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PMID: 11976302 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Identification of two prpDBC gene clusters in Corynebacterium glutamicum and their involvement in propionate degradation via the 2-methylcitrate cycle.

Journal of bacteriology ·Vol. 184 ·No. 10 ·2002-05-00 ·Pages 2728-39

Claes WA, Pühler A, Kalinowski J

Abstract

Genome sequencing revealed that the Corynebacterium glutamicum genome contained, besides gltA, two additional citrate synthase homologous genes (prpC) located in two different prpDBC gene clusters, which were designated prpD1B1C1 and prpD2B2C2. The coding regions of the two gene clusters as well as the predicted gene products showed sequence identities of about 70 to 80%. Significant sequence similarities were found also to the prpBCDE operons of Escherichia coli and Salmonella enterica, which are known to encode enzymes of the propionate-degrading 2-methylcitrate pathway. Homologous and heterologous overexpression of the C. glutamicum prpC1 and prpC2 genes revealed that their gene products were active as citrate synthases and 2-methylcitrate synthases. Growth tests showed that C. glutamicum used propionate as a single or partial carbon source, although the beginning of the exponential growth phase was strongly delayed by propionate for up to 7 days. Compared to growth on acetate, the specific 2-methylcitrate synthase activity increased about 50-fold when propionate was provided as the sole carbon source, suggesting that in C. glutamicum the oxidation of propionate to pyruvate occurred via the 2-methylcitrate pathway. Additionally, two-dimensional gel electrophoresis experiments combined with mass spectrometry showed strong induction of the expression of the C. glutamicum prpD2B2C2 genes by propionate as an additional carbon source. Mutational analyses revealed that only the prpD2B2C2 genes were essential for the growth of C. glutamicum on propionate as a sole carbon source, while the function of the prpD1B1C1 genes remains obscure.

MeSH Terms
Base Sequence Citrate (si)-Synthase/genetics Citrates/metabolism Corynebacterium/genetics,growth & development,metabolism DNA, Bacterial/chemistry Molecular Sequence Data Multigene Family/physiology Oxo-Acid-Lyases/genetics Propionates/metabolism
Chemicals
Citrates DNA, Bacterial Propionates 2-methylcitric acid Citrate (si)-Synthase 2-methylcitrate synthase Oxo-Acid-Lyases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Claes Wilfried A
Lehrstuhl für Genetik, Fakultät für Biologie, Universität Bielefeld, Postfach 100131, 33501 Bielefeld, Germany.
Pühler Alfred
Kalinowski Jörn
References (44)
44 references, click to expand
  1. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum.
    Gene. 1994 Jul 22;145(1):69-73 PMID: 8045426
  2. Citrate synthase and 2-methylcitrate synthase: structural, functional and evolutionary relationships.
    Microbiology. 1998 Apr;144 ( Pt 4):929-35 PMID: 9579066
  3. Cloning, sequence analysis, expression and inactivation of the Corynebacterium glutamicum pta-ack operon encoding phosphotransacetylase and acetate kinase.
    Microbiology. 1999 Feb;145 ( Pt 2):503-13 PMID: 10075432
  4. The prpE gene of Salmonella typhimurium LT2 encodes propionyl-CoA synthetase.
    Microbiology. 1999 Jun;145 ( Pt 6):1381-8 PMID: 10411265
  5. The methylcitric acid pathway in Ralstonia eutropha: new genes identified involved in propionate metabolism.
    Microbiology. 2001 Aug;147(Pt 8):2203-14 PMID: 11495997
  6. Propionate catabolism in Salmonella typhimurium LT2: two divergently transcribed units comprise the prp locus at 8.5 centisomes, prpR encodes a member of the sigma-54 family of activators, and the prpBCDE genes constitute an operon.
    J Bacteriol. 1997 Feb;179(3):928-40 PMID: 9006051
  7. Sequencing and expression of the gene encoding a cold-active citrate synthase from an Antarctic bacterium, strain DS2-3R.
    Eur J Biochem. 1997 Aug 15;248(1):49-57 PMID: 9310359
  8. pMECA: a cloning plasmid with 44 unique restriction sites that allows selection of recombinants based on colony size.
    Biotechniques. 1998 Jun;24(6):922-4, 926, 928 PMID: 9631181
  9. 2-Methylisocitrate lyases from the bacterium Escherichia coli and the filamentous fungus Aspergillus nidulans: characterization and comparison of both enzymes.
    Eur J Biochem. 2001 Jun;268(12):3577-86 PMID: 11422389
  10. The Legionella pneumophila prp locus; required during infection of macrophages and amoebae.
    Microb Pathog. 1999 Dec;27(6):369-76 PMID: 10588909
  11. Identification of the 2-methylcitrate pathway involved in the catabolism of propionate in the polyhydroxyalkanoate-producing strain Burkholderia sacchari IPT101(T) and analysis of a mutant accumulating a copolyester with higher 3-hydroxyvalerate content.
    Appl Environ Microbiol. 2002 Jan;68(1):271-9 PMID: 11772636
  12. Proteome analysis of Corynebacterium glutamicum.
    Electrophoresis. 2001 May;22(9):1712-23 PMID: 11425227
  13. In vitro conversion of propionate to pyruvate by Salmonella enterica enzymes: 2-methylcitrate dehydratase (PrpD) and aconitase Enzymes catalyze the conversion of 2-methylcitrate to 2-methylisocitrate.
    Biochemistry. 2001 Apr 17;40(15):4703-13 PMID: 11294638
  14. Methylcitrate synthase from Aspergillus nidulans: implications for propionate as an antifungal agent.
    Mol Microbiol. 2000 Mar;35(5):961-73 PMID: 10712680
  15. Growth Rate-Dependent Modulation of Carbon Flux through Central Metabolism and the Kinetic Consequences for Glucose-Limited Chemostat Cultures of Corynebacterium glutamicum.
    Appl Environ Microbiol. 1996 Feb;62(2):429-36 PMID: 16535231
  16. Fully automated genome analysis that reflects user needs and preferences. A detailed introduction to the MAGPIE system architecture.
    Biochimie. 1996;78(5):302-10 PMID: 8905148
  17. Corynebacterium glutamicum DNA is subjected to methylation-restriction in Escherichia coli.
    FEMS Microbiol Lett. 1994 Nov 1;123(3):343-7 PMID: 7988915
  18. Nucleotide sequence, expression and transcriptional analysis of the Corynebacterium glutamicum gltA gene encoding citrate synthase.
    Microbiology. 1994 Aug;140 ( Pt 8):1817-28 PMID: 7522844
  19. Strategy to sequence the genome of Corynebacterium glutamicum ATCC 13032: use of a cosmid and a bacterial artificial chromosome library.
    J Biotechnol. 2002 Apr 25;95(1):25-38 PMID: 11879709
  20. Propionate metabolism in Saccharomyces cerevisiae: implications for the metabolon hypothesis.
    Microbiology. 1994 Apr;140 ( Pt 4):717-22 PMID: 7912143
  21. LION and Degussa apply genomics to fermentation.
    Nat Biotechnol. 1998 Aug;16(8):715 PMID: 9702763
  22. The Saccharomyces cerevisiae ICL2 gene encodes a mitochondrial 2-methylisocitrate lyase involved in propionyl-coenzyme A metabolism.
    J Bacteriol. 2000 Dec;182(24):7007-13 PMID: 11092862
  23. Carbon-13 nuclear magnetic resonance study of metabolism of propionate by Escherichia coli.
    J Bacteriol. 1999 Jun;181(11):3562-70 PMID: 10348870
  24. Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants.
    Proc Natl Acad Sci U S A. 1990 Jun;87(12):4645-9 PMID: 2162051
  25. Structure and organization of the rrnD operon of 'Brevibacterium lactofermentum': analysis of the 16S rRNA gene.
    Microbiology. 1999 Apr;145 ( Pt 4):915-24 PMID: 10220171
  26. prpR, ntrA, and ihf functions are required for expression of the prpBCDE operon, encoding enzymes that catabolize propionate in Salmonella enterica serovar typhimurium LT2.
    J Bacteriol. 2000 Feb;182(4):905-10 PMID: 10648513
  27. Probability-based protein identification by searching sequence databases using mass spectrometry data.
    Electrophoresis. 1999 Dec;20(18):3551-67 PMID: 10612281
  28. Salmonella typhimurium LT2 catabolizes propionate via the 2-methylcitric acid cycle.
    J Bacteriol. 1999 Sep;181(18):5615-23 PMID: 10482501
  29. Comparative aspects of propionate metabolism.
    Comp Biochem Physiol B. 1989;92(2):227-31 PMID: 2647392
  30. Pathway analysis and metabolic engineering in Corynebacterium glutamicum.
    Biol Chem. 2000 Sep-Oct;381(9-10):899-910 PMID: 11076021
  31. Protoplast transformation of glutamate-producing bacteria with plasmid DNA.
    J Bacteriol. 1984 Jul;159(1):306-11 PMID: 6145700
  32. High resolution two-dimensional electrophoresis of proteins.
    J Biol Chem. 1975 May 25;250(10):4007-21 PMID: 236308
  33. Isoleucine synthesis in Corynebacterium glutamicum: molecular analysis of the ilvB-ilvN-ilvC operon.
    J Bacteriol. 1993 Sep;175(17):5595-603 PMID: 8366043
  34. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  35. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis.
    Gene. 1983 Dec;26(1):101-6 PMID: 6323249
  36. PCR-mediated recombination and mutagenesis. SOEing together tailor-made genes.
    Mol Biotechnol. 1995 Apr;3(2):93-9 PMID: 7620981
  37. Quantitative determination of metabolic fluxes during coutilization of two carbon sources: comparative analyses with Corynebacterium glutamicum during growth on acetate and/or glucose.
    J Bacteriol. 2000 Jun;182(11):3088-96 PMID: 10809686
  38. Translational coupling during expression of the tryptophan operon of Escherichia coli.
    Genetics. 1980 Aug;95(4):785-95 PMID: 6162715
  39. Propionic acid metabolism and poly-3-hydroxybutyrate-co-3-hydroxyvalerate (P3HB-co-3HV) production by Burkholderia sp.
    J Biotechnol. 2000 Jan 21;76(2-3):165-74 PMID: 10656331
  40. The Staden sequence analysis package.
    Mol Biotechnol. 1996 Jun;5(3):233-41 PMID: 8837029
  41. Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli.
    Gene. 1988 Sep 30;69(2):301-15 PMID: 3069586
  42. Propionate oxidation in Escherichia coli: evidence for operation of a methylcitrate cycle in bacteria.
    Arch Microbiol. 1997 Nov;168(5):428-36 PMID: 9325432
  43. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  44. The Corynebacterium xerosis composite transposon Tn5432 consists of two identical insertion sequences, designated IS1249, flanking the erythromycin resistance gene ermCX.
    Plasmid. 1995 Sep;34(2):119-31 PMID: 8559800
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
2002-05-00
Pages
2728-39
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC135033
Subset
IM
Databases
GENBANK
AF434798, AF434799
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