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Formation, Uptake and Bioaccumulation of Methylmercury in Coastal Seas – a Baltic Sea Case Study

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Formation, Uptake and Bioaccumulation of Methylmercury in Coastal Seas – a Baltic Sea Case Study Formation, uptake and bioaccumulation of methylmercury in coastal seas – a Baltic Sea case study Aleksandra Skrobonja Department of Chemistry Umeå 2019 This work is protected by the Swedish Copyright Legislation (Act 1960:729) Dissertation for PhD ISBN: 978-91-7855-177-4 Cover: Sampling cruise, incubation, and mesocosm experiment by Aleksandra Skrobonja Electronic version available at http://umu.diva-portal.org/ Printed by: The service centre in KBC, Umeå University, Sweden 2019 Mojim najdražima. Hvala što verujete u mene. Table of Contents Abstract............................................................................................................................... ii List of publications ......................................................................................................... iii Enkel sammanfattning på svenska ...................................................................................... v 1. Introduction ................................................................................................................ 1 1.1. Mercury as a pollutant ............................................................................................. 1 1.2. Formation of MeHg .................................................................................................. 2 1.3. Uptake of MeHg ....................................................................................................... 3 1.4. Bioaccumulation of MeHg ....................................................................................... 4 1.5. Aims of the thesis..................................................................................................... 6 2. Materials and Methods............................................................................................... 7 2.1. Study sites ................................................................................................................ 7 2.2. Experimental approaches ........................................................................................ 8 2.2.1. Field sampling ................................................................................................... 8 2.2.2. Determination of total Hg and MeHg in aqueous samples and biota .............. 8 2.2.3. Methylation and demethylation rate constants ............................................... 9 2.2.4. DOC, humic matter content and ancillary data .............................................. 10 2.2.5. Microalgal cultivation ..................................................................................... 10 2.2.6. Mesocosm experiment ................................................................................... 11 3. Results and discussion .............................................................................................. 14 3.1. Organic matter input impacts MeHg formation and cycling (Paper I) ................... 15 3.2. The role of water column redoxclines on MeHg formation and cycling (Paper II) 18 3.3. Uptake kinetics of MeHg in a freshwater alga exposed to MeHg-thiol complexes (Paper III) ...................................................................................................................... 21 3.4. Multiple impacts of humic-rich dissolved organic carbon on methylmercury accumulation in heterotrophic pelagic food webs (Paper IV) ...................................... 27 3.5. Future research remarks ........................................................................................ 33 4. Conclusions ............................................................................................................... 35 5. Acknowledgements .................................................................................................. 37 6. Literature .................................................................................................................. 39 i Abstract Methylmercury (MeHg) is a potent neurotoxin which can bioaccumulate to harmful levels in aquatic food webs. Methylmercury formation is a predominantly biotic process which involves phylogenically diverse microorganisms (e.g. iron- or sulfate-reducing bacteria). The formation of MeHg is related to the presence of organic matter (OM) which contains substrates essential for methylating microbes and reduced sulfur ligands (thiols, RSH) that form strong bonds with inorganic mercury (HgII) and affect its bioavailability. In aquatic systems, MeHg is bio-concentrated from the water column to the base of the food web and this step is crucial for MeHg levels found at higher trophic levels. Trophic transfer processes of MeHg in the food web are also of great importance. Discharge of OM in coastal areas affects light conditions needed for phytoplankton growth, and promotes heterotrophy, i.e. bacteria production. This may lead to a shift from the phytoplankton- based to the longer bacteria-based (microbial loop) food web and influence the amount of bioaccumulated MeHg in higher trophic levels. Methylmercury levels in predatory biota is thus affected by the bioavailability of HgII for methylation (studied in Paper I & II), MeHg speciation in the water column, crucial for MeHg incorporation at the base of the food web (Paper III), and the structure of the pelagic food web (Paper IV). In this thesis, it is shown that OM can act as a predictor of dissolved MeHg levels in estuarine and coastal systems. It impacts MeHg levels both by affecting HgII bioavailability (through Hg complexation with humic matter) and the activity of methylating microbes (providing metabolic electron donors) (Paper I). Moreover, elevated concentrations of particulate and dissolved HgII and MeHg, are associated with the presence of pelagic redoxclines in coastal seas. The redoxcline affects HgII speciation in the water column and its bioavailability for methylation (Paper II). It is further shown that the molecular structure of ligands in MeHg complexes affects the kinetics of MeHg uptake in phytoplankton. Rate constants for association of MeHg to the cell surface of a green algae were higher in treatments containing smaller thiol ligands of simpler structure than in treatments with larger thiols and more “branched” structure (Paper III). Finally, it is demonstrated that MeHg bioaccumulation in zooplankton can increase in systems with highly heterotrophic food webs and enhanced loadings of terrestrial OM (Paper IV). Such conditions are expected to occur in northern latitude coastal systems following climate changes. Key words: Mercury, methylmercury, bioaccumulation, mesososm, isotope tracers, methylation, demethylation, stability constant, kinetic model, coastal sea, ICPMS, LC-MS/MS ii List of publications Publications included in this thesis I. Organic matter drives high interannual variability in methylmercury concentrations in a subarctic coastal sea Anne L. Soerensen, Amina T. Schartup, Aleksandra Skrobonja and Erik Björn Environmental Pollution, 2017, 229, 531-538 II. Deciphering the Role of Water Column Redoxclines on Methylmercury Cycling Using Speciation Modeling and Observations from the Baltic Sea Anne L. Soerensen, Amina T. Schartup, Aleksandra Skrobonja, Sylvain Bouchet, David Amoroux, Van Liem-Nguyen and Erik Björn Global Biogeochemical Cycles, 2018, 32, 1498-1513 III. Uptake kinetics of methylmercury in a freshwater alga exposed to methylmercury complexes with environmentally relevant thiols Aleksandra Skrobonja, Zivan Gojkovic, Anne L. Soerensen, Per-Olof Westlund, Christiane Funk and Erik Björn Environmental Science & Technology, 2019, 53, 13757-13766 IV. Multiple impacts of humic-rich dissolved organic carbon on methylmercury accumulation in heterotrophic pelagic food webs Aleksandra Skrobonja, Sonia Brugel, Anne L. Soerensen, Evelina Griniene, Agneta Andersson and Erik Björn Manuscript in preparation Paper I was reprinted with permission from Environmental Pollution. Copyright © 2017, Elsavier Ltd. All rights reserved. Paper II was reprinted with permission from Global Biogeochemical Cycles. Copyright © 2018, American Geophysical Union. All rights reserved. Paper III was reprinted with permission from Environmental Science & Technology. Copyright © 2019, American Chemical Society. All rights reserved. iii Author contribution: Paper I. The author participated in the planning and execution of one of the field campaigns used in the study, performed the experimental analysis from samples collected during several field campaigns and commented on the manuscript. Paper II. The author participated in the planning and execution of one of the field campaigns used in the study, conducted most of the experimental work, participated in the data evaluation and commented on the manuscript. Paper III. The author formulated the scientific research objectives and led the planning of the study, performed most of the experiments and data processing and was lead author on the manuscript. Paper IV. The author was involved in formulating the scientific research objectives and approaches, led the planning of the study, performed the experiments related to the behavior of mercury in the system, processed the data and contributed significantly to the writing of the manuscript. iv Enkel sammanfattning på svenska Metylkvicksilver (MeHg) är ett potent neurotoxin som kan bioackumuleras till skadliga nivåer i akvatiska näringsvävar. Bildning av metylkvicksilver är en övervägande biotisk process som involverar olika mikroorganismer (t.ex. järn- eller sulfatreducerande bakterier). Bildningen av MeHg är relaterad till förekomst
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