Reductive Outer-Sphere Single Electron Transfer Is an Exception

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Reductive Outer-sphere Single Electron Transfer Is an Exception Rather than the Rule in Natural and Engineered Chlorinated Ethene Dehalogenation Benjamin Heckel, Stefan Cretnik, Sarah Kliegman, Orfan Shouakar-Stash, Kristopher McNeill, and Martin Elsner Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b01447 • Publication Date (Web): 20 Jul 2017 Downloaded from http://pubs.acs.org on July 21, 2017

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Environmental Science & Technology

1

Reductive Outer-sphere Single Electron Transfer Is

2

an Exception Rather than the Rule in Natural and

3

Engineered Chlorinated Ethene Dehalogenation

4

Benjamin Heckela, Stefan Cretnika, Sarah Kliegmanb, Orfan Shouakar-Stashc, Kristopher

5

McNeilld, Martin Elsner a, e*

6

a

7

Neuherberg, Germany

8

b

9

CA 91711

Institute of Groundwater Ecology, Helmholtz Zentrum München, Ingolstädter Landstr. 1, 85764

W. M. Keck Science Department, Claremont McKenna, Pitzer, and Scripps Colleges Claremont,

10

c

11

d

12

Switzerland.

13

e

14

Marchioninistrasse 17, D-81377 Munich, Germany.

Department of Earth Sciences, University of Waterloo, Waterloo, Ontario, Canada N2L 3G1 Institute of Biogeochemistry and Pollutant Dynamics (IBP), ETH Zurich, CH-8092 Zurich,

Chair of Analytical Chemistry and Water Chemistry, Technical University of Munich,

15 16

KEYWORDS Outer-sphere single electron transfer; reductive dehalogenation; dehalogenation

17

mechanism; radicals; kinetic isotope effect; compound-specific isotope analysis; groundwater

ACS Paragon Plus Environment

1


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1

contamination; chlorinated ethenes; trichloroethene, tetrachloroethene, dichloroethene,

2

chloroform; remediation; zero-valent iron; biodegradation;

3

ABSTRACT

4

Chlorinated ethenes (CEs) such as perchloroethylene, trichloroethylene and dichloroethylene are

5

notorious groundwater contaminants. Although reductive dehalogenation is key to their

6

environmental and engineered degradation, underlying reaction mechanisms remain elusive.

7

Outer-sphere reductive single electron transfer (OS-SET) has been proposed for such different

8

processes

9

dehalogenation. Compound-specific isotope effect (13C/12C,

as

Vitamin

B12-dependent

biodegradation

and 37

zero-valent

metal-mediated

Cl/35Cl) analysis offers a new

10

opportunity to test these hypotheses. Defined OS-SET model reactants (CO2 radical anions, S2--

11

doped graphene oxide in water) caused strong carbon (εC = -7.9‰ to -11.9‰), but negligible

12

chlorine isotope effects (εCl = -0.12‰ to 0.04‰) in CEs. Greater chlorine isotope effects were

13

observed in CHCl3 (εC = -7.7‰, εCl =-2.6‰), and in CEs when the exergonicity of C-Cl bond

14

cleavage was reduced in an organic solvent (reaction with arene radical anions in glyme).

15

Together, this points to dissociative OS-SET (SET to a σ* orbital concerted with C-Cl breakage)

16

in alkanes compared to stepwise OS-SET (SET to a π* orbital followed by C-Cl cleavage) in

17

ethenes. The non-existent chlorine isotope effects of chlorinated ethenes in all aqueous OS-SET

18

experiments contrast strongly with pronounced Cl isotope fractionation in all natural and

19

engineered reductive dehalogenations reported to date suggesting that OS-SET is an exception

20

rather than the rule in environmental transformations of chlorinated ethenes.

21


2

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1


Introduction.

2

Groundwater contamination by chlorinated ethenes is a prominent environmental problem of

3

our time. Left by a legacy of improper handling and disposal, these compounds are among the

4

most commonly found groundwater contaminants1. While they are resistant to degradation, they

5

are susceptible to reductive dehalogenation under reducing conditions.

6

remediation schemes therefore aim at removing these contaminants under anoxic conditions,

7

either through enhanced natural biodegradation3, or by installing trenches of reactive granular

8

metal, in particular zero-valent iron4, 5. These reactions, unfortunately, do not always lead to

9

complete dehalogenation/detoxification. Biotransformation sequentially replaces the chlorine

10

substituents by hydrogen atoms (hydrogenolysis) so that perchloroethylene (PCE) and

11

trichloroethene (TCE) are converted to more problematic cis-dichloroethene (cis-DCE) and vinyl

12

chloride (VC) before non-toxic ethene is formed.6 Dehalogenation with zero-valent metal also

13

shows release of problematic daughter compounds, but involves a parallel vicinal-dichloro

14

elimination pathway where two chlorine substituents are removed, offering a more direct avenue

15

to benign end products.7 The underlying reasons for these different reaction pathways have

16

eluded researchers for years.8 Electrons must clearly be transferred in some form since less

17

halogenated, more reduced daughter compounds are formed. The nature of this electron transfer

18

(ET), however, has been subject of debate. Following a convention from transition metal

19

chemistry 9, inner-sphere-electron transfer (IS-SET) is conceptualized to occur if electrons are

20

transferred between chemically associated electron donors and electron acceptors (i.e., the CE). 10

21

By contrast, outer-sphere-electron transfer (OS-SET) takes place if the donor and acceptor are

22

not associated through a chemical bond during ET.

23

some distance, usually from the highest occupied molecular orbital (HOMO) of the electron

24

donor (or a conduction band of an electron-donating metal) into the lowest unoccupied molecular

11

2

Most groundwater

In OS-SET, electrons are transferred over


3


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1

orbital (LUMO) of the electron acceptor (the CE). These concepts of non-adiabatic outer-sphere

2

SET and adiabatic inner-sphere SET have been treated in comprehensive textbooks12 and reviews

3

13

, but are intrinsically difficult to pinpoint in environmental transformations.

4

To elucidate the underlying mechanism of biotransformation, numerous studies have focused

5

on cob(I)alamin (Vitamin B12)14, the co-factor present in almost all reductive dehalogenases

6

identified to date 15. Inner-sphere reaction has been proposed in the form of nucleophilic addition

7

or nucleophilic substitution reactions by cob(I)alamin with the chlorinated ethene14. By contrast,

8

single electron transfer (either inner or outer-sphere) was proposed based on the detection of

9

trichlorovinyl radicals in reaction of TCE with Vitamin B12

16-18

. Both hypotheses are supported

10

by recent insight from crystal structures of the first heterologously expressed dehalogenases 19-21.

11

Studies either favor outer-sphere SET, both for the reductive dehalogenase VcrA from

12

Dehalococcoides mccartyi Strain VS

13

Sulfurospirillum multivorans (based on a distance of 5.8 Ǻ between Co(II) and TCE)

14

Alternatively, an inner-sphere mechanism by attack of Co at the halogen atom is proposed based

15

on the detection of direct Co-Br interactions in the reductive dehalogenase NpRdhA of

16

Nitratireductor pacificus.20

19

and the reductive dehalogenase PceA from 21

.

17

Competing mechanistic hypotheses have also been proposed for CE transformation by zero-

18

valent metals. Besides “indirect” reactions with by-products of iron corrosion such as activated

19

hydrogen22 or Fe(II), direct electron transfer at the metal surface (or from a conducting metal

20

oxide layer) is commonly invoked. 4, 23-26 Inner-sphere ET in the form of complexes at the metal

21

surface was proposed based on reactivity trends

22

(OS)-SET transfer has been invoked based on the consideration that metals likely transfer

23

electrons one at a time and that metals in aqueous solution are covered by a passive oxide layer 4,

24

26, 29

7

and computational calculations

27, 28

, whereas

. OS-SET would also be consistent with the observation that most CE dehalogenation rates


4

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1

correlate with redox potentials derived from LUMOs and one-electron reduction potentials

2

(linear free energy relationships, LFERs)

3

different mechanisms32 so that they cannot uniquely answer the questions of underlying reaction

4

chemistry: which bonds are broken in the chlorinated ethenes, in what order are they broken, and

5

by attack of what reaction partner? Therefore, even though recent research has explored LFERs

6

(or quantitiative structure activity relationships, QSARs) as pragmatic approaches to forecast

7

transformation rates in the environment (33 and refs cited therein), a fundamental understanding

8

of underlying chemical reaction mechanisms – the knowledge that is crucial to tailor the

9

transformation chemistry of remediation schemes – has so far eluded researchers.

10

Multiple element (37Cl/35Cl,

13

25, 30, 31

. However, such LFERs may arise owing to

C/12C) isotope effect measurements are currently emerging as a

11

potential approach to close this gap34-38. Analytical advances39,

12

measure compound-specific isotope ratios of single chlorinated ethene compounds (e.g., PCE,

13

TCE) at their natural isotopic abundance in chemical model reactions and natural samples. At

14

natural abundance, such isotope ratios 13C/12C and

15

to an international reference material:

16

δ 13 C =

37

have made it possible to

Cl/35Cl are expressed as difference relative

( 13 C / 12 C Sample − 13 C / 12 C S tan dard ) 13

40

C / 12 C S tan dard

( 37 Cl / 35Cl Sample − 37 Cl / 35Cl S tan dard )

(1)

17

δ Cl =

18

∆δ 13 C = δ 13 C − δ 13 C initial

(3)

19

∆δ 37 Cl = δ 37 Cl − δ 37 Cl initial

(4)

37

37

Cl / 35Cl S tan dard

(2)

20

where 13C/12CSample and 13C/12CStandard are the isotope ratios of sample and international reference

21

standard, whereas δ13Cinital and δ13C and are isotope values at the beginning of a transformation

22

and a given time point, respectively. To determine isotope effects, these values are subsequently


5


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1

evaluated according to the Rayleigh equation41, which corresponds to analogous equations from

2

chemistry 42 43 for the case that isotope ratios are measured at natural abundance44

3

δ 13 C = δ 13 C initial + [ε C ⋅ ln f ]

4

Here f is the residual fraction of the substrate in a closed system (i.e. the concentration at time

5

point t divided through the concentration at time point zero). The resultant isotopic enrichment

6

factor εC is the equivalent of a compound-specific kinetic isotope effect: it expresses the

7

difference in reaction rates of molecules containing light and heavy isotopes, respectively. For

8

example, a value of -9‰ indicates that heavy isotopologues (with the label randomly distributed

9

across the molecule) reacted 9‰ (0.9%) more slowly than light isotopologues. This corresponds

10

to a compound-specific kinetic isotope effect of 12k/13k = 1.009. Equivalent expressions are valid

11

for the evaluation of chlorine isotope effects.45

12

(5)

Similar to classical position-specific isotope effect studies from (bio)chemistry

43, 46

,

13

compound-specific isotope effects reflect underlying transition states and, therefore, represent an

14

underexplored sensitive tool for distinguishing different reaction mechanisms. Mechanistic

15

distinction is easiest when isotope values of two elements are plotted against each other, because

16

the slope (here: λ = ∆δ13C/∆δ37Cl ≈ εC/εCl ≈ (1-12k/13k)/(1-35k/37k)) represents the compound-

17

specific isotope effects of the two elements relative to each other

18

increasing number of studies have reported compound-specific isotope effects εC, εCl and λ ≈

19

εC/εCl of chlorinated ethenes in biodegradation

20

and transformation by zero-valent iron

21

mechanistic insight until today because it did not include isotope effect reference data for defined

22

OS-SET reactions.

35, 54

36-38, 49-52

47, 48

. In recent years, an

, dehalogenation by Vitamin B12

36, 53

,

. This data, however has offered only limited


6

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To close this knowledge gap, we conducted outer-sphere SET reactions in water and in an

2

organic solvent, and measured associated changes in carbon and chlorine isotope values of

3

chlorinated ethenes. To facilitate OS-SET in water, we employed two systems: CO2 radical

4

anions55 and graphene oxide that had been doped with electrons from a sodium sulfide solution56.

5

CO2 radical anions transfer an electron to form stable CO2, whereas graphene oxide shuttles

6

electrons and protons from the donors (sulfide and water) to the acceptor (the chlorinated

7

ethene)57-59. In the organic solvent dimethoxyethane (glyme), OS-SET was modeled with radical

8

anions of naphthalene and pyrene, which readily transfer an electron to regain their aromaticity60.

9

All reagents have in common that they are not conducive to direct (inner-sphere) bond

10

interactions and are, therefore, regarded as outer-sphere single electron transfer agents.60 To

11

probe for differences in OS-SET between chlorinated alkenes and alkanes, an additional

12

experiment investigated the reaction of CO2 radical anions with chloroform. Finally, to test the

13

hypothesis that OS-SET is a common mechanism in different environmental dehalogenation

14

reactions, we compared our results to reported values for multi-element isotope fractionation of

15

chlorinated ethenes from dehalogenation by vitamin B12, by dehalogenating bacteria, and by iron

16

metal.

17 18

Materials & Methods

19

Chemicals.

20

A list of all chemicals is provided in the supporting information.

21

Reactions in Water.

22

Reactions with CO2 Radical Anions. To prepare reactions of CO2 radical anions with PCE,

23

TCE, cis-DCE and CHCl3, 40 mL vials were filled with 38 mL of deoxygenized water containing

24

the respective chlorinated target compound (10 µL, corresponding to between 0.09 mmol to 0.13


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mmol) together with sodium formate (1.2 g,17.5 mmol). Vials were kept closed and anoxic, were

2

stirred (300 rpm) and heated to 80°C. To start the reaction, one milliliter of sodium persulfate

3

dissolved in deoxygenized water (70 mg; 0.29 mmol) was injected to trigger formation of CO2

4

radical anions according to:

5

(6)

6

(7)

7 8

At selected time points, samples of the reaction solution (0.3 mL) were taken and injected into

9

an 8 mL-vial containing a H2O2 solution (7 mL, 0.5 %) so that CO2 radical anions were quenched

10

and the reaction was stopped. From these 8 mL-vials, samples were withdrawn for analysis of

11

substrate concentrations, as well as for carbon, chlorine and hydrogen isotope analysis.

12

Concentrations were measured immediately after quenching and 24 hours later to ensure that

13

there was indeed no further reaction of the chlorinated target compounds (e.g., with remaining

14

CO2 radical anions or through reaction with hydroxyl radicals formed according to

15

(8)

16

The same quenching reaction (scavenging of peroxo species such as peroxide, superoxide, etc. by

17

formate and CO2 radical anions) also ensured that there was no oxidative breakdown of

18

chlorinated ethenes during the OS-SET experiment. Furthermore, a control was run with PCE

19

and sodium persulfate, but without sodium formate to exclude that isotope values were

20

influenced by a parallel reaction of PCE with sodium persulfate. (data shown in Supporting

21

Information). Three identical replicates were conducted for each experiment.

22


8

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1

Reactions with Graphene Oxide in the Presence of Sodium Sulfide. Reactions were

2

conducted in 40 mL-vials containing solid sodium sulfide (2.4 g, 30.7 mmol) and a graphene

3

oxide solution (0.4 mL, 2000 mg/L). To start the reaction, 38 mL of a PCE stock solution (2.3

4

mM, 0.09 mmol) containing TRIS (Tris(hydroxymethyl)-aminomethane) (500 mg, 4.1 mmol) at

5

pH 7, was injected. The reaction was conducted on a stir plate at 25°C in an anoxic chamber with

6

an atmosphere of 97% N2 and 3% H2. Over 60 days, fourteen samples of 0.5 mL were taken and

7

injected into 8 mL-vials containing a H2O2 solution (7 mL, 0.5%) to stop the reaction. From

8

these 8 mL-vials samples were withdrawn for subsequent analysis of substrate concentrations, as

9

well as for carbon and chlorine isotope analysis. To complement the experiment at pH 7, a

10

reaction of PCE (1.2 mM) was performed in exactly the same way at pH 2 with the exception

11

that no TRIS buffer was used and that 6 samples were taken over 8 days.

12 13

Reactions in an Organic Solvent

14

Reactions with Radical Anions of Naphthalene and Pyrene. For a detailed description see

15

the Supporting Information. All modifications were conducted in an anoxic glovebox. Radical

16

anion solutions were prepared from solutions of naphthalene or pyrene through reaction with

17

sodium metal in glyme. Solutions were filtered and added to stock solutions of PCE and TCE at

18

six different concentrations so that different degrees of CE degradation were achieved. To enable

19

headspace analysis of the chlorinated target compounds, aliquots of the completed reaction

20

mixtures were subsequently added to deionized water from where chlorinated analytes could

21

partition into the headspace. Headspace samples were withdrawn for subsequent analysis of

22

substrate concentrations, as well as for carbon and chlorine isotope analysis.

23 24

Analytical Methods


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A detailed description of concentration analysis as well as isotope measurements (carbon and

2

chlorine) is provided in the supporting information. Briefly, concentrations were measured by gas

3

chromatography-mass spectrometry (GC-MS) and isotope values by gas chromatography –

4

isotope ratio mass spectrometry (GC-IRMS). For

5

online combusted to CO261 whereas 37Cl/35Cl analysis was conducted on intact CE isotopologue

6

molecules39, 40..

13

C/12C analysis separated analyte peaks were

7 8 9

Results and Discussion Aqueous Reductive OS-SET Reagents Induced Chlorine Isotope Effects in Chloroform, but

10

not in Chlorinated Ethenes.

11

CO2 radical anions were generated in situ by oxidation of sodium formate by sulfate radicals

12

according to Eq. 7. Consistent with their low reduction potential (CO2/CO2.-: -1.9 V)62 they

13

induced rapid transformation of chlorinated ethenes and CHCl3, corresponding to a total duration

14

of experiments of between 13 min and 60 min for the CEs and 30 min for CHCl3 (see Supporting

15

Information). Despite similarly rapid kinetics, isotope effects showed pronounced differences

16

between CEs and CHCl3, as illustrated in Figure 1a-c. While carbon isotope effects could be

17

observed in both substances, as expressed by the carbon isotope enrichment factors of -11.9‰

18

+/- 1.0‰ for TCE and -17.7‰ +/- 0.8‰ for CHCl3 (Figure 1a), chlorine isotope effects were

19

only observed for CHCl3 (-2.6‰ +/- 0.2‰) and not for TCE (0.04‰ +/- 0.03‰) (Figure 1b).

20

This disparity is visually represented in the dual-element isotope plot of TCE and CHCl3 of

21

Figure 1c. Since isotope effects in CHCl3 are expressed for both elements, they result in a finite

22

slope for CHCl3 of λ = ∆δ13C/∆δ37Cl = 6.7 ± 0.4 ≈ εC/εCl. By contrast, due to the absence of

23

chlorine isotope effects in TCE, the dual-element isotope slope of TCE was close to infinity. The

24

same trend was observed not only for TCE, but also for PCE and cis-DCE (Figure 1c, Table 1).


10

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1

To further confirm the absence of chlorine isotope effects in the reaction of CEs by OS-SET

2

reagents in water, a second experiment was conducted with PCE, graphene oxide and sodium

3

sulfide in aqueous solution at pH 7 and pH 2. TCE was formed as main product clearly

4

demonstrating the occurrence of reductive dehalogenation (Figure S5a, S5b; in the OS-SET

5

reaction with CO2 radical anions we did not observe products by neither GC-MS nor direct

6

aqueous injection-MS/MS, likely because the reaction mixture contained numerous reactive

7

species with the potential to trap radial intermediates and form unknown products.). Even though

8

transformation of PCE by doped graphene oxide was much slower than with CO2 radical anions

9

(duration over two months), the isotope effect results were consistent: Figure 1d shows the

10

occurrence of carbon isotope effects, but no change in chlorine isotope values (Figure S3 and

11

S4). Taken together, these results are consistent with OS-SET to the chlorinated alkane CHCl3

12

that is concerted with C-Cl bond cleavage so that a chlorine isotope effect could be observed. In

13

contrast, OS-SET to the chlorinated ethenes is consistent with a stepwise – or at least

14

asynchronous – process that involved C-Cl bond cleavage only after the rate-determining step so

15

that chlorine isotope effects were not observable.


11


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1 2

Figure 1. Model reagents for OS-SET in water caused chlorine isotope effects in

3

chloroform, but not in chlorinated ethenes. Isotopic enrichment factors of carbon (a) and

4

chlorine (b) for TCE and CHCl3 in reaction with CO2 radical anions were obtained by fitting


12

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1

experimental data according to Equation 5. The dual-element isotope slope in panel (c) – where

2

changes in carbon isotope values are plotted against changes in chlorine isotope values – is an

3

alternative way to visualize the presence of carbon, but the absence of chlorine isotope effects in

4

different chlorinated ethenes. Panel (d) shows that the same absence of chlorine isotope effects

5

was also observed for reaction of PCE with graphene oxide as alternative OS-SET reagent. Error

6

bars correspond to the analytical uncertainty (±0.5‰ for carbon, ±0.2‰ for chlorine isotope

7

analysis). Regressions are represented together with their 95% confidence intervals.

8 9

Chlorine Isotope Effects Were Partly Recovered when Chlorinated Ethenes Were Reacted

10

with OS-SET Reagents in an Organic Solvent.

11

The finding that C-Cl bond cleavage in chlorinated ethenes was not concerted / synchronous with

12

OS-SET in our aqueous experiments raises the question whether chlorine isotope effects can be

13

recovered by slowing down C-Cl bond cleavage so that it becomes (partially) rate-limiting. Since

14

a large component of the driving force of aqueous dehalogenation reactions is the high Gibbs

15

enthalpy that is released due to chloride solvation 63, additional experiments were conducted with

16

OS-SET reagents in an organic solvent. Figure 2 shows dual-element isotope slopes for reaction

17

of (a) PCE and (b) TCE with OS-SET model reactants (naphthalene and pyrene radical anions) in

18

glyme. Also here, the SET reactions resulted in steep slopes λ = ∆δ13C/∆δ37Cl ≈ εC/εCl for both

19

PCE and TCE, indicative of large carbon isotope effects of between εC = -10.5‰ +/- 1.7‰ and -

20

27.0‰ +/- 4.0‰ (Table 1). In contrast to SET reactions in water, however, we did observe small

21

changes in chlorine isotope values (εCl = -0.7‰ +/- 0.2‰ to -2.5‰ +/- 0.3‰, Table 1) indicating

22

that C-Cl bond cleavage became at least partially rate-limiting so that chlorine isotope effects

23

were recovered.

24


13


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1 2

Figure 2. OS-SET reagents caused small chlorine isotope effects when chlorinated ethenes

3

were brought to reaction in the organic solvent glyme. Dual-element isotope plots show

4

carbon and chlorine isotope effects in reaction of (a) PCE and (b) TCE with radical anions of

5

pyrene and naphthalene in glyme compared to reactions of the same substances with CO2 radical

6

anions as OS-SET reagents in water. Error bars correspond to the analytical uncertainty (±0.5‰

7

for carbon, ±0.2‰ for chlorine isotope analysis). Regressions are represented together with their

8

95% confidence intervals.

9 10

Our Observations Are Consistent with a Dissociative OS-SET in Chlorinated Alkanes

11

Compared to a Stepwise Process in Chlorinated Ethenes.

12

A mechanistic model explaining our results must take into account (1) the different chlorine

13

isotope effects in CHCl3 and chlorinated ethenes when reacting with OS-SET reagents and (2)


14

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1

the observation that chlorine isotope effects of chlorinated ethenes were partly recovered when

2

the OS-SET was conducted in an organic solvent.

3 4

Figure 3: Mechanistic hypothesis of a concerted dissociative OS-SET in chlorinated alkanes

5

versus a stepwise (or asynchronous) process in chlorinated ethenes. Energy diagrams are

6

sketched together with molecular orbitals of the chlorinated compounds. They illustrate (a) the

7

transfer of an electron into the σ* orbital of the C-Cl bond of a chlorinated alkane (CHCl3)

8

compared to (b) a SET into the π* orbital of the C-C bond of a chlorinated ethenel. Both

9

reactions are driven downhill by the Gibbs enthalpy of solvation of the chloride ion in water. In

10

contrast, panel (c) sketches OS-SET to chlorinated ethenes in an organic solvent where the

11

driving force of C-Cl bond cleavage is reduced by the absence of this solvation energy.

12 13

Addressing the first point, the different chlorine isotope effects in reactions of CHCl3 and CEs

14

can be rationalized from their electronic structures, where the LUMO orbitals are a σ* and π*


15


Page 16 of 31

1

orbital, respectively. Adding an electron to the σ*-orbital in CHCl3 is believed to cause

2

immediate (i.e., concerted) carbon-chlorine bond cleavage (Figure 3a)64. By contrast, addition of

3

an electron to the π*-orbital of the CEs causes a weakening of the π-π bond, but not necessarily

4

immediate bond cleavage. Indeed, the non-existent chlorine isotope effect in chlorinated ethenes

5

strongly suggests that the chlorine atom was cleaved in a subsequent step (Figure 3b). Hence, we

6

hypothesize that OS-SET into a σ*-orbital of CHCl3 leads to a concerted reaction, whereas OS-

7

SET into a π*-orbital of chlorinated ethenes involves a stepwise (or asynchronous) reaction.

8 9

Considering the second point, a possible explanation for the observation that CE chlorine isotope

10

effects were partly recovered when OS-SET was conducted in an organic solvent is provided by

11

Figure 3b and 3c. According to our hypothesis of a stepwise process the transformation would

12

involve two activation barriers: one barrier (EA1) for the transfer of an electron into the π*-orbital

13

of the chlorinated ethene and a second barrier (EA2) for subsequent cleavage of the C-Cl bond. As

14

discussed above, solvation of the chloride ion in water is strongly exergonic

15

Hammond’s postulate,65 this lowers the second activation barrier (EA2) (Figure 3b). In an organic

16

solvent, by contrast, the driving force is lower so that the height of the second activation barrier

17

(EA2) is less reduced compared to the first (EA1) (Figure 3c).A strong driving force of the second

18

step will cause practically all intermediate CE radical anions to react onwards to form products

19

so that hardly any molecule partitions back to the reactant side (Figure 3b). Hence, the chlorine

20

isotope effect from C-Cl bond cleavage in EA2 will not be observable in the reactant. This

21

masking / demasking of kinetic isotope effects is expressed by mathematical expressions for an

22

apparent kinetic isotope effect in a two-step reaction: 47

23

ε apparent =

(

)

k −1 k2 ⋅ ε 1equ + ε 2kin + ⋅ ε 1kin k −1 + k 2 k −1 + k 2


63

. In line with

(Eq. 9)

16

Page 17 of 31


1

where k-1 and k2 are the reaction rates of intermediate CE radical anions back to reactant and

2

onward to product. ε 1kin and ε 1equ are kinetic / equilibrium isotope effects of the OS-SET in step 1

3

(non-zero for carbon, zero for chlorine) whereas ε 2kin is the kinetic isotope effect of the C-Cl

4

bond cleavage in step 2 (non-zero for both carbon and chlorine). Equations equivalent to 9 are

5

well established expressions in the chemical43, biochemical66 and biogeochemical67 literature

6

(see ref.

7

 (E )  respective Arrhenius equations k i = Ai ⋅ exp− Ai  and multiplication of numerator and  R ⋅T 

8

denominator by

9

ε apparent

47

and references cited therein). Substitution of the rate constants k-1 and k2 by the

1  (E )  1  (E )  ⋅ exp A1  ⋅ ⋅ exp A 2  gives the expression47 A1  R ⋅ T  A2  R ⋅T 

 1  1  E   E    ⋅ exp A1   ⋅ exp A 2    R ⋅ T   R ⋅ T   A2  A1 = ⋅ ε 1equ + ε 2kin + ⋅ ε 1kin 1 1 (E )  1 (E )   (E )  1 (E )  ⋅ exp A1  + ⋅ exp A 2  ⋅ exp A1  + ⋅ exp A 2  A1 A1  R ⋅ T  A2  R ⋅T   R ⋅ T  A2  R ⋅T 

(

)

10 11

(Eq. 10)

12

where A is the pre exponential factor of the Arrhenius equation, R is the universal gas constant,

13

T is the absolute temperature, EA1 is the energy difference between reactant state and transition

14

state one and EA2 the energy difference between reactant state and transition state two (see Figure

15

3). The equation expresses the same phenomenon as derived above: that the apparent kinetic

16

isotope effect is a weighted average of the isotope effects of each step, where the weight is given

17

by the height of the respective activation barriers. In water (Figure 3b) the apparent kinetic

18

isotope effect of the reaction of TCE with CO2 radical anions is, therefore, hypothesized to

19

reflect the OS-SET of the first step (εC = -11.9‰; εCl = 0.03‰) whereas in glyme (Figure 3c) the

20

reaction of TCE with naphthalene radical anions likely represents a weighted average of both


17


Page 18 of 31

1

steps (εC = -27.0‰; εCl = -2.5‰). It is noteworthy that the apparent kinetic isotope effects were

2

little affected by the nature of the reductant (CO2 radical anions vs. doped graphene, see Table 1),

3

even though the reaction rates scaled, as predicted 68, with the reduction potential of the electron

4

donor. This can be explained by Equation 9, where ε apparent is independent of k1 (i.e., the rate of

5

electron transfer) but instead depends on k-1 and k2.

6

Our hypothesis of a concerted mechanism for chloroform and a stepwise mechanism for

7

chlorinated ethenes is further in perfect agreement with electrochemical observations by Savéant

8

and coworkers69-72 . In cyclic voltammetry they determined, a symmetric factor (α) which

9

strongly supported a concerted mechanism for chlorinated methanes70, whereas for chlorinated

10

ethenes the authors inferred a stepwise mechanism70, 72.

11


18

Page 19 of 31


1


19


Page 20 of 31

1

Figure 4. Multi-element isotope effects of chlorinated ethenes in natural and engineered

2

reductive dehalogenation are systematically different from reductive OS-SET in water.

3

Dual-element isotope plots of carbon and chlorine in OS-SET reaction with CO2 radical anions

4

(this study) are compared to data for biodegradation of PCE (panel a) by Desulfitobacterium sp.

5

strain Viet1 50, to data for transformation of TCE (panel b) with Vitamin B12 36 and metallic iron

6

35

7

that show such large isotope fractionation that they reflect the underlying (bio)chemical reaction

8

rather than mass transfer or enzyme binding (see Table 1). Shaded areas illustrate trends of

9

isotope fractionation for OS-SET (grey), metallic iron (pink) and biodegradation (green) from

10

published literature studies (see Table 1). Error bars correspond to the analytical uncertainty

11

(±0.5‰ for carbon, ±0.2‰ for chlorine). Regressions are represented together with their 95%

12

confidence intervals.

, and to data for transformation of cis-DCE (panel c) with metallic iron 35. Examples are chosen

13 14

Systematically Different Isotope Fractionation Trends Suggest that OS-SET Is Not a

15

Common Mechanism in Natural and Engineered CE Reductive Dehalogenations

16

In Figure 4, multi-element isotope effect trends of PCE and TCE from the OS-SET experiments

17

with CO2 radical anions are compared to literature data on reductive biodegradation and on

18

dehalogenation by zero-valent iron. Example data on natural and engineered transformations

19

(biodegradation of PCE by Desulfitobacterium sp. strain Viet1, reductive dehalogenation of TCE

20

by Vitamin B12, transformation of TCE with metallic iron) are shown together with shaded areas

21

representing literature values reported to date. The literature data includes experiments with

22

mixed cultures, pure strains, isolated reductive dehalogenases and purified corrinoids, as listed in

23

Table 1. Table entries with │εcarbon │< 6‰ are tagged with an asterisk to mark experiments with

24

particularly low isotope fractionation that could reflect slow mass transfer or enzyme binding


20

Page 21 of 31


1

instead of the underlying (bio)chemical reaction53. The rest of the entries, in contrast, may be

2

taken to reflect to a large extent the underlying reaction chemistry. Even though Figure 4 does

3

illustrate some isotope effect variability in natural and engineered reductive dehalogenation, the

4

combined data still clearly cluster outside the range of our OS-SET experiments in water. The

5

distinguishing feature is the presence of chlorine isotope fractionation in all reactions of PCE,

6

TCE and cis-DCE with organisms or zero valent iron reported to date, compared to the total

7

absence of a chlorine isotope effect with OS-SET reagents in our experiments. This is

8

particularly true in cases in which both εC and εCl are so large that they reflect intrinsic isotope

9

effects of the reaction rather than binding isotope effect of substrate-enzyme association (see

10

Table 1). This combined data, therefore, indicates that OS-SET reaction mechanisms are an

11

exception rather than the rule in natural biodegradation or engineered reactions with zero valent

12

iron: if present at all, Figure 4 and Table 1 demonstrate that an OS-SET would represent a minor

13

reaction channel so that the observable isotope fractionation is dominated by different,

14

simultaneously occurring reaction mechanisms In further support of this statement, Constantin et

15

al 70 report that rate constants of PCE and TCE with Vitamin B12 and reductive dehalogenases

16

cannot be reconciled with an SET mechanism. Instead, they infer more intimate interactions

17

between the substrate and the electron donor where the chlorinated ethene enters the cobalt

18

coordination sphere, supporting an inner-sphere rather than outer-sphere mechanism.

19


21


Page 22 of 31

1

Table 1: Literature overview of results from dual-element (C, Cl) isotope studies targeting

2

reductive dehalogenation of PCE, TCE and cis-DCE in biodegradation and metallic iron-

3

mediated transformation. Values are stated together with their 95% confidence intervals. Entries

4

with an asterisk (*) indicate cases in which observable εC were so small that they likely reflect

5

isotope effects of substrate-enzyme association etc. in addition to the intrinsic (bio)chemical

6

reaction.

7 εC [‰] OS-SET in an organic solvent PCE pyrene

-10.5±1.7

εCl [‰]

-0.7±0.2

dual-element isotope trend [λ λ ≈ εC/ εCl]

references

15.1±1.4

this study

PCE naphthalene

-15.4±1.5

-1.5±0.1

12.8±2.5

this study

TCE pyrene

-26.5±2.6

-1.9±0.1

13.7±1.2

this study

TCE naphthalene

-27.0±4.0

-2.5±0.3

11.0±0.5

this study

PCE CO2 radical anions

-7.6±0.8

0.04±0.12

∞ (-11.3±47)

this study

PCE graphene oxide/sodium sulfide pH 7

-9.3±0.9

0.05±0.18

∞ (-10.6±24.5)

this study

PCE graphene oxide/sodium sulfide pH 2

-7.9±1.4

-0.3±0.3

∞ (12.4±15.7)

this study

TCE CO2 radical anions

-11.9±1.0

0.04±0.03

∞ (148.5±112.2)

this study

cis-DCE CO2 radical anions

-10.5±0.7

-0.12±0.06

∞ (51.5±32.1)

this study

CHCl3 CO2 radical anions

-17.7±0.8

-2.6±0.2

6.7±0.4

this study

-19.0±0.9

-5.0±0.1

3.7±0.2

Cretnik et al. 201450

-5.6±0.7

-2.0±0.5

2.8

Wiegert et al. 201337

-3.6±0.2

-1.2±0.1

2.7±0.3

Badin et al. 201451

-0.7±0.1

-0.9±0.1

0.7±0.2

Badin et al. 201451

-1.4±0.1

-0.6±0.2

2.2±0.5

Renpenning et al. 201453

-1.3±0.1

-0.4±0.1

2.8±0.5


Norpseudo-B12 (purified cofactor)

-25.3±0.8

-3.6±0.4

6.9±0.7


Nor-B12 (purified cofactor)

-23.7±1.2

-4.8±0.9

5.0±0.8


Cyano-B12 (purified cofactor)

-22.4±0.8

-4.8±0.2

4.6±0.2


OS-SET in water

Reductive biodegradation of PCE Desulfitobacterium sp. strain Viet1 Enrichment culture dominated by Desulfitobacterium aromaticivorans UKTL* Sulphurospirillum spp. enrichment culture harboring PceA-TCE* Sulphurospirillum . enrichment culture harboring PceA-DCE* Reductive dehalogenase from Sulphurospirillum multivorans (norpseudo-B12)* Reductive dehalogenase from Sulphurospirillum multivorans (norB12)*


22

Page 23 of 31


Dicyanocobinamid (purified cofactor)

-25.2±0.5

-3.4±0.4

7.0±0.8


Reductive biodegradation of TCE Geobacter lovleyi

-12.2±0.5

-3.6±0.1

3.3±0.1

Cretnik et al. 201336

-9.1±0.6 -8.6±0.0

-2.7±0.6 -2.6±0.2

3.4±0.2 3.2±0.2

Cretnik et al. 201336 Buchner et al. 201552

-8.8±0.2

-2.4±0.2

3.4±0.2

Buchner et al. 201552

-9.0±0.2

-3.1±0.3

2.8±0.3


-9.0±0.2

-2.6±0.1

3.5±0.2


-16.4±1.5

-3.6±0.3

4.5

Kuder et al. 201338

-8.8±2.0

-3.5±0.5

2.5

Wiegert et al. 201337

-20±0.5

-3.7±0.2

5.3±0.3


-20.2±1.1

-3.9±0.6

5±0.8


Norpseudo-B12 (purified cofactor)

-18.5±2.8

-4.2±0.8

4.5±0.8


Nor-B12 (purified cofactor)

-15.1±2.7

-3.9±1.0

3.7±0.3


Dicyanocobinamid (purified cofactor)

-16.5±0.7

-3.9±0.5

4.2±0.6


Cyano-Vitamin B12 (purified cofactor) Cyano-Vitamin B12 (purified cofactor)

-15±2.0 -16.1±0.9

-3.2±1.0 -4.0±0.2

4.4±0.7 3.8±0.2

Renpenning et al. 201453 Cretnik et al. 201336

Cobaloxime (chemical model reactant) Reduction by metallic iron

-21.3±0.5 -14.9±0.9

-3.5±0.1 -2.6±0.2

6.1±0.2 5.2±0.3

Cretnik et al. 201336 Audí-Miró et al.201335

Reduction by metallic iron

-12.4

-3.0

4.2

Lojkasek-Lima et al. 201254

Reductive biodegradation of cis-DCE Mixed culture harboring Dehalococcoides -26.8

-3.2

8.4

Kuder et al. 201338

Mixed culture harboring Dehalococcoides -18.5±1.8

-1.6±0.1

11.6

Abe et al. 200934

Mixed culture harboring Dehalococcoides -18.5±1.3 Reduction by metallic iron -20.5±1.8

-1.4±0.2 -6.2±0.8

13.2 3.1±0.2

Abe et al. 200934 Audí-Miró et al.201335

Desulfitobacterium hafniense Y51

Dehalococcoides (two species) Enrichment culture dominated by Desulfitobacterium aromaticivorans UKTL Reductive dehalogenase from Sulphurospirillum multivorans (norpseudo-B12) Reductive dehalogenase from Sulphurospirillum multivorans (nor-B12)

1 2 3

Environmental Significance

4

Pinpointing detailed chemical reaction mechanisms in complex natural and engineered

5

transformations is intrinsically difficult. Methods employed to characterize electron transfer

6

encounter complexes in laboratory experiments – spectral elucidation, electrochemical

7

characterization73 or even X-ray structure analysis13 – are not accessible in natural environments.

8

Yet it is this knowledge about the manner and order of chemical bond cleavage that provides the


23


Page 24 of 31

1

key to understanding subsequent transformation pathways leading to problematic vs. benign

2

daughter products in remediation schemes. This study takes advantage of a new opportunity –

3

multi-element isotope effect analysis of organic compounds at natural isotopic abundance – to

4

evaluate whether outer-sphere single electron transfer, a mechanism that has frequently been

5

invoked, but not been proven, is involved in natural and engineered reductive dehalogenation

6

reactions.

7

Experiments with chemical model reactants made it possible to derive a consistent mechanistic

8

explanation for the absence of chlorine isotope effects in chlorinated ethene transformation by

9

aqueous OS-SET reagents. Our results indicate the occurrence of a stepwise OS-SET (SET to a

10

π* orbital followed by C-Cl cleavage) in chlorinated ethenes compared to a dissociative OS-SET

11

(SET to a σ* orbital concerted with C-Cl breakage) in chlorinated alkanes (Figure 3). Building on

12

this mechanistic understanding, the consistent absence of chlorine isotope effects in aqueous OS-

13

SET could be compared to the consistent presence of chlorine isotope effects in all

14

biodegradation studies and in all metallic iron-mediated dehalogenation reactions of PCE and

15

TCE reported to date (Figure 4). The discrepancy strongly suggests that OS-SET is an exception

16

rather than the rule in natural and engineered reductive dehalogenation reactions. This result is

17

relevant to guide future research on the organic reaction chemistry of environmental reductive

18

dehalogenations. Our results indicate that product formation cannot necessarily be derived from

19

chlorinated vinyl radicals resulting from initial outer-sphere electron transfer, and that reactivity

20

cannot necessarily be predicted from Marcus theory of outer-sphere non-adiabatic ET 11. Instead,

21

our results point to inner-sphere interactions, consistent with organometallic reactions at metal

22

surfaces and in reductive dehalogenases which still warrant exploration. Future research should

23

be directed at characterizing the underlying reaction chemistry of chlorinated ethene degradation.

24

Together with the recent structural elucidation of reductive dehalogenases, the new opportunity


24

Page 25 of 31


1

of multi-element isotope effect analysis at natural isotopic abundance may enable pursuit of this

2

goal.

3 4

ASSOCIATED CONTENT

5

Supporting Information Overview of the analytical methods and experimental setup. The

6

Supporting Information is available free of charge on the ACS Publications Website.

7 8

AUTHOR INFORMATION

9

Corresponding Author

10

* Chair of Analytical Chemistry and Water Chemistry, Technical University of Munich,

11

Marchioninistrasse 17, D-81377 Munich, Germany. Phone: +49 89 2180-78231; e-mail:

12

[email protected].

13

Author Contributions

14

The manuscript was written through contributions of all authors. All authors have given approval

15

to the final version of the manuscript.

16

Notes

17

The authors declare no competing financial interest.

18

ACKNOWLEDGMENT

19

This work was supported by the German Research Foundation (DFG), EL 266/3-1/2, as well as

20

by the Initiative and Networking Fund of the Helmholtz Association. S.K., and K.M. gratefully

21

acknowledge support from the U.S. National Science Foundation (Grant no. CHE-0809575), as


25


1

well as by funds from ETH Zürich. We thank two anonymous reviewers for helpful comments

2

which improved the quality of the manuscript.

3

REFERENCES

4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43

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Graphical Abstract 54x48mm (600 x 600 DPI)


Reductive Outer-Sphere Single Electron Transfer Is an Exception

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