Kinetic analysis and substrate specificity of Escherichia coli dimethyl sulfoxide reductase

Simala‐Grant, Joanne L.; Weiner, Joël H.

doi:10.1099/13500872-142-11-3231

Cited by 55 publications

(50 citation statements)

References 36 publications

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“…E. coli synthesizes several molybdoreductases which can act on MetSO. These enzymes are members of the so-called dimethyl sulfoxide reductase family and include the dimethyl sulfoxide/ TMAO (trimethylamine N-oxide) reductase DmsA (25) and the TMAO reductase TorZ (8). However, DmsA is synthesized Growth experiments were carried out as described for panel A except that glycerol was used as a carbon source and arabinose was present to induce expression of plasmid-borne genes.…”

Section: Discussionmentioning

confidence: 99%

Methionine Sulfoxide Reduction and Assimilation in Escherichia coli : New Role for the Biotin Sulfoxide Reductase BisC

et al. 2005

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Methionine ranks among the amino acids most sensitive to oxidation, which converts it to a racemic mixture of methionine-S-sulfoxide (Met-S-SO) and methionine-R-sulfoxide (Met-R-SO). The methionine sulfoxide reductases MsrA and MsrB reduce free and protein-bound MetSO, MsrA being specific for Met-S-SO and MsrB for Met-R-SO. In the present study, we report that an Escherichia coli metB 1 auxotroph lacking both msrA and msrB is still able to use either of the two MetSO enantiomers. This indicates that additional methionine sulfoxide reductase activities occur in E. coli. BisC, a poorly characterized biotin sulfoxide reductase, was identified as one of these new methionine sulfoxide reductases. BisC was purified and found to exhibit reductase activity with free Met-S-SO but not with free Met-R-SO as a substrate. Moreover, a metB 1 msrA msrB bisC strain of E. coli was unable to use Met-S-SO for growth, but it retained the ability to use Met-R-SO. Mass spectrometric analyses indicated that BisC is unable to reduce protein-bound Met-S-SO. Hence, this study shows that BisC has an essential role in assimilation of oxidized methionines. Moreover, this work provides the first example of an enzyme that reduces free MetSO while having no activity on peptide-bound MetSO residues.

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Section: Discussionmentioning

confidence: 99%

Methionine Sulfoxide Reduction and Assimilation in Escherichia coli : New Role for the Biotin Sulfoxide Reductase BisC

et al. 2005

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“…As shown previously, unlike the membranous DMSO reductase and the Rhodobacter DorA enzyme, TorA is unable to reduce DMSO (23,42,43,45). As expected, when the strain LCB504 harboring plasmid ptorCAD was grown in minimal media in the presence of DMSO, no growth was detected (Table 2).…”

Section: Gene Organization and Putative Products Of The Bisz Locusmentioning

confidence: 73%

“…The kinetic study was performed on the purified product of torZ (bisZ) as described in the Materials and Methods. The compounds tested were structurally related to TMAO or DMSO and have been previously used to determine the specificity of TorA and the membranous DMSO reductase of E. coli (23,45).…”

Section: Gene Organization and Putative Products Of The Bisz Locusmentioning

confidence: 99%

“…In this family of molybdoenzymes, three groups of enzymes can be defined, as follows: (i) the specific TMAO reductases encoded by torA of E. coli or Shewanella massilia, which do not have any S-oxide reductase activity and can only reduce TMAO as a natural substrate (13, 23); (ii) the TMAO-DMSO reductases like the DmsA subunit of the E. coli membranous DMSO reductase or the periplasmic DorA and DmsA enzymes of Rhodobacter capsulatus and Rhodobacter sphaeroides, respectively, which are able to reduce a wide range of Nand S-oxide compounds, including DMSO and TMAO (42,45); and (iii) the biotin d-sulfoxide reductases like BisC from E. coli and the biotin sulfoxide (BSO) reductase from R. sphaeroides, which are cytoplasmic enzymes involved primarily in the recycling of biotin from BSO (33,34). An in vitro study showed that the R. sphaeroides enzyme can also poorly reduce other Nand S-oxides like TMAO and DMSO (17,34).…”

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confidence: 99%

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The torYZ ( yecK bisZ ) Operon Encodes a Third Respiratory Trimethylamine N -Oxide Reductase in Escherichia coli

et al. 2000

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The bisZ gene of Escherichia coli was previously described as encoding a minor biotin sulfoxide (BSO) reductase in addition to the main cytoplasmic BSO reductase, BisC. In this study, bisZ has been renamed torZ based on the findings that (i) the torZ gene product, TorZ, is able to reduce trimethylamine N-oxide (TMAO) more efficiently than BSO; (ii) although TorZ is more homologous to BisC than to the TMAO reductase TorA (63 and 42% identity, respectively), it is located mainly in the periplasm as is TorA; (iii) torZ belongs to the torYZ operon, and the first gene, torY (formerly yecK), encodes a pentahemic c-type cytochrome homologous to the TorC cytochrome of the TorCAD respiratory system. Furthermore, the torYZ operon encodes a third TMAO respiratory system, with catalytic properties that are clearly different from those of the TorCAD and the DmsABC systems. The torYZ and the torCAD operons may have diverged from a common ancestor, but, surprisingly, no torD homologue is found in the sequences around torYZ. Moreover, the torYZ operon is expressed at very low levels under the conditions tested, and, in contrast to torCAD, it is not induced by TMAO or dimethyl sulfoxide.Escherichia coli can survive in various growth conditions owing to its ability to adapt in response to environmental changes. For example, in anaerobiosis and according to the exogenous electron acceptor present in the medium, this organism synthesizes the energetically more appropriate respiratory system (18). Sometimes, more than one respiratory system is produced for a given substrate. For instance, reduction of nitrate can be carried out by at least three respiratory systems (10). At high concentrations of nitrate, only the membranous NarG system is synthesized (46), whereas at very low concentrations, the periplasmic Nap system is produced (36). The operon encoding a third system (NarZ) is expressed during the early stationary phase under control of s , irrespective of the presence of nitrate (8). Accordingly, whatever the nitrate concentration and the growth phase, at least one of the nitrate reductases is synthesized in the cell (8,36).Trimethylamine N-oxide (TMAO) is reduced to the volatile compound trimethylamine (TMA) by at least two respiratory systems, the TorCAD and the DmsABC systems (5, 29). The torCAD operon, which encodes the periplasmic Tor system, is induced in the presence of TMAO by the TorS-TorR twocomponent regulatory system (25), whereas the membranous dimethyl sulfoxide (DMSO) reductase system, encoded by the dmsABC operon, is synthesized constitutively in anaerobiosis (5). The reason for the presence in the same host of several systems dedicated to a common substrate is still unclear, but one possibility is that they allow the cell to better adapt to changing environmental conditions during the different growth phases.The terminal reductase of the inducible Tor pathway, TorA, encoded by the torA gene, is a periplasmic molybdoenzyme of 90 kDa (29) that is thought to receive electrons from the membrane pool of menaquinone ...

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“…These enzymes, called TorA, were found in particular in the periplasm of Escherichia coli and Shewanella species (6,10,20). The DMSO reductases, called DorA or DmsA, can reduce a wide range of N-and S-oxide compounds, including DMSO and TMAO (25,26). They are present in many species, including enterobacteria and Rhodobacter species (19).…”

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confidence: 99%

Effects of ISSo 2 Insertions in Structural and Regulatory Genes of the Trimethylamine Oxide Reductase of Shewanella oneidensis

et al. 2003

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We have isolated three Shewanella oneidensis mutants specifically impaired in trimethylamine oxide (TMAO) respiration. The mutations arose from insertions of an ISSo2 element into torA, torR, and torS, encoding, respectively, the TMAO reductase TorA, the response regulator TorR, and the sensor TorS. Although TorA is not the sole enzyme reducing TMAO in S. oneidensis, growth analysis showed that it is the main respiratory TMAO reductase. Use of a plasmid-borne torE-lacZ fusion confirmed that the TorS-TorR phosphorelay mediates TMAO induction of the torECAD operon.Trimethylamine oxide (TMAO) is a widespread osmoprotective constituent of aquatic animals (17) which can be used by many bacteria as an alternative terminal electron acceptor (3). Reduction of TMAO to the volatile compound trimethylamine generally involves molybdenum-containing enzymes of the same family (6). However, based on their substrate specificity, these enzymes can be divided into two subfamilies: the TMAO reductase and the dimethyl sulfoxide (DMSO) reductase groups. The TMAO reductase enzymes are highly specific, since they can reduce exclusively TMAO as a natural compound or related artificial compounds (13). These enzymes, called TorA, were found in particular in the periplasm of Escherichia coli and Shewanella species (6,10,20). The DMSO reductases, called DorA or DmsA, can reduce a wide range of N-and S-oxide compounds, including DMSO and TMAO (25,26). They are present in many species, including enterobacteria and Rhodobacter species (19).It has been recently shown in E. coli that the TorA protein binds to the pentaheme c-type cytochrome TorC (8). The latter is anchored to the inner membrane and allows electron transfer between the membranous quinone pool and the periplasmic terminal enzyme TorA. In E. coli and Shewanella species, the genes encoding the components of the TMAO reductase system are clustered in the torCAD and torECAD operons, respectively (6,10,20). Three regulatory genes called torR, torS, and torT are found near the tor operons. A detailed analysis of the Tor regulatory elements of E. coli revealed that TorS is the transmembrane sensor that detects the presence of TMAO in the medium and monitors the proper maturation of TorC (9, 15). TorS contains three phosphorylation sites and transphosphorylates the response regulator TorR by a fourstep phosphorelay under inducing conditions (14). Once phosphorylated, TorR activates torCAD expression (2). TorT is a periplasmic protein essential for tor operon induction, but its precise role remains unclear (16).Genes of Shewanella oneidensis encoding proteins homologous to TorS, TorR, and TorT of E. coli were identified and called torS, torR, and torT (10). However, as no S. oneidensis mutant was available, their regulatory functions were investigated by reconstitution experiments in E. coli. This approach showed that the three proteins seem to be essential for induction of the tor operon of S. oneidensis.Isolation of S. oneidensis mutants specifically affected in TMAO respiration. To iso...

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Kinetic analysis and substrate specificity of Escherichia coli dimethyl sulfoxide reductase

Cited by 55 publications

References 36 publications

Methionine Sulfoxide Reduction and Assimilation in Escherichia coli : New Role for the Biotin Sulfoxide Reductase BisC

Methionine Sulfoxide Reduction and Assimilation in Escherichia coli : New Role for the Biotin Sulfoxide Reductase BisC

The torYZ ( yecK bisZ ) Operon Encodes a Third Respiratory Trimethylamine N -Oxide Reductase in Escherichia coli

Effects of ISSo 2 Insertions in Structural and Regulatory Genes of the Trimethylamine Oxide Reductase of Shewanella oneidensis

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