Volatile Organic Sulfur Compounds of Environmental Interest

Research: Science and Education

Volatile Organic Sulfur Compounds of Environmental Interest: Dimethyl Sulfide and Methanethiol An Introductory Overview Thomas G. Chasteen* Department of Chemistry, Sam Houston State University, Huntsville, TX 77341-2117; *[email protected] Ronald Bentley Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260

In recent years, volatile organic sulfur compounds, VOSCs, have been assigned environmental roles in global warming, acid precipitation, and cloud formation. Two important members of the VOSC group are dimethyl sulfide, (CH3)2S, DMS, and methanethiol, CH3SH, MT; their degradation products are also involved. Atmospheric VOSCs are formed by anthropogenic, geochemical, and biological processes. DMS commands particular attention since it accounts for about 75% of the global sulfur cycle and since very large quantities are produced biotically, especially in marine environments. The total release of DMS from the oceans is about 38–40 million metric tons per annum. Moreover, much of the biotically-produced DMS is degraded by microorganisms before release to the atmosphere. MT is also an important

Atmospheric oxidation

DMSⴚII

SVIO42ⴚ

(CH3)2S0O (CH3)2SIIO2 SIVO2 Atmosphere Marine, Terrestrial ecosystems

ⴚII

DMS

ⴚII

DMSP

Met

H2SⴚII

Bacterial reduction

ⴚ

SVIO42

Figure 1. The global sulfur cycle in terms of oxidation and reduction. (Met is methionine, DMS is dimethyl sulfide, and DMSP is dimethylsulfoniopropionate.)

Table 1. Oxidation States for Sulfur Compounds Chemical Form of Sulfur

Oxidation State

Inorganic

Organic

SO3, SO42−

---

+VI

SO2, H–SO3−, SO32−

CH3–SO3−

+IV

SO

CH3–SO2–CH3

+II

S

CH3–SO–CH3

0

--−

H–S , H–S–H

CH3–S–S–CH3

᎑I

CH3–S–CH3, CH3–S–H

᎑II

NOTE: Data from ref 8.

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component of the VOSC mix and by a methylation process it can be converted to DMS. In abbreviated terms, the global sulfur cycle consists of two opposed processes. Terrestrial biochemical reactions primarily involving plants and microorganisms reduce sulfate to sulfide and the latter is converted to DMS mainly in the oceans. DMS is released from the oceans to the atmosphere. The second process, photochemical oxidation, occurs in the atmosphere; DMS is converted to several compounds, the final components being sulfur oxyacids and inorganic sulfate. The oxyacids and sulfate return to earth in acid rain and snow, thus completing the overall cycle (Figure 1). Undergraduates encounter sulfur as a group 16 element and are well acquainted with the rotten egg odor of H2S and the properties of acids such as H2SO4. Those exposed to biochemistry know of the sulfur-containing amino acids, and probably of penicillin. In organic chemistry, however, the main emphasis is on compounds containing C, H, O, and N, with little concern for organic sulfur compounds. The increasing environmental significance of VOSCs suggests that organic sulfur compounds warrant more attention in chemical education. There is much interesting chemistry involved in their formation and degradation and chemical principles can be reinforced by such study. This material can be incorporated into courses involving biochemistry, environmental chemistry, and atmospheric chemistry. We provide an overall introduction to VOSCs, suitable for undergraduates and instructors, painting our picture with a broad brush. The topic involves a number of disciplines and there is an enormous literature. Three books (1–3) and three reviews (4–6) provide a starting point for more in-depth information. Our wide focus is on the roles of DMS and MT and the chemical reactions involved in their biosynthesis and degradation. We make no attempt to discuss the many interrelationships in complex ecosystems, and environmental concerns receive little attention. Where possible, we use the IUBMB EC numbers for enzymes (7). A Note on Oxidation and Reduction As already suggested, many biotic and abiotic transformations of VOSCs involve oxidation or reduction and are conveniently discussed in terms of oxidation numbers. We follow the common practice of regarding sulfur as more electronegative than carbon (8). Elemental sulfur (written as S or S8) has oxidation number of 0, while the most reduced environmental forms, DMS and MT, have oxidation numbers of ᎑II (Table 1). The most oxidized inorganic form is

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sulfate ion with oxidation number of +VI and the most oxidized organic form is methanesulfonate ion, with oxidation number of +IV.

R

R

R

S

+

R

2

O O H3C

H3C

+ CH3

O

S

−

+

O−

S CH3

3

4

Scheme I. Reaction to add a methyl group to a thioether.

H

O

H

O

H3C

H3C

O−

S+

H3C

H

−

4

HO

H 2C

+

S

O−

C

H3C

H

H 6

5

Scheme II. Elimination reaction to form DMS, 5.

H3N + H H3C

oxoglutarate

O−

S O

glutamate

7

O NADPH, H

ⴙ

H3C

O− S 8

NADPⴙ

O

H OH H3C

O−

AdoMet

S O

9

AdoHcy

H H3C ?

(CH3)2– S+– CH2– CH2– COOH

•

1

2

O2

In sea grasses, the second methyl is added initially by conversion of Met to its methyl sulfonium salt, S-methylmethionine. However, the best understood pathway is in algae where enzyme preparations from Enteromorpha intestinalis were examined (14). In this case, the second methyl is added in the penultimate reaction. The enzymes that were studied are as follows: Met aminotransferase, forming 4-methylthio2-oxobutyrate, MTOB, 8; MTOB reductase, forming 4-methylthio-2-hydroxybutyrate, MTHB, 9; MTHB-methyl-

CH3

1

CH3– S– CH2– CH2– CH(NH2)– COOH

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2

S

Dimethyl Sulfide: Properties and Biosynthesis DMS, the sulfur analog of dimethyl ether, is a liquid with a low bp (38 ⬚C) and an odor often described as disagreeable. The carefully purified material, however, is not unpleasant and when diluted with air, the odor is that of seaweed (9). At appropriate concentrations, DMS is actually a flavor component in some foods and alcoholic beverages (4, 10). However, beyond a certain level, DMS may result in an off flavor. It can be formed nonenzymatically in food processing and contributes to the characteristic “sulfur” odor observed on cooking broccoli and cauliflower. This odor may account for the fact that cauliflower suffers from “consumer rejection” (11). The unpleasant odor is almost certainly due to a complex combination of the thiols, sulfides, and disulfide, the ᎑II and slightly more oxidized ᎑I forms of sulfur (12). Although DMS is produced by several biosynthetic pathways, we focus on the major role of the sulfonium salt, dimethylsulfoniopropionate, (CH3)2⫺S+⫺CH2CH2COO−, DMSP, as a precursor. The sulfur atom in thioethers, R1⫺S⫺R2, 1, contains two unshared electron pairs and can react with a cation such as CH3+ to form a sulfonium salt, 2 (Scheme I). In principle, DMSP, 4, may be regarded as the sulfonium salt of 3-methylthiopropionate, 3. (Another sulfonium salt familiar to biochemistry students is S-adenosylmethionine, AdoMet, an important donor of methyl groups.) On treatment with NaOH, DMSP undergoes an elimination reaction forming DMS, 5, and acrylate, 6 (Scheme II). This process is analogous to the Hofmann degradation of a quaternary ammonium salt. DMSP has several physiological roles. It functions as an osmoprotective agent (osmolyte) in many algae, bacteria, and some plants living in marine environments and has cryoprotectant and antioxidant properties. It is present in many organisms sometimes at high concentrations; in marine algae, for instance, there are levels of 100–400 mmol L᎑1 (13). DMSP biosynthesis begins with the sulfur-containing amino acid, L-methionine, Met, 7, (Scheme III; for the somewhat complex biosynthesis of Met itself, a biochemistry text should be consulted). The pathway requires addition of a second methyl group and both decarboxylation and deamination, not necessarily in that order:

CH3

+

1

OH O−

+

S

H3C

O 10

H2O

O H3C

+

O−

S CH3

+ CO2

4

Scheme III. Synthesis of DMSP, 4, from L-methionine, 7.


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transferase, forming dimethylsulfonio-2-hydroxybutyrate, DMSHB, 10. The latter acid underwent a final oxidative decarboxylation, probably by the action of a so far unidentified oxygenase enzyme. In living systems, DMSP is converted to DMS and acrylate by enzymes now known as DMSP-lyases, EC 4.4.1.3. They were originally named as dimethylpropiothetin demethylases, using an older name for DMSP. The reaction mechanism for this lyase-catalyzed elimination is presumably analogous to that of the alkaline decomposition of DMSP (Scheme II). Several of these DMSP-lyases have been purified to electrophoretic homogeneity. The acrylate is further reduced to propionate in anaerobic bacteria or, by addition of water, is converted to 3-hydroxypropionate. Further metabolic routes are available for propionate and 3hydroxypropionate.

CH3– S– CH2– CH(NH2)– COOH CH3SH + CH3– CO– COOH + NH3 MT is also formed by methylation of sulfide ion catalyzed by enzymes termed thiol S -methyltransferases, EC 2.1.1.9. The methyl donor is AdoMet, which, in the usual manner, is converted to S-adenosyl homocysteine, AdoHcy: AdoMet + SH −

Such enzyme activities are widespread (19) and recently several thiol methyltransferase isoenzymes were purified to homogeneity from red cabbage (20). Some methyltransferases carry out the further methylation of MT to DMS:

AdoMet + CH3– SH

Methanethiol: Properties and Biosynthesis

CH3– S– CH2– CH2– CH(NH2)– COOH CH3SH + CH3– CH2– CO– COOH + NH3 This enzyme has been purified and crystallized; X-ray crystal structures are available (17, 18). Pyridoxal phosphate is a cofactor and the reaction is a typical γ elimination from the pyridoxal phosphate–amino acid complex (biochemistry instructors could ask students to deduce the mechanism). A similar demethiolation forming MT occurs in the action of S -alkylcysteine lyase, EC 4.4.1.6, on S-methylcysteine:

O

H3CO

O

O O

−

X

Scheme IV. Methylation of sulfide from methylated aromatic compounds to form MT and DMS.

AdoHcy + CH3–S– CH3

Moreover, some bacteria methylate sulfide using methyl groups derived from methoxylated aromatic compounds. Thus, both MT and DMS were formed from methoxy groups of syringate, 11, and 5-hydroxyvanillate, 12, by Parasporobacterium paucivorans (Scheme IV). The completely demethoxylated product was 3,4,5-trihydroxybenzoate, 13 (21). Finally, an alternative metabolic pathway for MT formation involves demethylation and demethiolation of DMSP. In anoxic marine sediments, DMSP underwent two successive demethylations forming 3-methylthiopropionate, 3, and 3-thiopropionate, 14 (Scheme V) (22). 3-Methylthiopropionate was also a substrate for a demethiolation yielding MT and unidentified components. An interesting possibility for this demethiolation is the use of a fatty acid β-oxidation pathway with the CoA derivative of 3-methylthiopropionate. This would lead to 3-oxo-3-methylthiopropionyl-CoA, 15, and subsequent cleavage with a further CoA molecule would form CH3–S–CO–S–CoA, 16, and acetyl-CoA, 17. The former, 16, would likely decompose to MT, CO2, and CoA–SH (Scheme V; biochemistry instructors could challenge students to derive this pathway from their knowledge of the usual β-oxidation pathway for fatty acids). Large quantities of MT are formed in complex ecosystems such as anoxic Sphagnum peat bogs and salt marsh sedi-

Methanethiol (in older literature, methyl mercaptan) is a gas, bp 6.0 ⬚C. It has a typical “mercaptan” odor sometimes described as that of rotten cabbage. However, as is the case with DMS, it has a flavor role at appropriate concentrations, for instance in some cheeses (15). Unhappily, its formation by mouth bacteria can result in malodorous breath (16). There are several pathways for the biotic synthesis of MT. In one, Met functions as a precursor (compare DMS formation). Met undergoes a “demethiolation” (i.e., removal of the CH3–SH group) and this elimination is catalyzed by methionine γ-lyase, EC 4.4.1.11:

C

AdoHcy + CH3– SH

OCH3

X–CH3

C

O

−

C X

OCH3

HO

HO


•

OH

OH

OH

OH

11

12

13 ⴚ X = SH or CH3SH

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•

O−

X–CH3

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ments. The further methylation of MT may actually be a major mechanism for DMS production in any environment (23). Biodegradation of Dimethyl Sulfide and Methanethiol In marine ecosystems, there is much degradation of DMS and MT, before the rest is released to the atmosphere. Under aerobic conditions, some bacteria (e.g., Hyphomicrobium sp., Thiobacillus sp.) use a dimethyl sulfide monooxygenase to form MT and formaldehyde: + CH3–S– CH3 + O2 + NAD(P)H + H

CH3– SH + HCHO + NAD(P)+ + H2O However, there has apparently been no detailed study of such an enzyme and the activity is unstable (24). The MT is further metabolized by methanethiol oxidase, EC 1.8.3.4, (sometimes, called methyl mercaptan oxidase): CH3– SH + O2 + H2O

HCHO + H2S + H2O2

O H3C

O

+

S

O

−

O−

HS

CH3

H3C

3

O

O CoA

H3C

S

S 15 CoA–SH

O

O H3C

CoA S

S

+

+ CH3–SO– CH3 + 2 H + 2 e −

This is an example of a two electron oxidation with S(᎑II) in DMS being oxidized to a formal oxidation state of 0 in the sulfoxide (8). The reverse (reductive) process, conversion of DMSO to DMS, is also carried out by enzymes termed DMSO reductases. There is, in fact, a defined group of enzymes, the DMSO reductase family, and dimethyl sulfide dehydrogenase is a member of this family. These enzymes are characterized by the presence of a molybdenum cofactor, bis(molybdopterin) guanine dinucleotide (29). The details of the enzymatic electron transfer processes are too complex for consideration here; for those wishing further details the original literature should be consulted (27–29). Atmospheric Fate of Volatile Sulfur

O−

S

CH3–S– CH3 + H2O

14

O

4

The latter enzyme has been purified from Hyphomicrobium EG (grown on dimethyl sulfoxide) and Thiobacillus thioparus (grown on DMS) (25, 26). The reaction mechanism is not well understood. A further process is conversion of DMS to dimethyl sulfoxide, DMSO, by a dimethyl sulfide dehydrogenase (dimethyl sulfide : acceptor oxidoreductase). The enzyme present in Rhodovulum sulfidophilum (earlier, Rhodobacter sulfidophilus) has been much investigated (27, 28). This enzyme enables the organism, a purple photosynthetic bacterium, to grow photoautotrophically with DMS as the sole electron donor. In its simplest form, the reaction may be written as follows:

CoA S

H3C

16

17

?

CH3SH + CO2 + CoA–SH

Scheme V. Metabolic pathway starting from DMSP to form MT.

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Ultimately, given the oxidative nature of the earth’s atmosphere, the fate of volatile sulfur is oxidation to sulfoxide, sulfur dioxide, sulfite or sulfate (30). Many of these atmospheric oxidations are powered by the ubiquitous hydroxyl radical, present at daylight concentrations of only about 5 × 106 radicals cm᎑3 of air (31). At night, nitrate radicals derived from daylight oxidation of nitrogen oxides, replace hydroxyl radicals as oxidizing agents (30). Although precise details are lacking as to the mechanism, the atmospheric oxidation processes probably proceed via a series of radical-containing steps and can produce the following from DMS: DMSO; dimethyl sulfone, (CH3)2SO2; methanesulfinic acid, CH3SOOH; methanesulfonic acid, CH3SO2OH; and ultimately SO42−. MT is oxidized initially to dimethyl disulfide, CH3–S–S–CH3 and thence to further products. The atmospheric lifetime of MT and DMS and many of the more oxidized species is relatively short, maybe a few hours to a day or two (32). The photochemical oxidation process eventually promotes the removal of volatile sulfur and its return to the bio- and geosphere. The more oxidized products are more water soluble and, in the case of sulfate, form aerosols which can act as cloud condensation nuclei; however, low humidity and lack of humidity can keep these aerosols aloft for days to weeks (33). Ultimately therefore, they are removed via wet or dry deposition from the troposphere before they can get to the stratosphere (34). In summary, from


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a biotic standpoint, reduced sulfur, S(᎑II), is mobilized and to some degree volatilized by biological processes and then redeposited following atmospheric oxidation to S(+IV) or S(+VI). And while the quantity of biogenic sulfur released is relatively large, this is approximately one-fifth of total sulfur emissions in the Northern Hemisphere (35). Final Comment It is our hope that this very general account of the two VOSCs, DMS and MT, will stimulate interest in the environmental roles of these interesting sulfur compounds and perhaps lead to a more general concern with the organic chemistry and biochemistry of sulfur compounds in the undergraduate curriculum. Acknowledgments TGC is grateful for support from a Robert A. Welch department grant. Helpful comments and suggestions from the reviewers are acknowledged with gratitude. Literature Cited 1. Biogenic Sulfur in the Environment; Saltzman, E. S., Cooper, W. J., Eds.; ACS Symposium Series, 393, American Chemical Society: Washington, DC, 1989. 2. Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds; Kiene, R. P., Visscher, P. T., Keller, M. D., Kirst, G. O., Eds.; Plenum Press: New York, 1995. 3. Microbiology of Trace Gases: Sources, Sinks and Global Change Processes; Murrell, J. C., Kelly, D. P., Eds.; Springer: Berlin, 1996. 4. Kadota, H.; Ishida, Y. Ann. Rev. Microbiol. 1972, 26, 127. 5. Lomans, B. P.; van der Drift, C.; Pol, A.; Op den Camp, J. M. Cell. Mol. Life Sci. 2002, 59, 575. 6. Yoch, D. C. Appl. Environ. Microbiol. 2002, 68, 5804. 7. Webb, E. C. Enzyme Nomenclature: Recommendation of the Nomenclature Committee of the International Union of Biochemistry and Molecular Biology on the Nomenclature and Classification of Enzymes; Academic Press: San Diego, CA, 1992; the information is also available at the Enzyme Nomenclature Web site. www.chem.qmul.ac.uk/iubmb/enzyme (accessed Jun 2004). 8. Bentley, R.; Franzen, J.; Chasteen, T. G. Biochem. Mol. Biol. Educ. 2002, 30, 288. 9. Challenger, F. Aspects of the Organic Chemistry of Sulphur; Butterworth: London, 1959; p 8. 10. Ferreira, A. C. S.; Rodrigues, P.; Hogg, T.; Guedes de Pinho, P. J. Agric. Food Chem. 2002, 51, 727. 11. Engel, E.; Baty, C.; Le Corre, D.; Souchon, I.; Martin, N. J. Agric. Food Chem. 2002, 50, 6459. 12. Di Pentima, J. H; Rios, J. J.; Clememte, A.; Olias, J. M. J.

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Agric. Food Chem. 1995, 43, 1310. 13. Sunda, W.; Kleber, D. J.; Kiene, R. P.; Huntsman, S. Nature, 2002, 418, 317. 14. Summers, P. S.; Nolte, K. D.; Cooper, A. J. L.; Borgeas, H.; Leustek, T.; Rhodes, D.; Hanson, A. D. Plant Physiol. 1998, 116, 369. 15. Bonnarme, P.; Lapadatescu, C.; Yvon, M.; Spinnler, H. E. J. Dairy Res. 2001, 68, 663. 16. Yoshimura, M.; Nakano, Y.; Yamashita, Y.; Oho, T.; Saito, T.; Koga, T. Infect. Immun. 2000, 68, 6912. 17. Sridhar, V.; Xu, M.; Han, Q.; Sun, X.; Tan, Y.; Hoffman, R. M.; Prasad, G. S. Acta Crystal. Sect. D, Biol. Crystallogr. 2000, 56, 1665. 18. Motoshima, H.; Inagaki, K.; Kumasaka, T.; Furuichi, M.; Inoue, H.; Tamura, T.; Esaki, N.; Soda, K.; Tanaka, N.; Yamamoto, M.; Tanaka, H. J. Biochem. Tokyo 2000, 128, 349. 19. Drotar, A.; Burton, G. A.; Tavernier, J. E.; Fall, R. Appl. Environ. Microbiol. 1987, 53, 1626. 20. Attieh, J.; Sparace, S. A.; Saini, H. S. Arch. Biochem. Biophys. 2000, 380, 257. 21. Lomans, B. P.; Leijdekkers, P.; Wesselink, J.-J.; Bakkes, P.; Pol, A.; van der Drift, C.; Op den Camp, H. J. M. Appl. Environ. Microbiol. 2001, 67, 4017. 22. Kiene, R. P.; Taylor, B. F. Appl. Environ. Microbiol. 1988, 54, 2208. 23. Kiene, R. P.; Hines, M. E. Appl. Environ. Microbiol. 1995, 61, 2720. 24. Borodina, E.; Kelly, D. P.; Rainey, F. A.; Ward-Rainey, N. L.; Wood, A. P. Arch. Microbiol. 2000, 173, 425. 25. Suylen, G. M. H.; Large, P. J.; van Dijken, J. F.; Kuenen, J. G. J. Gen. Microbiol. 1987, 133, 2989. 26. Gould, W. D.; Kanagawa, T. J. Gen. Microbiol. 1992, 138, 217. 27. McDevitt, C. A.; Hanson, G. R.; Noble, C. J.; Cheesman, M. R.; McEwan, A. G. Biochemistry 2002, 41, 15234. 28. McDevitt, C. A.; Hugenholtz, P.; Hanson, G. R.; McEwan, A. G. Mol. Microbiol. 2002, 44, 1575. 29. Kisker, C.; Schindelin, H.; Rees, D. C. Ann. Rev. Biochem. 1997, 66, 233. 30. Wayne, R. P. Chemistry of Atmospheres, 2nd ed.; Oxford University Press: Oxford, United Kingdom, 1994; p 225. 31. Sarwar, G.; Corsi, R.; Kimura, Y.; Allen, D.; Weschler, C. J. Atmos. Environ. 2002, 36, 3973. 32. Falbe-Hansen, H.; Sorensen, S.; Jensen, N. R.; Pedersen, T.; Hjorth, J. Atmos. Environ. 2000, 34, 1543. 33. Chen, L.-W.; Doddridge, B. G.; Dickerson, R. R.; Chow, J. C.; Henry, R. C. Atmos. Environ. 2002, 36, 4541. 34. Wilson, J. C. In Perspectives in Environmental Chemistry; Macalady, D. L., Ed.; Oxford: New York, 1998; Chapter 15. 35. Bates, T. S.; Lamb, B. K.; Guenther, A.; Dignon, J.; Stoiber, R. E. J. Atmos. Chem. 1992, 14, 315.


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Volatile Organic Sulfur Compounds of Environmental Interest

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