Sulfonate-sulfur metabolism and its regulation in Escherichia coli

Abstract. In the absence of sulfate and cysteine, Escherichia coli can use aliphatic sulfonates as a source of sulfur for growth. Starvation for sulfate leads to the expression of the tauABCD and ssuEADCB genes. Each of these gene clusters encodes an ABC-type transport system required for uptake of aliphatic sulfonates and a desulfonation enzyme. The TauD protein is an α-ketoglutarate-dependent dioxygenase that preferentially liberates sulfite from taurine (2-aminoethanesulfonic acid). SsuD is a monooxygenase that catalyzes the oxygenolytic desulfonation of a range of aliphatic sulfonates other than taurine. Its cosubstrate is FMNH2, which is provided by SsuE, an NAD(P)H-dependent FMN reductase. In contrast to many other bacteria, E. coli is unable to grow with arylsulfonates or with sulfate esters as sulfur source. The tau and ssu systems thus provide all genes for the utilization of known organosulfur sources by this organism, except the as yet unidentified gene(s) that enable some E. coli strains to grow with methanesulfonate or cysteate as a sulfur source. Expression of the tau and ssu genes requires the LysR-type transcriptional regulatory proteins CysB and Cbl. Synthesis of Cbl itself is under control of the CysB protein, and the CysB protein may therefore be regarded as the master regulator for sulfur assimilation in E. coli, while the Cbl protein functions as an accessory element specific for utilization of sulfur from organosulfur sources.

[1]  K. Schlossmann,et al.  Biosynthesis of cysteine from serine and hydrogen sulphide. , 1957 .

[2]  J. Lawrence,et al.  Methionine-to-Cysteine Recycling inKlebsiella aerogenes , 2001, Journal of bacteriology.

[3]  Y. Murooka,et al.  Regulation of arylsulfatase synthesis by sulfur compounds in Klebsiella aerogenes , 1975, Journal of bacteriology.

[4]  C. Nakatsu,et al.  Distribution of the tfdA Gene in Soil Bacteria That Do Not Degrade 2,4-Dichlorophenoxyacetic Acid (2,4-D) , 1997, Microbial Ecology.

[5]  T. Leisinger,et al.  Characterization of α-Ketoglutarate-dependent Taurine Dioxygenase from Escherichia coli * , 1997, The Journal of Biological Chemistry.

[6]  M. J. Ryle,et al.  Stopped-flow kinetic analysis of Escherichia coli taurine/alpha-ketoglutarate dioxygenase: interactions with alpha-ketoglutarate, taurine, and oxygen. , 1999, Biochemistry.

[7]  E. Leadbetter,et al.  Microbial Assimilation and Dissimilation of Sulfonate Sulfur , 1995 .

[8]  R. Hausinger,et al.  Herbicide-Degrading α-Keto Acid-Dependent Enzyme TfdA: Metal Coordination Environment and Mechanistic Insights† , 1999 .

[9]  T. Leisinger,et al.  Involvement of CysB and Cbl regulatory proteins in expression of the tauABCD operon and other sulfate starvation-inducible genes in Escherichia coli , 1997, Journal of bacteriology.

[10]  Geoffrey J. Barton,et al.  Crystal structure of isopenicillin N synthase is the first from a new structural family of enzymes , 1995, Nature.

[11]  R. Hausinger,et al.  Purification and characterization of 2,4-dichlorophenoxyacetate/alpha-ketoglutarate dioxygenase. , 1993, The Journal of biological chemistry.

[12]  F. Junker,et al.  Microbial desulfonation. , 1998, FEMS microbiology reviews.

[13]  Ploeg,et al.  Identification of sulfate starvation-regulated genes in Escherichia coli: a gene cluster involved in the utilization of taurine as a sulfur source , 1996, Journal of bacteriology.

[14]  R. Iwanicka-Nowicka,et al.  A new gene, cbl, encoding a member of the LysR family of transcriptional regulators belongs to Escherichia coli cys regulon. , 1995, Gene.

[15]  M. Kertesz,et al.  A Novel Reduced Flavin Mononucleotide-Dependent Methanesulfonate Sulfonatase Encoded by the Sulfur-Regulatedmsu Operon of Pseudomonas aeruginosa , 1999, Journal of bacteriology.

[16]  T. Leisinger,et al.  Deletion Analysis of the Escherichia coli Taurine and Alkanesulfonate Transport Systems , 2000, Journal of bacteriology.

[17]  T. Leisinger,et al.  Characterization of a Two-component Alkanesulfonate Monooxygenase from Escherichia coli* , 1999, The Journal of Biological Chemistry.

[18]  M. Kertesz,et al.  Genetic organization of sulphur‐controlled aryl desulphonation in Pseudomonas putida S‐313 , 1999, Molecular microbiology.

[19]  R. Bender.  The role of the NAC protein in the nitrogen regulation of Klebsiella aerogenes , 1991, Molecular microbiology.

[20]  M. Uría-Nickelsen,et al.  Sulphonate utilization by enteric bacteria. , 1993, Journal of general microbiology.

[21]  R. Hausinger,et al.  Site-directed mutagenesis of 2,4-dichlorophenoxyacetic acid/alpha-ketoglutarate dioxygenase. Identification of residues involved in metallocenter formation and substrate binding. , 2000, The Journal of biological chemistry.

[22]  F. Brockman,et al.  Cloning, sequencing, and analysis of a gene cluster from Chelatobacter heintzii ATCC 29600 encoding nitrilotriacetate monooxygenase and NADH:flavin mononucleotide oxidoreductase , 1997, Journal of bacteriology.

[23]  M. Quadroni,et al.  Analysis of global responses by protein and peptide fingerprinting of proteins isolated by two-dimensional gel electrophoresis. Application to the sulfate-starvation response of Escherichia coli. , 1996, European journal of biochemistry.

[24]  M. Kertesz.  Riding the sulfur cycle--metabolism of sulfonates and sulfate esters in gram-negative bacteria. , 2000, FEMS microbiology reviews.

[25]  G N Murshudov,et al.  The structure of the cofactor-binding fragment of the LysR family member, CysB: a familiar fold with a surprising subunit arrangement. , 1997, Structure.

[26]  T. Leisinger,et al.  The Escherichia coli ssuEADCB Gene Cluster Is Required for the Utilization of Sulfur from Aliphatic Sulfonates and Is Regulated by the Transcriptional Activator Cbl* , 1999, The Journal of Biological Chemistry.

[27]  N. M. Kredich,et al.  Residue threonine‐149 of the Salmonella typhimurium CysB transcription activator: mutations causing constitutive expression of positively regulated genes of the cysteine regulon , 1994, Molecular microbiology.

[28]  S. Shima,et al.  Structure of coenzyme F(420) dependent methylenetetrahydromethanopterin reductase from two methanogenic archaea. , 2000, Journal of molecular biology.

[29]  A. Khodursky,et al.  Nitrogen regulatory protein C-controlled genes of Escherichia coli: scavenging as a defense against nitrogen limitation. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[30]  R. Roberts.  Studies of biosynthesis in escherichia coli , 1955 .

[31]  Hilla Peretz,et al.  Ju n 20 03 Schrödinger ’ s Cat : The rules of engagement , 2003 .

[32]  M. Kertesz,et al.  Characterization of a Sulfur-regulated Oxygenative Alkylsulfatase from Pseudomonas putida S-313* , 2000, The Journal of Biological Chemistry.

[33]  A. Fisher,et al.  The 1.5-Å Resolution Crystal Structure of Bacterial Luciferase in Low Salt Conditions* , 1996, The Journal of Biological Chemistry.

[34]  R. Hausinger,et al.  Cloning and Characterization of a Sulfonate/α-Ketoglutarate Dioxygenase from Saccharomyces cerevisiae , 1999, Journal of bacteriology.