Kinetics of Decomposition of Thiocyanate in Natural AquaticSystemsIrina 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 inwaters and sediments of marine and limnic systems under variousredox conditions, oxic, anoxic (nonsulfidic, nonferruginous,nonmanganous), ferruginous, sulfidic, and manganous, for up to200-day period at micromolar concentrations of thiocyanate. Thedecomposition rates in natural aquatic systems were found to becontrolled by microbial processes under both oxic and anoxicconditions. The Michaelis−Menten model was applied fordescription of the decomposition kinetics. The decompositionrate in the sediments was found to be higher than in the watersamples. Under oxic conditions, thiocyanate degradation was fasterthan under anaerobic conditions. In the presence of hydrogensulfide, the decomposition rate increased compared to anoxicnonsulfidic conditions, whereas in the presence of iron(II) or manganese(II), the rate decreased. Depending on environmentalconditions, half-lives of thiocyanate in sediments and water columns were in the ranges of hours to few dozens of days, and fromdays to years, respectively. Application of kinetic parameters presented in this research allows estimation of rates of thiocyanatecycling and its concentrations in the Archean ocean.

■ INTRODUCTION

Thiocyanate (NCS−) is formed in various natural and industrialprocesses. It was found in waste waters from coal and oilprocessing, steel manufacturing, and the petrochemicalindustry.1−5 Thiocyanate concentrations of up to 17 mmol·L−1 were detected in coal plant wastewaters4,6 and in goldextraction wastewaters.7,8 In electroplating, dyeing, photo-finishing, thiourea, and pesticide production the concentrationof NCS− in wastewater effluents is in the range of 0.09−2mmol·L−1.9 Thiocyanate is toxic to aquatic species with LC50

values of 0.01 to 0.5 mmol·L−1 reported for Daphnia magna.10

Natural sources of thiocyanate include plants, biological andabiotic decomposition of organic matter, and in vivodetoxification of cyanide.11−14 Several species of bacteria,algae, fungi, plants, and animals are physiologically capable ofdetoxifying cyanide, and in most cases one of the end productsof detoxification is thiocyanate.10,15 Another importantmechanism of thiocyanate formation in natural aquatic systemsis the reaction between hydrogen cyanide and sulfide oxidationintermediates, which contain sulfur−sulfur bonds, such ascolloidal sulfur,16 polysulfides,17 thiosulfate, and tetrathio-nate.18,19 Reaction with thiosulfate is ∼1000 times slowerthan reaction with polysulfides,17,20,21 and is catalyzed byCu(II) and sulfur transferases from the rhodanese family.15,22

Concentrations of hydrogen cyanide in polluted aquaticsystems may reach levels toxic to aquatic life.23 In nonpollutedaqueous systems, hydrogen cyanide concentrations are usuallyvery low due to fast degradation by plants, fungi and bacteria in

aquatic systems, as well as to chemical transformations,volatilization and adsorption.24−26

The presence of thiocyanate was recorded in various naturalnonpolluted aquatic systems, for example in stratified lakesRogoznica in Croatia (up to 288 nmol·L−1) and Green Lake(NY, USA) (up to 274 nmol·L−1).19 In these lakes thiocyanateis produced in the anoxic, sulfide-rich sediments and diffuses tothe chemocline, where it is consumed by oxidative processes,which are likely biologically enhanced. In the oxic North Seawater thiocyanate was detected at concentrations up to 13nmol·L−1.16 In saltmarsh sediment of the Delaware GreatMarsh, thiocyanate concentrations are up to 2.28 μmol·L−1 inpore-water and up to 15.6 μmol·kg−1 in wet sediment.26 Inthese sediments, concentrations of thiocyanate precursors,cyanide-reactive zerovalent sulfur and free hydrogen cyanide areas high as 78 μmol·L−1 and 1.9 μmol·L−1, respectively.Coexistence of hydrogen cyanide, polysulfides and thiocyanateallows attribution of thiocyanate formation to the abioticreactions between hydrogen cyanide and reduced sulfur species.Thiocyanate was also found in concentrations 23−40 μmol·L−1in the Red Sea Atlantis II Deep brine.27 Reactions betweenabiotically formed hydrogen cyanide and reduced sulfur specieswere proposed as the source of thiocyanate in the brine. The

Received: September 17, 2017Revised: December 25, 2017Accepted: December 28, 2017Published: December 28, 2017

Article

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

© 2017 American Chemical Society 1234 DOI: 10.1021/acs.est.7b04723Environ. Sci. Technol. 2018, 52, 1234−1243

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same processes were proposed to result in thiocyanateformation in the hydrothermal springs and pools in theYellowstone National Park, where it was detected atconcentrations 133−791 μmol·L−1.28

Although concentrations of thiocyanate in modern aquaticsystems are low,16,19,26,28 this may be not the case for the iron-rich water column of the Archean ocean. Existence of largeatmospheric fluxes of both hydrogen cyanide and zerovalentsulfur to Archean ocean has been suggested.29−34 These worksprovide constraints on cyanide and zerovalent sulfur fluxes butlack of data regarding rates of thiocyanate degradation underenvironmental conditions in the presence of dissolved iron(II)prevents estimation of thiocyanate concentrations and its fate inthe Archean ocean.Multiple investigations focused on the isolation and

identification of microorganisms that are responsible forthiocyanate biodegradation under controlled conditions.35−52

Thiocyanate-degrading bacteria have been isolated fromactivated sludge,41 steel plant wastewater,53 gold mine tailingsites,43,50,51 and extreme alkaline54 and hypersaline55,56 environ-ments. The end products of NCS− degradation are ammonium,carbon dioxide, and sulfate, subsequent to the formation ofcyanate57−62 or carbonyl sulfide63−67 as intermediates. A varietyof autotrophic bacteria are capable of using NCS− as their soleenergy source via sulfur oxidation. Chemolithotrophic bacteriautilize hydrogen sulfide formed on the initial step of NCS−

degradation and products of its incomplete oxidation(polysulfide, elemental sulfur, or thiosulfate) as an energysource for growth, oxidizing sulfide to sulfate.41,63,68,69

Utilization of nitrogen released from thiocyanate as ammoniahas also been reported.58 A number of heterotrophic bacteriautilize NCS− as a source of nitrogen and sulfur46,50,52,70,71 aswell as energy source.38,44 Heterotrophic bacteria were shownto utilize thiocyanate at concentrations as high as 100 mmol·L−1.70

In biotechnological systems for thiocyanate removal, whichare operating under high concentrations of thiocyanate (up to120 mmol·L−1 and oxic conditions10,36,43,72−79), rates ofthiocyanate decomposition are high. Under oxic conditions

the rates may be as high as 83 mmol·L−1·d−1 at 1 mmol·L−1

concentration of thiocyanate (Table 1). Thiobacillus speciesisolated from steel plant wastewater, are able to degrade 5.2mmol·L−1 of NCS− over 8 days under anaerobic denitrifyingconditions.53 Rates of thiocyanate degradation depend not onlyon oxygen concentrations,3,53,80,81 but also on concentrations ofnutrients. It was shown that concentrations of NH3 > 70 μmol·L−1 may inhibit76 and phosphate concentrations >500 μmol·L−1 may stimulate thiocyanate biodegradation.8

Currently, metabolic pathways for thiocyanate degradationare known and the rates of its degradation in bioreactors arepublished, but no data on kinetics of decomposition ofthiocyanate in natural aquatic systems is available. The mainaim of the present research is to fill this gap and to provideconstraints on rates of decomposition of thiocyanate in limnicand marine water columns and sediments at various redoxconditions, which are relevant for modern and ancient naturalaquatic systems. To achieve this goal, we have determinedkinetic parameters of thiocyanate degradation in natural aquaticand sedimentary systems at various salinities and concen-trations of thiocyanate, oxygen, hydrogen sulfide, and iron(II).

■ MATERIALS AND METHODS

Materials. Solutions for measurements of the kineticsparameters of thiocyanate degradation were prepared in Milli-Qwater, Mediterranean Sea water, Red Sea water, Lake Kinneret(Lake Tiberias) water. Slurries were prepared from Red Sea andLake Kinneret sediments. All reagents were purchased fromSigma-Aldrich and were at least 98% pure. Potassiumthiocyanate (KSCN) (99%), sodium sulfide nonahydrate(Na2S·9H2O) (98%), and iron(II) sulfate heptahydrate(FeSO4·7H2O) (99%) were used without further purification.Nitrogen gas (99.999%) was purchased from Maxima ltd, Israel.Test tubes, screw caps with hole and septum, and aluminumcaps were purchased from Romical, Ltd., Israel, and Labco, Ltd.,UK; butyl rubber stoppers were purchased from Geo-MicrobialTechnologies, Inc., USA.

Samples Preparation and Treatment. Water andsediment samples were collected from various locations in

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

system conditions [NCS−]o (mmol·L−1) rate (μmol·L−1·d−1) ref

Lake Kinneret and Mediterranean Sea water oxic 0.003 0.026−0.23 this workanoxic 0.003 0.0048−0.021 this work

Lake Kinneret and Red Sea sediment oxic 0.003 2.1−2.4 this workanoxic 0.003 0.0074−0.023 this work

gold mine tailing storage facility microbial consortium in synthetic medium oxic 0.003 ∼5.4 43activated sludge mixed liquor oxic 0.003 110 72wastewater with cultivated microorganisms oxic 0.003 2800 36Lake Kinneret and Mediterranean Sea water oxic 1 0.43−0.90 this work

anoxic 1 0.034−0.34 this workLake Kinneret and Red Sea sediment oxic 1 45−49 this work

anoxic 1 0.078−0.61 this workgold mine tailing storage facility microbial consortium in synthetic medium oxic 1 ∼1700 43activated sludge mixed liquor oxic 1 2100 72wastewater with cultivated microorganisms oxic 1 82500 36water enrichment with Klebsiella species oxic 0.4−3.9 ∼860 79enrichment cultures from steel plant wastewater oxic 5.7 ∼1.9 53enrichment cultures from steel plant wastewater anoxic 4.7−5.6 ∼0.79 53activated sludge anoxic 1.7 0 3brine liquor with mixed methanogenic cultures anoxic 2.5 0 80a simulated wastewater containing phenol, thiocyanate, and ammonia-nitrogen anoxic 1.9−10.3 0 81

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Israel (Tables 2 and 3). Sediment cores and water samples werecollected from the Red Sea (29°30′N, 34°55′E), theMediterranean Sea (32°49′N, 34°59′E), and Lake Kinneret(32°50′N, 35°35′E) in May 2015−December 2016. Sedimentsamplings were performed with a multicorer, Lake Kinneret,and Red Sea waters were sampled with Niskin bottles,Mediterranean Sea water was sampled manually near theshore. The water and cores were stored at 25 ± 1 °C in thedark and processed in <1 day after sampling.The rates of decomposition of thiocyanate in water were

measured in the following sets of samples: (1) oxic watersample without pretreatment; (2) anoxic, nonsulfidic watersamples, which were stripped of oxygen or hydrogen sulfide bypurging for 90 min with nitrogen in a glovebag; (3) ferruginous,prepared by adding of iron sulfate to the target concentration100 μmol·L−1 of Fe(II); (4) sulfidic, prepared by addingsodium sulfide to the target concentration 100 μmol·L−1 ofS(II) and 50 μmol·L−1 H2SO4 for pH adjustment (Table 2).Nonautoclaved water samples were distributed to 12 mL testtubes. The tubes were filled without a headspace andhermetically closed using a screw cap with hole and septum.KSCN was injected into the test tubes with samples to thefollowing target concentrations: 3, 10, 30, 100, and 300 μmol·L−1.The rates of decomposition of thiocyanate in the sediments

were measured in the samples from the locations presented inTable 3. Both Red Sea (Gulf of Aqaba) water and sedimentcores were sampled at 561 m water depth. The cores weresectioned into slices: 1−2 cm (oxic), 8−12 cm (manganous),20−24 cm (ferruginous), and 30−34 cm (anaerobic zone with[H2S], [Fe

2+], [Mn2+] < 1.5 μmol·L−1). Sulfidic Lake Kinneretwater and sediment cores were sampled below the chemoclineat 37 m depth. The cores were sectioned into slices: 5−10 cm(sulfidic), 12−17 cm (anaerobic zone, [H2S], [Fe

2+], [Mn2+] <2.5 μmol·L−1), and 20−25 cm (ferruginous zone). Additionalcore was sampled above the chemocline at 32 m water depthfor oxic (upper 0−5 mm) sediment layer.For experiments under anoxic conditions, the cores were cut

under a constant flow of nitrogen and immediately transferredto a glovebag with N2 atmosphere. For killed controlexperiments, marine and limnic waters were sterilized byautoclaving at 120 ± 3 °C for 20 min to prevent the effect ofmicrobial community from the water column on thedegradation rate in sediment samples. Sediments were diluted(1:1) with autoclaved bottom water (except for oxic Kinneretsediment, which was diluted with autoclaved oxic water from 1m depth) and transferred to the 50 mL test tubes, which werehermetically closed using a hand crimper with a rubber stopperand aluminum cap. For experiments under simulated anoxicconditions, autoclaved oxic seawater and sulfidic limnic water

were purged with nitrogen under a nitrogen atmosphere in aglovebag. Sulfidic conditions were simulated by addition of thesodium sulfide as described above. After distribution to the testtubes, slurry samples were spiked by KCSN solution to thetarget concentrations of NCS− in slurry pore-waters: 3, 10, 30,100, 300, and 1000 μmol·L−1. The rates of NCS−

decomposition at concentrations >1 mmol·L−1 were notmeasured as (1) these concentrations are not relevant fornatural aquatic systems and (2) some works36,73 report that atthese concentrations the microbial decomposition of thiocya-nate is substrate-inhibited; although there is also evidence forhigh thiocyanate decomposition rates at higher concentrations.For each water and sediment sample, an identical sample

autoclaved at 120 ± 3 °C for 20 min was prepared in order toprovide a sterilized control. All types of autoclaved sampleswere prepared in 35 mL (water samples) and in 50 mL(sediment samples) tubes and were hermetically closed with arubber stopper and aluminum cap.All sterilized and nonsterilized samples were prepared and

analyzed in triplicates. Hermetically closed samples wereincubated at 25 ± 1 °C. Subsamples were taken from thesamples by syringes immediately prior to analysis. Subsamplingof anoxic samples was carried out in the glovebag (typically<0.2% O2 v/v) to maintain anoxic conditions in the sample.The rate of thiocyanate decomposition was studied bymeasurement of thiocyanate concentrations in multiplesubsamples during 35−200 day period.

Analytical Methods. Thiocyanate was quantified by anAgilent Technologies 1200 HPLC system with multiplewavelength UV−visible detector operated at 220 nm. ANomura Chemical, Japan, Develosil RPAQUEOUS C30reverse phase column (150 mm × 4.6 mm × 5 mm) wasused for HPLC separation of thiocyanate. The column wasmodified according to Rong et al.82 by pumping 5% aqueoussolution of PEG-20 000 at 0.3 mL·min−1 rate for at least 3 h.Hydrogen sulfide was measured spectrophotometrically by themethylene blue method according to Cline83 by LaMotteSMART Spectro spectrophotometer. Fe2+ was quantifiedspectrophotometrically by ferrozine method according toStookey.84 Manganese was analyzed spectrophotometricallyusing the 1-(2-Pyridylazo)-2-naphthol (PAN) method.85 Oxy-gen level was monitored using an optical oxygen meter with aRetractable Needle-Type Oxygen microsensor (tip diameter∼50 μm, MDL of 0.625 μmol·L−1, Firesting-Pyroscience)placed on a micromanipulator.86 Data was collected viamicroprofiling software (Profix) with 2-point calibration. Theoptode needle was inserted into the sample through the septumof the HPLC-vial which was filled and closed in the glovebag.

Approach for Estimation of NCS− Degradation Rate.Quantitative interpretation of biodegradation kinetics is based

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

sampleno. system

depth(m) sampling date

initialconditions treatment final conditions

WC-1 Lake Kinneret 1 17 Jun, 2015 oxic no oxic, pH 8.1WC-2 Lake Kinneret 37 17 Jun, 2015 sulfidic N2 purge [O2] < 1 μmol·L−1, [H2S] < 1 μmol·L−1, pH 7.8WC-3 Lake Kinneret 37 17 Jun, 2015 sulfidic no sulfidic ([H2S] = 35 μmol·L−1), pH = 7.7WC-4 Lake Kinneret 37 17 Jun, 2015 sulfidic N2 purge, FeSO4 spiking ferruginous ([Fe(II)] = 81 μmol·L−1), pH 7.9WC-5 Mediterranean Sea 1 17 May, 2015 oxic no oxic, pH 8.4WC-6 Mediterranean Sea 1 17 May, 2015 oxic N2 purge [O2] < 1 μmol·L−1, pH 8.4WC-7 Mediterranean Sea 1 17 May, 2015 oxic N2 purge, Na2S spiking sulfidic ([H2S] = 118 μmol·L−1), pH 8.3WC-8 Mediterranean Sea 1 17 May, 2015 oxic N2 purge, FeSO4 spiking ferruginous ([Fe(II)] = 95 μmol·L−1), pH 8.7

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on substrates degradation via catalyzed reactions, which arecarried out by the organisms bearing the specific enzymes.Therefore, rates of substrate degradation are generally depend-ent on the enzyme and substrate concentrations (e.g.,Michaelis−Menten kinetics model).In natural aquatic systems degradation of thiocyanate may be

performed by a single organism, as well as by microbialconsortium. It has been shown that the Michaelis−Mentenmodel87 (eq 1) can be applied for description of microbialutilization of cyanide and thiocyanate in activated sludgereactors,3 as well as for determination of the effect ofconcentration of organic pollutants on their biodegradationrate by natural microbial communities.88 Thus, in this study wewill define “apparent” parameters of Michaelis−Menten model,which correspond to degradation of thiocyanate by nondefinedmicrobial community. Katayama et al.63 showed thatthiocyanate-degradation catalyzed by enzyme isolated fromThiobacillus thioparus cells, followed Michaelis−Menten-typekinetics. In this work, the Michaelis−Menten model wasapplied to nonautoclaved samples.

=+

VV

K[S]

[S]max

(1)

where V is the rate of thiocyanate decomposition at the givenconcentration (μmol·L−1·day−1), Vmax is the apparent maximumrate of thiocyanate decomposition (μmol·L−1·day−1), K is theapparent half-saturation constant (corresponding to thesubstrate concentration at which the reaction rate is 50% ofthe Vmax (μmol·L

−1), 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 decreaseof concentration versus time. An overall dependence wasestablished by plotting the calculated thiocyanate degradationrates versus initial thiocyanate concentrations. For estimation ofthe specific degradation rate, reaction rate was measured onlyon the initial stage of thiocyanate degradation, wherethiocyanate degradation rate had linear dependence on time.Apparent Vmax and K values were calculated by fitting curves todata using nonlinear regression and performing a nonlinear fitanalysis in MATLAB.

■ RESULTS AND DISCUSSION

In all sterilized samples (water and sediments), the variation ofthiocyanate concentration was <3% of initial concentrationduring the whole incubation period (data not shown). Thisindicates chemical stability of thiocyanate in aquatic systems ina wide range of environmentally relevant conditions, forexample, in the presence as well as in the absence of sediments,oxygen, hydrogen sulfide, and dissolved iron in marine, as wellas in limnic waters.In all nonautoclaved samples with initial thiocyanate

concentrations of 3 μmol·L−1, decomposition was not observedduring the first 26−100 days of incubation, except for oxicsediments and some oxic Mediterranean seawater samples inwhich the lag periods were <12 h and <12 days, respectively(Table 4). With an increase of NCS− concentrations, the lagperiod increased by 25−63%. After the lag period, thethiocyanate concentrations decreased in all nonsterilizedsamples. The lag period likely reflects the time which isrequired for adaptation to a new substrate and an increase inT

able

3.SamplingandProcessingProtocolsforPreparation

ofSedimentSamples

sample

no.

system

depth

(m)

depthbsf

(cm)

sampling

date

initial

conditions

treatm

ent

finalconditions

S-1

Lake

Kinneret

320−

0.5

1Dec,2016

oxic

dilutio

nwith

water

oxic,p

H8.0

S-2

Lake

Kinneret

3712−17

1Dec,2016

anoxic

dilutio

nwith

N2-purged

water

[O2]<1μm

ol·L

−1 ,[H

2S]=2.5μm

ol·L

−1 ,[Fe(II)]

=0.5μm

ol·L

−1 ,[M

n(II)]

=0.5μm

ol·L

−1 ,pH

7.6

S-3

Lake

Kinneret

375−

101Dec,2016

sulfidic

dilutio

nwith

sulfidicwater

sulfidic([H

2S]=39

μmol·L

−1 ,[Fe(II)]

=0.5μm

ol·L

−1 ,[M

n(II)]

=0.5),p

H7.5

S-4

Lake

Kinneret

3720−25

1Dec,2016

ferruginous

dilutio

nwith

N2-purged

water

ferruginous([Fe(II)]=40

μmol·L

−1 ,[M

n(II)]

=2μm

ol·L

−1 ),p

H7.8

S-5

Red

Sea

561

0−2

20Sep,

2016

oxic

dilutio

nwith

water

oxic,p

H8.8

S-6

Red

Sea

561

30−34

20Sep,

2016

anoxic

dilutio

nwith

N2-purged

water

[O2]<1μm

ol·L

−1 ,[H

2S]=1.5μm

ol·L

−1 ,[Fe(II)]

=0.5μm

ol·L

−1 ,[M

n(II)]

=0.5μm

ol·L

−1 ,pH

8.4

S-7

Red

Sea

561

30−34

20Sep,

2016

anoxic

dilutio

nwith

N2-purged

water,N

a 2S

spiking

sulfidic([H

2S]=75

μmol·L

−1 ,[Fe(II)]

=1.5μm

ol·L

−1 ,[M

n(II)]

=1μm

ol·L

−1 ),p

H8.6

S-8

Red

Sea

561

20−24

20Sep,

2016

ferruginous

dilutio

nwith

N2-purged

water

ferruginous([Fe(II)]=37

μmol·L

−1 ,[M

n(II)]

=2.5μm

ol·L

−1 ),p

H8.7

S-9

Red

Sea

561

8−12

20Sep,

2016

manganous

dilutio

nwith

N2-purged

water

manganous

([Fe(II)]=2μm

ol·L

−1 ,[M

n(II)]

=35

μmol·L

−1 ),p

H8.3

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cell concentrations as a response to thiocyanate amend-ment.43,51

On the basis of the specific degradation rate at each initialsubstrate concentration, the apparent kinetic parameters of theMichaelis−Menten model for each analyzed system weredetermined (Table 5). Experimental rates and the model dataversus initial NCS− concentration were plotted; the thiocyanatedecomposition rates and their Michaelis−Menten model fits arepresented in Figure 1. Apparent parameters of the Michaelis−Menten model were used to calculate thiocyanate half-lives atvarious concentrations (Figure 2). The lag time was notincluded in determination of the half-life time.Degradation of NCS− in Water Columns. Influence of

redox conditions. The thiocyanate degradation rates in LakeKinneret waters decreased in the following order: oxic > sulfidic> anoxic > ferruginous (Figures 1a and 2a). In seawatersamples, the trend was similar: oxic > sulfidic ≈ anoxic >ferruginous (Figures 1b and 2a). Relatively low rate ofthiocyanate degradation under anaerobic conditions is charac-teristic for thiocyanate-decomposing bacteria and may beexplained by lower yield of metabolic energy associated withutilization of electron acceptors, which are weaker thanoxygen.53,59,89 Since the only electron acceptor proven tosupport thiocyanate oxidation by bacteria in the absence ofoxygen is nitrate, degradation of thiocyanate in these systems islikely to be nitrate-limited. In the anoxic waters of LakeKinneret, nitrate concentrations are <37 μmol·L−1, but can beas well <4 μmol·L−1 in the benthic boundary layer.90 The

difference in thiocyanate decomposition rates in the absenceand in the presence of dissolved iron and hydrogen sulfide maybe attributed to differences in microbial community structure inthe presence of different electron donors. Calculatedconcentrations of thiocyanate-iron complex, Fe(SCN)+, are<0.08 μmol·L−1. This concentration corresponds to the samplewith the highest concentrations of Fe2+ (95 μmol·L−1) andthiocyanate (1 mmol·L−1) and the stability constant of 0.84mol−1·L for Fe(SCN)+ complex.91 Therefore, iron complex-ation should not significantly affect the observed decrease ofiron or thiocyanate concentrations.

Comparison between Marine and Limnic Systems. In oxicMediterranean Sea water, the thiocyanate half-life was shorterthan in oxic Lake Kinneret water. We attribute this difference tofaster adaptation of local microbial communities in seawater toan increase in NCS− concentrations. This explanation issupported by longer lag periods observed in the case of oxiclimnic water. Another support for this explanation comes fromcomparison of thiocyanate degradation rates in the presence ofhydrogen sulfide. In Lake Kinneret water, which was sulfidicduring the sampling, degradation rates were higher than in theMediterranean Sea water, which was oxic at the time ofsampling but was amended with hydrogen sulfide. In the lattercase, the microbial community has to adapt to drasticallychanged conditions. Our observations show that the influenceof salinity on thiocyanate degradation rates is less pronouncedfor all systems than influence of oxygen.

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 142lag time (d) 37 74 58 72

Mediterranean Sea water incubation period (d) 164 164 130 141lag time (d) <12 79 71 75

Lake Kinneret sediment incubation period (d) 35 150 150 150lag time (d) <1 46 35 45

Red Sea sediment incubation period (d) 35 157 157 157 157lag time (d) <1 35 26 45 45

Table 5. Coefficients of the Michaelis−Menten Equationa

sample no. system initial conditions final conditions K (μmol·L−1) Vmax (μmol·L−1·day−1)

WC-1 LK oxic oxic 48 ± 11 0.450 ± 0.032WC-2 LK sulfidic anoxic 59 ± 17 0.145 ± 0.014WC-3 LK sulfidic sulfidic 48 ± 13 0.355 ± 0.030WC-4 LK sulfidic ferruginous 29 ± 10 0.052 ± 0.006WC-5 MS oxic oxic 9 ± 3 0.905 ± 0.07WC-6 MS oxic anoxic 31 ± 8 0.167 ± 0.010WC-7 MS oxic sulfidic 75 ± 20 0.251 ± 0.023WC-8 MS oxic ferruginous 18 ± 3 0.035 ± 0.006S-1 LK oxic oxic 61 ± 10 52 ± 3S-2 LK anoxic anoxic 57 ± 20 0.351 ± 0.029S-3 LK sulfidic sulfidic 89 ± 29 0.663 ± 0.039S-4 LK ferruginous ferruginous 28 ± 8 0.081 ± 0.006S-5 RS oxic oxic 65 ± 24 48 ± 2S-6 RS anoxic anoxic 58 ± 12 0.356 ± 0.019S-7 RS anoxic sulfidic 69 ± 21 0.575 ± 0.044S-8 RS ferruginous ferruginous 55 ± 18 0.155 ± 0.014S-9 RS manganous manganous 51 ± 14 0.166 ± 0.021

aWC, water column; S, sediment; LK, Lake Kinneret; MS, Mediterranean Sea; RS, Red Sea.

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

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Degradation of NCS− in Sediments. Influence of RedoxConditions. In both marine (Red Sea) and limnic (LakeKinneret) sediments, NCS− degradation was found to be fasterthan in aquatic samples, especially under aerobic conditions,due to the higher density of microbial biomass compared towater.92,93 In oxic sediment samples a decrease of NCS−

concentration was observed already in <12 h. In the sampleswith an initial NCS− concentration ≤300 μmol·L−1, it wascompletely degraded in 14 days. The rates of NCS−

decomposition under various redox conditions change in thesame order as in water samples: oxic > sulfidic > anoxic >ferruginous ≈ manganous (Figure 1c−e). Concentrations ofnitrate in the anoxic Red Sea sediments are ≤6.5 μmol·L−1 inthe upper 5 cm and <1 μmol·L−1 in the deeper sediments.94,95

In the anoxic sediments of Lake Kinneret concentrations ofnitrate are ≤0.01 μmol·L−1.96

Comparison between Marine and Limnic Systems. Incontrast to water column, the differences in thiocyanatedecomposition rates between limnic and marine sedimentswere minor (Figure 2b). The Lake Kinneret sediments arecharacterized by high concentration of methane (up to 3 mmol·L−1).96,97 Our results did not demonstrate any effect of thepresence of methanogenic microorganisms on the rates of

thiocyanate degradation. This observation agrees well with theresults reported by Hung and Pavlostathis80 and Sahariah andChakraborty,81 who found that thiocyanate is stable under themethanogenic conditions.

Comparison of Thiocyanate Degradation Rates inNatural Systems and under Controlled Conditions. Compar-ison of thiocyanate decomposition rates reported in presentwork and those calculated for the same range of thiocyanateconcentrations from kinetic parameters measured undercontrolled conditions are presented in Table 1. The rates ofdecomposition in nonpolluted natural aquatic systems areexpected to be much lower than in the industrial systems due to(1) much lower microbial density and (2) lower concentrationsof nutrients. Indeed, rates of thiocyanate decomposition in oxicsediments were found to be lower by 2−4.5 orders ofmagnitude as compared to activated sludge and wastewatermicrobial cultures.36,43,72 Under anoxic conditions, NCS−

decomposition generally was not detected in industrialsystems,3,80,81 except for steel plant wastewater with highconcentrations of NCS− (4.7−5.6 mmol·L−1).53 Rates ofthiocyanate decomposition calculated from the data presentedby Grigor’eva et al.53 are only slightly higher than thosedetected 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, detailedunderstanding of processes controlling stability of thiocyanatein natural aquatic systems is lacking. Future work shouldinclude detection of microbial species responsible forthiocyanate degradation in natural aquatic systems, evaluationof microbial community shifts as a response to thiocyanatepollution and identification of specific metabolic pathways ofthiocyanate degradation under various environmental con-ditions.

Implications for the Archean Oceans. The Michaelis−Menten model for the ferruginous Mediterranean seawater wasapplied to estimate the steady-state concentration ofthiocyanate in the Archean Ocean. Ferruginous conditionsmay have been a dominant characteristic of the anoxic oceanicwater column throughout much of Earth’s history.98 Based onestimated concentration of iron in the deep Archeanocean,99−104 flux of elemental sulfur produced by photolysisof SO2,

30−32,34 and sulfate concentrations in the Archeanseawater,105−107 we have estimated concentration of poly-sulfides,108 the most reactive zerovalent sulfur species in theArchean ocean to be in the 4−40 nmol·L−1 range. Atmosphericreactions between methane and nitrogen compounds arethought to have led to the formation of free hydrogencyanide,29,33 which is a precursor for the formation ofthiocyanate. Calculated thiocyanate concentration in theArchean ocean based on rates of formation of thiocyanatefrom polysulfide and hydrogen cyanide17 and on rates of itsdecomposition from this work is ∼6.5 nmol·L−1. An importantpoint to note is that despite the very low concentration ofNCS−, the entire deposition flux of HCN, which was suggestedto be an important precursor of RNA, proteins, and lipids,109 islost via this pathway, with likely implications for estimates ofcyanide concentrations.110 Work on a comprehensive model ofthe coupled sulfur and cyanide cycles is ongoing, and will be thetopic of a future publication.

Figure 2. Estimated half-lives of thiocyanate degradation in aquatic (a)and sedimentary systems (b). Solid lines represent seawater samples;dashed lines represent limnic samples. Black color represents samplesunder oxic conditions, red color represents samples under anoxicconditions, green color represents samples under sulfidic condition,blue color represents samples under ferruginous conditions, andpurple color represents samples under manganous conditions.

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■ AUTHOR INFORMATION

Corresponding Author*E-mail: alexey93@gmail.com.

ORCID

Alexey Kamyshny Jr.: 0000-0002-1053-2858NotesThe authors declare no competing financial interest.

■ ACKNOWLEDGMENTS

This work was supported by the Marie Curie Actions CIGPCIG10-GA-2011-303740 (ThioCyAnOx) Grant. I.H. ac-knowledges a Starting Grant (337183) from the EuropeanResearch Council. The authors would like to thank WernerEckert, Asaph Rivlin, Valeria Boyko, and Hanni Leibowitz forhelp with natural water and sediment sampling and Orit Sivanand Ariel Kushmaro for help with samples processing andanalyses.

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