Methylmercury Effect and Distribution in Two Extremophile Microalgae Strains Dunaliella salina and Coccomyxa onubensis from Andalusia (Spain)

. 2024 Feb 21 ; 12 (3) : . [epub] 20240221

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38543485

Grantová podpora
FEDER UHU 202065 European Regional Development Fund FEDER program of Andalusia (Spain) 2014-2020

Odkazy

PubMed 38543485
PubMed Central PMC10972382
DOI 10.3390/microorganisms12030434
PII: microorganisms12030434
Knihovny.cz E-zdroje

The main entrance point of highly toxic organic Hg forms, including methylmercury (MeHg), into the aquatic food web is phytoplankton, which is greatly represented by various natural microalgal species. Processes associated with MeHg fate in microalgae cells such as uptake, effects on cells and toxicity, Hg biotransformation, and intracellular stability are detrimental to the process of further biomagnification and, as a consequence, have great importance for human health. The study of MeHg uptake and distribution in cultures of marine halophile Dunaliella salina and freshwater acidophilic alga Coccomyxa onubensis demonstrated that most of the MeHg is imported inside the cell, while cell surface adhesion is insignificant. Almost all MeHg is removed from the culture medium after 72 h. Significant processes in rapid MeHg removal from liquid medium are its abiotic photodegradation and volatilization associated with algal enzymatic activity. The maximum intracellular accumulation for both species was in 80 nM MeHg-exposed cultures after 24 h of exposure for D. salina (from 27 to 34 µg/gDW) and at 48 h for C. onubensis (up to 138 µg/gDW). The different Hg intakes in these two strains could be explained by the lack of a rigid cell wall in D. salina and the higher chemical ability of MeHg to pass through complex cell wall structures in C. onubensis. Electron microscopy studies on the ultrastructure of both strains demonstrated obvious microvacuolization in the form of many very small vacuoles and partial cell membrane disruption in 80 nM MeHg-exposed cultures. Results further showed that Coccomyxa onubensis is a good candidate for MeHg-contaminated water reclamation due to its great robustness at nanomolar concentrations of MeHg coupled with its very high intake and almost complete Hg removal from liquid medium at the MeHg levels tested.

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Bravo A.G., Cosio C. Biotic Formation of Methylmercury: A Bio–Physico–Chemical Conundrum. Limnol. Oceanogr. 2020;65:1010–1027. doi: 10.1002/lno.11366. PubMed DOI PMC

Karimi R., Fitzgerald T.P., Fisher N.S. A Quantitative Synthesis of Mercury in Commercial Seafood and Implications for Exposure in the United States. Environ. Health Perspect. 2012;120:1512–1519. doi: 10.1289/ehp.1205122. PubMed DOI PMC

Beauvais-Flück R., Slaveykova V.I., Cosio C. Cellular Toxicity Pathways of Inorganic and Methyl Mercury in the Green Microalga Chlamydomonas reinhardtii. Sci. Rep. 2017;7:8034. doi: 10.1038/s41598-017-08515-8. PubMed DOI PMC

Scheuhammer A.M., Meyer M.W., Sandheinrich M.B., Murray M.W. Effects of Environmental Methylmercury on the Health of Wild Birds, Mammals, and Fish. Ambio. 2007;36:12–18. doi: 10.1579/0044-7447(2007)36[12:EOEMOT]2.0.CO;2. PubMed DOI

Santos J.P., Mehmeti L., Slaveykova V.I. Simple Acid Digestion Procedure for the Determination of Total Mercury in Plankton by Cold Vapor Atomic Fluorescence Spectroscopy. Methods Protoc. 2022;5:29. doi: 10.3390/mps5020029. PubMed DOI PMC

Lee C.-S., Fisher N.S. Bioaccumulation of Methylmercury in a Marine Copepod. Environ. Toxicol. Chem. 2017;36:1287–1293. doi: 10.1002/etc.3660. PubMed DOI PMC

Monastero R.N., Karimi R., Nyland J.F., Harrington J., Levine K., Meliker J.R. Mercury Exposure, Serum Antinuclear Antibodies, and Serum Cytokine Levels in the Long Island Study of Seafood Consumption: A Cross-Sectional Study in NY, USA. Environ. Res. 2017;156:334–340. doi: 10.1016/j.envres.2017.03.037. PubMed DOI

Nyholt K., Jardine T.D., Villamarín F., Jacobi C.M., Hawes J.E., Campos-Silva J.V., Srayko S., Magnusson W.E. High Rates of Mercury Biomagnification in Fish from Amazonian Floodplain-Lake Food Webs. Sci. Total Environ. 2022;833:155161. doi: 10.1016/j.scitotenv.2022.155161. PubMed DOI

Capo E., Broman E., Bonaglia S., Bravo A.G., Bertilsson S., Soerensen A.L., Pinhassi J., Lundin D., Buck M., Hall P.O.J., et al. Oxygen-Deficient Water Zones in the Baltic Sea Promote Uncharacterized Hg Methylating Microorganisms in Underlying Sediments. Limnol. Oceanogr. 2022;67:135–146. doi: 10.1002/lno.11981. DOI

Pinto E.P., Paredes E., Bellas J. Influence of Microplastics on the Toxicity of Chlorpyrifos and Mercury on the Marine Microalgae Rhodomonas lens. Sci. Total Environ. 2023;857:159605. doi: 10.1016/j.scitotenv.2022.159605. PubMed DOI

Winder M., Sommer U. Phytoplankton Response to a Changing Climate. Hydrobiologia. 2012;698:5–16. doi: 10.1007/s10750-012-1149-2. DOI

B-Béres V., Stenger-Kovács C., Buczkó K., Padisák J., Selmeczy G.B., Lengyel E., Tapolczai K. Ecosystem Services Provided by Freshwater and Marine Diatoms. Hydrobiologia. 2022;850:2707. doi: 10.1007/s10750-022-04984-9. DOI

Boening D.W. Ecological Effects, Transport, and Fate of Mercury: A General Review. Chemosphere. 2000;40:1335–1351. doi: 10.1016/S0045-6535(99)00283-0. PubMed DOI

Thera J.C., Kidd K.A., Stewart A.R., Bertolo R.F., O’Driscoll N.J. Using Tissue Cysteine to Predict the Trophic Transfer of Methylmercury and Selenium in Lake Food Webs. Environ. Pollut. 2022;311:119936. doi: 10.1016/j.envpol.2022.119936. PubMed DOI

Wiklund J.A., Kirk J.L., Muir D.C.G., Evans M., Yang F., Keating J., Parsons M.T. Anthropogenic Mercury Deposition in Flin Flon Manitoba and the Experimental Lakes Area Ontario (Canada): A Multi-Lake Sediment Core Reconstruction. Sci. Total Environ. 2017;586:685–695. doi: 10.1016/j.scitotenv.2017.02.046. PubMed DOI

Ullrich T.W.T., Abdrashitova S.A. Mercury in the Aquatic Environment: A Review of Factors Affecting Methylation. Crit. Rev. Environ. Sci. Technol. 2001;31:241–293. doi: 10.1080/20016491089226. DOI

Eklöf K., Bishop K., Bertilsson S., Björn E., Buck M., Skyllberg U., Osman O.A., Kronberg R.-M., Bravo A.G. Formation of Mercury Methylation Hotspots as a Consequence of Forestry Operations. Sci. Total Environ. 2018;613–614:1069–1078. doi: 10.1016/j.scitotenv.2017.09.151. PubMed DOI

Gworek B., Dmuchowski W., Baczewska-Dąbrowska A.H. Mercury in the Terrestrial Environment: A Review. Environ. Sci. Eur. 2020;32:128. doi: 10.1186/s12302-020-00401-x. DOI

Mahboob S., Al-Ghanim K.A., Al-Misned F., Shahid T., Sultana S., Sultan T., Hussain B., Ahmed Z. Impact of Water Pollution on Trophic Transfer of Fatty Acids in Fish, Microalgae, and Zoobenthos in the Food Web of a Freshwater Ecosystem. Biomolecules. 2019;9:231. doi: 10.3390/biom9060231. PubMed DOI PMC

Fuentes J.L., Huss V.A.R., Montero Z., Torronteras R., Cuaresma M., Garbayo I., Vílchez C. Phylogenetic Characterization and Morphological and Physiological Aspects of a Novel Acidotolerant and Halotolerant Microalga Coccomyxa onubensis sp. nov. (Chlorophyta, Trebouxiophyceae) J. Appl. Phycol. 2016;28:3269–3279. doi: 10.1007/s10811-016-0887-3. DOI

Silverman M.P., Lundgren D.G. Studies on the chemoautotrophic iron bacterium Ferrobacillus ferrooxidans. J. Bacteriol. 1959;77:642–647. doi: 10.1128/jb.77.5.642-647.1959. PubMed DOI PMC

Guillard R.R., Ryther J.H. Studies of Marine Planktonic Diatoms. I. Cyclotella Nana Hustedt, and Detonula Confervacea (Cleve) Gran. Can. J. Microbiol. 1962;8:229–239. doi: 10.1139/m62-029. PubMed DOI

Skrobonja A., Gojkovic Z., Soerensen A.L., Westlund P.-O., Funk C., Björn E. Uptake Kinetics of Methylmercury in a Freshwater Alga Exposed to Methylmercury Complexes with Environmentally Relevant Thiols. Environ. Sci. Technol. 2019;53:13757–13766. doi: 10.1021/acs.est.9b05164. PubMed DOI

Gojkovic Z., Vilchez C., Torronteras R., Vigara J., Gomez-Jacinto V., Janzer N., Gomez-Ariza J.-L., Marova I., Garbayo I. Effect of Selenate on Viability and Selenomethionine Accumulation of Chlorella sorokiniana Grown in Batch Culture. Sci. World J. 2014;2014:13. doi: 10.1155/2014/401265. PubMed DOI PMC

Doan T.T.Y., Sivaloganathan B., Obbard J.P. Screening of Marine Microalgae for Biodiesel Feedstock. Biomass Bioenergy. 2011;35:2534–2544. doi: 10.1016/j.biombioe.2011.02.021. DOI

Gojkovic Z., Lu Y., Ferro L., Toffolo A., Funk C. Modeling Biomass Production during Progressive Nitrogen Starvation by North Swedish Green Microalgae. Algal Res. 2020;47:101835. doi: 10.1016/j.algal.2020.101835. DOI

Moye H.A., Miles C.J., Phlips E.J., Sargent B., Merritt K.K. Kinetics and Uptake Mechanisms for Monomethylmercury between Freshwater Algae and Water. Environ. Sci. Technol. 2002;36:3550–3555. doi: 10.1021/es011421z. PubMed DOI

McCord J.M., Fridovich I. The Utility of Superoxide Dismutase in Studying Free Radical Reactions: I. Radicals generated by the interaction of sulfite, dimethyl sulfoxide, and oxygen. J. Biol. Chem. 1969;244:6056–6063. doi: 10.1016/S0021-9258(18)63505-7. PubMed DOI

Robles M., Torronteras R., Ostojic C., Oria C., Cuaresma M., Garbayo I., Navarro F., Vílchez C. Fe (III)-Mediated Antioxidant Response of the Acidotolerant Microalga Coccomyxa onubensis. Antioxidants. 2023;12:610. doi: 10.3390/antiox12030610. PubMed DOI PMC

Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein Measurement with the Folin Phenol Reagent. J. Biol. Chem. 1951;193:265–275. doi: 10.1016/S0021-9258(19)52451-6. PubMed DOI

Hammer Ø., Harper D., Ryan P. Past: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontol. Electron. 2001;4:1–9.

Gorski P.R., Armstrong D.E., Hurley J.P., Krabbenhoft D.P. Influence of Natural Dissolved Organic Carbon on the Bioavailability of Mercury to a Freshwater Alga. Environ. Pollut. 2008;154:116–123. doi: 10.1016/j.envpol.2007.12.004. PubMed DOI

Masojídek J., Torzillo G., Koblížek M. Photosynthesis in Microalgae. In: Richmond A., Hu Q., editors. Handbook of Microalgal Culture. John Wiley & Sons; Hoboken, NJ, USA: 2005.

Le Faucheur S., Campbell P.G.C., Fortin C., Slaveykova V.I. Interactions between Mercury and Phytoplankton: Speciation, Bioavailability, and Internal Handling. Environ. Toxicol. Chem. 2014;33:1211–1224. doi: 10.1002/etc.2424. PubMed DOI

Beauvais-Flück R., Slaveykova V.I., Cosio C. Transcriptomic and Physiological Responses of the Green Microalga Chlamydomonas reinhardtii during Short-Term Exposure to Subnanomolar Methylmercury Concentrations. Environ. Sci. Technol. 2016;50:7126–7134. doi: 10.1021/acs.est.6b00403. PubMed DOI

Lu C.M., Chau C.W., Zhang J.H. Acute Toxicity of Excess Mercury on the Photosynthetic Performance of Cyanobacterium, S. Platensis—Assessment by Chlorophyll Fluorescence Analysis. Chemosphere. 2000;41:191–196. doi: 10.1016/S0045-6535(99)00411-7. PubMed DOI

Wu Y., Wang W.-X. Accumulation, Subcellular Distribution and Toxicity of Inorganic Mercury and Methylmercury in Marine Phytoplankton. Environ. Pollut. 2011;159:3097–3105. doi: 10.1016/j.envpol.2011.04.012. PubMed DOI

Beauvais-Flück R., Slaveykova V.I., Cosio C. Molecular Effects of Inorganic and Methyl Mercury in Aquatic Primary Producers: Comparing Impact to A Macrophyte and A Green Microalga in Controlled Conditions. Geosciences. 2018;8:393. doi: 10.3390/geosciences8110393. DOI

Bravo A.G., Faucheur S.L., Monperrus M., Amouroux D., Slaveykova V.I. Species-Specific Isotope Tracers to Study the Accumulation and Biotransformation of Mixtures of Inorganic and Methyl Mercury by the Microalga Chlamydomonas reinhardtii. Environ. Pollut. 2014;192:212–215. doi: 10.1016/j.envpol.2014.05.013. PubMed DOI

Oren A. The Ecology of Dunaliella in High-Salt Environments. J. Biol. Res. 2014;21:23. doi: 10.1186/s40709-014-0023-y. PubMed DOI PMC

Barkay T., Gu B. Demethylation—The Other Side of the Mercury Methylation Coin: A Critical Review. ACS Environ. Au. 2022;2:77–97. doi: 10.1021/acsenvironau.1c00022. PubMed DOI PMC

Gojkovic Z., Skrobonja A., Funk C., Garbayo I., Vílchez C. The Role of Microalgae in the Biogeochemical Cycling of Methylmercury (MeHg) in Aquatic Environments. Phycology. 2022;2:344–362. doi: 10.3390/phycology2030019. DOI

Soerensen A.L., Schartup A.T., Skrobonja A., Björn E. Organic Matter Drives High Interannual Variability in Methylmercury Concentrations in a Subarctic Coastal Sea. Environ. Pollut. 2017;229:531–538. doi: 10.1016/j.envpol.2017.06.008. PubMed DOI

Quiroga-Flores R., Guédron S., Achá D. High Methylmercury Uptake by Green Algae in Lake Titicaca: Potential Implications for Remediation. Ecotoxicol. Environ. Saf. 2021;207:111256. doi: 10.1016/j.ecoenv.2020.111256. PubMed DOI

Simmons-Willis T.A., Koh A.S., Clarkson T.W., Ballatori N. Transport of a Neurotoxicant by Molecular Mimicry: The Methylmercury-L-Cysteine Complex Is a Substrate for Human L-Type Large Neutral Amino Acid Transporter (LAT) 1 and LAT2. Biochem. J. 2002;367:239–246. doi: 10.1042/bj20020841. PubMed DOI PMC

Li Y., Li D., Song B., Li Y. The Potential of Mercury Methylation and Demethylation by 15 Species of Marine Microalgae. Water Res. 2022;215:118266. doi: 10.1016/j.watres.2022.118266. PubMed DOI

Cossart T., Garcia-Calleja J., Santos J.P., Kalahroodi E.L., Worms I.A.M., Pedrero Z., Amouroux D., Slaveykova V.I. Role of Phytoplankton in Aquatic Mercury Speciation and Transformations. Environ. Chem. 2022;19:104–115. doi: 10.1071/EN22045. DOI

Borovkov A.B., Gudvilovich I.N., Memetshaeva O.A., Avsiyan A.L., Lelekov A.S., Novikova T.M. Morphological and morphometrical features in Dunaliella salina (Chlamydomonadales, Dunaliellaceae) during the two-phase cultivation mode. Ecol. Monten. 2019;22:157–165. doi: 10.37828/em.2019.22.12. DOI

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