Biogeochemical Aspects of Mercury Methylation in the Ice of the Amur River R.A

Kriosfera Zemli, 2017, vol. XXI, No. 2, pp. 21–27 http://www.izdatgeo.ru

DOI: 10.21782/EC2541-9994-2017-1(21-27) BIOGEOCHEMICAL ASPECTS OF MERCURY METHYLATION IN THE ICE OF THE AMUR RIVER R.A. Kiper1, L.M. Kondratyeva1, E.M. Golubeva2 1Institute of Water and Ecological Problems, FEB RAS, 56, Dikopolceva str., Khabarovsk, 680000, Russia; [email protected] 2 Institute of Tectonics and Geophysics, FEB RAS, 65, Kim-Yu-Chen str., Khabarovsk, 680000, Russia; [email protected] The results of studying the content of heterotrophic bacteria, mercury and volatile organic compounds, including ethyl acetate, in the ice layer of the Amur River and the Pemzenskaya Channel are discussed. The maximum amount of cultivated heterotrophic bacteria participating in biotransformation of organic compounds of diff erent origin was found in the Amur River near the left bank in the 30–40 cm layer of ice containing particles of detritus. Ethyl acetate was established to be the main substance contained in diff erent layers of ice; its maximum concentration (18.2 mg/L) was recorded in the middle of the Amur River in the 40–70 cm layer of ice. In the 20–30 cm ice layer from the Pemzenskaya Channel, the following pollutants were found near the right bank: acetaldehyde (4.1 mg/L), benzene (0.5 mg/L) and styrene (2.0 mg/L). Higher mercury concentrations ranging from 0.13 to 0.14 μg/L characterized the upper layers of ice near the right bank of the Amur River and the left bank of the Pemzenskaya Channel. The combination of these components in the ice layer preconditions methylation of mercury. Methylmercury, ice, volatile organic matter, biotransformation

INTRODUCTION Previously mercury contamination of the Amur The factors contributing to methylation of mer- River was discussed due to the operation of the Amur cury in the Amur River in the winter period are the pulp and cardboard factory and accumulation of mer- limit of oxygen, discharge of insufficiently treated cury-containing waste. In the 1990s, the workers of wastewater, recharge of underground iron-containing the Institute of Water and Ecological Problems, FEB waters and activation of the processes of sulfate re- RAS, carried out detailed studies of the geochemical duction in the bed silt. The problem of mercury be- background and contamination of the territory of the comes especially important for the entire river basin Amur basin with heavy metals. Industrial centers due to trans-borderline contamination of the Amur (Khabarovsk, Amursk, Komsomolsk-on-the-Amur) River due to its tributary the Songhua River (China), and the Songhua River were referred to as sources of winter discharge from water reservoirs and the spring industrial pollution. Averaged data were presented on outﬂ ow of ice into the coastal waters of the Far Eas- the content of mercury in the bed silt for the mid- tern seas [Kondratyeva et al., 2013; Kondratyeva and dle and lower Amur River – 0.20 mg/kg (0.10– Zhukov, 2014]. 0.46 mg/kg). Increased content of mercury (without Several sources of the mercury contamination of indicating concentrations) was found in the fish the Amur River may be identiﬁ ed. caught in that period. Significant accumulation of 1. Trans-borderline supply of mercury from the heavy metals and mercury was recorded in the sur- territory of China with the waters of the Songhua face layer of the bed silt of the mouth zone of the River, in which, according to Chinese researchers, the Amur River, where active sedimentation of suspend- content of mercury was 0.009–0.069 μg/dm3. It is ed matter takes place [Kot, 1994]. The seasonal stud- known that in the period from 1958 to 1982, the river ies conducted in 2012–2014 by the Krai Center of was contaminated by discharge of wastewater from Environmental Monitoring and Emergency Predic- the Jinlin Chemical Co chemical factory (a large pro- tion of Khabarovsk krai demonstrated the increase in ducer of acetaldehyde from acetylene), in which mer- the content of mercury to 2–3 maximum permissible cury sulfate (II) was used as a catalyst. A large part of concentration values in the spring period. Many au- this mercury was accumulated in bottom sediments thors note an increase in the migration ability of mer- and gradually migrated into the water medium [ Jiang cury, which is mostly caused by transformation of et al., 2006; Zhang et al., 2010b]. mercury into methylmercury, due to the microbio- 2. The land runoff from the territories of gold logical activity in the presence of organic matter [Er- production by the amalgamation method [Stepanov et makov, 2010; Moiseenko, 2010; Liu et al., 2012]. al., 2003], from the Lana vermilion field and from

21 R.A. KIPER ET AL. abandoned storages of granosan pesticide, which was product, acetate, formed [Wasik et al., 2012]. The used in the period of 1963–1989 in the territory of study of the biochemical mechanism of mercury the Amur region [Koval, 2003]. methylation with participation of SRB showed the 3. Discharge of technical water containing a presence of at least two ways of this process with ace- large amount of detritus from reservoirs of the hydro- tyl-CoA used and without it [Liu et al., 2012]. It has electric power plants built on the Zeya-Bureya plain been demonstrated in the studies of individual SRB [Kondratyeva et al., 2013]. strains that mercury methylation most often takes 4. In addition, atmospheric transfer of mercury place in the bed silt. Yet, this process may occur not over the territory of the Amur River basin is possible only in the bed silt but also in the water mass [Eckley when coal is burnt and during forest fi res [Yudovich and Hintelmann, 2006] and in the periphyton com- and Ketris, 2010]. munities of fresh-water ecosystems [Guimaraes et al., Despite the studies of many years, a number of 2006], where other groups of bacteria also play a large questions related to mercury methylation remain un- role in mineralization of carbon. solved [Liu et al., 2012]: the way of mercury transport Iron-reducing and methane-producing bacteria to cells (whether active or facilitated transport); it is may take part in the methylation of mercury [Roh et not clear yet by which chemical mechanism the meth- al., 2006; Hamelin et al., 2011]. Several strains of Geo- yl group is transported into mercury, what kind of bacter, Desulfuromonas and Shewanella were tested contribution syntrophy makes in the process of mer- for the methylating activity. The representatives of cury methylation; the mechanism of oxidative de- the former two geni produced methylmercury when composition of methylmercury by microorganisms is cultivated with Fe(III), whereas Shewanella spp. did at the stage of investigation; the influence of sub- not methylate mercury under nitrate-reducing condi- stances contained in individual components of eco- tions and in the presence of Fe(III). In addition, Geo- systems on mercury methylation has not yet been bacter metallireducens and Geobacter sulfurreducens completely studied. Still open is the issue of the rela- methylated mercury by using either fumarate or ni- tionship between microbial communities and their trate, thus indicating that reduction of iron is not potential for mercury methylation in diff erent com- obligatory for mercury methylation. ponents of the aqueous ecosystems. Humic acids play a signifi cant role in the biogeo- The rate of microbial mercury methylation de- chemical processes of mercury methylation. Forma- pends on a number of environmental factors which tion of insoluble complexes with humic acids retards may affect the bioavailability of mercury and the transformation of mercury and creates a possibility of structure of the microbial community: the water tem- its deposition, while formation of soluble complexes perature, pH, the oxidation-reduction potential, with fulvic acids boosts its migration. A high content availability of nutrients and acceptors of electrons, as of organic matter with prevalence of humic acids, well as the presence of ligands and absorbing surfaces. oxygen defi cit, and neutral or subacid medium con- These parameters cannot be considered independent- tribute to the processes of mercury alkylation [Erma- ly from each other, as they often interact, with the kov, 2010]. It was established that in the winter peri- resulting complex system of biogeochemical process- od the content of humic acids in the Amur River de- es formed. creases to a minimum [Levshina, 2006]; under such The methylation processes are especially intense conditions, concentration of mobile mercury may in- in the upper layers of the bottom sediments, rich in crease. organic matter (OM), in the substances suspended in There are reports that mercury may be methyla- water, as well as in slime covering fi sh [Moiseenko, ted in the snow. The scientists of the Khanty-Mansi 2010]. As a rule, chlorides boost the methylation pro- autonomous region discovered sevenfold presence of cess, whereas sulfates in large concentrations inhibit mercury in the places of snow deposition from terri- it [Ermakov, 2010]. tories of settlements versus the background mercury The majority of microorganisms methylating content [Moskovchenko and Babushkin, 2012]. A brief mercury are referred to Deltaproteobacteria. Many review was published on the role of mercury in the studies are aimed at answering the question whether cryosphere [Durnford and Dastoor, 2011]. Mercury- the methylating activity is randomly distributed resistant microorganisms were identifi ed in the Arc- among proteobacteria or whether it correlates with tic snow and ice [Moller et al., 2011]. Some scientists phylogenetic appurtenance [Kerin et al., 2006]. It is believe that the living activity of microbes stops at known that sulfate-reducing bacteria (SRB), capable the temperatures below 0 °С [Brouchkov et al., 2011], of oxidizing different sources of carbon in a wide but, as shown in the permafrost studies [Rivkina et al., range of temperatures, are the key microbiological 2000], the metabolic activity of microorganisms may methylator of mercury in many aqueous systems [So- be sustained at –20 °С. kolova, 2010]. Mercury-methylating SRB, including The recent results of studying the genetic, evolu- representatives of the Desulfovibrionaceae family, tionary and biochemical aspects of mercury methyla- may oxidize carbon sources, with an intermediate tion have shown that diff erent taxonomic groups may

22 BIOGEOCHEMICAL ASPECTS OF MERCURY METHYLATION IN THE ICE OF THE AMUR RIVER take part in this process (Proteobacteria, Firmicutes, RAS, during the winter expedition to the Amur River Archаea), which occupy diff erent ecological niches guided by A.N. Makhinov. The ice cores were drilled and which account for the global scales of mercury with an auger (the internal diameter 16 cm) in the methylation both under aerobic and anaerobic condi- cross section (from the left bank to the right bank) in tions [Acha et al., 2012; Podar et al., 2015]. In accor- the main bed of the Amur River and the Pemzenskaya dance with metagenomics analysis, microbial commu- Channel in the area of the city of Khabarovsk. The ice nities of fresh-water ecosystems, tropic and Arctic cores were sawed into slabs considering its inhomoge- seas, underground waters, soils of diff erent regions, neous structure on ice cleaned from snow, and then bogged areas the permafrost zone and rice ﬁ elds have the slabs were stored in a freezing chamber with the an environmental potential for mercury methylation temperature –18 °С. [Zhang et al., 2010а; Lehnherr et al., 2012; Wasik et al., To conduct chemical and microbiological tests, 2012; Gilmour et al., 2013]. melts of diff erent ice layers were used. The ice speci- Contamination of river ice with mercury is stu- mens were melted at room temperature with all the died much rarer than pollution of the Arctic ice. The aseptic rules observed. The ice was placed into steri- previously held investigations testify to mercury pol- lized containers covered with lids. The amount of lution of diff erent components of the ecosystem of the cultivated heterotrophic bacteria (CHB) was de- Amur River, including bed silt and ice [Kondratyeva, termined by culturing 0.1 mL of melted ice onto 2010; Kondratyeva et al., 2012, 2013]. The study of 10 times diluted peptone agar by the limit dilutions the ice of the Amur and Songhua Rivers after the an- me thod, with subsequent re-calculation per 1 mL of thropogenic disaster in China in November 2005 melt-water and was expressed in colony-forming showed that the amount of microorganisms belonging units (CFU/mL). Microbiological cultures were to diff erent physiological groups essentially increased grown three times. The diagrams demonstrate the in the presence of various organic substances which average amounts of the microorganisms found. The accumulated in the ice mass [Kondratyeva et al., content of volatile organic matter was determined by 2011a; Kondratyeva and Fisher, 2012]. the gas chromatography method (the Shimadzu It is to be emphasized that complex microbial GC-2010 gas chromatograph), in accordance with consortia consisting of diff erent taxonomic groups the ISO 11423-1 standard (analyst A.G. Zhukov). take part in the carbon cycle. Heterotrophic bacteria Mercury concentration was determined with an in- (aerobic and opportunistically anaerobic) play an im- ductively coupled plasma emission mass spectrometer portant role in the transformation and mineralization ICP-MS Elan DRC II PerkinElmer (USA). of organic matter. Destroying highly molecular and stable organic substances of diff erent origin, changing RESULTS AND DISCUSSION the oxidation-reduction potential of their habitats Pollution of natural waters takes place all the and supplying metabolic products as donors and ac- year round. However, it is very diffi cult to monitor ceptors of electrons, they create prerequisites for the the quality of water in the rivers of Siberia and of the growth of anaerobic groups of bacteria (sulfate reduc- Russian Far East in the winter period. One of the pos- ing, iron-recovering, denitrifying and methanotro- sible ways of overcoming these diffi culties is to carry phic bacteria). The presence of heterotrophic bacteria our simultaneous examination of ice layer by layer, in ice is one of the important prerequisites for forming using spectral, chromatographic and microbiological conditions for mercury methylation by specialized methods. Layer-by-layer examination of ice at the groups of bacteria at the end of the freeze-up. There- end of the freeze-up period allows making retro- fore, the following conditions are required for the spective analysis of contamination of the stream eco- process of mercury methylation: the presence of mer- systems in the period of formation of the ice cover cury compounds and of organic matter, ensuring [Kond ratyeva, 2010]. Sampling ice cores in the longi- functioning of microbial complexes; formation of tudinal and latitudinal sections of the streams allows sources of methyl radicals for mercury methylation. the character of their contamination in space to be The purpose of this study was to conduct a bio- evaluated, whereas layer-by-layer investigation of ice geochemical examination of ice cores and to analyze was carried out in time, over the period of ice cover the conditions needed for mercury methylation in the formation. Organic substances of natural and anthro- period of the freeze-up in the main bed of the Amur pogenic origin may be identiﬁ ed in diff erent ice lay- River of the Pemzenskaya Channel in the area of the ers, present in the water at the time of formation of city of Khabarovsk. the given ice layer, as well as products of bacterial metabolism. OBJECTS AND METHODS OF STUDY Microbiological transformation of organic mat- Ice cores were obtained by drilling at the end of ter is an important factor which determines the for- the freeze-up period of 2011/12 by the researchers of mat of mercury existence. Soluble organic matter the Institute of Water and Ecological Problems, FEB usu ally boosts microbial activity and thus may con-

23 R.A. KIPER ET AL.

Fig. 1. Change in the amount of cultivated heterotrophic bacteria in diff erent layers of ice of the Amur River (a) and the Pemzenskaya Channel (b) in the directions: left bank, middle fl ow, right bank (March 2012). tribute to synthesis of methylmercury. Microbiologi- mic robiological processes to take place in these layers cal investigations of river ice specimens sampled in of ice with a high content of HB. 2012 in the area of Khabarovsk showed that the high Earlier, in the mouth zones of the large Amur amount of cultured heterotrophic bacteria (HB) is tributaries (the Zeya and Bureya Rivers), characte- observed in the main bed of the Amur River near the rized by an increased content of humic substances, left and right banks, whereas the amount in the mid- we discovered actively growing sulfate reducing bac- dle fl ow of the river is minimal (Fig. 1). teria, while the microbial community displayed resis- Maximum amount of HB was found near the left tance to mercury salts [Kondratyeva et al., 2011b, bank of the river in the 30–40-cm layer of ice. Detri- 2013]. tus was present in the melt of this layer of ice. The Based on the many years’ studies we conducted, amount of HB near the right bank of the river gradu- we concluded that the composition of volatile organic ally increased towards the lower layers of ice but it substances in ice changes from year to year; yet, me- did not reach the maximum values near the left bank. thylated compounds are practically always present In accordance with the microbiological test of there. For example, in 2005–2006, after an anthro- the ice melts sampled from Pemzenskaya Channel, pogenic disaster in China, methylated derivatives of the quality of water in it in the period of formation of benzene dominated, which are potential sources of the ice cover was much higher, which was refl ected in methyl radicals. In the winter period of 2010/11, all the lower amount of bacteria in diff erent layers, com- the ice samples taken from the water along the right pared to the trunk of the Amur River. bank of the Amur River contained dichloromethane The distribution of microorganisms by the layers and butyl acetate. In some lower layers of ice, toge- of ice may be related to the specifi c character of the ther with the high concentrations of dichloromethane transport of organic matter with water masses in the and butyl acetate, there were isopropylbenzene and period of formation of the ice cover. The high amount methylated derivatives of benzene (о- and р-xylols). of HB in the 30–40-cm layer of ice near the left bank It is to be pointed out that dichloromethane was also in the trunk of the Amur River may be related to present in the ice sampled from the Pemzenskaya technical discharge of water from the Bureya and Chan nel; however, its concentrations were lower Zeya water reservoirs located upstream on the left- than those in the trunk of the Amur River [Kondra- bank territory of the basin. It was previously noted tyeva et al., 2012]. that water masses with a high content of HB were As the studies conducted in the Amur River in transported along the left bank of the river in the 2011–2012 showed, the qualitative and quantitative autumn period, especially at the time of fl oods in the composition of volatile components in the under-ice basins of the Zeya and Bureya Rivers [Kondratyeva et water and in the lower layers of ice diff ered signifi - al., 2013]. The amount of heterotrophic bacteria in cantly (Table 1). Ethyl acetate was the dominant diff erent layers of ice refl ects the content of nitrogen- component in diff erent layers of ice sampled from the containing and aromatic organic compounds of diff er- cross sectional profile of the Amur River and the ent origin. Microbial complexes create prerequisites Pemzenskaya Channel. Higher concentrations of for transformation of organic matter to products en- ethyl acetate were found in the lower layers of ice suring methylation processes. We can assume active than in the under-ice water. We can suppose that this

24 BIOGEOCHEMICAL ASPECTS OF MERCURY METHYLATION IN THE ICE OF THE AMUR RIVER component common for the ice is a product of micro- Table 1. Content of volatile organic matter (mg/L) biological decomposition of high-molecular organic in the lower layer of ice and in the under-ice water matter of diff erent origin transported in the period of of the Amur River in the area of Khabarovsk ice cover formation. (March 2012) During studies of the layers of the ice cores, high Left bank Middle fl ow Right bank concentrations of ethyl acetate were discovered in Component the trunk of the Amur River in the middle fl ow and Water Ice Water Ice Water Ice near the right bank (Fig. 2). Maximum concentrati- Hexane 4.6 bdl 16.8 3.0 6.4 3.2 on (18.2 mg/L) of ethyl acetate was recorded in the Ethyl acetate 1.9 3.3 4.2 18.2 2.8 9.9 lower 40–70-cm-thick layer of ice. High concentra- Styrene 7.4 3.6 6.1 3.7 5.3 1.7 tions of ethyl acetate (8.0–11.1 mg/L) were also found in the middle fl ow of the Pemzenskaya Chan- N o t e. Bdl – below detection limit. nel for the entire mass of ice. In the layers of ice formed at the beginning of the freeze-up near the river (2.0 mg/L) were found near the right bank in the banks, its concentrations were 2–3 times lower. In 20–30-cm-thick layer of ice. Near the left bank, in ad- addition, near the right bank of the river, acetalde- dition to ethyl acetate, cyanoethylene, which is found hyde (4.1 mg/L), benzene (0.5 mg/L) and styrene in the wastewater of the textile industry, hexane and

Fig. 2. The concentration of ethyl acetate in diff erent layers of ice of the Amur River (а) and of the Pemzen- skaya Channel (b) in the directions: left bank, middle ﬂ ow, right bank (March 2012).

Fig. 3. The concentration of mercury in diff erent layers of ice of the Amur River (а) and the Pemzenskaya Channel (b) in the directions: left bank, middle ﬂ ow, right bank (March 2012).

25 R.A. KIPER ET AL. styrene were identified in the ice layer 30–45 cm come involved in the processes of transformation. thick. We can suppose that in the period of the freeze- Diff erent representatives of heterotrophic psychro- up, components of wastewater come from the trunk of philic microorganisms creating conditions for the the Amur River, illegally discharged by the industrial growth of specialized groups of bacteria methylating enterprises located along the Pemzenskaya Channel. mercury may take part in them. In accordance with the literature data [Plata et Considering the regional specifics of seasonal al., 2005; Il’chenko and Shcherbakova, 2008], ethyl changes in the content of humic substances in the acetate may be formed as a result of microbiological Amur River, the presence of accessible organic matter transformation of natural organic matter. Ethyl ace- in ice and development of mercury-resistant cryomic- tate we found in the river ice may be both of anthro- robiocenoses in them, it is possible to predict forma- pogenic origin (from wastewater) and of microbio- tion of conditions for microbiological methylation of logical origin. mercury and its inclusion into biogeochemical cycles. The studies of ice in March 2012 (Fig. 3) showed During the spring ice drift and during ice melting, the highest concentration of mercury in the upper methylated mercury, which has increased bioavaila- layers of ice near the right bank of the Amur River bility, may be included into the trophic networks of (0.13 μg/L) and near the left bank of the Pemzen- the Amur River and be drifted to the coastal areas of skaya Channel (0.14 μg/L). In the middle of these the Sea of Okhotsk and of the Sea of Japan. streams, mercury concentration in all the layers of ice was either minimal (0.01 or 0.02 μg/L) or below the References μ detection limit (less than 0.001 g/L). Acha, D., Pabo, C.A., Hintelmann, H., 2012. Mercury methyla- In analyzing diff erent layers of ice, we observed tion and hydrogen sulfide production among unexpected gradual reduction of mercury concentration from the strains isolated from periphyton of two macrophytes of the upper layer to the lower layer. This may be related to Amazon. FEMS Microbiol Ecol. 80, 637–645. the increased mercury concentration in the water at Brouchkov, A.V., Melnikov, V.P., Schelchkova, M.V., Griva, G.I., the beginning of formation of the ice cover due to the Repin, V.E., Brenner, E.V., Tanaka, M., 2011. Biogeochemis- try of permafrost in Central Yakutia. 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