Transcriptional Profiling of Caulobacter crescentus during Growth on Complex and Minimal Media

ABSTRACT Microarray analysis was used to examine gene expression in the freshwater oligotrophic bacterium Caulobacter crescentus during growth on three standard laboratory media, including peptone-yeast extract medium (PYE) and minimal salts medium with glucose or xylose as the carbon source. Nearly 400 genes (approximately 10% of the genome) varied significantly in expression between at least two of these media. The differentially expressed genes included many encoding transport systems, most notably diverse TonB-dependent outer membrane channels of unknown substrate specificity. Amino acid degradation pathways constituted the largest class of genes induced in PYE. In contrast, many of the genes upregulated in minimal media encoded enzymes for synthesis of amino acids, including incorporation of ammonia and sulfate into glutamate and cysteine. Glucose availability induced expression of genes encoding enzymes of the Entner-Doudoroff pathway, which was demonstrated here through mutational analysis to be essential in C. crescentus for growth on glucose. Xylose induced expression of genes encoding several hydrolytic exoenzymes as well as an operon that may encode a novel pathway for xylose catabolism. A conserved DNA motif upstream of many xylose-induced genes was identified and shown to confer xylose-specific expression. Xylose is an abundant component of xylan in plant cell walls, and the microarray data suggest that in addition to serving as a carbon source for growth of C. crescentus, this pentose may be interpreted as a signal to produce enzymes associated with plant polymer degradation.

[1]  Malik Beshir Malik,et al.  Applied Linear Regression , 2005, Technometrics.

[2]  R. Conrad,et al.  Different degradation pathways for glucose and fructose in Rhodopseudomonas capsulata , 1977, Archives of Microbiology.

[3]  M. Wheelis,et al.  Genetic control of the histidine dissimilatory pathway in Pseudomonas putida , 1973, Molecular and General Genetics MGG.

[4]  Peter Karp,et al.  PseudoCyc, A Pathway-Genome Database for Pseudomonas aeruginosa , 2003, Journal of Molecular Microbiology and Biotechnology.

[5]  C. Nesbø Faculty Opinions recommendation of Carbohydrate-induced differential gene expression patterns in the hyperthermophilic bacterium Thermotoga maritima. , 2003 .

[6]  U. Jenal,et al.  The Caulobacter cell cycle: timing, spatial organization and checkpoints. , 2002, Current opinion in microbiology.

[7]  William Lee,et al.  Genome-tools: a flexible package for genome sequence analysis. , 2002, BioTechniques.

[8]  Peter D. Karp,et al.  The Pathway Tools software , 2002, ISMB.

[9]  E. C. Teixeira,et al.  Comparison of the genomes of two Xanthomonas pathogens with differing host specificities , 2002, Nature.

[10]  C. Stephens,et al.  Use of the Caulobacter crescentus Genome Sequence To Develop a Method for Systematic Genetic Mapping , 2002, Journal of bacteriology.

[11]  Lucy Shapiro,et al.  Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[12]  S. Nicolson,et al.  Xylose as a nectar sugar: from biochemistry to ecology. , 2000, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[13]  Ramon Gonzalez,et al.  Global Gene Expression Differences Associated with Changes in Glycolytic Flux and Growth Rate in Escherichia coli during the Fermentation of Glucose and Xylose , 2002, Biotechnology progress.

[14]  M S Gelfand,et al.  Computational analysis of the transcriptional regulation of pentose utilization systems in the gamma subdivision of Proteobacteria. , 2001, FEMS microbiology letters.

[15]  M S Gelfand,et al.  Transcriptional regulation of pentose utilisation systems in the Bacillus/Clostridium group of bacteria. , 2001, FEMS microbiology letters.

[16]  J R Maddock,et al.  Analysis of the outer membrane proteome of Caulobacter crescentus by two‐dimensional electrophoresis and mass spectrometry , 2001, Proteomics.

[17]  Ian T. Paulsen,et al.  Complete genome sequence of Caulobacter crescentus , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Douglas L. Brutlag,et al.  BioProspector: Discovering Conserved DNA Motifs in Upstream Regulatory Regions of Co-Expressed Genes , 2000, Pacific Symposium on Biocomputing.

[19]  Michael Y. Galperin,et al.  The COG database: new developments in phylogenetic classification of proteins from complete genomes , 2001, Nucleic Acids Res..

[20]  H. McAdams,et al.  Global analysis of the genetic network controlling a bacterial cell cycle. , 2000, Science.

[21]  R. Jensen,et al.  A New Class of Glutamate Dehydrogenases (GDH) , 2000, The Journal of Biological Chemistry.

[22]  D. Botstein,et al.  DNA microarray analysis of gene expression in response to physiological and genetic changes that affect tryptophan metabolism in Escherichia coli. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[23]  P. van Gelder,et al.  Structure and function of bacterial outer membrane proteins: barrels in a nutshell , 2000, Molecular microbiology.

[24]  G. Church,et al.  Conservation of DNA regulatory motifs and discovery of new motifs in microbial genomes. , 2000, Genome research.

[25]  R. Sonti,et al.  Mutants of Xanthomonas oryzae pv. oryzae deficient in general secretory pathway are virulence deficient and unable to secrete xylanase. , 2000, Molecular plant-microbe interactions : MPMI.

[26]  J. Visser,et al.  The Aspergillus niger transcriptional activator XlnR, which is involved in the degradation of the polysaccharides xylan and cellulose, also regulates d‐xylose reductase gene expression , 2000, Molecular microbiology.

[27]  D. Hodgson Primary metabolism and its control in streptomycetes: a most unusual group of bacteria. , 2000, Advances in microbial physiology.

[28]  I. Holland,et al.  ABC transporters: bacterial exporters-revisited five years on. , 1999, Biochimica et biophysica acta.

[29]  B. Snel,et al.  Pathway alignment: application to the comparative analysis of glycolytic enzymes. , 1999, The Biochemical journal.

[30]  Anders Krogh,et al.  Prediction of Signal Peptides and Signal Anchors by a Hidden Markov Model , 1998, ISMB.

[31]  J. Coulton,et al.  TonB‐dependent iron acquisition: mechanisms of siderophore‐mediated active transport † , 1998, Molecular microbiology.

[32]  D. Lipman,et al.  A genomic perspective on protein families. , 1997, Science.

[33]  Lucy Shapiro,et al.  Cell Type-Specific Phosphorylation and Proteolysis of a Transcriptional Regulator Controls the G1-to-S Transition in a Bacterial Cell Cycle , 1997, Cell.

[34]  L. Shapiro,et al.  Isolation and characterization of a xylose-dependent promoter from Caulobacter crescentus , 1997, Journal of bacteriology.

[35]  S. Brunak,et al.  SHORT COMMUNICATION Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites , 1997 .

[36]  Charles Elkan,et al.  Fitting a Mixture Model By Expectation Maximization To Discover Motifs In Biopolymer , 1994, ISMB.

[37]  L. Shapiro,et al.  An unusual promoter controls cell‐cycle regulation and dependence on DNA replication of the Caulobacter fliLM early flagellar operon , 1993, Molecular microbiology.

[38]  G R Jacobson,et al.  Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. , 1993, Microbiological reviews.

[39]  B. Ely Genetics of Caulobacter crescentus. , 1991, Methods in enzymology.

[40]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[41]  F. Khambaty,et al.  Utilization of histidine by Caulobacter crescentus. , 1988, Journal of general microbiology.

[42]  C. M. Ross,et al.  Regulation of tryptophan biosynthesis in Caulobacter crescentus , 1988, Journal of bacteriology.

[43]  A. Bourquin,et al.  Metabolism of aromatic compounds by Caulobacter crescentus , 1987, Journal of bacteriology.

[44]  L. Shapiro,et al.  Fatty acid degradation in Caulobacter crescentus , 1986, Journal of bacteriology.

[45]  S. Weisberg,et al.  Applied Linear Regression (2nd ed.). , 1986 .

[46]  P. Hirsch Microbial life at extremely low nutrient levels. , 1986, Advances in space research : the official journal of the Committee on Space Research.

[47]  P. Postma,et al.  Phosphoenolpyruvate:carbohydrate phosphotransferase system of bacteria. , 1985, Microbiological reviews.

[48]  T. Lessie,et al.  Pseudomonas cepacia mutants blocked in the Entner-Doudoroff pathway , 1982, Journal of bacteriology.

[49]  J S Poindexter,et al.  The caulobacters: ubiquitous unusual bacteria. , 1981, Microbiological reviews.

[50]  L. Shapiro,et al.  Galactose catabolism in Caulobacter crescentus , 1978, Journal of bacteriology.

[51]  B Ely,et al.  Ammonia assimilation and glutamate formation in Caulobacter crescentus , 1978, Journal of bacteriology.

[52]  G. H. Elkan,et al.  Glucose catabolism in two derivatives of a Rhizobium japonicum strain differing in nitrogen-fixing efficiency , 1977, Journal of bacteriology.

[53]  R. C. Johnson,et al.  Isolation of spontaneously derived mutants of Caulobacter crescentus. , 1977, Genetics.

[54]  Kolodziej Bj,et al.  Pathway of glucose catabolism in Caulobacter crescentus. , 1976 .

[55]  R. Riley,et al.  Pathway of glucose catabolism in Caulobacter crescentus. , 1976, Microbios.

[56]  L. Arthur,et al.  Carbohydrate Catabolism of Selected Strains in the Genus Agrobacterium , 1975, Applied microbiology.

[57]  W. T. Blevins,et al.  6-Phosphogluconate dehydratase deficiency in pleiotropic carbohydrate-negative mutant strains of Pseudomonas aeruginosa , 1975, Journal of bacteriology.

[58]  J. Poindexter BIOLOGICAL PROPERTIES AND CLASSIFICATION OF THE CAULOBACTER GROUP , 1964, Bacteriological reviews.

[59]  B. Magasanik,et al.  The degradation of histidine by Aerobacter aerogenes. , 1955, The Journal of biological chemistry.

[60]  N. Entner,et al.  Glucose and gluconic acid oxidation of Pseudomonas saccharophila. , 1952, The Journal of biological chemistry.

[61]  A. Henrici,et al.  Studies of Freshwater Bacteria , 1935, Journal of bacteriology.

[62]  A. Harden Bacterial Metabolism , 1930, Nature.