Cite This: Environ. Sci. Technol. 2018, 52, 1234−1243 pubs.acs.org/est

Kinetics of Decomposition of Thiocyanate in Natural Aquatic Systems Irina Kurashova,† Itay Halevy,‡ and Alexey Kamyshny, Jr.*,†

† Department of Geological and Environmental Sciences, Ben-Gurion University of the Negev, Beer Sheva, Israel 84105 ‡ Department of Earth and Planetary Sciences, Weizmann Institute of Science, Rehovot, Israel 76100

ABSTRACT: Rates of thiocyanate degradation were measured in and sediments of marine and limnic systems under various redox conditions, oxic, anoxic (nonsulfidic, nonferruginous, nonmanganous), ferruginous, sulfidic, and manganous, for up to 200-day period at micromolar concentrations of thiocyanate. The decomposition rates in natural aquatic systems were found to be controlled by microbial processes under both oxic and anoxic conditions. The Michaelis−Menten model was applied for description of the decomposition kinetics. The decomposition rate in the sediments was found to be higher than in the samples. Under oxic conditions, thiocyanate degradation was faster than under anaerobic conditions. In the presence of hydrogen sulfide, the decomposition rate increased compared to anoxic nonsulfidic conditions, whereas in the presence of (II) or manganese(II), the rate decreased. Depending on environmental conditions, half-lives of thiocyanate in sediments and water columns were in the ranges of hours to few dozens of days, and from days to years, respectively. Application of kinetic parameters presented in this research allows estimation of rates of thiocyanate cycling and its concentrations in the Archean ocean.

■ INTRODUCTION aquatic systems, as well as to chemical transformations, 24−26 Thiocyanate (NCS−) is formed in various natural and industrial volatilization and adsorption. processes. It was found in waters from coal and oil The presence of thiocyanate was recorded in various natural nonpolluted aquatic systems, for example in stratified lakes processing, steel manufacturing, and the petrochemical −1 1−5 · Rogoznica in Croatia (up to 288 nmol·L ) and Green Lake industry. Thiocyanate concentrations of up to 17 mmol −1 19 −1 4,6 (NY, USA) (up to 274 nmol·L ). In these lakes thiocyanate L were detected in coal plant wastewaters and in gold fi ff extraction wastewaters.7,8 In electroplating, dyeing, photo- is produced in the anoxic, sul de-rich sediments and di uses to finishing, , and pesticide production the concentration the chemocline, where it is consumed by oxidative processes, of NCS− in wastewater effluents is in the range of 0.09−2 which are likely biologically enhanced. In the oxic North Sea · −1 9 water thiocyanate was detected at concentrations up to 13 mmol L . Thiocyanate is toxic to aquatic species with LC50 −1 16 −1 10 nmol·L . In saltmarsh sediment of the Delaware Great Downloaded via WEIZMANN INST OF SCIENCE on September 20, 2018 at 06:31:37 (UTC). values of 0.01 to 0.5 mmol·L reported for Daphnia magna. μ · −1 See https://pubs.acs.org/sharingguidelines for options on how to legitimately share published articles. Natural sources of thiocyanate include plants, biological and Marsh, thiocyanate concentrations are up to 2.28 mol L in μ · −1 26 abiotic decomposition of , and in vivo pore-water and up to 15.6 mol kg in wet sediment. In − detoxification of .11 14 Several species of , these sediments, concentrations of thiocyanate precursors, algae, fungi, plants, and animals are physiologically capable of cyanide-reactive zerovalent and free are μ · −1 μ · −1 detoxifying cyanide, and in most cases one of the end products as high as 78 mol L and 1.9 mol L , respectively. fi of detoxification is thiocyanate.10,15 Another important Coexistence of hydrogen cyanide, polysul des and thiocyanate mechanism of thiocyanate formation in natural aquatic systems allows attribution of thiocyanate formation to the abiotic is the reaction between hydrogen cyanide and sulfide oxidation reactions between hydrogen cyanide and reduced sulfur species. − μ · −1 intermediates, which contain sulfur−sulfur bonds, such as Thiocyanate was also found in concentrations 23 40 mol L 27 colloidal sulfur,16 polysulfides,17 , and tetrathio- in the Red Sea Atlantis II Deep brine. Reactions between nate.18,19 Reaction with thiosulfate is ∼1000 times slower abiotically formed hydrogen cyanide and reduced sulfur species than reaction with polysulfides,17,20,21 and is catalyzed by were proposed as the source of thiocyanate in the brine. The Cu(II) and sulfur transferases from the family.15,22 Concentrations of hydrogen cyanide in polluted aquatic Received: September 17, 2017 systems may reach levels toxic to aquatic life.23 In nonpolluted Revised: December 25, 2017 aqueous systems, hydrogen cyanide concentrations are usually Accepted: December 28, 2017 very low due to fast degradation by plants, fungi and bacteria in Published: December 28, 2017

© 2017 American Chemical Society 1234 DOI: 10.1021/acs.est.7b04723 Environ. Sci. Technol. 2018, 52, 1234−1243 Environmental Science & Technology Article

Table 1. Rates of Thiocyanate Degradation in Natural and Controlled Systems

− · −1 μ · −1· −1 system conditions [NCS ]o (mmol L ) rate ( mol L d ) ref Lake Kinneret and Mediterranean Sea water oxic 0.003 0.026−0.23 this work anoxic 0.003 0.0048−0.021 this work Lake Kinneret and Red Sea sediment oxic 0.003 2.1−2.4 this work anoxic 0.003 0.0074−0.023 this work gold mine tailing storage facility microbial consortium in synthetic medium oxic 0.003 ∼5.4 43 activated sludge mixed liquor oxic 0.003 110 72 wastewater with cultivated oxic 0.003 2800 36 Lake Kinneret and Mediterranean Sea water oxic 1 0.43−0.90 this work anoxic 1 0.034−0.34 this work Lake Kinneret and Red Sea sediment oxic 1 45−49 this work anoxic 1 0.078−0.61 this work gold mine tailing storage facility microbial consortium in synthetic medium oxic 1 ∼1700 43 activated sludge mixed liquor oxic 1 2100 72 wastewater with cultivated microorganisms oxic 1 82500 36 water enrichment with Klebsiella species oxic 0.4−3.9 ∼860 79 enrichment cultures from steel plant wastewater oxic 5.7 ∼1.9 53 enrichment cultures from steel plant wastewater anoxic 4.7−5.6 ∼0.79 53 activated sludge anoxic 1.7 0 3 brine liquor with mixed methanogenic cultures anoxic 2.5 0 80 a simulated wastewater containing phenol, thiocyanate, and - anoxic 1.9−10.3 0 81 same processes were proposed to result in thiocyanate the rates may be as high as 83 mmol·L−1·d−1 at 1 mmol·L−1 formation in the hydrothermal springs and pools in the concentration of thiocyanate (Table 1). Thiobacillus species Yellowstone National Park, where it was detected at isolated from steel plant wastewater, are able to degrade 5.2 − − concentrations 133−791 μmol·L−1.28 mmol·L 1 of NCS over 8 days under anaerobic denitrifying Although concentrations of thiocyanate in modern aquatic conditions.53 Rates of thiocyanate degradation depend not only systems are low,16,19,26,28 this may be not the case for the iron- on concentrations,3,53,80,81 but also on concentrations of rich water column of the Archean ocean. Existence of large nutrients. It was shown that concentrations of NH >70μmol· − 3 atmospheric fluxes of both hydrogen cyanide and zerovalent L 1 may inhibit76 and phosphate concentrations >500 μmol· − − 8 sulfur to Archean ocean has been suggested.29 34 These works L 1 may stimulate thiocyanate . provide constraints on cyanide and zerovalent sulfur fluxes but Currently, metabolic pathways for thiocyanate degradation lack of data regarding rates of thiocyanate degradation under are known and the rates of its degradation in bioreactors are environmental conditions in the presence of dissolved iron(II) published, but no data on kinetics of decomposition of prevents estimation of thiocyanate concentrations and its fate in thiocyanate in natural aquatic systems is available. The main fi the Archean ocean. aim of the present research is to ll this gap and to provide Multiple investigations focused on the isolation and constraints on rates of decomposition of thiocyanate in limnic identification of microorganisms that are responsible for and marine water columns and sediments at various redox − thiocyanate biodegradation under controlled conditions.35 52 conditions, which are relevant for modern and ancient natural Thiocyanate-degrading bacteria have been isolated from aquatic systems. To achieve this goal, we have determined activated sludge,41 steel plant wastewater,53 gold mine tailing kinetic parameters of thiocyanate degradation in natural aquatic sites,43,50,51 and extreme alkaline54 and hypersaline55,56 environ- and sedimentary systems at various salinities and concen- − fi ments. The end products of NCS degradation are ammonium, trations of thiocyanate, oxygen, hydrogen sul de, and iron(II). dioxide, and sulfate, subsequent to the formation of − − cyanate57 62 or carbonyl sulfide63 67 as intermediates. A variety ■ MATERIALS AND METHODS − of autotrophic bacteria are capable of using NCS as their sole Materials. Solutions for measurements of the kinetics energy source via sulfur oxidation. Chemolithotrophic bacteria parameters of thiocyanate degradation were prepared in Milli-Q fi − utilize hydrogen sul de formed on the initial step of NCS water, Mediterranean Sea water, Red Sea water, Lake Kinneret degradation and products of its incomplete oxidation (Lake Tiberias) water. Slurries were prepared from Red Sea and (polysulfide, elemental sulfur, or thiosulfate) as an energy Lake Kinneret sediments. All reagents were purchased from 41,63,68,69 source for growth, oxidizing sulfide to sulfate. Sigma-Aldrich and were at least 98% pure. Utilization of nitrogen released from thiocyanate as ammonia thiocyanate (KSCN) (99%), sodium sulfide nonahydrate 58 · has also been reported. A number of heterotrophic bacteria (Na2S 9H2O) (98%), and iron(II) sulfate heptahydrate − 46,50,52,70,71 · fi utilize NCS as a source of nitrogen and sulfur as (FeSO4 7H2O) (99%) were used without further puri cation. well as energy source.38,44 Heterotrophic bacteria were shown Nitrogen gas (99.999%) was purchased from Maxima ltd, Israel. to utilize thiocyanate at concentrations as high as 100 mmol· Test tubes, screw caps with hole and septum, and aluminum − L 1.70 caps were purchased from Romical, Ltd., Israel, and Labco, Ltd., In biotechnological systems for thiocyanate removal, which UK; butyl rubber stoppers were purchased from Geo-Microbial are operating under high concentrations of thiocyanate (up to Technologies, Inc., USA. − − 120 mmol·L 1 and oxic conditions10,36,43,72 79), rates of Samples Preparation and Treatment. Water and thiocyanate decomposition are high. Under oxic conditions sediment samples were collected from various locations in

1235 DOI: 10.1021/acs.est.7b04723 Environ. Sci. Technol. 2018, 52, 1234−1243 Environmental Science & Technology Article

Table 2. Sampling and Processing Protocols for Preparation of Water Samples

sample depth initial no. system (m) sampling date conditions treatment final conditions WC-1 Lake Kinneret 1 17 Jun, 2015 oxic no oxic, pH 8.1 fi μ · −1 μ · −1 WC-2 Lake Kinneret 37 17 Jun, 2015 sul dic N2 purge [O2]<1 mol L ,[H2S] < 1 mol L , pH 7.8 fi fi μ · −1 WC-3 Lake Kinneret 37 17 Jun, 2015 sul dic no sul dic ([H2S] = 35 mol L ), pH = 7.7 fi μ · −1 WC-4 Lake Kinneret 37 17 Jun, 2015 sul dic N2 purge, FeSO4 spiking ferruginous ([Fe(II)] = 81 mol L ), pH 7.9 WC-5 Mediterranean Sea 1 17 May, 2015 oxic no oxic, pH 8.4 μ · −1 WC-6 Mediterranean Sea 1 17 May, 2015 oxic N2 purge [O2]<1 mol L , pH 8.4 fi μ · −1 WC-7 Mediterranean Sea 1 17 May, 2015 oxic N2 purge, Na2S spiking sul dic ([H2S] = 118 mol L ), pH 8.3 μ · −1 WC-8 Mediterranean Sea 1 17 May, 2015 oxic N2 purge, FeSO4 spiking ferruginous ([Fe(II)] = 95 mol L ), pH 8.7

Israel (Tables 2 and 3). Sediment cores and water samples were were purged with nitrogen under a nitrogen atmosphere in a collectedfromtheRedSea(29°30′N, 34°55′E), the glovebag. Sulfidic conditions were simulated by addition of the Mediterranean Sea (32°49′N, 34°59′E), and Lake Kinneret sodium sulfide as described above. After distribution to the test (32°50′N, 35°35′E) in May 2015−December 2016. Sediment tubes, slurry samples were spiked by KCSN solution to the samplings were performed with a multicorer, Lake Kinneret, target concentrations of NCS− in slurry pore-waters: 3, 10, 30, and Red Sea waters were sampled with Niskin bottles, 100, 300, and 1000 μmol·L−1.TheratesofNCS− Mediterranean Sea water was sampled manually near the decomposition at concentrations >1 mmol·L−1 were not shore. The water and cores were stored at 25 ± 1 °C in the measured as (1) these concentrations are not relevant for dark and processed in <1 day after sampling. natural aquatic systems and (2) some works36,73 report that at The rates of decomposition of thiocyanate in water were these concentrations the microbial decomposition of thiocya- measured in the following sets of samples: (1) oxic water nate is substrate-inhibited; although there is also evidence for sample without pretreatment; (2) anoxic, nonsulfidic water high thiocyanate decomposition rates at higher concentrations. samples, which were stripped of oxygen or hydrogen sulfide by For each water and sediment sample, an identical sample purging for 90 min with nitrogen in a glovebag; (3) ferruginous, autoclaved at 120 ± 3 °C for 20 min was prepared in order to prepared by adding of iron sulfate to the target concentration provide a sterilized control. All types of autoclaved samples 100 μmol·L−1 of Fe(II); (4) sulfidic, prepared by adding were prepared in 35 mL (water samples) and in 50 mL sodium sulfide to the target concentration 100 μmol·L−1 of (sediment samples) tubes and were hermetically closed with a μ · −1 S(II) and 50 mol L H2SO4 for pH adjustment (Table 2). rubber stopper and aluminum cap. Nonautoclaved water samples were distributed to 12 mL test All sterilized and nonsterilized samples were prepared and tubes. The tubes were filled without a headspace and analyzed in triplicates. Hermetically closed samples were hermetically closed using a screw cap with hole and septum. incubated at 25 ± 1 °C. Subsamples were taken from the KSCN was injected into the test tubes with samples to the samples by syringes immediately prior to analysis. Subsampling following target concentrations: 3, 10, 30, 100, and 300 μmol· of anoxic samples was carried out in the glovebag (typically −1 L . <0.2% O2 v/v) to maintain anoxic conditions in the sample. The rates of decomposition of thiocyanate in the sediments The rate of thiocyanate decomposition was studied by were measured in the samples from the locations presented in measurement of thiocyanate concentrations in multiple Table 3. Both Red Sea (Gulf of Aqaba) water and sediment subsamples during 35−200 day period. cores were sampled at 561 m water depth. The cores were Analytical Methods. Thiocyanate was quantified by an sectioned into slices: 1−2 cm (oxic), 8−12 cm (manganous), Agilent Technologies 1200 HPLC system with multiple 20−24 cm (ferruginous), and 30−34 cm (anaerobic zone with wavelength UV−visible detector operated at 220 nm. A 2+ 2+ μ · −1 fi [H2S], [Fe ], [Mn ] < 1.5 mol L ). Sul dic Lake Kinneret Nomura Chemical, Japan, Develosil RPAQUEOUS C30 water and sediment cores were sampled below the chemocline reverse phase column (150 mm × 4.6 mm × 5 mm) was at 37 m depth. The cores were sectioned into slices: 5−10 cm used for HPLC separation of thiocyanate. The column was fi − 2+ 2+ fi 82 (sul dic), 12 17 cm (anaerobic zone, [H2S], [Fe ], [Mn ]< modi ed according to Rong et al. by pumping 5% aqueous 2.5 μmol·L−1), and 20−25 cm (ferruginous zone). Additional solution of PEG-20 000 at 0.3 mL·min−1 rate for at least 3 h. core was sampled above the chemocline at 32 m water depth Hydrogen sulfide was measured spectrophotometrically by the for oxic (upper 0−5 mm) sediment layer. methylene blue method according to Cline83 by LaMotte For experiments under anoxic conditions, the cores were cut SMART Spectro spectrophotometer. Fe2+ was quantified under a constant flow of nitrogen and immediately transferred spectrophotometrically by ferrozine method according to 84 to a glovebag with N2 atmosphere. For killed control Stookey. Manganese was analyzed spectrophotometrically experiments, marine and limnic waters were sterilized by using the 1-(2-Pyridylazo)-2-naphthol (PAN) method.85 Oxy- autoclaving at 120 ± 3 °C for 20 min to prevent the effect of gen level was monitored using an optical oxygen meter with a microbial from the water column on the Retractable Needle-Type Oxygen microsensor (tip diameter degradation rate in sediment samples. Sediments were diluted ∼50 μm, MDL of 0.625 μmol·L−1, Firesting-Pyroscience) (1:1) with autoclaved bottom water (except for oxic Kinneret placed on a micromanipulator.86 Data was collected via sediment, which was diluted with autoclaved oxic water from 1 microprofiling software (Profix) with 2-point calibration. The m depth) and transferred to the 50 mL test tubes, which were optode needle was inserted into the sample through the septum hermetically closed using a hand crimper with a rubber stopper of the HPLC-vial which was filled and closed in the glovebag. and aluminum cap. For experiments under simulated anoxic Approach for Estimation of NCS− Degradation Rate. conditions, autoclaved oxic seawater and sulfidic limnic water Quantitative interpretation of biodegradation kinetics is based

1236 DOI: 10.1021/acs.est.7b04723 Environ. Sci. Technol. 2018, 52, 1234−1243 Environmental Science & Technology Article

on substrates degradation via catalyzed reactions, which are carried out by the bearing the specific . , pH 7.6 , pH 8.4 1 1 Therefore, rates of substrate degradation are generally depend- − − L L · · ent on the and substrate concentrations (e.g.,

mol mol Michaelis−Menten kinetics model). μ μ ), pH 8.6 1

− In natural aquatic systems degradation of thiocyanate may be L · performed by a single , as well as by microbial

mol −

μ consortium. It has been shown that the Michaelis Menten model87 (eq 1) can be applied for description of microbial , [Mn(II)] = 0.5 , [Mn(II)] = 0.5

1 1 utilization of cyanide and thiocyanate in activated sludge − − ), pH 8.7

1 3 L L ), pH 8.3 ), pH 7.8 · ·

− ff 1 1 reactors, as well as for determination of the e ect of L − − · L L mol mol · · concentration of organic pollutants on their biodegradation μ μ , [Mn(II)] = 0.5), pH 7.5 , [Mn(II)] = 1 mol

1 1 88 μ − − mol mol rate by natural microbial communities. Thus, in this study we L L μ μ · · will define “apparent” parameters of Michaelis−Menten model,

mol mol fi μ μ which correspond to degradation of thiocyanate by nonde ned 63

nal conditions microbial community. Katayama et al. showed that fi , [Fe(II)] = 0.5 , [Fe(II)] = 0.5 1 1 thiocyanate-degradation catalyzed by enzyme isolated from − − L L · · , [Mn(II)] = 2 , [Mn(II)] = 2.5 − 1 1

, [Mn(II)] = 35 Thiobacillus thioparus cells, followed Michaelis Menten-type − − 1 − L L mol mol

· · − L kinetics. In this work, the Michaelis Menten model was μ μ · , [Fe(II)] = 0.5 , [Fe(II)] = 1.5 1 1 mol mol

− − applied to nonautoclaved samples. mol μ μ L L μ · · S] = 2.5 S] = 1.5 mol mol 2 2 [S]V μ μ V = max ,[H ,[H 1 1 [S] + K (1) − − L L · · S] = 39 S] = 75 2 2

mol mol where V is the rate of thiocyanate decomposition at the given μ μ μ · −1· −1 concentration ( mol L day ), Vmax is the apparent maximum −1 −1 dic ([H dic ([H ]<1 ]<1 μ · · 2 2 fi fi rate of thiocyanate decomposition ( mol L day ), K is the

sul apparent half-saturation constant (corresponding to the S

2 substrate concentration at which the reaction rate is 50% of μ · −1 the Vmax ( mol L ), and [S] is the concentration of substrate (μmol·L−1). Specific degradation rate at each initial substrate concen- tration was analytically estimated by fitting the data for decrease dic water sul fi -purged water-purged water [O ferruginous-purged ([Fe(II)] water = 40 [O -purged water-purged water ferruginous ([Fe(II)] = 37 manganous ([Fe(II)] = 2 of concentration versus time. An overall dependence was -purged water, Na 2 2 2 2 2 2 established by plotting the calculated thiocyanate degradation rates versus initial thiocyanate concentrations. For estimation of the specific degradation rate, reaction rate was measured only

spiking on the initial stage of thiocyanate degradation, where thiocyanate degradation rate had linear dependence on time. fi Apparent Vmax and K values were calculated by tting curves to data using nonlinear regression and performing a nonlinear fit dic dilution with sul initial fi analysis in MATLAB. conditions treatment ferruginous dilution with N manganous dilution with N anoxic dilution with N oxicanoxic dilution with water dilution with N oxic, pH 8.8 ■ RESULTS AND DISCUSSION In all sterilized samples (water and sediments), the variation of date 2016 2016 2016 2016 2016 sampling thiocyanate concentration was <3% of initial concentration during the whole incubation period (data not shown). This indicates chemical stability of thiocyanate in aquatic systems in 24 20 Sep, 34 20 Sep, 25 1 Dec, 2016 ferruginous dilution with N 34 20 Sep, 17 1 Dec, 2016 anoxic dilution with N 12 20 Sep, 10 1 Dec, 2016 sul 2 20 Sep, 0.5 1 Dec, 2016 oxic dilution with water oxic, pH 8.0 − − − − − a wide range of environmentally relevant conditions, for − − − − (cm)

depth bsf example, in the presence as well as in the absence of sediments, oxygen, hydrogen sulfide, and dissolved iron in marine, as well as in limnic waters. (m)

depth In all nonautoclaved samples with initial thiocyanate concentrations of 3 μmol·L−1, decomposition was not observed during the first 26−100 days of incubation, except for oxic sediments and some oxic Mediterranean seawater samples in which the lag periods were <12 h and <12 days, respectively (Table 4). With an increase of NCS− concentrations, the lag period increased by 25−63%. After the lag period, the thiocyanate concentrations decreased in all nonsterilized fl no. system S-8 Red Sea 561 20 S-9 Red Sea 561 8 S-3 Lake Kinneret 37S-7 5 Red Sea 561 30 S-4 Lake Kinneret 37 20 S-5S-6 Red Sea Red Sea 561 561 0 30 S-2 Lake Kinneret 37 12 S-1 Lake Kinneret 32 0 samples. The lag period likely re ects the time which is sample

Table 3. Sampling and Processing Protocols for Preparation of Sediment Samples required for adaptation to a new substrate and an increase in

1237 DOI: 10.1021/acs.est.7b04723 Environ. Sci. Technol. 2018, 52, 1234−1243 Environmental Science & Technology Article

Table 4. Lag Times for Thiocyanate Decomposition at 3 μmol·L−1 Concentration

final conditions system time oxic anoxic sulfidic ferruginous manganous Lake Kinneret water incubation period (d) 156 164 112 142 lag time (d) 37 74 58 72 Mediterranean Sea water incubation period (d) 164 164 130 141 lag time (d) <12 79 71 75 Lake Kinneret sediment incubation period (d) 35 150 150 150 lag time (d) <1 46 35 45 Red Sea sediment incubation period (d) 35 157 157 157 157 lag time (d) <1 35 26 45 45

a Table 5. Coefficients of the Michaelis−Menten Equation

fi μ · −1 μ · −1· −1 sample no. system initial conditions nal conditions K ( mol L ) Vmax ( mol L day ) WC-1 LK oxic oxic 48 ± 11 0.450 ± 0.032 WC-2 LK sulfidic anoxic 59 ± 17 0.145 ± 0.014 WC-3 LK sulfidic sulfidic 48 ± 13 0.355 ± 0.030 WC-4 LK sulfidic ferruginous 29 ± 10 0.052 ± 0.006 WC-5 MS oxic oxic 9 ± 3 0.905 ± 0.07 WC-6 MS oxic anoxic 31 ± 8 0.167 ± 0.010 WC-7 MS oxic sulfidic 75 ± 20 0.251 ± 0.023 WC-8 MS oxic ferruginous 18 ± 3 0.035 ± 0.006 S-1 LK oxic oxic 61 ± 10 52 ± 3 S-2 LK anoxic anoxic 57 ± 20 0.351 ± 0.029 S-3 LK sulfidic sulfidic 89 ± 29 0.663 ± 0.039 S-4 LK ferruginous ferruginous 28 ± 8 0.081 ± 0.006 S-5 RS oxic oxic 65 ± 24 48 ± 2 S-6 RS anoxic anoxic 58 ± 12 0.356 ± 0.019 S-7 RS anoxic sulfidic 69 ± 21 0.575 ± 0.044 S-8 RS ferruginous ferruginous 55 ± 18 0.155 ± 0.014 S-9 RS manganous manganous 51 ± 14 0.166 ± 0.021 aWC, water column; S, sediment; LK, Lake Kinneret; MS, Mediterranean Sea; RS, Red Sea. cell concentrations as a response to thiocyanate amend- difference in thiocyanate decomposition rates in the absence ment.43,51 and in the presence of dissolved iron and hydrogen sulfide may On the basis of the specific degradation rate at each initial be attributed to differences in microbial community structure in substrate concentration, the apparent kinetic parameters of the thepresenceofdifferent electron donors. Calculated Michaelis−Menten model for each analyzed system were concentrations of thiocyanate-iron complex, Fe(SCN)+, are determined (Table 5). Experimental rates and the model data μ · −1 − <0.08 mol L . This concentration corresponds to the sample versus initial NCS concentration were plotted; the thiocyanate with the highest concentrations of Fe2+ (95 μmol·L−1) and − fi − decomposition rates and their Michaelis Menten model ts are thiocyanate (1 mmol·L 1) and the stability constant of 0.84 − − presented in Figure 1. Apparent parameters of the Michaelis mol 1·L for Fe(SCN)+ complex.91 Therefore, iron complex- Menten model were used to calculate thiocyanate half-lives at ation should not significantly affect the observed decrease of various concentrations (Figure 2). The lag time was not iron or thiocyanate concentrations. included in determination of the half-life time. − Comparison between Marine and Limnic Systems. In oxic Degradation of NCS in Water Columns. Influence of Mediterranean Sea water, the thiocyanate half-life was shorter redox conditions. The thiocyanate degradation rates in Lake than in oxic Lake Kinneret water. We attribute this difference to Kinneret waters decreased in the following order: oxic > sulfidic faster adaptation of local microbial communities in seawater to > anoxic > ferruginous (Figures 1a and 2a). In seawater − samples, the trend was similar: oxic > sulfidic ≈ anoxic > an increase in NCS concentrations. This explanation is ferruginous (Figures 1band2a). Relatively low rate of supported by longer lag periods observed in the case of oxic thiocyanate degradation under anaerobic conditions is charac- limnic water. Another support for this explanation comes from teristic for thiocyanate-decomposing bacteria and may be comparison of thiocyanate degradation rates in the presence of fi fi explained by lower yield of metabolic energy associated with hydrogen sul de. In Lake Kinneret water, which was sul dic utilization of electron acceptors, which are weaker than during the sampling, degradation rates were higher than in the oxygen.53,59,89 Since the only electron acceptor proven to Mediterranean Sea water, which was oxic at the time of support thiocyanate oxidation by bacteria in the absence of sampling but was amended with hydrogen sulfide. In the latter oxygen is , degradation of thiocyanate in these systems is case, the microbial community has to adapt to drastically likely to be nitrate-limited. In the anoxic waters of Lake changed conditions. Our observations show that the influence Kinneret, nitrate concentrations are <37 μmol·L−1, but can be of salinity on thiocyanate degradation rates is less pronounced as well <4 μmol·L−1 in the benthic boundary layer.90 The for all systems than influence of oxygen.

1238 DOI: 10.1021/acs.est.7b04723 Environ. Sci. Technol. 2018, 52, 1234−1243 Environmental Science & Technology Article

Figure 1. Thiocyanate degradation rates as a function of the initial thiocyanate concentration in Lake Kinneret water (a) and Mediterranean Sea water (b), in oxic Lake Kinneret and Red Sea sediments (c), anoxic Lake Kinneret sediment (d), and anoxic Red Sea sediment (e). Open symbols represent experiment data; solid symbols represent apparent K of the Michaelis−Menten equation; broken lines represent the model based on the apparent Michaelis−Menten kinetic parameters. Black color represents samples under oxic conditions, red color represents samples under anoxic conditions, green color represents samples under sulfidic condition, blue color represents samples under ferruginous conditions, and purple color represents samples under manganous conditions.

1239 DOI: 10.1021/acs.est.7b04723 Environ. Sci. Technol. 2018, 52, 1234−1243 Environmental Science & Technology Article

thiocyanate degradation. This observation agrees well with the results reported by Hung and Pavlostathis80 and Sahariah and Chakraborty,81 who found that thiocyanate is stable under the methanogenic conditions. Comparison of Thiocyanate Degradation Rates in Natural Systems and under Controlled Conditions. Compar- ison of thiocyanate decomposition rates reported in present work and those calculated for the same range of thiocyanate concentrations from kinetic parameters measured under controlled conditions are presented in Table 1. The rates of decomposition in nonpolluted natural aquatic systems are expected to be much lower than in the industrial systems due to (1) much lower microbial density and (2) lower concentrations of nutrients. Indeed, rates of thiocyanate decomposition in oxic sediments were found to be lower by 2−4.5 orders of magnitude as compared to activated sludge and wastewater microbial cultures.36,43,72 Under anoxic conditions, NCS− decomposition generally was not detected in industrial systems,3,80,81 except for steel plant wastewater with high concentrations of NCS− (4.7−5.6 mmol·L−1).53 Rates of thiocyanate decomposition calculated from the data presented by Grigor’eva et al.53 are only slightly higher than those detected in the anoxic sediments in this work at 1 mmol·L−1 concentration (Table 1). Although mechanisms and pathways of thiocyanate degra- dation under controlled conditions are well studied, detailed understanding of processes controlling stability of thiocyanate in natural aquatic systems is lacking. Future work should include detection of microbial species responsible for thiocyanate degradation in natural aquatic systems, evaluation of microbial community shifts as a response to thiocyanate Figure 2. Estimated half-lives of thiocyanate degradation in aquatic (a) pollution and identification of specific metabolic pathways of and sedimentary systems (b). Solid lines represent seawater samples; thiocyanate degradation under various environmental con- dashed lines represent limnic samples. Black color represents samples ditions. under oxic conditions, red color represents samples under anoxic − conditions, green color represents samples under sulfidic condition, Implications for the Archean Oceans. The Michaelis blue color represents samples under ferruginous conditions, and Menten model for the ferruginous Mediterranean seawater was purple color represents samples under manganous conditions. appliedtoestimatethesteady-state concentration of thiocyanate in the Archean Ocean. Ferruginous conditions Degradation of NCS− in Sediments. Influence of Redox may have been a dominant characteristic of the anoxic oceanic 98 Conditions. In both marine (Red Sea) and limnic (Lake water column throughout much of Earth’s history. Based on Kinneret) sediments, NCS− degradation was found to be faster estimated concentration of iron in the deep Archean − than in aquatic samples, especially under aerobic conditions, ocean,99 104 flux of elemental sulfur produced by photolysis 30−32,34 due to the higher density of microbial compared to of SO2, and sulfate concentrations in the Archean − − water.92,93 In oxic sediment samples a decrease of NCS seawater,105 107 we have estimated concentration of poly- concentration was observed already in <12 h. In the samples fi 108 − − sul des, the most reactive zerovalent sulfur species in the with an initial NCS concentration ≤300 μmol·L 1, it was − · −1 − Archean ocean to be in the 4 40 nmol L range. Atmospheric completely degraded in 14 days. The rates of NCS reactions between and nitrogen compounds are decomposition under various redox conditions change in the fi thought to have led to the formation of free hydrogen same order as in water samples: oxic > sul dic > anoxic > cyanide,29,33 which is a precursor for the formation of ferruginous ≈ manganous (Figure 1c−e). Concentrations of − thiocyanate. Calculated thiocyanate concentration in the nitrate in the anoxic Red Sea sediments are ≤6.5 μmol·L 1 in − Archean ocean based on rates of formation of thiocyanate the upper 5 cm and <1 μmol·L 1 in the deeper sediments.94,95 from polysulfide and hydrogen cyanide17 and on rates of its In the anoxic sediments of Lake Kinneret concentrations of ∼ · −1 nitrate are ≤0.01 μmol·L−1.96 decomposition from this work is 6.5 nmol L . An important point to note is that despite the very low concentration of Comparison between Marine and Limnic Systems. In − ff NCS , the entire deposition flux of HCN, which was suggested contrast to water column, the di erences in thiocyanate 109 decomposition rates between limnic and marine sediments to be an important precursor of RNA, , and , is were minor (Figure 2b). The Lake Kinneret sediments are lost via this pathway, with likely implications for estimates of characterized by high concentration of methane (up to 3 mmol· cyanide concentrations.110 Work on a comprehensive model of L−1).96,97 Our results did not demonstrate any effect of the the coupled sulfur and cyanide cycles is ongoing, and will be the presence of methanogenic microorganisms on the rates of topic of a future publication.

1240 DOI: 10.1021/acs.est.7b04723 Environ. Sci. Technol. 2018, 52, 1234−1243 Environmental Science & Technology Article ■ AUTHOR INFORMATION (16) Kamyshny, A. Improved cyanolysis protocol for detection of zero-valent sulfur in natural aquatic systems. Limnol. Oceanogr.: Corresponding Author Methods 2009, 7, 442−448. *E-mail: [email protected]. (17) Luthy, R. G.; Bruce, S. G., Jr. Kinetics of reaction of cyanide and ORCID reduced sulfur species in aqueous solutions. Environ. Sci. Technol. 1979, 13, 1481−1487. Alexey Kamyshny Jr.: 0000-0002-1053-2858 (18) Dzombak, D. A.; Ghosh, R. S.; Young, T. C. In Cyanide in Water Notes and ; Dzombak, D. A., Ghosh, R. S., Wong-Chong, G. M., Eds.; − The authors declare no competing financial interest. CRC Press: Boca Raton, 2006; pp 57 92. (19) Kamyshny, A.; Zerkle, A. L.; Mansaray, Z. F.; Ciglenecki,̌ I.; Bura-Nakic,́ E.; Farquhar, J.; Ferdelman, T. G. 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