos, A. (2015). Proteomic profiling of gill GSTs in Mytilus galloprovincialis from the North of Portugal and Galicia evidences variations at protein isoform level with a possible relation with water quality. Marine Environmental Research, 110, 152-161. https://doi.org/10.1016/j.marenvres.2015.08.008

  • Bianchi, T. S. (2013). Estuaries: Where the river meets the sea. Nature Education Knowledge, 4, 12.

  • Blanchette, B. N., & Singh, B. R. (2002). Isolation and characterization of glutathione-S-transferase isozyme Q3 from the northern quahog, Mercinaria mercinaria. Journal of Protein Chemistry, 21, 151-159. https://doi.org/10.1023/A:1015368532136

  • Boening, D. W. (1999). An evaluation of bivalves as biomonitors of heavy metals pollution in marine waters. Environmental Monitoring and Assessment, 55, 459-470. https://doi.org/10.1023/A:1005995217901

  • Boillot, C., Martinez Bueno, M. J., Munaron, D., Le Dreau, M., Mathieu, O., David, A., Fenet, H., Casellas, C., & Gomez, E. (2015). In vivo exposure of marine mussels to carbamazepine and 10-hydroxy-10,11-dihydro-carbamazepine: Bioconcentration and metabolization. Science of the Total Environment, 532, 564-570. https://doi.org/10.1016/j.scitotenv.2015.05.067

  • Bradford, M. M. (1976). A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analutical Biochemistry 72(1-2), 248-254. https://doi.org/10.1016/0003-2697(76)90527-3

  • Campos, A., Tedesco, S., Vasconcelos, V., & Cristobal, S. (2012). Proteomic research in bivalves: Towards the identification of molecular markers of aquatic pollution. Journal of Proteomics, 75(14), 4346-4359. https://doi.org/10.1016/j.jprot.2012.04.027

  • Casas, S., Gonzalez, J. L., Andral, B., & Cossa, D. (2008). Relation between metal concentration in water and metal content in marine mussels (Mytilus galloprovincialis): Impact of physiology. Environmental Toxicology and Chemistry, 27(7), 1543-1552. https://doi.org/10.1897/07-418.1

  • Chetoui, I., Bejaoui, S., Fouzai, C., Trabelsi, W., Nechi, S., Chelbi, E., Ghalghaf, M., El Cafsi, M., & Soudani, N. (2019). Effect of lead graded doses in Mactra Corallina gills: Antioxidants status, cholinergic function and histopathological studies. Journal of Drug Design and Medicinal Chemistry, 5(1), Article 1. https://doi.org/10.11648/j.jddmc.20190501.11

  • Choi, J. Y., Yu, J., Yang, D. B., Ra, K., Kim, K. T., Hong, G. H., & Shin, K. H. (2011). Acetylthiocholine (ATC)–cleaving cholinesterase (ChE) activity as a potential biomarker of pesticide exposure in the Manila clam, Ruditapes philippinarum, of Korea. Marine Environmental Research, 71(3), 162-168. https://doi.org/10.1016/j.marenvres.2010.12.007

  • Çomaklı, V., Kuzu, M., & Demirdăg, R. (2015). Characterization and purification of glutathione S-transferase from the liver and gill tissues of Ăgrı Balık lake trout Salmo trutta labrax and the effects of heavy metal ions on its activity. Journal of Aquatic Animal Health, 27(3), 145-151. https://doi.org/10.1080/08997659.2015.1032441

  • Cossu, C., Doyotte, A., Babut, M., Exinger, A., & Vasseur, P. (2000). Antioxidant biomarkers in freshwater bivalves, Unio tumidus, in response to different contamination profiles of aquatic sediments. Ecotoxicology and Environmental Safety, 45(2), 106-121. https://doi.org/10.1006/eesa.1999.1842

  • Dabwan, A. H. A., & Taufiq, M. (2016). Bivalves as bio-indicators for heavy metals detection in Kuala Kemaman, Terengganu, Malaysia. Indian Journal of Science and Technology, 9(9), 1-6. https://doi.org/10.17485/ijst/2016/v9i9/88708

  • de Almeida, E. A., Bainy, A. C. D., de Melo Loureiro, A. P., Martinez, G. R., Miyamoto, S., Onuki, J., Barbosa, L. F., Garcia, C. C. M., Prado, F. M., Ronsein, G. E., Sigolo, C. A., Barbosa, C. B., Martins, A. M. G., de Medeiros, M. H. G., & Di Mascio, P. (2007). Oxidative stress in Perna perna and other bivalves as indicators of environmental stress in the Brazilian marine environment: Antioxidants, lipid peroxidation and DNA damage. Comparative Biochemistry and Physiology: A Molecular and Integrative Physiology, 146(4), 588-600. https://doi.org/10.1016/j.cbpa.2006.02.040

  • Edward, F. B., Yap, C. K., Ismail, A., & Tan, S. G. (2009). Interspecific variation of heavy metal concentrations in the different parts of tropical intertidal bivalves. Water, Air, and Soil Pollution, 196, 297-309. https://doi.org/10.1007/s11270-008-9777-x

  • Ercal, N., Gurer-Orhan, H., & Aykin-Burns, N. (2001). Toxic metals and oxidative stress part I: Mechanisms involved in metal-induced oxidative damage. Current Topics in Medicinal Chemistry, 1(6), 529-539. https://doi.org/10.2174/1568026013394831

  • Espinoza, H. M., Williams, C. R., & Gallagher, E. P. (2012). Effect of cadmium on glutathione S-transferase and metallothionein gene expression in coho salmon liver, gill and olfactory tissues. Aquatic Toxicology, 110-111, 37-44. https://doi.org/10.1016/j.aquatox.2011.12.012

  • Famme, P., Riisgård, H., & Jørgensen, C. (1986). On direct measurement of pumping rates in the mussel Mytilus edulis. Marine Biology, 92, 323-327. https://doi.org/10.1007/BF00392672

  • Farrington, J. W., Tripp, B. W., Tanabe, S., Subramanian, A., Sericano, J. L., Wade, T. L., Knap, A. H. & Edward, D. (2016). Edward D. Goldberg’s proposal of “the mussel watch”: Reflections after 40 years. Marine Pollution Bulletin, 110(1), 501-510. https://doi.org/10.1016/j.marpolbul.2016.05.074

  • Fitzpatrick, P. J., Krag, T. O. B., Hojrup, P., & Sheehan, D. (1995). Characterization of a glutathione S-transferase and a related glutathione-binding protein from gill of the blue mussel, Mytilus edulis. Biochemical Journal, 305(1), 145-150. https://doi.org/10.1042/bj3050145

  • Fitzpatrick, P. J., O’Halloran, J., Sheehan, D., & Walsh, A. R. (1997). Assessment of a glutathione S-transferase and related proteins in the gill and digestive gland of Mytilus edulis (L.), as potential organic pollution biomarkers. Biomarkers, 2(1), 51-56. https://doi.org/10.1080/135475097231977

  • Flora, G., Gupta, D., & Tiwari, A. (2012). Toxicity of lead: A review with recent updates. Interdisciplinary Toxicology, 5(2), 47-58. https://doi.org/10.2478/v10102-012-0009-2

  • Fukunaga, A., & Anderson, M. J. (2011). Bioaccumulation of copper, lead and zinc by the bivalves Macomona liliana and Austrovenus stutchburyi. Journal of Experimental Marine Biology and Ecology, 396(2), 244-252. https://doi.org/10.1016/j.jembe.2010.10.029

  • Gurer, H., & Ercal, N. (2000). Can antioxidants be beneficial in the treatment of lead poisoning? Free Radical Biology and Medicine, 29(10), 927-945. https://doi.org/10.1016/S0891-5849(00)00413-5

  • Habig, W. H., Pabst, M. J., & Jakoby, W. B. (1974). Glutathione S transferases. The first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry, 249(22), 7130-7139. https://doi.org/10.1016/S0021-9258(19)42083-8

  • Halliwell, B., & Gutteridge, J. M. C. (1989). Protection against oxidants in biological systems: the superoxide theory of oxygen toxicity. In B. Halliwell & J. M. C. Gutteridge (Eds.), Free Radical in Biology and Medicine (pp. 86-123). Clarendon Press.

  • Hamli, H., Idris, M. H., Kamal, A. H. M., & King, W. S. (2012). Diversity of edible mollusc (Gastropoda and Bivalvia) at selected divison of Sarawak, Malaysia. International Journal on Advanced Science, Engineering and Information Technology, 2(4), 5-7.

  • Harsono, N. D. B. D., Ransangan, J., Denil, D. J., & Kar, S. T. (2017). Heavy metals in marsh clam (Polymesoda expansa) and green mussel (Perna viridis) along the northwest coast of Sabah, Malaysia. Borneo Journal of Marine Science and Aquaculture, 1, 25-32. https://doi.org/10.51200/bjomsa.v1i.987

  • Helmholz, H., Ruhnau, C., Pröfrock, D., Erbslöh, H. B., & Prange, A. (2016). Seasonal and annual variations in physiological and biochemical responses from transplanted marine bioindicator species Mytilus spp. during a long term field exposure experiment. Science of the Total Environment, 565, 626-636. https://doi.org/10.1016/j.scitotenv.2016.04.202

  • Hoarau, P., Damiens, G., Roméo, M., Gnassia-Barelli, M., & Bebianno, M. J. (2006). Cloning and expression of a GST-pi gene in Mytilus galloprovincialis. Attempt to use the GST-pi transcript as a biomarker of pollution. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology, 143(2), 196-203. https://doi.org/10.1016/j.cbpc.2006.02.007

  • Hoarau, P., Garello, G., Gnassia-Barelli, M., Romeo, M., & Girard, J. P. (2002). Purification and partial characterization of seven glutathione S-transferase isoforms from the clam Ruditapes decussatus. European Journal of Biochemistry, 269(17), 4359-4366. https://doi.org/10.1046/j.1432-1033.2002.03141.x

  • Hossain, M., Othman, S., Bujang, J. S., & Lim, M. T. (2001). Distribution of copper in the Sepang mangrove reserve forest environment, Malaysia, Journal of Tropical Forest Science, 13(1), 130-139.

  • Hossain, M. S., Ahmed, M. K., Liyana, E., Hossain, M. S., Jolly, Y. N., Kabir, M. J., Akter, S., & Rahman, M. S. (2021). A case study on metal contamination in water and sediment near a coal thermal power plant on the Eastern Coast of Bangladesh. Environments, 8(10), Article 108. https://doi.org/10.3390/environments8100108

  • Hsu, P. C., & Guo, Y. L. (2002). Antioxidant nutrients and lead toxicity. Toxicology 180(1), 33-44. https://doi.org/10.1016/S0300-483X(02)00380-3

  • Hussein, A., & Khaled, A. (2014). Determination of metals in tuna species and bivalves from Alexandria, Egypt. Egyptian Journal of Aquatic Research, 40(1), 9-17. https://doi.org/10.1016/j.ejar.2014.02.003

  • Ismail, A., & Ramli, R. (1997). Trace metals in sediments and molluscs from an estuary receiving pig farms effluent, Environmental Technology, 18(5) 509-515. https://doi.org/10.1080/09593331808616566

  • Istomina, A., Mazur, A., Chelomin, V., Kukla, S., Slobodskova, V., Zvyagintsev, A., Kolosova, L., Zhukovskaya, A., & Fedorets, Y. (2020). The different biomarkers in the assessment of the marine environmental quality using the representative species Mytilus trossulus. Water, Air, and Soil Pollution, 231(8), Article 403. https://doi.org/10.1007/s11270-020-04782-w

  • Jensen, J., Kyvsgaard, N. C., Battisti, A., & Baptiste, K. E. (2018). Environmental and public health related risk of veterinary zinc in pig production-using Denmark as an example. Environment International, 114, 181-190. https://doi.org/10.1016/j.envint.2018.02.007

  • Jozefczak, M., Remans, T., Vangronsveld, J., & Cuypers, A. (2012). Glutathione is a key player in metal-induced oxidative stress defenses. International Journal of Molecular Sciences, 13(3), 3145-3175. https://doi.org/10.3390/ijms13033145

  • Kaaya, A., Najimi, S., Ribera, D., Narbonne, J. F., & Moukrim, A. (1999). Characterization of glutathione S-transferases (GST) activities in Perna perna and Mytilus galloprovincialis used as a biomarker of pollution in the Agadir marine bay (South of Morocco). Bulletin of Environmental Contamination and Toxicology, 62, 623-629.

  • Ketterer, B., Coles, B., & Meyer, D. J. (1983). The role of glutathione in detoxication. Environmental Health Perspectives, 49, 59-69. https://doi.org/10.1289/ehp.834959

  • Krause-Nehring, J., Brey, T., & Thorrold, S. R. (2012). Centennial records of lead contamination in Northern Atlantic bivalves (Arctica islandica). Marine Pollution Bulletin, 64(2), 233-240. https://doi.org/10.1016/j.marpolbul.2011.11.028

  • Krishnakumar, P. K., Qurban, M. A., & Sasikumar, G. (2018). Biomonitoring of trace metals in the coastal waters using bivalve molluscs. In H. E. M. Saleh & E. E. Adham (Eds.), Trace Elements - Human Health and Environment. Intech Open. https://doi.org/10.5772/intechopen.76938

  • Krishnan, K., Saion, E., Halimah, M. K., & Yap, C. K. (2023). Utilizing mollusk soft tissue and shells as biomarkers for monitoring heavy metal pollution in mangrove forests. MethodsX, 11, Article 102281. https://doi.org/10.1016/j.mex.2023.102281

  • Krishnan, K., Saion, E. B., Yap, C. K., Chong, M. Y., & Nadia, A. S. (2022). Determination of trace elements in sediments samples by using neutron activation analysis. Journal of Experimental Biology and Agricultural Sciences, 10(1), 21-31. https://doi.org/10.18006/2022.10(1).21.31.

  • Lamine, I., Chahouri, A., Moukrim, A., & Alla, A. A. (2023). The impact of climate change and pollution on trematode-bivalve dynamics. Marine Environmental Research, 191, Article 106130. https://doi.org/10.1016/j.marenvres.2023.106130

  • Leonard, S. S., Harris, G. K., & Shi, X. (2004). Metal-induced oxidative stress and signal transduction. Free Radical Biology and Medicine, 37(12), 1921-1942. https://doi.org/10.1016/j.freeradbiomed.2004.09.010

  • Li, Z., Ma, Z., van der Kuijp, T. J., Yuan, Z., & Huang, L. (2014). A review of soil heavy metal pollution from mines in China: Pollution and health risk assessment. Science of the Total Environment, 468/469, 843-853.

  • Livingstone, D. R. (1993). Biotechnology and pollution monitoring: use of molecular biomarkers in the aquatic environment. Journal of Chemical Technology & Biotechnology, 57(3), 195-211.

  • Livingstone, D. R. (2001). Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Marine Pollution Bulletin, 42(8), 656-666. https://doi.org/10.1016/S0025-326X(01)00060-1

  • Martins, J. C., Leão, P. N., & Vasconcelos, V. (2009). Differential protein expression in Corbicula fluminea upon exposure to a Microcystis aeruginosa toxic strain. Toxicon, 53(4), 409-416. https://doi.org/10.1016/j.toxicon.2008.12.022

  • Martins, J. C., Campos, A., Osório, H., da Fonseca, R., & Vasconcelos, V. (2014). Proteomic profiling of cytosolic glutathione transferases from three bivalve species: Corbicula fluminea, Mytilus galloprovincialis and Anodonta cygnea. International Journal of Molecular Sciences, 15(2), 1887-1900. https://doi.org/10.3390/ijms15021887

  • Mohd Hamdan, D. D., Md. Shah, J., Gumpulan, F., Foo, J., & Awang Lukman, K. (2020). The North Borneo Iranun’s community’s ethnomedicine knowledge on marsh clam (Geloina expansa). Asian Journal of Ethnobiology, 3(1), 30-38. https://doi.org/10.13057/asianjethnobiol/y030105

  • Marszalek, M., Kowalski, Z., & Makara, A. (2019). The possibility of contamination of water-soil environment as a result of the use of pig slurry. Ecological Chemistry and Engineering S, 26(2), 313-330. https://doi.org/10.1515/eces-2019-0022

  • McCarty, L. S., Power, M., & Munkittrick, K. R. (2002). Bioindicators versus biomarkers in ecological risk assessment. Human and Ecological Risk Assessment: An International Journal, 8(1), 159-164. https://doi.org/10.1080/20028091056791

  • Moore, J. N., & Langner, H. W. (2012). Can a river heal itself? Natural attenuation of metal contamination in river sediment. Environmental Science & Technology, 46(5), 2616-2623. https://doi.org/10.1021/es203810j

  • Moral, R., Perez-Murcia, M. D., Perez-Espinosa, A., Moreno-Caselles, J., Paredes, C., & Rufete, B. (2008). Salinity, organic content, micronutrients and heavy metals in pig slurries from South-Eastern Spain. Waste Management, 28(2), 367-371. https://doi.org/10.1016/j.wasman.2007.01.009

  • Morton, B. (1976). The biology and functional morphology of the Southeast Asian mangrove bivalve, Polymesoda (Geloina) erosa (Solander, 1786) (Bivalvia: Corbiculidae). Canadian Journal of Zoology, 54(4), 482-500. https://doi.org/10.1139/z76-055

  • Ong, M. C., & Ibrahim, A. (2017). Determination of selected metallic elements in marsh clam, Polymesoda expansa, collected from Tanjung Lumpur Mangrove Forest, Kuantan, Pahang. Borneo Journal of Marine Science and Aquaculture, 1, 65-70.

  • Ong, M. C., Kamaruzaman, M. I., Chuen, Y. J., Yunus, K., & Bidai, J. (2017). Metals contamination using Polymesoda expansa (Marsh Clam) as bio-indicator in Kelantan River, Malaysia. Malaysian Journal of Analytical Sciences, 21(3), 597–604. https://doi.org/10.17576/mjas-2017-2103-09

  • Pérez, E., Blasco, J., & Solé, M. (2004). Biomarker responses to pollution in two invertebrate species: Scrobicularia plana and Nereis diversicolor from the Cádiz bay (SW Spain). Marine Environmental Research, 58(2-5), 275-279. https://doi.org/10.1016/j.marenvres.2004.03.071

  • Phillips, D. J. H., & Rainbow, P. S. (1994). Biomonitoring of trace aquatic contaminants. Springer Science & Business Media.

  • Poutiers, J. M. (1998). Bivalves: Acephala, Lamellibranchia, Polycypoda. In: K. E. Carpenter & V. H. Niem (Eds.), Food the Living Marine Resources of the Western Central Pacific, Volume 1, Seaweed, Corals, Bivalves and Gastropods (pp 123-362). FAO, United Nations.

  • Puerto, M., Campos, A., Prieto, A., Cameán, A., Almeida, A. M. de, Coelho, A. V., & Vasconcelos, V. (2011). Differential protein expression in two bivalve species; Mytilus galloprovincialis and Corbicula fluminea; exposed to Cylindrospermopsis raciborskii cells. Aquatic Toxicology, 101(I), 109-116. https://doi.org/10.1016/j.aquatox.2010.09.009

  • Rajeshkumar, S., & Li, X. (2018). Bioaccumulation of heavy metals in fish species from the Meiliang Bay, Taihu Lake, China. Toxicology Reports, 5, 288-295. https://doi.org/10.1016/j.toxrep.2018.01.007

  • Ramsie, S. A., Zulkifli, S.Z., Mohamat-Yusuf, F., & Ismail, A. (2014). Geochemical fractionations of heavy metals in sediments of Sepang Besar, Acta Biologica Malaysiana, 3,(1) 1-9.

  • Regoli, F. (2000). Total oxyradical scavenging capacity (TOSC) in polluted and translocated mussels: A predictive biomarker of oxidative stress. Aquatic Toxicology, 50(4), 351-361. https://doi.org/10.1016/S0166-445X(00)00091-6

  • Regoli, F., Pellegrini, D., Cicero, A. M., Nigro, M., Benedetti, M., Gorbi, S., Fattorini, D., D’Errico, G., Di Carlo, M., Nardi, A., Gaion, A., Scuderi, A., Giuliani, S., Romanelli, G., Berto, D., Trabucco, B., Guidi, P., Bernardeschi, M., Scarcelli, V., & Frenzilli, G. (2014). A multidisciplinary weight of evidence approach for environmental risk assessment at the Costa Concordia wreck: Integrative indices from Mussel Watch. Marine Environmental Research, 96, 92-104. https://doi.org/10.1016/j.marenvres.2013.09.016

  • Revathy, K. S., Umasuthan, N., Lee, Y., Choi, C. Y., Whang, I., & Lee, J. (2012). First molluscan theta-class Glutathione S-Transferase: Identification, cloning, characterization and transcriptional analysis post immune challenges. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 162(1-3), 10-23. https://doi.org/10.1016/j.cbpb.2012.02.004

  • Saed, K., Ismail, A., Omar, H., & Kusnan, M. (2002). Accumulation of heavy metals (Zn, Cu, Pb, Cd) in flat-tree oysters Isognomon alatus exposed to pig farm effluent. Toxicological and Environmental Chemistry, 82(1-2), 45-58. https://doi.org/10.1080/713746657

  • Sáenz, L. A., Seibert, E. L., Zanette, J., Fiedler, H. D., Curtius, A. J., Ferreira, J. F., Alves de Almeida, E., Marques, M. R. F., & Bainy, A. C. D. (2010). Biochemical biomarkers and metals in Perna perna mussels from mariculture zones of Santa Catarina, Brazil. Ecotoxicology and Environmental Safety, 73(5), 796-804. https://doi.org/10.1016/j.ecoenv.2010.02.015

  • Secretary-General, U. (2017). Progress towards the sustainable development goals: Report of the Secretary-General, UN. United States of America. https://policycommons.net/artifacts/127525/progress-towards-the-sustainable-development-goals/182695/ on 01 Apr 2024.

  • Sharaf, H. M., & Shehata, A. M. (2015). Heavy metals and hydrocarbon concentrations in water, sediments and tissue of Cyclope neritea from two sites in Suez Canal, Egypt and histopathological effects. Journal of Environmental Health Science and Engineering, 13, Article 14. https://doi.org/10.1186/s40201-015-0171-5

  • Shenai-Tirodkar, P. S., Gauns, M. U., Mujawar, M. W. A., & Ansari, Z. A. (2017). Antioxidant responses in gills and digestive gland of oyster Crassostrea madrasensis (Preston) under lead exposure. Ecotoxicology and Environmental Safety, 142, 87-94. https://doi.org/10.1016/j.ecoenv.2017.03.056

  • Shukor, N. A., Krishnan, K., Shing, W. L., Ariffin, N., & Yong, W. L. (2023). The pollution characteristics of harmful heavy metal in surface sediment of Sepang River, Malaysia. Environment and Ecology Research, 11(4), 579-585. https://doi.org/10.13189/eer.2023.110406

  • Singh, S. (2014, July 3). Ban on pig farming in Bukit Pelanduk still in force. The Star. https://www.thestar.com.my/news/nation/2014/07/03/1998-ban-on-pig-farming-in-bukit-pelanduk-still-in-force/

  • Sorenson, E. M. (1991). Metal poisoning in fish. CRC Press.

  • Turkmen, A., Turkmen, M., Tepe, Y., & Akyurt, I. (2005). Heavy metals in three commercially valuable fish species from Iskenderun Bay, Northern East Mediterranean Sea, Turkey. Food Chemistry, 91(1), 167-172. https://doi.org/10.1016/j.foodchem.2004.08.008

  • Umasuthan, N., Revathy, K. S., Lee, Y., Whang, I., Choi, C. Y., & Lee, J. (2012). A novel molluscan sigma-like glutathione S-transferase from Manila clam, Ruditapes philippinarum: Cloning, characterization and transcriptional profiling. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 155(4), 539-550. https://doi.org/10.1016/j.cbpc.2012.01.001

  • Valko, M., Morris, H., & Cronin, M. T. (2005). Metals, toxicity and oxidative stress. Current Medicinal Chemistry, 12(10), 1161-1208. https://doi.org/10.2174/0929867053764635

  • Van der Oost, R., Beyer, J., & Vermeulen, N. P. E. (2003). Fish bioaccumulation and biomarkers in environmental risk assessment: A review. Environmental Toxicology and Pharmacology, 13(2), 57-149. https://doi.org/10.1016/S1382-6689(02)00126-6

  • Vasconcelos, V. M., Wiegand, C., & Pflugmacher, S. (2007). Dynamics of glutathione-S-transferases in Mytilus galloprovincialis exposed to toxic Microcystis aeruginosa cells, extracts and pure toxins. Toxicon, 50(6), 740-745. https://doi.org/10.1016/j.toxicon.2007.06.010

  • Viarengo, A. (1989). Heavy metals in marine invertebrates: mechanisms of regulation and toxicity at the cellular level. CRC Critical Reviews in Aquatic Sciences, 1, 295-317.

  • Vidal, M. L., Rouimi, P., Debrauwer, L., & Narbonne, J. F. (2002). Purification and characterisation of glutathione S-transferases from the freshwater clam Corbicula fluminea (Müller). Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology, 131(4), 477-489. https://doi.org/10.1016/S1532-0456(02)00039-X

  • Wadige, C. P. M., Taylor, A. M., Maher, W. A., Ubrihien, R. P., & Krikowa, F. (2014). Effects of lead-spiked sediments on freshwater bivalve, Hyridella australis: linking organism metal exposure-dose-response. Aquatic Toxicology, 149, 83-93. https://doi.org/10.1016/j.aquatox.2014.01.017

  • Wang, W., Mai, K., Zhang, W., Ai, Q., Yao, C., Li, H., & Liufu, Z. (2009). Effects of dietary copper on survival, growth and immune response of juvenile abalone, Haliotis discus hannai Ino. Aquaculture, 297(1-4), 122-127. https://doi.org/10.1016/j.aquaculture.2009.09.006

  • Wedepohl, K. H. (1995). The composition of the continental crust. Geochimica et Cosmochimica Acta, (59)7, 1217-1232.

  • Wei, J., Duan, M., Li, Y., Nwankwegu, A. S., Ji, Y., & Zhang, J. (2019). Concentration and pollution assessment of heavy metals within surface sediments of the Raohe Basin, China. Scientific Reports, 9(1), 1-7. https://doi.org/10.1038/s41598-019-49724-7

  • Winterbourn, C. C. (2008). Reconciling the chemistry and biology of reactive oxygen species. Nature Chemical Biology, 4(5), 278-286. https://doi.org/10.1038/nchembio.85

  • WoRMS Editorial Board. (2022). World Register of Marine Species. https://www.marinespecies.org at VLIZ.

  • Xu, L., Zheng, G. J., Lam, P. K. S., & Richardson, B. J. (1999). Relationship between tissue concentrations of polycyclic aromatic hydrocarbons and DNA adducts in green-lipped mussels (Perna viridis). Ecotoxicology, 8, 73-82. https://doi.org/10.1023/A:1008910617843

  • Ya, N. A., Singh, H. R., Ramli, N. H., Makhtar, N., Mohd Rashid, H. N., Dzakaria, N., & Samat, A. (2014). Fish diversity in Sepang Besar estuary - A preliminary analysis. International Journal of Advances in Agricultural and Environmental Engineering, 1(2), 229-233.

  • Yaakub, N., Rohalin, W. M., & Nordin, R. H. (2019). Bioconcentration of cadmium and nickel in mud clams (Polymesoda expansa) at Balok River, Pahang. Journal of Applied Science and Process Engineering, 6(2), 362-368. https://doi.org/10.33736/jaspe.1783.2019

  • Yahya, N., Idris, I., Rosli, N. S., & Bachok, Z. (2018). Population dynamics of mangrove clam, Geloina expansa (Mousson, 1849) (Mollusca, Bivalvia) in a Malaysian mangrove system of South China Sea. Journal of Sustainability Science and Management, 13(5), 203-216.

  • Yahya, N., Idris, I., Rosli, N. S., & Bachok, Z. (2020). Mangrove-associated bivalves in Southeast Asia: A review. Regional Studies in Marine Science, 38, Article 101382. https://doi.org/10.1016/j.rsma.2020.101382.

  • Yang, H. L., Nie, L. J., Zhu, S. G., & Zhou, X. W. (2002). Purification and characterization of a novel glutathione S-transferase from Asaphis dichotoma. Archives of Biochemistry and Biophysics, 403(2), 202-208. https://doi.org/10.1016/S0003-9861(02)00223-0

  • Yang, H. L., Zeng, Q. Y., Li, E. Q., Zhu, S. G., & Zhou, X. W. (2004). Molecular cloning, expression and characterization of glutathione S-transferase from Mytilus edulis. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 139(2), 175-182. https://doi.org/10.1016/j.cbpc.2004.06.019

  • Yang, H. L., Zeng, Q.Y., Nie, L. J., Zhu, S. G., & Zhou, X. W. (2003). Purification and characterization of a novel glutathione S-transferase from Atactodea striata. Biochem. Biophysical Research Communications, 307(3), 626-631. https://doi.org/10.1016/S0006-291X(03)01221-X

  • Yap, C. K., Edward, F. B., & Tan, S. G. (2014). Bivalve Polymesoda erosa: Its potentials as a biomonitor and food safety concern. Pertanika Journal of Tropical Agricultural Science, 37(1), 19-38.

  • Yap, C. K, & Chew, W. (2011). A higher metal bioavailability and contamination of trace metals in Pantai Lido than Sungai Semerak: Evidence from trace metal concentrations in Polymesoda expansa and surface sediments. Malaysian Applied Biology, 40(1), 55-59.

  • Yap, C. K., & Al-Mutairi, K. A. (2022). Ecological-health risks of potentially toxic metals in mangrove sediments near estuaries after years of piggery farming bans in Peninsular Malaysia. Sustainability (Switzerland), 14(3), 1525. https://doi.org/10.3390/su14031525

  • Yap, C. K., Ismail, A., Ching, H. L., & Tan, S. (2007). Interpretation of copper and zinc contamination in the aquatic environment of Peninsular Malaysia with special reference to a polluted river, Sepang River. Wetland Science, 5, 311-321.

  • Yap, C. K., Cheng, W. H., Karami, A., & Ismail, A. (2016). Health risk assessments of heavy metal exposure via consumption of marine mussels collected from anthropogenic sites. Science of the Total Environment, 553, 285-296. https://doi.org/10.1016/j.scitotenv.2016.02.092

  • Yap, C. K., Chew, W., Cheng, W. H., Okamura, H., Harino, H., Peng, S. H. T., Ismail, M.S., & Seng, C. (2019). Higher bioavailability and contamination by copper in the edible mussels, snails and horseshoe crabs at Kampung Pasir Puteh: Evidence of an industrial effluent receiving site at Pasir Gudang area. Advancements in Bioequivalence & Bioavailability, 2(5), 000548. https://doi.org/10.31031/ABB.2019.02.000548

  • Yap, C. K., Ismail, A., Edward, F. B., Tan, S. G., & Siraj, S. S. (2006). Use of different soft tissues of Perna viridis as biomonitors of bioavailability and contamination by heavy metals (Cd, Cu, Fe, Pb, Ni, and Zn) in a semi-enclosed intertidal water, the Johore Straits. Toxicological and Environmental Chemistry, 88(4), 683-695. https://doi.org/10.1080/02772240600874139

  • Yuan, Y., Jin, M., Xiong, J., & Zhou, Q. (2019). Effects of dietary dosage forms of copper supplementation on growth, antioxidant capacity, innate immunity enzyme activities and gene expressions for juvenile Litopenaeus vannamei. Fish and Shellfish Immunology, 84, 1059-1067. https://doi.org/10.1016/j.fsi.2018.10.075

  • Zarykhta, V. V., Zhang, Z., Kholodkevich, S. V., Kuznetsova, T. V., Sharov, A. N., Zhang, Y., Sun, K., Lv, M., & Feng, Y. (2019). Comprehensive assessments of ecological states of Songhua River using chemical analysis and bivalves as bioindicators. Environmental Science and Pollution Research, 26, 33341-33350. https://doi.org/10.1007/s11356-019-06349-7

  • Zhang, H., Pan, L., & Tao, Y. (2014). Toxicity assessment of environmental pollutant phenanthrene in clam Venerupis philippinarum using oxidative stress biomarkers. Environmental Toxicology and Pharmacology, 37(2), 697-704. https://doi.org/10.1016/j.etap.2014.01.018

  • Zhang, D., Wang, X., & Zhou, Z. (2017). Impacts of small-scale industrialized swine farming on local soil, water and crop qualities in a Hilly Red Soil Region of Subtropical China. International Journal of Environmental Research and Public Health, 14(12), Article 1524. https://doi.org/10.3390/ijerph14121524

  • Zhu, J., Li, R., Zhang, Z., Mao, H., & Fan, Z. (2013). Heavy metal contents in pig manure and feeds under intensive farming and potential hazard on farmlands in Shaanxi Province, China. Chinese Society for Agricultural Machinery.

ISSN 1511-3701

e-ISSN 2231-8542

Article ID

JST-4439-2023

Download Full Article PDF

Share this article

Related Articles