Changes in fatty acid profile of Holothuria forskali muscle following acute mercury exposure
DOI:
https://doi.org/10.3989/gya.0335201Keywords:
Acute exposure, Fatty acid composition, Holothuria forskali, Indices of lipid peroxidation, Mercuric chloride (HgCl2), Sea cucumberAbstract
The present study aimed to document the interaction between mercury (Hg), as a model chemical stressor to an aquatic organism, and Fatty acid (FA) profile in the longitudinal muscle of the sea cucumber Holothuria forskali. To assess the sensitivity of this species to the toxic effects of Hg, young H. forskali were exposed to gradual doses of Hg (40, 80 and160 µg·L-1) for 96 h. The results showed that following Hg exposure, the FA profile of H. forskali corresponded to an increase in the level of saturated fatty acids, and the decrease in the level of monounsaturated and polyunsaturated fatty acids. The most prominent changes in the FA composition were recorded at the lowest dose with noticeable decreases in linoleic, arachidonic and eicosapentaenoic acid levels and an increase of docosahexaenoic acid. The occurrence of a state of oxidative stress induced by Hg contamination was evidenced by the enhanced levels of malondialdehyde, hydrogen peroxide and lipid hydroperoxide. Overall, the low concentration of mercury exerted the most obvious effects on lipid metabolism, suggesting that changes in fatty acid composition may be act as an early biomarker to assess mercury toxicity in this ecologically and economically important species.
Downloads
References
Balshaw S, Edwards JW, Ross KE, Daughtry BJ. 2008. Mercury distribution in the muscular tissue of farmed southern bluefin tuna (Thunnus maccoyii) is inversely related to the lipid content of tissues. Food Chem. 111, 616- 621. https://doi.org/10.1016/j.foodchem.2008.04.041
Bhamre PR, Thorat SP, Desai AE. 2010. Evaluation of acute toxicity of mercury, cadmium and zinc to a freshwater mussel Lamellidens consobrinus. Our Nat. 8, 180-184. https://doi.org/10.3126/on.v8i1.4326
Bordbar S, Anwar F, Saari N. 2011. High-value components and bioactives from sea cucumbers for functional foods-A Review. Mar. Drugs 9 (10), 1761-1805. https://doi.org/10.3390/md9101761 PMid:22072996 PMCid:PMC3210605
Calder PC. 2015. Marine omega-3 fatty acids and inflammatory processes: effects, mechanisms and clinical relevance. Biochim. Biophys. Acta Mol. Cell Biol Lipids 1851, 469-484. https://doi.org/10.1016/j.bbalip.2014.08.010 PMid:25149823
Cecchi G, Basini S, Castano C. 1985. Méthanolyse rapide des huiles en solvant. Rev. Franc. Corps Gras 4, 63-164.
Da Costa F, Robert R, Quéré C, Wikfors GH, Soudant P. 2015. Essential fatty acid assimilation and synthesis in larvae of the bivalve Crassostrea gigas. Lipids 50 (5), 503-511. https://doi.org/10.1007/s11745-015-4006-z PMid:25771891
Dailianis S. 2011. Environnemental impact of anthropogenic activities: the use of mussels as a reliable tool for monitoring marine pollution. In: McGevin, L.E. (Ed.), Mussels: Anatomy. Habitat and Environmental Impact. Nova Science Publishers. Inc. pp. 1-30.
Dindia LA, Faught EL, Leonenko Z, Thomas RH, Vijayan MM. 2013. Rapid cortisol signaling in response to acute stress involves changes in plasma membrane order in rainbow trout liver. Am. J. Physiol. Endoc. M. 304, E1157-E1166 https://doi.org/10.1152/ajpendo.00500.2012 PMid:23531621
Delaporte M, Soudant P, Moal J, Kraffe E, Marty Y, Samain J.F .2005. Incorporation and modification of dietary fatty acids in gill polar lipids by two bivalve species Crassostrea gigas and Ruditapes philippinarum. Comp. Biochem. Phys. A 140, 460-470. https://doi.org/10.1016/j.cbpb.2005.02.009 PMid:15936706
Folch J, Lees M, Sloane-Stanley GA. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226 (1) 497-509. https://doi.org/10.1016/S0021-9258(18)64849-5
Flores JS, Torres-Jasso JH, Rojas-Bravo D, Reyna-Villela ZM, Erandis D, Torres-Sánchez ED. 2019. Effects of Mercury, Lead, Arsenic and Zinc to Human Renal Oxidative Stress and Functions: A Review. J. Heavy Met. Toxicity Dis. 4, 1-2.
Filimonova V, Gonçalves F, Marques JC, De Troch M, Gonçalves ANN. 2016. Fatty acid profiling as bioindicator of chemical stress in marine organisms: A review. Ecol. Indic. 67, 657-672. https://doi.org/10.1016/j.ecolind.2016.03.044
Ferain A, Bonnineau C, Neefs I, Das K, Larondelle Y, Rees JF, Debier C, Lemaire B. 2018. Transcriptional effects of phospholipid fatty acid profile on rainbow trout liver cells exposed to methylmercury. Aquat. Toxicol. 199, 174-187. https://doi.org/10.1016/j.aquatox.2018.03.025 PMid:29649756
Funari SS, Barceló F, Escribá PV. 2003. Effects of oleic acid and its congeners, elaidic and stearic acids, on the structural properties of phosphatidylethanolamine membranes. J. Lipid R. 44, 567-575. https://doi.org/10.1194/jlr.M200356-JLR200 PMid:12562874
Gonçalves A, Mesquita A, Verdelhos T, Coutinho J, Marques J, Gonçalves F. 2016. Fatty acids profiles as indicator of stress induced by of a common herbicide on two marine bivalves species: Cerastoderma edule (Linnaeus, 1758) and Scrobicularia plana (da Costa, 1778). Ecol. Indic. 63, 209-218. https://doi.org/10.1016/j.ecolind.2015.12.006
Holman TR. 1954. Autoxidation of fats and related substances. In Progress in the Chemistry of Fats and Other Lipids. Academic Press, New York. 2, 491-514. https://doi.org/10.1016/0079-6832(54)90004-X
Jiang ZY, Hunt JV, Wolf SP. 1992. Detection of lipid hydroperoxides using Fox method. Anal. Biochem. 202, 384-389. https://doi.org/10.1016/0003-2697(92)90122-N
Kotronen A, Seppanen-Laakso T, Westerbacka J, Arola J, Ruskeepaa AL, Yki-Jarvinen H, Oresic M. 2011. Comparison of lipid and fatty acid composition of the liver, subcutaneous and intra-abdominal adipose tissue, and serum. Obesity 18, 937-944. https://doi.org/10.1038/oby.2009.326 PMid:19798063
Lushchak VI. 2011. Environmentally induced oxidative stress in aquatic animals. Aquatic Toxicol. 719 (101), 13-30. https://doi.org/10.1016/j.aquatox.2010.10.006 PMid:21074869
Liu X, Wang L, Feng Z, Song X, Zhu X. 2017b. Molecular cloning and functional characterization of the fatty acid delta 6 desaturase (FAD6) gene in the sea cucumber Apostichopus japonicus. Aquac. Res. 48, 4991-5003. https://doi.org/10.1111/are.13317
Los DA, Murata N. 2004. Membrane fluidity and its roles in the perception of environmental signals. Biochim. Biophys. Acta 1666, 142-157. https://doi.org/10.1016/j.bbamem.2004.08.002 PMid:15519313
Munro D, Banh S, Sotiri, Tamanna N, Treberg J. 2016. The thioredoxin and glutathione‐dependent H2O2 consumption pathways in muscle mitochondria: Involvement in H2O2 metabolism and consequence to H2O2 efflux assays. Free Radic. Biol. Med. 96, 334-346. https://doi.org/10.1016/j.freeradbiomed.2016.04.014 PMid:27101737
Ma XZ, Pang ZD, Wang JH, Song Z, Zhao LM, Du XJ, Deng XL. 2018. The role and mechanism of KCa3.1 channels in human monocyte migration induced by palmitic acid. Exp. Cell Res. 369, 208-217. https://doi.org/10.1016/j.yexcr.2018.05.020 PMid:29792849
Mayurasakorn K, Niatsetskaya ZV, Sosunov SA, Williams JJ, Zirpoli H, Vlasakov I, Ten VS. 2016. DHA but not EPA emulsions preserve neurological and mitochondrial function after brain hypoxia-ischemia in neonatal mice. PLOS One 11. https://doi.org/10.1371/journal.pone.0160870 PMid:27513579 PMCid:PMC4981459
Navarro PG, García-Sanz S, Tuya F. 2014. Contrasting displacement of the sea cucumber Holothuria arguinensis between adjacent nearshore habitats. J. Exp. Mar. Biol. Ecol. 453, 123-130. https://doi.org/10.1016/j.jembe.2014.01.008
Neves M, Castro BB, Vidal T, Vieira R, Marques JC, Coutinho JAP, Gonçalves F. 2015. Biochemical and populational responses of an aquatic bioindicator species, Daphnia longispina, to a commercial formulation of an herbicide (primextraç gold TZ) and its active ingredient (S-metolachlor). Ecol. Indic. 53, 220-230. https://doi.org/10.1016/j.ecolind.2015.01.031
Oliveira P, Lopes-Lima M, Machado J, Guilhermino L. 2015. Comparative sensitivity of European native (Anodonta anatina) and exotic (Corbicula fluminea) bivalves to mercury. Estuar. Coast. Shelf Sci. 167, 191-198. https://doi.org/10.1016/j.ecss.2015.06.014
Ou P, Wolff SP. 1996. A discontinuous method for catalase determination at near physiological concentrations of H2O2 and its application to the study of H2O2 fluxes within cells. J. Biochem. Biophys. Meth. 31 (1-2), 59-67. https://doi.org/10.1016/0165-022X(95)00039-T
Patrick L. 2002. Mercury toxicity mercury toxicity and antioxidants: Part 1: role of glutathione and alpha-lipoic acid in the treatment of mercury toxicity. Altern. Med. Rev. 7 (6), 456-471.
Rabeh, Telahigue K, Bejaoui S, Hajji T, Nechi S, Chelbi E, EL Cafsi M, Soudani N. 2019. Effects of mercury graded doses on redox status, metallothione in levels and genotoxicity in the intestine of sea cucumber Holothuria forskali. Chem. Ecol. 35 (3), 204-218. https://doi.org/10.1080/02757540.2018.1546292
Rabei A, Hichami A, Beldi H, Bellenger S, Khan NA, Soltani N. 2018. Fatty acid composition, enzyme activities and metallothioneins in Donax trunculus (Mollusca, Bivalvia) from polluted and reference sites in the Gulf of Annaba (Algeria): pattern of recovery during transplantation. Environ. Pollut. 237, 900-907. https://doi.org/10.1016/j.envpol.2018.01.041 PMid:29455915
Ruiz-Gutierrez V, Muriana FJ, Guerrero A, Cert AM, Villar J. 1996. Plasma lipids, erythrocyte membrane lipids and blood pressure of hypertensive women after ingestion of dietary oleic acid from two different sources. J. Hypertens 14, 1483- 1490. https://doi.org/10.1097/00004872-199612000-00016 PMid:8986934
Ruiz F, González-Regalado ML, Muñoz JM, Abad M, Toscano A, Prudencio MI, Dias MI. 2014. Distribution of heavy metals and pollution pathways in a shallow marine shelf: assessment for a future management. J. Environ. Sci. Technol. 11, 1249. https://doi.org/10.1007/s13762-014-0576-1
Silva CO, Simões T, Novais SC, Pimparel I, Granada L, Soares AM, Barata C, Lemos MF. 2017. Fatty acid profile of the sea snail Gibbula umbilicalis as a biomarker for coastal metal pollution. Sci. Total Environ. 15 (586), 542-550. https://doi.org/10.1016/j.scitotenv.2017.02.015 PMid:28202240
Signa G, Di Leonardo R, Vaccaro A, Tramati CD, Mazzola A, Vizzini S. 2015. Lipid and fatty acid biomarkers as proxies for environmental contamination in caged mussels Mytilus galloprovincialis. Ecol. Indic. 57, 384-394. https://doi.org/10.1016/j.ecolind.2015.05.002
Sicuro B, Levine J. 2011. Sea cucumber in the Mediterranean: a potential species for aquaculture in the Mediterranean. Rev. Fish. Sci. 19, 299-304. https://doi.org/10.1080/10641262.2011.598249
Tayemeh MB, Esmailbeigi M, Shirdel I, Joo HS, Johari SA, Banan A, Nourani H, Mashhadi H, Jami MJ, Tabarrok M. 2020. Perturbation of fatty acid composition, pigments, and growth indices of Chlorella vulgaris in response to silver ions and nanoparticles: A new holistic understanding of hidden ecotoxicological aspect of pollutants. Chemosphere 238, 124576 https://doi.org/10.1016/j.chemosphere.2019.124576 PMid:31421462
Thyrring J, Juhl BK, Holmstrup M, Blicher ME, Sejr M. 2015. Does acute lead (Pb) contamination influence membrane fatty acid composition and freeze tolerance in intertidal blue mussels in arctic Greenland? Ecotel. 24, 2036-2042. https://doi.org/10.1007/s10646-015-1539-0 PMid:26438355
Turk Culha S, Dereli H, Karaduman FR, Culha M. 2016. Assessment of trace metal contamination in the sea cucumber (Holothuria tubulosa) and sediments from the Dardanelles Strait (Turkey). Environ. Sci. Pollut. R. 23 (12), 11584-11597. https://doi.org/10.1007/s11356-016-6152-0 PMid:26931662
Telahigue K, Rabeh I, Bejaoui S, Hajji T, Nechi S, Chelbi E, El Cafsi M, Soudani N. 2018. Mercury disrupts redox status, up-regulates metallothionein and induces genotoxicity in respiratory tree of sea cucumber (Holothuria forskali). Drug. Chem. Toxicol. 43 (3), 287-297. https://doi.org/10.1080/01480545.2018.1524475 PMid:30554537
Telahigue K, Rabeh I, Hajji T, Trabelsi W, Bejaoui S, Chouba L, El Cafsi M, Soudani N. 2019. Effects of acute mercury exposure on fatty acid composition and oxidative stress biomarkers in Holothuria forskali body wall. Ecotox. Environ. Safe. 169, 516-522. https://doi.org/10.1016/j.ecoenv.2018.11.051 PMid:30472476
Uttara B, Singh AV, Zamboni P, Mahajan RT. 2009. Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr. Neuropharmacol. 7, 65-74. https://doi.org/10.2174/157015909787602823 PMid:19721819 PMCid:PMC2724665
Verlecar XN, Jena KB, Chainy GBN. 2008. Modulation of antioxidant defences in digestive gland of Pernaviridis (L.), on mercury exposures. Chemosphere 71, 1977-1985. https://doi.org/10.1016/j.chemosphere.2007.12.014 PMid:18329067
Vigh L, Nakamoto H, Landry J, Gomez-Muñoz A, Harwood DJL, Horvath I. 2007. Membrane regulation of the stress response from prokaryotic models to mammalian cells. Ann. N. Y. Acad. Sci. 1113, 40-51. https://doi.org/10.1196/annals.1391.027 PMid:17656573
Wang P, Wang R, Wang C, Qian J, Hou J. 2016. Exposure-dose-response relationships of the freshwater bivalve Corbicula fluminea to inorganic mercury in sediments. J. Comput. Theor. Nanosci. 13, 5714-5723. https://doi.org/10.1166/jctn.2016.5476
Published
How to Cite
Issue
Section
License
Copyright (c) 2021 Consejo Superior de Investigaciones Científicas (CSIC)

This work is licensed under a Creative Commons Attribution 4.0 International License.
© CSIC. Manuscripts published in both the print and online versions of this journal are the property of the Consejo Superior de Investigaciones Científicas, and quoting this source is a requirement for any partial or full reproduction.
All contents of this electronic edition, except where otherwise noted, are distributed under a Creative Commons Attribution 4.0 International (CC BY 4.0) licence. You may read here the basic information and the legal text of the licence. The indication of the CC BY 4.0 licence must be expressly stated in this way when necessary.
Self-archiving in repositories, personal webpages or similar, of any version other than the final version of the work produced by the publisher, is not allowed.