1887

Microbiology Society logo

Volume 161, Issue 11

The metabolism of ()-3-hydroxybutyrate is regulated by the enhancer-binding protein PA2005 and the alternative sigma factor RpoN in PAO1 Free

Abstract

A variety of soil-dwelling bacteria produce polyhydroxybutyrate (PHB), which serves as a source of energy and carbon under nutrient deprivation. Bacteria belonging to the genus do not generally produce PHB but are capable of using the PHB degradation product ()-3-hydroxybutyrate [()-3-HB] as a growth substrate. Essential to this utilization is the NAD-dependent dehydrogenase BdhA that converts ()-3-HB into acetoacetate, a molecule that readily enters central metabolism. Apart from the numerous studies that had focused on the biochemical characterization of BdhA, there was nothing known about the assimilation of ()-3-HB in , including the genetic regulation of expression. This study aimed to define the regulatory factors that govern or dictate the expression of the gene and ()-3-HB assimilation in PAO1. Importantly, expression of the gene was found to be specifically induced by ()-3-HB in a manner dependent on the alternative sigma factor RpoN and the enhancer-binding protein PA2005.This mode of regulation was essential for the utilization of ()-3-HB as a sole source of energy and carbon. However, non-induced levels of expression were sufficient for PAO1 to grow on ( ± )-1,3-butanediol, which is catabolized through an ()-3-HB intermediate. Because this is, we believe, the first report of an enhancer-binding protein that responds to ()-3-HB, PA2005 was named HbcR for ()-3-ydroxyutyrate atabolism egulator.

  • Received:
  • Accepted:
  • Published Online:
© 2015 The Authors
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000163
2015-11-01
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/161/11/2232.html?itemId=/content/journal/micro/10.1099/mic.0.000163&mimeType=html&fmt=ahah

References

  1. Akram M. (2013). A focused review of the role of ketone bodies in health and diseaseJ Med Food 16965–967 [View Article][PubMed]. [Google Scholar]
  2. Anderson A.J., Dawes E.A. (1990). Occurrence, metabolism, metabolic role, and industrial uses of bacterial polyhydroxyalkanoatesMicrobiol Rev 54450–472[PubMed]. [Google Scholar]
  3. Barrios H., Valderrama B., Morett E. (1999). Compilation and analysis of σ54-dependent promoter sequencesNucleic Acids Res 274305–4313 [View Article][PubMed]. [Google Scholar]
  4. Brashear A., Cook G.A. (1983). A spectrophotometric, enzymatic assay for d-3-hydroxybutyrate that is not dependent on hydrazineAnal Biochem 131478–482 [View Article][PubMed]. [Google Scholar]
  5. Buck M., Cannon W. (1992). Specific binding of the transcription factor sigma-54 to promoter DNANature 358422–424 [View Article][PubMed]. [Google Scholar]
  6. Conway K., Boddy C.N. (2012). Sigma 54 Promoter Database. (www.sigma54.ca).
  7. Feller C., Günther R., Hofmann H.J., Grunow M. (2006). Molecular basis of substrate recognition in d-3-hydroxybutyrate dehydrogenase from Pseudomonas putidaChemBioChem 71410–1418 [View Article][PubMed]. [Google Scholar]
  8. Heurlier K., Dénervaud V., Pessi G., Reimmann C., Haas D. (2003). Negative control of quorum sensing by RpoN (σ54) in Pseudomonas aeruginosa PAO1J Bacteriol 1852227–2235 [View Article][PubMed]. [Google Scholar]
  9. Huisman G.W., de Leeuw O., Eggink G., Witholt B. (1989). Synthesis of poly-3-hydroxyalkanoates is a common feature of fluorescent pseudomonadsAppl Environ Microbiol 551949–1954[PubMed]. [Google Scholar]
  10. Ito K., Nakajima Y., Ichihara E., Ogawa K., Katayama N., Nakashima K., Yoshimoto T. (2006). D-3-hydroxybutyrate dehydrogenase from Pseudomonas fragi: molecular cloning of the enzyme gene and crystal structure of the enzymeJ Mol Biol 355722–733 [View Article][PubMed]. [Google Scholar]
  11. Jacobs M.A., Alwood A., Thaipisuttikul I., Spencer D., Haugen E., Ernst S., Will O., Kaul R., Raymond C., other authors. (2003). Comprehensive transposon mutant library of Pseudomonas aeruginosaProc Natl Acad Sci U S A 10014339–14344 [View Article][PubMed]. [Google Scholar]
  12. Jendrossek D., Handrick R. (2002). Microbial degradation of polyhydroxyalkanoatesAnnu Rev Microbiol 56403–432 [View Article][PubMed]. [Google Scholar]
  13. Jendrossek D., Schirmer A., Schlegel H.G. (1996). Biodegradation of polyhydroxyalkanoic acidsAppl Microbiol Biotechnol 46451–463 [View Article][PubMed]. [Google Scholar]
  14. Kersters K., De Ley J. (1963). The oxidation of glycols by acetic acid bacteriaBiochim Biophys Acta 71311–331 [View Article][PubMed]. [Google Scholar]
  15. Kovach M.E., Elzer P.H., Hill D.S., Robertson G.T., Farris M.A., Roop R.M. II, Peterson K.M. (1995). Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettesGene 166175–176 [View Article][PubMed]. [Google Scholar]
  16. Lu J.N., Tappel R.C., Nomura C.T. (2009). Mini review: biosynthesis of poly(hydroxyalkanoates)Polym Rev (Phila Pa) 49226–248 [View Article]. [Google Scholar]
  17. Lundgren B.R., Thornton W., Dornan M.H., Villegas-Peñaranda L.R., Boddy C.N., Nomura C.T. (2013). Gene PA2449 is essential for glycine metabolism and pyocyanin biosynthesis in Pseudomonas aeruginosa PAO1J Bacteriol 1952087–2100 [View Article][PubMed]. [Google Scholar]
  18. Lundgren B.R., Villegas-Peñaranda L.R., Harris J.R., Mottern A.M., Dunn D.M., Boddy C.N., Nomura C.T. (2014). Genetic analysis of the assimilation of C5-dicarboxylic acids in Pseudomonas aeruginosa PAO1J Bacteriol 1962543–2551 [View Article][PubMed]. [Google Scholar]
  19. Morett E., Segovia L. (1993). The sigma 54 bacterial enhancer-binding protein family: mechanism of action and phylogenetic relationship of their functional domainsJ Bacteriol 1756067–6074[PubMed]. [Google Scholar]
  20. Mountassif D., Andreoletti P., Cherkaoui-Malki M., Latruffe N., El Kebbaj M.S. (2010). Structural and catalytic properties of the d-3-hydroxybutyrate dehydrogenase from Pseudomonas aeruginosaCurr Microbiol 617–12 [View Article][PubMed]. [Google Scholar]
  21. Nakajima Y., Ito K., Ichihara E., Ogawa K., Egawa T., Xu Y., Yoshimoto T. (2005). Crystallization and preliminary X-ray characterization of d-3-hydroxybutyrate dehydrogenase from Pseudomonas fragiActa Crystallogr F Struct Biol Cryst Commun 6136–38 [View Article][PubMed]. [Google Scholar]
  22. Paithankar K.S., Feller C., Kuettner E.B., Keim A., Grunow M., Sträter N. (2007). Cosubstrate-induced dynamics of d-3-hydroxybutyrate dehydrogenase from Pseudomonas putidaFEBS J 2745767–5779 [View Article][PubMed]. [Google Scholar]
  23. Pardee A.B., Jacob F., Monod J. (1959). The genetic control and cytoplasmic expression of inducibility in the synthesis of β-galactosidase by E. coliJ Mol Biol 1165–178 [View Article]. [Google Scholar]
  24. Studholme D.J., Buck M. (2000). The biology of enhancer-dependent transcriptional regulation in bacteria: insights from genome sequencesFEMS Microbiol Lett 1861–9 [View Article][PubMed]. [Google Scholar]
  25. Tate R.L., Mehlman M.A., Tobin R.B. (1971). Metabolic fate of 1,3-butanediol in the rat: conversion to β-hydroxybutyrateJ Nutr 1011719–1726[PubMed]. [Google Scholar]
  26. Timm A., Steinbüchel A. (1990). Formation of polyesters consisting of medium-chain-length 3-hydroxyalkanoic acids from gluconate by Pseudomonas aeruginosa and other fluorescent pseudomonadsAppl Environ Microbiol 563360–3367[PubMed]. [Google Scholar]
  27. Toyama H., Fujii A., Matsushita K., Shinagawa E., Ameyama M., Adachi O. (1995). Three distinct quinoprotein alcohol dehydrogenases are expressed when Pseudomonas putida is grown on different alcoholsJ Bacteriol 1772442–2450[PubMed]. [Google Scholar]
  28. Ugwu C.U., Tokiwa Y., Ichiba T. (2011). Production of (R)-3-hydroxybutyric acid by fermentation and bioconversion processes with Azohydromonas lataBioresour Technol 1026766–6768 [View Article][PubMed]. [Google Scholar]
  29. Winsor G.L., Lam D.K., Fleming L., Lo R., Whiteside M.D., Yu N.Y., Hancock R.E., Brinkman F.S. (2011). Pseudomonas Genome Database: improved comparative analysis and population genomics capability for Pseudomonas genomesNucleic Acids Res 39D596–D600 [View Article]. [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000163
Loading
The metabolism of (R)-3-hydroxybutyrate is regulated by the enhancer-binding protein PA2005 and the alternative sigma factor RpoN in Pseudomonas aeruginosa PAO1
Microbiology 161, 2232 (2015); https://doi.org/10.1099/mic.0.000163
/content/journal/micro/10.1099/mic.0.000163
/content/journal/micro/10.1099/mic.0.000163
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error