Phylogenetic Analysis of L4-Mediated Autogenous Control of the S10 Ribosomal Protein Operon

ABSTRACT We investigated the regulation of the S10 ribosomal protein (r-protein) operon among members of the gamma subdivision of the proteobacteria, which includes Escherichia coli. InE. coli, this 11-gene operon is autogenously controlled by r-protein L4. This regulation requires specific determinants within the untranslated leader of the mRNA. Secondary structure analysis of the S10 leaders of five enterobacteria (Salmonella typhimurium,Citrobacter freundii, Yersinia enterocolitica,Serratia marcescens, and Morganella morganii) and two nonenteric members of the gamma subdivision (Haemophilus influenzae and Vibrio cholerae) shows that these foreign leaders share significant structural homology with the E. coli leader, particularly in the region which is critical for L4-mediated autogenous control in E. coli. Moreover, these heterologous leaders produce a regulatory response to L4 oversynthesis in E. coli. Our results suggest that an E. coli-like L4-mediated regulatory mechanism may operate in all of these species. However, the mechanism is not universally conserved among the gamma subdivision members, since at least one,Pseudomonas aeruginosa, does not contain the required S10 leader features, and its leader cannot provide the signals for regulation by L4 in E. coli. We speculate that L4-mediated autogenous control developed during the evolution of the gamma branch of proteobacteria.

[1]  M. Nomura,et al.  DNA sequences of promoter regions for the str and spc ribosomal protein operons in E. coli , 1978, Cell.

[2]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[3]  L. Lindahl,et al.  A hairpin structure upstream of the terminator hairpin required for ribosomal protein L4-mediated attenuation control of the S10 operon of Escherichia coli , 1996, Journal of bacteriology.

[4]  L. Lindahl,et al.  Ribosomal protein L4 from Escherichia coli utilizes nonidentical determinants for its structural and regulatory functions. , 1996, RNA: A publication of the RNA Society.

[5]  T. Henkin,et al.  The rpsD gene, encoding ribosomal protein S4, is autogenously regulated in Bacillus subtilis , 1991, Journal of bacteriology.

[6]  L. Lindahl,et al.  Ribosomal protein L4 of Escherichia coli: in vitro analysis of L4-mediated attenuation control. , 1991, Biochimie.

[7]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Ross A. Overbeek,et al.  The RDP (Ribosomal Database Project) , 1997, Nucleic Acids Res..

[9]  D. Belin,et al.  Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter , 1995, Journal of bacteriology.

[10]  T. Henkin,et al.  Cloning and analysis of the spc ribosomal protein operon of Bacillus subtilis: comparison with the spc operon of Escherichia coli. , 1989, Nucleic acids research.

[11]  J. Ingraham,et al.  Relationship between the concentration of nucleoside triphosphates and the rate of synthesis of RNA. , 1973, Journal of molecular biology.

[12]  L. Lewandowski,et al.  A mutation suppressing streptomycin dependence. I. An effect on ribosome function. , 1967, Journal of molecular biology.

[13]  C. Turnbough,et al.  Transcription regulation by initiating NTP concentration: rRNA synthesis in bacteria. , 1997, Science.

[14]  L. Lindahl,et al.  Regulation of the Escherichia coli S10 ribosomal protein operon by heterologous L4 ribosomal proteins. , 1995, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[15]  L. Lindahl,et al.  Escherichia coli ribosomal protein L4 stimulates transcription termination at a specific site in the leader of the S10 operon independent of L4-mediated inhibition of translation. , 1990, Journal of molecular biology.

[16]  L. Freedman,et al.  Autogenous control of the S10 ribosomal protein operon of Escherichia coli: genetic dissection of transcriptional and posttranscriptional regulation. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[17]  F. Sor,et al.  Transcriptional organization of the S10, spc and alpha operons of Escherichia coli. , 1990, Biochimica et biophysica acta.

[18]  G. Golderer,et al.  Autogenous translational regulation of the ribosomal MvaL1 operon in the archaebacterium Methanococcus vannielii , 1994, Journal of bacteriology.

[19]  L. Lindahl,et al.  Diverse mechanisms for regulating ribosomal protein synthesis in Escherichia coli. , 1994, Progress in nucleic acid research and molecular biology.

[20]  U. K. Laemmli,et al.  Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 , 1970, Nature.

[21]  M. Nomura,et al.  Regulation of the S10 ribosomal protein operon in E. coli: Nucleotide sequence at the start of the operon , 1981, Cell.

[22]  L. Lindahl,et al.  Ribosomal protein L4 stimulates in vitro termination of transcription at a NusA-dependent terminator in the S10 operon leader. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[24]  G. Sarkis,et al.  Genome structure of mycobacteriophage D29: implications for phage evolution. , 1998, Journal of molecular biology.

[25]  A. E. Walter,et al.  Coaxial stacking of helixes enhances binding of oligoribonucleotides and improves predictions of RNA folding. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Y. Sha,et al.  Role of NusA in L4-mediated attenuation control of the S10 r-protein operon of Escherichia coli. , 1995, Journal of molecular biology.

[27]  Y. Sha,et al.  RNA determinants required for L4-mediated attenuation control of the S10 r-protein operon of Escherichia coli. , 1995, Journal of molecular biology.

[28]  L. Freedman,et al.  Genetic dissection of stringent control and nutritional shift-up response of the Escherichia coli S10 ribosomal protein operon. , 1985, Journal of molecular biology.

[29]  M. Nomura,et al.  DNA sequence of the promoter region for the alpha ribosomal protein operon in Escherichia coli. , 1980, The Journal of biological chemistry.

[30]  L. Lindahl,et al.  Protein L4 of the E. coli ribosome regulates an eleven gene r protein operon , 1980, Cell.

[31]  L. Lindahl,et al.  Ribosomal protein L4 and transcription factor NusA have separable roles in mediating terminating of transcription within the leader of the S10 operon of Escherichia coli. , 1992, Genes & development.

[32]  Y. Sha,et al.  Analysis of the Bacillus subtilis S10 ribosomal protein gene cluster identifies two promoters that may be responsible for transcription of the entire 15-kilobase S10-spc-alpha cluster , 1997, Journal of bacteriology.

[33]  B L Maidak,et al.  The RDP-II (Ribosomal Database Project) , 2001, Nucleic Acids Res..

[34]  F. Ayala,et al.  Tempo, Mode, the Progenote, and the Universal Root , 1995 .

[35]  E V Koonin,et al.  Gene order is not conserved in bacterial evolution. , 1996, Trends in genetics : TIG.

[36]  M. Waterman.  Mathematical Methods for DNA Sequences , 1989 .

[37]  Michael Y. Galperin,et al.  Prokaryotic genomes: the emerging paradigm of genome-based microbiology. , 1997, Current opinion in genetics & development.

[38]  Walter E. Hill,et al.  The Ribosome : structure, function, and evolution , 1990 .

[39]  O. Maaløe,et al.  DNA replication and the division cycle in Escherichia coli , 1967 .

[40]  T. Henkin,et al.  Cloning and analysis of the Bacillus subtilis rpsD gene, encoding ribosomal protein S4 , 1990, Journal of bacteriology.

[41]  L. Lindahl,et al.  Autogenous control is not sufficient to ensure steady-state growth rate-dependent regulation of the S10 ribosomal protein operon of Escherichia coli , 1990, Journal of bacteriology.

[42]  J R Roth,et al.  Selfish operons: horizontal transfer may drive the evolution of gene clusters. , 1996, Genetics.

[43]  P. Shen,et al.  Secondary structure of the leader transcript from the Escherichia coli S10 ribosomal protein operon. , 1988, Nucleic acids research.

[44]  R. Fleischmann,et al.  Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. , 1995, Science.

[45]  L. Lindahl,et al.  Operon-specific regulation of ribosomal protein synthesis in Escherichia coli. , 1979, Proceedings of the National Academy of Sciences of the United States of America.