Sulfonates: novel electron acceptors in anaerobic respiration

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© Springer-Verlag 1996

O R I G I N A L PA P E R

Thomas J. Lie · Thomas Pitta · Edward R. Leadbetter · Walter Godchaux III · Jared R. Leadbetter

Sulfonates: novel electron acceptors in anaerobic respiration

Received: 2 May 1996 / Accepted: 8 June 1996

Abstract The enrichment and isolation in pure culture of a bacterium, identified as a strain of Desulfovibrio, able to release and reduce the sulfur of isethionate (2-hydroxyethanesulfonate) and other sulfonates to support anaerobic respiratory growth, is described. The sulfonate moiety was the source of sulfur that served as the terminal electron acceptor, while the carbon skeleton of isethionate functioned as an accessory electron donor for the reduction of sulfite. Cysteate (alanine-3-sulfonate) and sulfoacetaldehyde (acetaldehyde-2-sulfonate) could also be used for anaerobic respiration, but many other sulfonates could not. A survey of known sulfate-reducing bacteria revealed that some, but not all, strains tested could utilize the sulfur of some sulfonates as terminal electron acceptor. Isethionate-grown cells of Desulfovibrio strain IC1 reduced sulfonate-sulfur in preference to that of sulfate; however, sulfate-grown cells reduced sulfate-sulfur in preference to that of sulfonate. Key words Sulfonate metabolism · Sulfate-reducing bacteria · Dissimilatory reduction of sulfonate-sulfur · Desulfovibrio

Introduction Sulfonates are organosulfur compounds (Fig. 1) in which the sulfur atom is covalently bound to a carbon atom and

T. J. Lie · E. R. Leadbetter (Y) · W. Godchaux III Department of Molecular and Cell Biology, University of Connecticut, Storrs CT 06269-2131, USA Tel. +1-860-486-1931; Fax +1-860-486-1936 email: [email protected] T. Pitta Rowland Institute for Science, Cambridge MA 02142, USA J. R. Leadbetter Department of Microbiology, Michigan State University, East Lansing, MI 48824, USA

Fig. 1 Structures and trivial names of some aliphatic sulfonates. Sulfur oxidation state: +5

in which the sulfur is at an oxidation state of +5 (Vairavamurthy et al. 1993). Examples of sulfonates produced by diverse biota include sulfonolipids of bacteria, coenzyme M of methanogenic Archaea, sulfoquinovosyl diglyceride of phototrophs, isethionate of the squid axon, and taurine of vertebrate heart muscle and of several algae [for a short review, see Seitz and Leadbetter (1995)]. Taurine is also included in several „health“ drinks. Many sulfonate detergents, chemical dyes, and biological buffers (e.g., Hepes and Mopso) are products of industrial processes and have been introduced into natural habitats. Sulfonate-sulfur has been detected in forest soils (Fitzgerald 1976; Watwood et al. 1988) and in marine sediments (Vairavamurthy et al. 1994); the precise chemical structures of these organosulfur compounds remain unknown. For some time it has been known that sulfonates can be metabolized as sole sources of carbon, energy, and (often) sulfur for aerobic bacterial growth (Stapley and Starkey 1970; Hashim et al. 1992; Thompson et al. 1995). More recent studies demonstra