Metabolism of Natural Polymeric Sulfur Compounds
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1 35 2 Metabolism of Natural Polymeric Sulfur Compounds Priv.-Doz. Dr. Christiane Dahl 1, Dr. Alexander Prange 2, Prof. Dr. Ralf Steudel 3 1 Institut f r Mikrobiologie und Biotechnologie, Rheinische Friedrich-Wilhelms- Universit t Bonn, Meckenheimer Allee 168, D Bonn, Germany; Tel.: ; Fax: ; ChDahl@uni-bonn.de 2 Institut f r Mikrobiologie und Biotechnologie, Rheinische Friedrich-Wilhelms- Universit t Bonn, Meckenheimer Allee 168, D Bonn, Germany; Tel.: ; Fax: ; A.Prange@gmx.de 3 Institut f r Chemie, Sekr. C2, Technische Universit t Berlin, Strasse des 17. Juni 135, D Berlin, Germany; Tel.: ; Fax: ; steudel@schwefel.chem.tu-berlin.de 1 Introduction Historical Outline Chemical Structures Hydrogen Sulfide and Inorganic Polysulfides Chemistry, Structures and Characterization Occurrence Metabolism under Oxidative Conditions Metabolism under Reductive Conditions Elemental and Biologically Produced Sulfur Chemistry, Structures and Characterization Solid Sulfur Liquid and Gaseous Sulfur Sulfur Sols Bacterial Sulfur Globules Occurrence Metabolism under Oxidative Conditions Metabolism under Reductive Conditions... 48
2 36 2 Metabolism of Natural Polymeric Sulfur Compounds 6 Polythionates Chemistry, Structures and Characterization Occurrence Metabolism under Oxidative Conditions Tetrathionate Formation Tetrathionate Oxidation Trithionate and Other Polythionates Metabolism under Reductive Conditions Organic Polysulfanes Chemistry, Structures and Characterization Occurrence Metabolism under Oxidative Conditions Metabolism under Reductive Conditions Summary Outlook and Perspectives Patents References SQR XANES sulfide:quinone oxidoreductase X-ray absorption near-edge structure 1 Introduction Sulfur atoms, like carbon atoms, show a strong tendency to catenation, forming long homoatomic chains or homocyclic rings of various sizes. This holds particularly true if the sulfur is in a low oxidation state and if the coordination number is 2. The best-known examples for this behavior are the many allotropes of elemental sulfur which consist of rings and chains of almost all sizes. While the cyclo-s 8 molecule, crystallizing at 258C as orthorhombic a-s 8, represents the most stable form, almost all other ring sizes from S 6 to S 20 have been synthesized as pure crystalline materials (Steudel, 1982, 1984, 2000). In addition, polymeric sulfur consisting of very long chains in either a random coil conformation or as a helix is known (Steudel et al., 1984). Although these materials are very hydrophobic and practically insoluble in water, shorter chains with hydrophilic endgroups may be water-soluble. For example, the inorganic polysulfide dianions S n are also known as solid salts as in both aqueous and nonaqueous solutions. The same holds true for the polythionate dianions S n O 6 with n > 2. By contrast, the chain-like diorganopolysulfanes such as dimethyl pentasulfane are highly hydrophobic and water-insoluble. In this chapter the term polymeric is used for compounds containing at least three sulfur atoms linked together. The S±S bonds in these compounds are very reactive under both reductive and
3 1 Introduction 37 Tab. 1 Examples of the nine oxidation states that sulfur atoms can adopt Sulfide Disulfide Sulfur Dichlorodisulfane Sulfoxylate Dithionite Sulfite Dithionate Sulfate HS S 2 S 8 S 2 Cl 2 SO 2 S 2 O 4 SO 3 S 2 O 6 SO 4 oxidative conditions. Reduction (uptake of electrons) results in a bond cleavage to give anions, whilst oxidation (uptake of oxygen) will provide oxides or a number of oxoanions with sulfate being the final oxidation product. On the other hand, the oxidation of anions such as hydrogen sulfide HS by loss of electrons yields products containing S±S bonds (e.g., polysulfides or elemental sulfur). The reversibility of these redox reactions and the many oxidation states that sulfur can adopt (see Table 1) make sulfur chemistry extremely interesting, but rather complex. Reactions of this type occur naturally in habitats where sulfur bacteria either oxidize reduced sulfur compounds, or reduce oxidized sulfur species. Elemental sulfur in the form of S 8 occurs naturally in huge deposits together with limestone (calcite CaCO 3 ), clay, anhydrite, or gypsum (CaSO 4 ). Its origin is explained by Reactions (1) and (2), which may take place either thermochemically or enzymatically as the consequence of the activity of sulfur bacteria (Hutcheon et al., 1995; CH 4 represents any hydrocarbon or organic matter): CaSO 4 CH 4! CaCO 3 H 2 S H 2 O (1) CaSO 4 3H 2 S CO 2! CaCO S 8 3H 2 O (2) Sulfur bacteria also take part in the global geobiochemical cycle of sulfur (Middelburg, 2000; Br ser et al., 2000). In addition, elemental sulfur is found in volcanic areas as a result of the oxidation of hydrogen sulfide (from volcanic gases) in air. Another characteristic property of compounds containing S±S bonds is their sensitivity towards light of wavelengths shorter than ca. 450 nm. Homolytic cleavage with the formation of sulfur radicals occurs on illumination (Steudel et al., 1989a). The major available forms of sulfur in nature are sulfate or sulfide in water or soil, and sulfur dioxide in the atmosphere (Brown, 1982; Middelburg, 2000), whilst thiosulfate, polythionates, sulfoxides, and elemental sulfur play a smaller but significant role. Sulfur in a nonpolymeric form is abundant in all organisms, appearing in many organic compounds with highly diverse biological functions such as amino acids, (poly)peptides, enzyme cofactors, antibiotics, lipids, or carbohydrates. The ubiquitous occurrence of organic disulfanes such as cystine and oxidized glutathione is also well established, while the rather widespread natural occurrence of tri- and higher polysulfanes with organic substituents has been demonstrated only relatively recently (Steudel and Kustos, 1994). The biological roles of inorganic sulfur compounds are rather restricted: either they serve as sources for sulfur assimilation and incorporation into the above-mentioned organic compounds, or they are employed as donors or acceptors of electrons for dissimilatory energy-generating electron transport. Assimilatory sulfur metabolism is very common in prokaryotes as well as in eukaryotes (animals, however, are generally not able to reduce sulfate). In contrast, sulfur-based energy generation with concomitant mass transformation occurs almost exclusively among prokaryotes
4 38 2 Metabolism of Natural Polymeric Sulfur Compounds Fig. 1 A simplified overview of the biological sulfur cycle in nature. (archaea and bacteria). The biological sulfur cycle (Figure 1) is therefore dominated by microorganisms. Inorganic sulfur compounds such as sulfide, polysulfides, sulfur, sulfite, thiosulfate, and various polythionates can serve as electron donors for the energy-generating systems of many photo- and chemotrophic bacteria (Brune, 1995; Kelly et al., 1997; Friedrich, 1998), of some archaea (Stetter, 1996), and even of some eukarya (Grieshaber and Vˆlkel, 1998). It should be mentioned that most of the sulfur oxidation observed in members of the Eukarya is mediated by lithoautotrophic bacterial endosymbionts (Nelson and Fisher, 1995). Although in general sulfate is the major oxidation product of reduced sulfur compound oxidation, other end-products may be formed depending on the organism. Further differences are found in the ability to use the various sulfur compounds. As a consequence, sulfur oxidation pathways are found to be widely variable and may involve different nonpolymeric and polymeric intermediates. In a reversal of dissimilatory sulfur oxidation, many prokaryotes can utilize a variety of organic and inorganic sulfur compounds (sulfate, sulfite, thiosulfate, organic sulfoxides, elemental sulfur, inorganic polysulfides, and organic disulfanes) as terminal electron acceptors of anaerobic respiration. This chapter summarizes the current knowledge about natural polymeric sulfur compounds, thereby focusing on the mass turnover reactions catalyzed by prokaryotes using sulfur compounds as the basis of their energy metabolism. We should also emphasize that polymeric sulfur compounds are not only produced by biological processes, but chemical, geochemical and biological processes are also interconnected in this respect. For details relating to particular aspects of this subject, the reader is referred to a number of reviews on the dissimilatory reduction of oxidized sulfur compounds ( Widdel and Hansen, 1992; Hansen, 1994; Hamilton, 1998; Hedderich et al., 1999), the
5 3 Chemical Structures 39 dissimilatory oxidation of reduced sulfur compounds (Harrison, 1984; Tr per, 1989; Pronk et al., 1990; Takakuwa, 1992; Brune, 1989, 1995; Kelly et al., 1997; Kelly, 1999; Friedrich, 1998; Imhoff, 1999; Overmann and van Gemerden, 2000; Friedrich et al., 2001), assimilatory S-reduction (Le Faou et al., 1990; Kredich, 1996; Marzluf, 1997; Leustek and Saito, 1999), organylsulfanes (Kelly and Smith, 1990; Steudel and Kustos, 1994), and polythioethers (see also Chapter 4, Polythioesters) (L tke-eversloh et al., 2001a,b). 2 Historical Outline The elucidation of the microbiology and biochemistry of sulfur bacteria, and the discovery and investigation of bacterial sulfur globules has a very long history. As long ago as 1786, M ller reported a colorless, egg-shaped alga with spherical inclusions, which was later recognized as a sulfur bacterium with sulfur inclusions by Warming (1875) and described as Monas muelleri (Thiovulum muelleri). In the 19th century, the purple sulfur bacterium Monas vinosa (Allochromatium vinosum) (Ehrenberg, 1838; Perty, 1852) and the chemotrophic, colorless sulfur bacterium Beggiatoa (Beggiato, 1838; Trevisan, 1842; Cohn, 1865) and their inclusions were discovered and described. However, it was not until 30 years later that Cramer (1870) and Cohn (1875) were able to identify the inclusions as elemental sulfur by extraction with carbon disulfide. The first detailed description of sulfur bacteria and sulfur globules was given by Winogradsky (1887), who proposed the term sulfur bacteria for organisms accumulating sulfur inside the cells. Winogradsky (1889) subsequently demonstrated the oxidation of hydrogen sulfide to sulfur under microaerophilic conditions in Beggiatoa. It was Beijerinck (1895) who discovered the sulfate-reducing bacteria and described a strict anaerobic bacterium, Spirillum desulfuricans, which uses malate to reduce sulfate to sulfide. Beijerinck recognized the difference between dissimilatory sulfate reduction and the release of assimilatory reduced sulfur. Following Beijerinck's initial work, van Delden (1903) reported on marine and salt-tolerant sulfate-reducing bacteria, while Elion (1925) described thermophilic types. Beijerinck also isolated the chemotrophic sulfur oxidizers Thiobacillus thioparus and Thiobacillus denitrificans (Beijerinck, 1904a,b). Nadson (1906) described the first green sulfur bacterium Chlorobium limicola, and Buder (1915, 1919) carried out fundamental studies on the physiology of purple sulfur bacteria. A good overview of the studies conducted during the early part of the 20th century is provided by Bavendamm (1924) and by Bunker (1936). Pioneering studies on the oxidation of sulfur in bacterial photosynthesis were performed by van Niel, whose classic studies on phototrophic sulfur bacteria and the accumulation of elemental sulfur may be considered as milestones, and provided the basis for further studies on sulfur compounds in photosynthesis (van Niel, 1931, 1936). During the second half of the 20th century, many scientists and research groups focused on diverse sulfur bacteria (metabolism, ecology, and genetics). For detailed information, the reader is referred to the reviews cited in the Introduction. 3 Chemical Structures The structures of the cyclo-octasulfur molecule S 8, the hexasulfide dianion S 6 in the cesium salt Cs 2 S 6, the pentathionate dianion
6 40 2 Metabolism of Natural Polymeric Sulfur Compounds S 5 O 6 in K 2 S 5 O 6, and the dimethylpentasulfane molecule (CH 3 ) 2 S 5 (Wells, 1984) are representative examples of the chemical compounds discussed in this chapter (Figure 2). 4 Hydrogen Sulfide and Inorganic Polysulfides Hydrogen sulfide, the most reduced form of sulfur, is ubiquitous in natural aqueous environments and is often accompanied by polysulfides. 4.1 Chemistry, Structures and Characterization In water, H 2 S is partly ionized, the equilibrium being strongly influenced by the ph value: H 2 S H 2 O > H 3 O HS K c ˆ 1.0 î 10 7 mol L 1 (208C) (3) Except at the highest ph values, the concentration of sulfide ions S is negligible (Phillips and Phillips, 2000). The electrochemical or chemical oxidation of hydrogen sulfide ions (by suitable oxidants in singleelectron steps) results in disulfide ions which may be oxidized further to higher inorganic polysulfides and eventually to elemental sulfur (Steudel, 1996): Fig. 2 Chemical structures of the sulfur-rich biopolymers cyclo-s 8, S 6, S 5 O 6 and (CH 3 ) 2 S 5. The conventional structural formulae as well as space-filling models are shown.
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