Abstract
Organosulfonates are important natural and man-made compounds, but until recently (T. J. Lie, T. Pitta, E. R. Leadbetter, W. Godchaux III, and J. R. Leadbetter. Arch. Microbiol. 166:204-210, 1996), they were not believed to be dissimilated under anoxic conditions. We also chose to test whether alkane- and arenesulfonates could serve as electron sinks in respiratory metabolism. We generated 60 anoxic enrichment cultures in mineral salts medium which included several potential electron donors and a single organic sulfonate as an electron sink, and we used material from anaerobic digestors in communal sewage works as inocula. None of the four aromatic sulfonates, the three unsubstituted alkanesulfonates, or the N-sulfonate tested gave positive enrichment cultures requiring both the electron donor and electron sink for growth. Nine cultures utilizing the natural products taurine, cysteate, or isethionate were considered positive for growth, and all formed sulfide. Two clearly different pure cultures were examined. Putative Desulfovibrio sp. strain RZACYSA, with lactate as the electron donor, utilized sulfate, aminomethanesulfonate, taurine, isethionate, and cysteate, converting the latter to ammonia, acetate, and sulfide. Strain RZATAU was identified by 16S rDNA analysis as Bilophila wadsworthia. In the presence of, e.g., formate as the electron donor, it utilized, e.g., cysteate and isethionate and converted taurine quantitatively to cell material and products identified as ammonia, acetate, and sulfide. Sulfite and thiosulfate, but not sulfate, were utilized as electron sinks, as was nitrate, when lactate was provided as the electron donor and carbon source. A growth requirement for 1,4-naphthoquinone indicates a menaquinone electron carrier, and the presence of cytochrome c supports the presence of an electron transport chain. Pyruvate-dependent disappearance of taurine from cell extracts, as well as formation of alanine and release of ammonia and acetate, was detected. We suspected that sulfite is an intermediate, and we detected desulfoviridin (sulfite reductase). We thus believe that sulfonate reduction is one aspect of a respiratory system transferring electrons from, e.g., formate to sulfite reductase via an electron transport system which presumably generates a proton gradient across the cell membrane.
Full Text
The Full Text of this article is available as a PDF (555.9 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Badziong W., Thauer R. K. Growth yields and growth rates of Desulfovibrio vulgaris (Marburg) growing on hydrogen plus sulfate and hydrogen plus thiosulfate as the sole energy sources. Arch Microbiol. 1978 May 30;117(2):209–214. doi: 10.1007/BF00402310. [DOI] [PubMed] [Google Scholar]
- Baron E. J., Summanen P., Downes J., Roberts M. C., Wexler H., Finegold S. M. Bilophila wadsworthia, gen. nov. and sp. nov., a unique gram-negative anaerobic rod recovered from appendicitis specimens and human faeces. J Gen Microbiol. 1989 Dec;135(12):3405–3411. doi: 10.1099/00221287-135-12-3405. [DOI] [PubMed] [Google Scholar]
- Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
- Chung K. T., Stevens S. E., Jr, Cerniglia C. E. The reduction of azo dyes by the intestinal microflora. Crit Rev Microbiol. 1992;18(3):175–190. doi: 10.3109/10408419209114557. [DOI] [PubMed] [Google Scholar]
- Denger K., Cook A. M. Assimilation of sulfur from alkyl- and arylsulfonates by Clostridium spp. Arch Microbiol. 1997 Feb-Mar;167(2-3):177–181. [PubMed] [Google Scholar]
- Denger K., Kertesz M. A., Vock E. H., Schon R., Magli A., Cook A. M. Anaerobic Desulfonation of 4-Tolylsulfonate and 2-(4-Sulfophenyl) Butyrate by a Clostridium sp. Appl Environ Microbiol. 1996 May;62(5):1526–1530. doi: 10.1128/aem.62.5.1526-1530.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ensley B. D., Gibson D. T., Laborde A. L. Oxidation of naphthalene by a multicomponent enzyme system from Pseudomonas sp. strain NCIB 9816. J Bacteriol. 1982 Mar;149(3):948–954. doi: 10.1128/jb.149.3.948-954.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Feigel B. J., Knackmuss H. J. Syntrophic interactions during degradation of 4-aminobenzenesulfonic acid by a two species bacterial culture. Arch Microbiol. 1993;159(2):124–130. doi: 10.1007/BF00250271. [DOI] [PubMed] [Google Scholar]
- Focht D. D., Williams F. D. The degradation of p-toluenesulfonate by a Pseudomonas. Can J Microbiol. 1970 May;16(5):309–316. doi: 10.1139/m70-056. [DOI] [PubMed] [Google Scholar]
- Holliger C., Kengen S. W., Schraa G., Stams A. J., Zehnder A. J. Methyl-coenzyme M reductase of Methanobacterium thermoautotrophicum delta H catalyzes the reductive dechlorination of 1,2-dichloroethane to ethylene and chloroethane. J Bacteriol. 1992 Jul;174(13):4435–4443. doi: 10.1128/jb.174.13.4435-4443.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huxtable R. J. Physiological actions of taurine. Physiol Rev. 1992 Jan;72(1):101–163. doi: 10.1152/physrev.1992.72.1.101. [DOI] [PubMed] [Google Scholar]
- Junker F., Field J. A., Bangerter F., Ramsteiner K., Kohler H. P., Joannou C. L., Mason J. R., Leisinger T., Cook A. M. Oxygenation and spontaneous deamination of 2-aminobenzenesulphonic acid in Alcaligenes sp. strain O-1 with subsequent meta ring cleavage and spontaneous desulphonation to 2-hydroxymuconic acid. Biochem J. 1994 Jun 1;300(Pt 2):429–436. doi: 10.1042/bj3000429. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kondo H., Ishimoto M. Enzymatic formation of sulfite and acetate from sulfoacetaldehyde, a degradation product of taurine. J Biochem. 1972 Aug;72(2):487–489. doi: 10.1093/oxfordjournals.jbchem.a129926. [DOI] [PubMed] [Google Scholar]
- Kondo H., Ishimoto M. Purification and properties of sulfoacetaldehyde sulfo-lyase, a thiamine pyrophosphate-dependent enzyme forming sulfite and acetate. J Biochem. 1975 Aug;78(2):317–325. doi: 10.1093/oxfordjournals.jbchem.a130910. [DOI] [PubMed] [Google Scholar]
- Kondo H., Ishimoto M. Taurine dehydrogenase. Methods Enzymol. 1987;143:496–499. doi: 10.1016/0076-6879(87)43089-9. [DOI] [PubMed] [Google Scholar]
- Lie T. J., Pitta T., Leadbetter E. R., Godchaux W., 3rd, Leadbetter J. R. Sulfonates: novel electron acceptors in anaerobic respiration. Arch Microbiol. 1996 Sep;166(3):204–210. doi: 10.1007/s002030050376. [DOI] [PubMed] [Google Scholar]
- Locher H. H., Leisinger T., Cook A. M. 4-Sulphobenzoate 3,4-dioxygenase. Purification and properties of a desulphonative two-component enzyme system from Comamonas testosteroni T-2. Biochem J. 1991 Mar 15;274(Pt 3):833–842. doi: 10.1042/bj2740833. [DOI] [PMC free article] [PubMed] [Google Scholar]
- POSTGATE J. R. Cytochrome c3 and desulphoviridin; pigments of the anaerobe Desulphovibrio desulphuricans. J Gen Microbiol. 1956 Jul;14(3):545–572. doi: 10.1099/00221287-14-3-545. [DOI] [PubMed] [Google Scholar]
- POSTGATE J. A diagnostic reaction of Desulphovibrio desulphuricans. Nature. 1959 Feb 14;183(4659):481–482. doi: 10.1038/183481b0. [DOI] [PubMed] [Google Scholar]
- Shimamoto G., Berk R. S. Taurine catabolism. II. biochemical and genetic evidence for sulfoacetaldehyde sulfo-lyase involvement. Biochim Biophys Acta. 1980 Sep 17;632(1):121–130. doi: 10.1016/0304-4165(80)90255-x. [DOI] [PubMed] [Google Scholar]
- Stipanuk M. H., Hirschberger L. L., De la Rosa J. Cysteinesulfinic acid, hypotaurine, and taurine: reversed-phase high-performance liquid chromatography. Methods Enzymol. 1987;143:155–160. doi: 10.1016/0076-6879(87)43028-0. [DOI] [PubMed] [Google Scholar]
- Thauer R. K., Jungermann K., Decker K. Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev. 1977 Mar;41(1):100–180. doi: 10.1128/br.41.1.100-180.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thysse G. J., Wanders T. H. Initial steps in the degradation of n-alkane-1-sulphonates by Pseudomonas. Antonie Van Leeuwenhoek. 1974;40(1):25–37. doi: 10.1007/BF00394550. [DOI] [PubMed] [Google Scholar]
- Widdel F., Pfennig N. Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids. I. Isolation of new sulfate-reducing bacteria enriched with acetate from saline environments. Description of Desulfobacter postgatei gen. nov., sp. nov. Arch Microbiol. 1981 Jul;129(5):395–400. doi: 10.1007/BF00406470. [DOI] [PubMed] [Google Scholar]
- Zürrer D., Cook A. M., Leisinger T. Microbial desulfonation of substituted naphthalenesulfonic acids and benzenesulfonic acids. Appl Environ Microbiol. 1987 Jul;53(7):1459–1463. doi: 10.1128/aem.53.7.1459-1463.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]