Role of Settling Particles on Mercury Methylation in the Oxic Water

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Role of settling particles on mercury methylation in the oxic water column of freshwater systems Elena Gascon Diez, Jean-Luc Loizeau, Claudia Cosio, Sylvain Bouchet, Thierry Adatte, David Amouroux, and ANDREA G BRAVO Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.6b03260 • Publication Date (Web): 27 Sep 2016 Downloaded from http://pubs.acs.org on September 29, 2016

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Environmental Science & Technology

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Role of settling particles on mercury methylation in the oxic water

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column of freshwater systems

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Elena Gascón Díez1, Jean-Luc Loizeau1, Claudia Cosio1, Sylvain Bouchet2, Thierry

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Adatte3, David Amouroux2 and Andrea G. Bravo5,* 1

Department F.-A. Forel for environmental and water sciences, University of Geneva, Boulevard Carl-Vogt

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66, 1211 Geneva 4, Switzerland

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2

Laboratoire de Chimie Analytique Bio-Inorganique et Environnement, Institut des Sciences Analytiques et

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de Physico-Chimie pour l’Environnement et les Matériaux, UMR 5254 CNRS, Université de Pau et des Pays

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de l’Adour, Hélioparc, 64053 Pau, France

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Institute of Earth Sciences (ISTE), University of Lausanne, 1015 Lausanne, Switzerland

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Limnology Department, Evolutionary Biology Centre, EBC, Norbyvägen 18D, 75236 Uppsala Sweden

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*[email protected]

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Abstract

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As the methylation of inorganic mercury to neurotoxic methylmercury has been attributed to the

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activity of anaerobic bacteria, the formation of methylmercury in the oxic water column of marine

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ecosystems has puzzled scientists over the past years. Here we show for the first time that

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methylmercury can be produced in particles sinking through oxygenated water column of lakes.

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Total mercury and methylmercury concentrations were measured in settling particles and in surface

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sediments of the largest freshwater lake in Western Europe (Lake Geneva). Whilst total mercury

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concentration differences between sediments and settling particles were not significant,

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methylmercury concentrations were up to ten-fold greater in settling particles. Methylmercury

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demethylation rate constants (kd) were of similar magnitude in both compartments. In contrast,

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mercury methylation rate constants (km) were one order of magnitude greater in settling particles.

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The net potential for methylmercury formation, assessed by the ratio between the two rate

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constants (km kd-1), was therefore up to ten times higher in settling particles, denoting that in-situ

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transformations likely contributed to the high methylmercury concentration found in settling

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particles. Mercury methylation was inhibited (~80 %) in settling particles amended with molybdate,

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demonstrating the prominent role of biological sulfate-reduction in the process.

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Keywords: methylmecury, mercury methylation, oxic water column, sediments, settling particles.

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1. Introduction

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Anthropogenic activities such as artisanal gold mining, waste disposal, metal and cement

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industries, and the burning of fossil-fuel fired power plants have greatly increased mercury (Hg)

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dispersion and concentration in aquatic systems worldwide1. Understanding the biological

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formation of the neurotoxic methylmercury (MeHg) in aquatic ecosystems is critical because MeHg

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is bio-accumulated and biomagnified in food webs, eventually affecting wildlife and human health2.

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It has been reported that methylation of inorganic-Hg (IHg) into MeHg mainly occurs at oxygen

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deficient water columns3 and/or sediments4-6 and is carried out by specific strains of a large set of

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potential methylators such as sulfate-reducing bacteria (SRB), iron-reducing bacteria (FeRB), and

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methanogens7, 8. As Hg-methylation is mainly carried out by anaerobic microorganisms, it has been

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assumed for a long time that compared to sediments MeHg formation in oxic environments, such

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as water columns, was negligible due to the presence of oxygen and the lower concentrations of

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bacteria and nutrients5, 9. Consequently Hg-methylation in pelagic freshwater systems remains

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largely less explored than in sediments. In marine environments however, Hg-methylation was

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recently reported to occur in the sub-oxic10, 11 and even in the oxic layer of the water column12-16.

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MeHg was hypothesized to be formed by microbes associated with sinking particulate organic

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matter (OM)12-18, but it remains unclear whether these organisms are aerobic or anaerobic. Indeed,

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the genes responsible for Hg-methylation (hgcAB) were rarely found in oxygenated layers of the

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open ocean19, suggesting that an unidentified metabolic pathway could be responsible for MeHg

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production in this environment. In fresh water ecosystems, MeHg formation has been extensively

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investigated in sediments6, 20-24 and biofilms25-30 but rarely in the hypolimnetic waters3, 31. MeHg

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formed in hypolimnetic waters compartment may actually represent a significant source of MeHg to

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the food chain when the volume of such water is larger than the volume of surface sediments3.

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Recent studies suggest that atmospheric Hg can be methylated32 and even accumulated in food

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chains33 within 24 hours after its deposition. Assuming that recently deposited Hg should

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theoretically reach anoxic waters or sediments to be methylated, there is still no experimental


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explanation for such rapid MeHg formation in aquatic ecosystems. Indeed, the fastest in-situ MeHg

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production, assessed by the addition of Hg-spikes on a lake ecosystem, was detected in anoxic

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bottom waters only after 72 hours34. We have thus hypothesized that rapid methylation32 of recently

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deposited Hg could only be explained if Hg methylation processes occur in the water column, in

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particular in settling particulate OM, even under oxic prevailing conditions. This can be of major

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concern in deep lakes and oceans where MeHg generated in the water column may be rapidly

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available to enter the aquatic food web because it does not need to diffuse out from the sediments3,

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inputs of IHg36, this study aims to provide an improved understanding of the drivers and sources

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controlling MeHg levels in aquatic systems.

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Here we measured Total-Hg (THg) and MeHg concentrations in settling particles and sediments of

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the largest freshwater lake in Western Europe (Lake Geneva) for two years and performed

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experimental studies to determine the rates, mechanisms, and factors controlling the MeHg

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concentrations found in its oxic water column. This study shows for the first time that IHg can be

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methylated in settling particles of oxic lake waters and suggest that SRB or organisms related to

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them such as syntrophs37 are involved in the process.

. As different concentrations of MeHg have been reported in water column of lakes with identical

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2. Materials and Methods

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Study site and sampling strategy

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Lake Geneva has an area of 580.1 km2, a maximum depth of 309 m and a volume of 89 km3. It is a

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oxic monomictic lake with infrequent complete turnover38. From December 2009 to September

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2011, sediments and settling particles were collected in Lake Geneva on a monthly basis at the

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sampling site NG2 (6º 35’ 0’’ E, 46º 30’ 6’’ N; Swiss coordinates (m): 534350 E, 150400 N). This

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site has been previously described by Graham

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supporting information (Figure S1). Briefly, NG2 is located at 138 m depth and 1100 m from an

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outlet pipe discharging in Vidy Bay both treated and untreated sewage water of a wastewater

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treatment plant (WWTP) located near the city of Lausanne20, 40-43.

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To collect the settling particles, we used a sediment trap system formed by a weight, an acoustic

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release, a sediment trap frame composed of six 80-cm-long Plexiglas tubes of 11 cm internal

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and detailed maps are presented in the



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diameter placed 5 m above the sediment (actual sampling depth: 132 m), and maintained by

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buoys44 (Figure S1). Sediments underneath the traps were recovered at the date of the sediment

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traps exchange, using two Mortimer gravity corers attached together from which the first centimeter

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was subsequently subsampled39. Furthermore, surface sediments (~ 1 cm depth) were collected

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during the summer 2010 using a Van Veen grab sampler at 15 additional sites (numbered EG1 -

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EG15) along a transect extending from Vidy Bay towards the main deep basin (Figure S2). An

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aliquot of the WWTP sewage sludge was also sampled for subsequent Hg analyses.

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Hg-methylation and demethylation rate constants in sediments and settling particles

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Sediment traps were placed back at NG2, on May 15th and were changed on June 10th, July 14th,

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and finally removed on August 14th, 2014. Hg-methylation rates were determined in the upper 1st

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cm of sediments, where the highest MeHg concentrations were previously observed43, and in

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settling particles. At 132 m depth in Lake Geneva, dissolved oxygen was ≥ 7 mgl-1, temperature

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5.5°C, conductivity ~ 300 µScm-1 and pH ~ 8 (Figure S3)45. A volume of 32 ml of sediments was

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collected from the top of a sediment core and was dispensed into a 40 ml vial (head-space glass

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vials with PTFE caps) and were amended with 55 µl of 10 mgl-1 of

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of

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overlying water were placed into a 40 ml vial, amended and shaken. To better constrain the role of

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anaerobic sulfate-reduction on the Hg-methylation, we also amended sediments and settling

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particles with molybdate (Na2MoO4; 2.4 mM final concentration), a specific inhibitor of the sulfate

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reducing metabolism24. Immediately after the Hg tracers’ amendment (t0), one sub-sample was

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centrifuged at 3500 rpm for 25 minutes to extract the pore water, and the supernatant water was

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filtered with 0.45 µm Sterivex syringe filters and stored in 15 ml PP flasks at -20ºC for subsequent

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anion measurements. Three remaining sediment sub-samples were frozen and freeze-dried. Thus,

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three control-replicate (no MoO42- addition) and three molybdate-replicate (with MoO42-) slurries

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were incubated close to lake temperature (4°C) in the dark. After 48h (tf), we collected the pore

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water as described for t0 and we used the remaining sediment for further determination of potential

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Hg-methylation. All sample manipulations were done under a N2-atmosphere.

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HgCl2 and 80 µl of 0.4 mgl-1

MeHgCl and shaken, creating a sort of slurry. Similarly, 32 ml of settling particles with their

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Laboratory Analyses

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THg and MeHg concentrations in sediments and settling particles

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For samples collected from 2009 to 2011, THg was analyzed by atomic absorption spectrometry

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following the procedure described by Szakova, et al. 46 using an automatic mercury analyzer (AMA-

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254). The absolute detection limit was 10 pg and the concentrations obtained for repeated

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analyses of certified reference material (CRM) never exceeded the range of concentration given for

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MESS-3 (National Research Council Canada). MeHg was extracted from sediments using HNO3

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leaching/CH2Cl2 and measured with a Cold Vapor Atomic Fluorescence Spectrophotometer47-49.

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The detection limit was 5 pg and the recovery of repeated extraction and analyses of the used

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CRM (ERM-CC580) were always above 85%. Incubations and analyses for the determination of Hg

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transformations were carried out according to Rodriguez-Gonzalez et al50. Briefly, IHg and MeHg

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were extracted from 200 mg of dry sediments or settling particles with HNO3 (6N) under focused

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microwave treatment and analyzed by species-specific isotope dilution, gas chromatography (GC)

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hyphenated to an inductively coupled plasma mass spectrometer (ICP-MS). Methodological

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detection limits for Hg species were 0.03 ng.g-1. The extraction and quantification were validated

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with a CRM (IAEA-405) and recoveries were 102 ± 7 and 97 ± 4 % for MeHg and IHg, respectively.

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The concentrations of the added and formed Hg species deriving from the enriched isotopes 199

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and 201 were calculated by isotopic pattern deconvolution methodology.

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Sulfate-reduction rates

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Sulfate (SO42-) consumption was measured in pore water of sediments and settling particles

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collected in sediment traps. To extract pore water, sediment core and trap samples were

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centrifuged (3500 rpm 25 min). Overlying water after centrifugation was filtered with 0.45 µm

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Sterivex syringe filters under a N2-atmosphere. Differences on SO42- concentrations between t0 and

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tf were used to calculate sulfate-reduction rates (SRR) in control and MoO42--amended samples.

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SO42- values were normalized with the chloride (Cl-) concentration that is constant during the

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incubation period. SO42- and Cl- concentrations were measured by ionic chromatography (IC)

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Dionex, AS19 IonPac column. Analyses were carried on duplicates and the accuracy was tested

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with the CRM ONTARIO-99 (Environment Canada).



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Total organic carbon, mineral carbon, Hydrogen Index and Oxygen Index

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Total Organic Carbon (TOC), hydrogen Index (HI) and Oxygen Index (OI) were determined by

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Rock-Eval® pyrolysis method Model 6 device (Vinci Technologies) following the procedure

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published by Espitalie, et al.

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in 4 main peaks: S1 peak («free» hydrocarbons released during the isothermal phase); S2 peak

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(hydrocarbons produced between 300 and 650°C); S3 peak (CO2 from pyrolysis of OM up to

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400°C); and S4 peak (CO2 released from residual OM below ca. 550°C during the oxidation step).

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Mineral carbon decomposition is recorded by the S3’ peak (pyrolysis-CO2 released above 400°C),

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and S5 peak (oxidation-CO2 released above 550°C). These peaks are used to calculate the amount

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of TOC and the amount of mineral carbon. In addition, the so-called hydrogen index (HI = S2/TOC)

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and oxygen index (OI = S3/TOC) are calculated. The HI and OI indexes are proportional to the H/C

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and O/C ratios of the organic matter, respectively, and can be used for OM classification in Van-

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Krevelen-like diagrams51, 52. HI is expressed in mg HC g–1 TOC, and OI in mg CO2 g–1 TOC. The

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CRM used was IFP 160000 Rock-Eval and the analyses were carried out on 50 - 100 mg of

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powdered dry sediment under standard conditions. Analytical precision was better than 0.05 wt.%

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(1σ) for TOC, 10 mg HC g–1 TOC (1σ) for HI, and 10 mg CO2 g–1 TOC (1σ) for OI.

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. During Rockeval® analyses, organic carbon decomposition resulted

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Total nitrogen analysis

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Total nitrogen content (% N) was analyzed in a CHN Elemental Analyzer (Carlo Erba Flash EA

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1112 CHNS/MAS200) using approximately 10 mg of dry powdered sediment. The carbon/nitrogen

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(C/N) ratio was calculated as the weight ratio of the TOC measured by the Rock-Eval pyrolysis (see

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above) and the N content analyzed by CHN Elemental Analyzer. Precision was better than 1%

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based on internal standard and replicate samples.

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Mineral composition diffraction analyses

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Bulk mineralogical composition was performed using a X-TRA Thermo-ARL Diffractometer,

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following the procedures described in Klug and Alexander

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semi-quantitative analysis of the bulk rock mineralogy (obtained by XRD patterns of random powder

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and Adatte, et al.


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. This method for

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samples) uses external standards with error margins varying between 5 and 10% for the

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phyllosilicates and 5% for grain minerals.

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Statistical analyses

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Normality was tested using the Shapiro-Wilk test. Annual THg concentration datasets followed a

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normal distribution in sediments and settling particles. However, MeHg and %MeHg/THg datasets

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followed a non-normal distribution; therefore the Mann-Whitney rank test was used to assess

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differences in median values between the two groups (sediments and settling particles). Similarly,

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correlations between C/N and %MeHg/THg were tested with Spearman rank order correlations.

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Finally, as Hg-methylation rates were normally distributed, one-way ANOVA tests were performed

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to compare the results of the three different incubation conditions versus the control group (Holm-

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Sidak method). Overall the significance level was set to 0.05. All the statistical analyses were

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performed with SigmaPlot 11.0 software.

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3. Results and Discussion

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3.1. Temporal trends of THg and MeHg concentrations in sediments and settling particles

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THg concentrations at NG2 ranged between 174 ± 4 and 270 ± 58 ngg-1 in sediments and from

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73.4 ± 0.4 to 257 ± 9 ngg-1 in settling particles (Figure 1). Differences in THg concentrations

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between sediments and settling particles were not statistically significant (p > 0.05). In contrast,

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MeHg concentrations were significantly higher (p < 0.05) in settling particles (from 0.62 ± 0.04 to

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11.38 ± 0.02 ngg-1) than in sediments (from 0.31 ± 0.03 to 1.67 ± 0.02 ngg-1). A significant

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seasonal pattern (p < 0.001) was, however, observed for THg concentrations in settling particles

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with the lowest values (< 100 ngg-1) registered during late summer-early fall compared to the

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winter period showing higher concentrations. MeHg concentrations were more variable throughout

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the sampling period and, contrary to THg, did not show any seasonal pattern. This contrasts with

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other studies where a high seasonal variability was reported, for example in estuarine suspended

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particles55. Likewise, the proportion of MeHg to THg (%MeHg/THg), also used as a proxy of net

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MeHg production19, was significantly higher in settling particles (0.4 % - 9.6 %) than in sediments

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(0.2 % to 0.8 %).



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Considering a concentration of suspended particles of 00.4 gm-3 (lake volume-weighted arithmetic

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mean) in Lake Geneva56, the estimated mass of particles in the whole lake is approximately 35,600

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tons. With a concentration of 3.6 ngg-1 of MeHg measured in the present study, the total amount of

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MeHg in the suspended particles in the whole water column is estimated to be around 130 g. This

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accounts for roughly 10 % of the total amount of MeHg contained in the 1st cm of the sediments. It

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thus represents a significant pool of MeHg in this ecosystem and should be considered in further

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studies to better predict and constrain all sources of MeHg to food webs in aquatic systems.

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3.2. THg and MeHg sources for Lake Geneva

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Previous studies demonstrated that the sewage water discharges alter sediment characteristics43

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and are the main source of pollutants for Vidy Bay57,58. Catchment inputs of THg to Vidy Bay are

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low compared to the releases of the WWTP43, 57, 58. In contrast, we have previously demonstrated

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that MeHg concentrations found in sediment mostly originates from in-situ production in

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sediments58 and that the higher Hg methylation rate constants were found closer to the pipe20. In

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this study, MeHg concentrations measured in fifteen surface sediment samples along a transect

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from the shore to the deeper part of Vidy Bay (Figure S2), show a clear decrease with distance

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from the WWTP. In particular, at site EG4 (Figure S2), 530 m away from the outlet pipe, the

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concentration of MeHg was approximately 30-fold lower than the most contaminated site (EG3)

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suggesting that at NG2, which was located at 1100 m from the outlet pipe, there was no effect of

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the catchment area and/or the WWTP inputs. Furthermore, the MeHg concentration measured in

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the WWTP sludge before its release was 1.6 ± 0.2 ngg-1, lower than the MeHg concentrations

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most often encountered in settling particles (Figure 1). Altogether, it suggests that the MeHg found

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in settling particles cannot be explained either by catchment inputs, or by the WWTP releases.

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3.3. Hg species transformation rates in sediments and settling particles

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The methylation rate constants (km) in sediments ranged from 1.0 x 10-3 to 6.8 x 10-3 day-1 from

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mid-May to mid-August, without following any particular trend (Figure 2). In contrast, km were about

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one order of magnitude higher (p < 0.05), in settling particles than in sediments and they also

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showed an increasing trend over the summer period, from 1.6 x 10-2 to 6.5 x 10-2 day-1 (Figure 2).


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These km values were similar to those measured in the anoxic hypolimnetic water of some

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Canadian lakes where km ranged between 4.1 x 10-3 and 1.5 x 10-2 day-1 3. On the other hand,

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MeHg demethylation rate constants (kd) in sediments and settling particles were on the same order

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of magnitude (Figure 2). No seasonal trend could be seen in the particles where kd ranged from

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0.086 to 0.219 day-1 while in sediments kd increased from 0.064 in spring to 0.330 day-1 for late

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summer. As a result, the km kd-1 ratios were 10-fold higher in settling particles than in sediments

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from June to August. Even if the bioavailability of added Hg tracers might differ from the natural Hg

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species, the km kd-1 ratios can be compared to the % MeHg/THg among sites and/or samples from

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the same site59. Our results thus clearly shows a higher potential for net MeHg production in the

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settling particles compared to surface sediments, confirming our previous hypotheses based solely

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on MeHg concentrations and higher proportions of MeHg to THg.

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The semi-confined conditions and a higher concentration of particles in the sediment traps,

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approximately two orders of magnitude, may have enhanced Hg methylation rates compared to the

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open water column. However, redox and O2 measurements in the sediment traps are very similar

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to in-situ conditions (Figure S3). In addition, there was indirect evidence that conditions remained

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oxic during the incubations. For example, the color of the incubated samples indicated that Fe was

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mainly found as Fe-oxyhydroxides and not as a ferrous-sulfide minerals suggesting a limited

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accumulation of H2S, Furthermore, the percentage of 199MeHg formed from the added 199IHg was in

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the same range as the ambient MeHg to IHg ratio found in the traps collected during the period

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2009-2011 (3.0 - 12.7 % vs 0.4 - 9.6 %, respectively). This similarity also confirmed the relevance

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of the incubations compared to in-situ conditions.

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Our results thus show that methylation of IHg occurs in the water column of Lake Geneva during

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the time span that particles take to settle out of the water column, which is around one month39, 56.

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Contrary to other lakes where Hg-methylation has been observed in the oxygen depleted water

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column, Lake Geneva, at 132 m depth, is oxic with ̴ 7 mgl-1 of O2 (Figure S3), implying that both

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settling particles and surface sediments remain in an oxic environment throughout the year. Our

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results, along with those obtained from filtered/unfiltered water, cited above3,

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settling particles are a potentially important compartment for MeHg production.

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indicate that


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3.4. Bacterial anaerobic metabolism contributes to Hg methylation in oxic water column

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Despite the fact that there are many organisms with the capacity to methylate Hg3,4,17, SRB have

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been specifically identified as important Hg-methylators in aquatic systems33,35. In this study,

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molybdate amendments led to an inhibition of around 80% of the Hg-methylation rates in

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sediments and between 60% and 90% in settling particles (Figure 3). The role of sulfate reduction

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on Hg methylation in settling particles is further supported by (i) the positive correlation between

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Hg-methylation rates and sulfate consumption and (ii) the concomitant inhibition of sulfate

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consumption and Hg-methylation. This study demonstrated the occurrence of biological Hg-

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methylation in settling particles of Lake Geneva and our results points to an important role of

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sulfate-reducers in the process; however, iron-reducing bacteria involvement is not excluded, as it

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was suggested previously in the sediments of Lake Geneva20. The use of direct probing of the

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recently discovered hgcA and hgcB gene cluster7 will be tremendously helpful in further studies to

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characterize the microbial Hg methylating community in settling particles and sediments. As

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biogeochemical conditions during incubations (O2 concentrations, temperature and bacterial

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anaerobic metabolism) were similar for both sediments and settling particles, we rather ascribed

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differences in MeHg production between the two compartments to OM quality driving both Hg

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availability and bacterial activity.

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3.5. Organic matter quality favors Hg-methylation in particles compared to sediments

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As the sampling station was far from the shore ( ̴ 2 km) and distant to major river inputs, OM in

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settling particles originates largely from phytoplankton. This is first confirmed by the abundance of

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diatoms and thecamoeba in the sediment traps (Figure S4). The mineralogy of settling particles

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and sediments are qualitatively and quantitatively very similar, except for calcite, which is more

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abundant in settling particles than in sediments, especially from July to September (Figure S5 and

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Figure S6). This increase in calcite in settling particles could be caused either by an enhanced

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precipitation due to the higher temperatures typically occurring in summer, either by an increase of

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biological productivity

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(R2: -0.85) and ii) quartz (R2: -0.82), both from detrital origin, confirms biological in-situ production

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of calcite (Table S1). Moreover C/N ratios and HI and OI indexes, which are indicators of sources

60, 61

. The negative correlation between calcite and i) phyllosilicates


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and degrees of biological and diagenetic alteration62, were measured in samples collected from

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December 2009 to September 2011 (Figure 4). The C/N ratios were higher in 2010 than 2011 in

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both compartments but overall always higher in sediments than in settling particles, meaning that

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OM in bulk sediment was either more degraded or more terrestrial than in settling particles. These

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results are further supported by the HI and OI indexes that can also differentiate the OM of algal

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origin from the more degraded or terrestrial OM63-65. Hi and OI indexes clearly discriminated OM

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composition between the settling particles and the sediments collected from 2009 to 2011 (Figure

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4) but also in the slurries made in 2014 (Figure S7). In the latter, OM in settling particles was more

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of algal origin and showed a less-reworked and degraded status than the sedimentary OM.

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Combined analyses of mineral and OM composition support that OM in settling particles was

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enriched in algal derived OM and less degraded than in sediments. This energy rich OM can serve

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as an electron-donor to provide energy and carbon to the Hg methylators and consequently

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enhance MeHg production in settling particles21. A MeHg enrichment in algae of settling particles

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compared to sediments could also contribute to MeHg concentrations in settling particles,

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especially over the summer.

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Several studies showed that Hg uptake by bacteria or phytoplankton microorganisms can be

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affected by low molecular weight thiols complexing Hg, and/or the degradation state and origin of

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the OM that binds Hg66, 67. In pelagic sea waters, the sinking particulate OM has already been

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suggested as the main compartment for Hg-methylation12. In this study we reveal that Hg

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methylation can also occur in oxic water columns of freshwater ecosystems likely due to the

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presence of fresh labile OM and micro anoxic environments in settling particles, as it was

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previously reported in pelagic sea waters14. Besides the type of OM determining the quality of the

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electron donors for Hg methylating bacteria, the redox potential within these micro anoxic

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environments and the formation of dissolved or nanoparticulate mercuric sulfides in these micro-

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environments likely effect Hg methylation processes in both settling particles and surface

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sediments68.

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3.6. Environmental Perspectives

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Settling particles in our study consisted of allochthonous material (quartz grains and clay particles)



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but also of autochthonous components such as diatom frustules, aggregates of organic mucilage

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(fecal pellet) and organo-mineral flocs (Figure S4). Abrupt changes of the inner physico-chemical

324

conditions, e.g. dissolved oxygen gradients at micrometer scale, have been observed in the sinking

325

organic particles of marine oxic water column69-71. Particle association creates a spot in the oxic

326

water column where suboxic or anoxic processes can occur due to the formation of microscale

327

oxyclines72, 73. The sulfate-reducing potential by anaerobic microbes in the reducing microzone of

328

such particles has been demonstrated in marine detrital aggregates74, and are supposed to be

329

strongly activated by the sharp oxygen gradient occurring in such particles. We suggest that such

330

suboxic/anaerobic microzones also develop in the lake settling particles and that they are ideal for

331

Hg methylation.

332

Despite our improved understanding of the microbial Hg-methylation, we have only a vague idea of

333

the MeHg sources for aquatic food web and factors that control the efficiency of that methylation.

334

This study demonstrates conclusively that Hg can be methylated within the lake oxic water column

335

to form MeHg to a greater extent than MeHg formed in the sediment, and we suggest that this

336

contribution has so far been underestimated. While our results provide evidence to conclude that

337

higher concentrations of MeHg in settling particles are caused by enhanced in-situ MeHg

338

production and by MeHg enrichment in algae, further studies are needed to accurately quantify the

339

total amount of MeHg that can be produced in settling particles of oxic water columns. The

340

identification of sources of MeHg has nevertheless far-reaching implications for central scientific

341

questions in Hg biogeochemistry and should be considered in future biogeochemical Hg cycling

342

models at regional and global scales. In fact, settling particles formed partially by planktonic

343

detritus might be an important source of MeHg for uptake into the food web20. As there are 27

344

million water bodies larger than 0.01 km2 excluding Caspian Sea and around 2000 larger than 100

345

km2 (i.e. Tanganyika, Victoria, Titicaca, Lake Baikal, the American Great Lakes and large Chinese

346

or Brazilian reservoirs)75 the formation of MeHg in the water column of freshwater systems might

347

be thus a global issue.

348 349

Acknowledgments

350

The authors thank Philippe Arpagaus and Neil Graham for their valuable help with sediment and


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settling particles sampling. Jean-Michel Jaquet for the analyses of electronic microscope. The work

352

was partly funded by Swiss National Foundation (project PDFMP2-123034) and Swedish Research

353

Council (project 2011-7192 grant to AGB). We thank Charles Verpoorter for providing the number

354

of water bodies (and their area) across the globe. We also thank Dolly Kothawala and Prof. Andrew

355

Barry for English editing and manuscript improvement.

356

Supporting Information

357

Additional 7 figures (Figures S1-S7, Table S1). This material is available free of charge via the

358

Internet at http://pubs.acs.org.

359

Map of Sampling site; MeHg concentrations in sediments of the Vidy Bay area; Dissolved oxygen

360

temperature and redox profiles in water column; OM microscopy; Mineralogical composition; HI vs

361

Ol; Correlation matrix between the different mineralogical components

362

4. References

363 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383 384 385 386 387 388 389 390 391

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Graphical abstract

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Figure 1. Concentrations of total mercury (THg), methylmercury (MeHg) and MeHg as THg percentage (%MeHg/THg) in settling particles (dash line) and sediments (solid line) in Lake Geneva from December 2009 to September 2011.

582 583 584 585



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Figure 2. A: Hg methylation (km), B: MeHg demethylation (kd) rate constants (day-1) and C: net MeHg formation (km kd-1ratio) of settling particles (light blue) and surface sediments (dark brown) from mid-May to mid-August 2014.

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Figure 3. A: percentage of methylation inhibited in settling particles and sediment samples amended with molybdate. B: Sulfate (SO42-) consumption in relation with km of settling particles in control settling particles (squares) and in molybdate amended settling particles (triangles).

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596 597 598



599 600 601

Figure 4. A: C/N ratio measured in settling particles (dash line) and sediments (solid line). B: Hydrogen index (HI) versus oxygen index (Ol) in all samples taken at NG2 from December 2009 to September 2011. Blue and brown symbols represent settling particles and sediments respectively.

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Role of Settling Particles on Mercury Methylation in the Oxic Water

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