Microbial Assimilation and Dissimilation of Sulfonate Sulfur

Abstract

A wide variety of microbes use sulfonate-sulfur as the sole sulfur source for biosynthesis even when the carbon of that sulfonate cannot be used as an energy source for growth. Our studies of bacteria, including members of the genera Comamonas and Escherichia, as well as ascomycetous and basidiomycetous yeasts indicate that the sulfur of many naturally-occurring sulfonates can be reduced and assimilated into cellular sulfur compounds during aerobic, respiratory growth. Other unrelated bacteria (e.g. members of the genera Clostridium, Klebsiella) are able to use sulfonate-sulfur for biosynthesis under anaerobic conditions. Sulfonate can also serve as the terminal electron acceptor for Desulfovibrio's anaerobic respiration. The breadth of microbial participation in sulfonate-sulfur transformations in the natural sulfur cycle is thus established.Sulfonates, organosulfur compounds containing the R-CH n -S0 3 H moiety, occur in the biosphere as a result of synthesis by diverse organisms and introduction by human activity. Naturally-produced sulfonates (see Table I for some examples) include taurine in the hearts and/or eyes of vertebrates (7, 2), coenzyme M in the methanogenic Archaea (3), aeruginosin, a pigment in some pseudomonads (4), the sulfonolipids of gliding bacteria (5) and diatoms (6), taurocholic acid in the digestive system of many mammals (7), sulfolactate in Bacillus subtilis spores (8), and isethionate in the axoplasm of squid (9). Some natural sulfonates are secondary products of the breakdown of other sulfur compounds. Methanesulfonate, for instance, is a product of the chemical oxidation in the atmosphere of dimethylsulfide (10, 11) which is produced by phytoplankton (12-14) and marsh grass (75). Thus, these biosynthesized sulfonates range from very simple short chains to aromatic structures. Examples of commercially-produced sulfonates include laboratory buffers such as HEPES, MOPS, and MES, the aminobenzenesulfonates which are used in the manufacture of dyes (16) and optical brighteners, the detergent-additive toluenesulfonate (77), and linear alkylsulfonate surfactants (18).It is to be expected that the naturally-occurring sulfonates, at least, would be 0097-6156/95/0612-0365$12.00/0

Bioavailability of water-polluting sulfonoaromatic compounds

“…Most xenobiotic organosulfonates which we and others have examined as sulfur sources for growth of aerobic bacteria, are subject to desulfonation (Table 1, Table 2; Dudley and Frost 1994; Kertesz et al 1994b;Key et al 1998;King and Quinn 1997;Laue et al 1996;Rein and Cook 1999;Seitz and Leadbetter 1995;ZuÈ rrer et al 1987), so we believe that there is an enormous potential for desulfonation in the natural environment, apart from those organisms which degrade natural and xenobiotic products as carbon sources. This is perhaps not surprising, given the large percentage of sulfonates in soil and sediment sulfur, and the facts that humic materials are sulfonates and subject to rapid¯ux in soil (reviewed in Cook et al 1998).…”

Thiosulfate as a metabolic product: the bacterial fermentation of taurine

“…The absence of an external electron acceptor and the internally balanced redox reactions, whereby oxidation of the carbon moiety to acetate and reduction of sulfonate moiety to thiosulfate occur, mark this as a fermentation. This is, thus, the first reported fermentation of a sulfonate [see review by Seitz and Leadbetter (1995)]. …”

“…Naturally occurring, defined organosulfonate compounds with the thermostable C-SO 3 -bond are not numerous [Seitz and Leadbetter 1995;see also Van Loon et al (1993)], but they occupy important metabolic and physiological niches, and taurine (2-aminoethanesulfonate), with its myriad functions in mammals and many other organisms (Huxtable 1992), is perhaps the best known. The catabolism of organosulfonates, whether of the natural products or of the numerous xenobiotic compounds, was thought to be the preserve of aerobic organisms (Denger et al 1996;Fuchs et al 1994), but this view changed when two research groups discovered that sulfonate sulfur could be assimilated by strictly anaerobic bacteria, Clostridium spp.…”

“…Seitz and Leadbetter (1995)]. Strain GKNTAU (with the similar strain GRZTAU) was found to represent a novel genus and to yield an initially unidentified fermentation product, thiosulfate, quantitatively from the sulfonate moiety of the substrate.…”

Assimilation of sulfur from alkyl- and arylsulfonates by Clostridium spp.

“…Discovery of desulfonation involving assimilation of the sulfur moiety (Chien et al 1995;Seitz and Leadbetter 1995;Denger et al 1996) was followed by dissimilation (reduction) associated with an anaerobic respiration (Lie et al 1996; H. Laue, K. Denger and A.M. Cook, unpublished work), by dissimilation (oxidation) coupled to nitrate respiration (Denger et al 1997), and by fermentation (K. Denger, H. Laue and A.M. Cook, unpublished work).…”