Anaerobic metabolism of the L-rhamnose fermentation product 1,2-propanediol in Salmonella typhimurium

Abstract

When grown anaerobically on L-rhamnose, Salmonella typhimurium excreted 1,2-propanediol as a fermentation product. Upon exhaustion of the methyl pentose, 1,2-propanediol was recaptured and further metabolized, provided the culture was kept under anaerobic conditions. n-Propanol and propionate were found in the medium as end products of this process at concentrations one-half that of 1,2-propanediol. As in Klebsiella pneumoniae (T. Toraya, S. Honda, and S. Fukui, J. Bacteriol. 139:3947, 1979), a diol dehydratase which transforms 1,2-propanediol to propionaldehyde and the enzymes involved in a dismutation that converts propionaldehyde to n-propanol and propionate were induced in S. typhimurium cultures able to transform 1,2-propanediol anaerobically.In Escherichia coli, L-rhamnose is metabolized by the sequential action of a rhamnose permease that transports the sugar across the membrane, a rhamnose isomerase (20) that converts it to L-rhamnulose, a rhamnulose kinase (21) that phosphorylates the L-rhamnulose to L-rhamnulose 1-phosphate, and an aldolase (5) that cleaves the L-rhamnulose 1-phosphate into dihydroxyacetone phosphate and L-lactaldehyde. Although no detailed description of the enzymes has been reported, the same pathway has been described in Salmonella typhosa (7) and Salmonella typhimurium (1).Under anaerobic conditions, E. coli induces an NADHdependent oxidoreductase that reduces L-lactaldehyde to 1,2-propanediol, which is excreted into the medium (4). On the basis of propanediol oxidoreductase activity induction and propanediol excretion, this fermentation mechanism has also been proposed for S. typhimurium (3). However, 1,2-propanediol, which is not further metabolized in anaerobic E. coli cultures, gradually disappears from the medium in S. typhimurium cultures maintained under similar anaerobic conditions (J. Badia, unpublished observation).Aerobic metabolism of 1,2-propanediol has been described for several species (9, 13) and for mutant cells of E. coli (18) able to grow on the diol. In all cases the first step is the oxidation to lactaldehyde through the action of an oxidoreductase. Lactaldehyde is subsequently metabolized to lactate and pyruvate (6,17). In contrast, anaerobic metabolism of 1,2-propanediol in Klebsiella pneumoniae (22) or Clostridium glycolicum (8) has been reported to be mediated by a coenzyme B12-dependent diol dehydratase that yields propionaldehyde, which is immediately metabolized by a dismutation to n-propanol and propionate.In this report we characterize the 1,2-propanediol transformation that occurs in S. typhimurium cultures and establish the metabolic pathway involved.

Protein Content of Polyhedral Organelles Involved in Coenzyme B 12 -Dependent Degradation of 1,2-Propanediol in Salmonella enterica Serovar Typhimurium LT2

“…As a group, these enzymes are sufficient to mediate the conversion of 1,2-PD to propionyl-CoA. Ado-B 12 -dependent diol dehydratase catalyzes the conversion of 1,2-PD to propionaldehyde, which is then converted to propionyl-CoA by the CoA-dependent propionaldehyde dehydrogenase (1,24,37). Adenosyltransferase and the PduGH reactivating factor are needed to maintain diol dehydratase in an active form (20).…”

“…Degradation occurs aerobically, or anaerobically if tetrathionate is added as a terminal electron acceptor (26). Based on biochemical studies, a pathway for 1,2-PD degradation has been proposed (24,37). Breakdown initiates with the conversion of 1,2-PD to propionaldehyde by Ado-B 12 -dependent diol dehydratase (1).…”

Biochemical evidence that the pduS gene encodes a bifunctional cobalamin reductase

“…1,2-PD is a major product of the fermentation of the common plant sugars rhamnose and fucose and is thought to be an important carbon source in anaerobic environments such as the large intestines of higher animals (Obradors et al, 1988;Toraya et al, 1980). Virtually all natural isolates of Salmonella degrade 1,2-PD and in vivo studies with mice have suggested that the degradation of this small molecule may be important for the interaction of S. enterica with its host organisms (Conner et al, 1998;Heithoff et al, 1999).…”

“…The pathway of 1,2-PD degradation begins with the conversion of 1,2-PD to propionaldehyde by AdoCbldependent diol dehydratase (Bobik et al, 1997;Obradors et al, 1988;Toraya et al, 1979). Subsequently, propionaldehyde is converted to propanol and propionate by alcohol dehydrogenase, CoA-dependent propionaldehyde dehydrogenase, phosphotransacylase and propionate kinase (Obradors et al, 1988;Toraya et al, 1979).…”

“…1,2-PD is a major product of the fermentation of the common plant sugars rhamnose and fucose and is thought to be an important carbon source in anaerobic environments such as the large intestines of higher animals (Obradors et al, 1988;Toraya et al, 1980). Virtually all natural isolates of Salmonella degrade 1,2-PD and in vivo studies with mice have suggested that the degradation of this small molecule may be important for the interaction of S. enterica with its host organisms (Conner et al, 1998;Heithoff et al, 1999).The pathway of 1,2-PD degradation begins with the conversion of 1,2-PD to propionaldehyde by AdoCbldependent diol dehydratase (Bobik et al, 1997;Obradors et al, 1988;Toraya et al, 1979). Subsequently, propionaldehyde is converted to propanol and propionate by alcohol dehydrogenase, CoA-dependent propionaldehyde dehydrogenase, phosphotransacylase and propionate kinase (Obradors et al, 1988;Toraya et al, 1979).…”