Regulation of lysine biosynthesis and transport genes in bacteria: yet another RNA riboswitch?

Comparative analysis of genes, operons and regulatory elements was applied to the lysine biosynthetic pathway in available bacterial genomes. We report identification of a lysine-specific RNA element, named the LYS element, in the regulatory regions of bacterial genes involved in biosynthesis and transport of lysine. Similarly to the previously described RNA regulatory elements for three vitamins (riboflavin, thiamin and cobalamin), purine and methionine regulons, this regulatory RNA structure is highly conserved on the sequence and structural levels. The LYS element includes regions of lysine-constitutive mutations previously identified in Escherichia coli and Bacillus subtilis. A possible mechanism of the lysine-specific riboswitch is similar to the previously defined mechanisms for the other metabolite-specific riboswitches and involves either transcriptional or translational attenuation in various groups of bacteria. Identification of LYS elements in Gram-negative gamma-proteobacteria, Gram-positive bacteria from the Bacillus/Clostridium group, and Thermotogales resulted in description of the previously uncharacterized lysine regulon in these bacterial species. Positional analysis of LYS elements led to identification of a number of new candidate lysine transporters, namely LysW, YvsH and LysXY. Finally, the most likely candidates for genes of lysine biosynthesis missing in Gram- positive bacteria were identified using the genome context analysis.

[1]  J. Felsenstein.  Evolutionary trees from DNA sequences: A maximum likelihood approach , 2005, Journal of Molecular Evolution.

[2]  N. A. Kuznetsov,et al.  Complex Systems: Control and Modeling Problems , 2004 .

[3]  M. Gelfand,et al.  Riboswitches: the oldest mechanism for the regulation of gene expression? , 2004, Trends in genetics : TIG.

[4]  M. Gelfand,et al.  Comparative Genomics of the Vitamin B12 Metabolism and Regulation in Prokaryotes* , 2003, Journal of Biological Chemistry.

[5]  T. Henkin,et al.  The L box regulon: Lysine sensing by leader RNAs of bacterial lysine biosynthesis genes , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Jeffrey E. Barrick,et al.  Riboswitches Control Fundamental Biochemical Pathways in Bacillus subtilis and Other Bacteria , 2003, Cell.

[7]  Vitaly Epshtein,et al.  The riboswitch-mediated control of sulfur metabolism in bacteria , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[8]  T. Henkin,et al.  Transcription termination control of the S box system: Direct measurement of S-adenosylmethionine by the leader RNA , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[9]  C. Hutton,et al.  Inhibitors of lysine biosynthesis as antibacterial agents. , 2003, Mini reviews in medicinal chemistry.

[10]  Natalia Ivanova,et al.  The ERGOTM genome analysis and discovery system , 2003, Nucleic Acids Res..

[11]  M. Gelfand,et al.  Comparative Genomics of Thiamin Biosynthesis in Procaryotes , 2002, The Journal of Biological Chemistry.

[12]  R. Breaker,et al.  An mRNA structure that controls gene expression by binding FMN , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Evgeny Nudler,et al.  Sensing Small Molecules by Nascent RNA A Mechanism to Control Transcription in Bacteria , 2002, Cell.

[14]  Ronald R. Breaker,et al.  Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression , 2002, Nature.

[15]  A. Lazcano,et al.  Molecular Evolution of the Lysine Biosynthetic Pathways , 2002, Journal of Molecular Evolution.

[16]  Ali Nahvi,et al.  Genetic control by a metabolite binding mRNA. , 2002, Chemistry & biology.

[17]  M. Gelfand,et al.  Regulation of riboflavin biosynthesis and transport genes in bacteria by transcriptional and translational attenuation. , 2002, Nucleic acids research.

[18]  Shih-Hsiung Wu,et al.  Cloning, Sequencing, Heterologous Expression, Purification, and Characterization of Adenosylcobalamin-dependentd-Ornithine Aminomutase from Clostridium sticklandii * , 2001, The Journal of Biological Chemistry.

[19]  N. Grishin,et al.  Genome trees constructed using five different approaches suggest new major bacterial clades , 2001, BMC Evolutionary Biology.

[20]  J. Carmichael,et al.  The American Society for Microbiology. , 2001, American clinical laboratory.

[21]  A. Bellmann,et al.  Expression control and specificity of the basic amino acid exporter LysE of Corynebacterium glutamicum. , 2001, Microbiology.

[22]  Characterization of Aspartate Kinase III of Bacillus subtilis , 2001, Bioscience, biotechnology, and biochemistry.

[23]  J. Lakowicz,et al.  Thermodynamics and dynamics of histidine-binding protein, the water-soluble receptor of histidine permease. Implications for the transport of high and low affinity ligands. , 2000, European journal of biochemistry.

[24]  Christopher H. Chang,et al.  Cloning, Sequencing, Heterologous Expression, Purification, and Characterization of Adenosylcobalamin-dependentd-Lysine 5,6-Aminomutase from Clostridium sticklandii * , 2000, The Journal of Biological Chemistry.

[25]  Michael Y. Galperin,et al.  The COG database: a tool for genome-scale analysis of protein functions and evolution , 2000, Nucleic Acids Res..

[26]  M. Nishiyama,et al.  A prokaryotic gene cluster involved in synthesis of lysine through the amino adipate pathway: a key to the evolution of amino acid biosynthesis. , 1999, Genome research.

[27]  M. Gelfand,et al.  A conserved RNA structure element involved in the regulation of bacterial riboflavin synthesis genes. , 1999, Trends in genetics : TIG.

[28]  Christian N. S. Pedersen,et al.  Fast evaluation of internal loops in RNA secondary structure prediction , 1999, Bioinform..

[29]  V. Méjean,et al.  The leader sequence of the Escherichia coli lysC gene is involved in the regulation of LysC synthesis. , 1998, FEMS Microbiology Letters.

[30]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[31]  S. Kochhar,et al.  Lysine-induced premature transcription termination in the lysC operon of Bacillus subtilis. , 1996, Microbiology.

[32]  F. Neidhart.  Escherichia coli and Salmonella. , 1996 .

[33]  T. Weisbrod,et al.  Genetic determination of the meso-diaminopimelate biosynthetic pathway of mycobacteria , 1994, Journal of bacteriology.

[34]  J. Wu,et al.  The lysP gene encodes the lysine-specific permease , 1992, Journal of bacteriology.

[35]  Y. Lu,et al.  Fine-structure mapping of cis-acting control sites in the lysC operon of Bacillus subtilis. , 1992, FEMS microbiology letters.

[36]  H. Paulus,et al.  Comparison of the three aspartokinase isozymes in Bacillus subtilis Marburg and 168 , 1990, Journal of bacteriology.

[37]  J. David Schaffer,et al.  Proceedings of the third international conference on Genetic algorithms , 1989 .

[38]  P. Stragier,et al.  Regulation of diaminopimelate decarboxylase synthesis in Escherichia coli. I. Identification of a lysR gene encoding an activator of the lysA gene. , 1983, Journal of molecular biology.