1887

Abstract

The CbrA/B system in pseudomonads is involved in the utilization of carbon sources and carbon catabolite repression (CCR) through the activation of the small RNAs in , and and in . Interestingly, previous works reported that the CbrA/B system activity in PAO1 and KT2442 responded differently to the presence of different carbon sources, thus raising the question of the exact nature of the signal(s) detected by CbrA. Here, we demonstrated that the CbrA/B/CrcZ(Y) signal transduction pathway is similarly activated in the two species. We show that the CbrA sensor kinase is fully interchangeable between the two species and, moreover, responds similarly to the presence of different carbon sources. In addition, a metabolomics analysis supported the hypothesis that CCR responds to the internal energy status of the cell, as the internal carbon/nitrogen ratio seems to determine CCR and non-CCR conditions. The strong difference found in the 2-oxoglutarate/glutamine ratio between CCR and non-CCR conditions points to the close relationship between carbon and nitrogen availability, or the relationship between the CbrA/B and NtrB/C systems, suggesting that both regulatory systems sense the same sort or interrelated signal.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.078873-0
2014-10-01
2019-11-17
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/10/2243.html?itemId=/content/journal/micro/10.1099/mic.0.078873-0&mimeType=html&fmt=ahah

References

  1. Abdou L. , Chou H. T. , Haas D. , Lu C. D. . ( 2011; ). Promoter recognition and activation by the global response regulator CbrB in Pseudomonas aeruginosa . . J Bacteriol 193:, 2784–2792. [CrossRef] [PubMed]
    [Google Scholar]
  2. Amador C. I. , Canosa I. , Govantes F. , Santero E. . ( 2010; ). Lack of CbrB in Pseudomonas putida affects not only amino acids metabolism but also different stress responses and biofilm development. . Environ Microbiol 12:, 1748–1761. [CrossRef] [PubMed]
    [Google Scholar]
  3. Asakura Y. , Kimura E. , Usuda Y. , Kawahara Y. , Matsui K. , Osumi T. , Nakamatsu T. . ( 2007; ). Altered metabolic flux due to deletion of odhA causes l-glutamate overproduction in Corynebacterium glutamicum . . Appl Environ Microbiol 73:, 1308–1319. [CrossRef] [PubMed]
    [Google Scholar]
  4. Choi K. H. , Kumar A. , Schweizer H. P. . ( 2006; ). A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. . J Microbiol Methods 64:, 391–397. [CrossRef] [PubMed]
    [Google Scholar]
  5. Collier D. N. , Hager P. W. , Phibbs P. V. Jr . ( 1996; ). Catabolite repression control in the Pseudomonads. . Res Microbiol 147:, 551–561. [CrossRef] [PubMed]
    [Google Scholar]
  6. Dagorn A. , Chapalain A. , Mijouin L. , Hillion M. , Duclairoir-Poc C. , Chevalier S. , Taupin L. , Orange N. , Feuilloley M. G. . ( 2013a; ). Effect of GABA, a bacterial metabolite, on Pseudomonas fluorescens surface properties and cytotoxicity. . Int J Mol Sci 14:, 12186–12204. [CrossRef] [PubMed]
    [Google Scholar]
  7. Dagorn A. , Hillion M. , Chapalain A. , Lesouhaitier O. , Duclairoir Poc C. , Vieillard J. , Chevalier S. , Taupin L. , Le Derf F. , Feuilloley M. G. . ( 2013b; ). Gamma-aminobutyric acid acts as a specific virulence regulator in Pseudomonas aeruginosa . . Microbiology 159:, 339–351. [CrossRef] [PubMed]
    [Google Scholar]
  8. dos Santos V. A. , Heim S. , Moore E. R. , Strätz M. , Timmis K. N. . ( 2004; ). Insights into the genomic basis of niche specificity of Pseudomonas putida KT2440. . Environ Microbiol 6:, 1264–1286. [CrossRef] [PubMed]
    [Google Scholar]
  9. Duetz W. A. , Marqués S. , de Jong C. , Ramos J. L. , van Andel J. G. . ( 1994; ). Inducibility of the TOL catabolic pathway in Pseudomonas putida (pWW0) growing on succinate in continuous culture: evidence of carbon catabolite repression control. . J Bacteriol 176:, 2354–2361.[PubMed]
    [Google Scholar]
  10. Duetz W. A. , Marqués S. , Wind B. , Ramos J. L. , van Andel J. G. . ( 1996; ). Catabolite repression of the toluene degradation pathway in Pseudomonas putida harboring pWW0 under various conditions of nutrient limitation in chemostat culture. . Appl Environ Microbiol 62:, 601–606.[PubMed]
    [Google Scholar]
  11. Feehily C. , Karatzas K. A. . ( 2013; ). Role of glutamate metabolism in bacterial responses towards acid and other stresses. . J Appl Microbiol 114:, 11–24. [CrossRef] [PubMed]
    [Google Scholar]
  12. Frimmersdorf E. , Horatzek S. , Pelnikevich A. , Wiehlmann L. , Schomburg D. . ( 2010; ). How Pseudomonas aeruginosa adapts to various environments: a metabolomic approach. . Environ Microbiol 12:, 1734–1747. [CrossRef] [PubMed]
    [Google Scholar]
  13. García-Mauriño S. M. , Pérez-Martínez I. , Amador C. I. , Canosa I. , Santero E. . ( 2013; ). Transcriptional activation of the CrcZ and CrcY regulatory RNAs by the CbrB response regulator in Pseudomonas putida . . Mol Microbiol 89:, 189–205. [CrossRef] [PubMed]
    [Google Scholar]
  14. Görke B. , Stülke J. . ( 2008; ). Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. . Nat Rev Microbiol 6:, 613–624. [CrossRef] [PubMed]
    [Google Scholar]
  15. Hervás A. B. , Canosa I. , Santero E. . ( 2010; ). Regulation of glutamate dehydrogenase expression in Pseudomonas putida results from its direct repression by NtrC under nitrogen-limiting conditions. . Mol Microbiol 78:, 305–319. [CrossRef] [PubMed]
    [Google Scholar]
  16. Hester K. L. , Lehman J. , Najar F. , Song L. , Roe B. A. , MacGregor C. H. , Hager P. W. , Phibbs P. V. Jr , Sokatch J. R. . ( 2000a; ). Crc is involved in catabolite repression control of the bkd operons of Pseudomonas putida and Pseudomonas aeruginosa . . J Bacteriol 182:, 1144–1149. [CrossRef] [PubMed]
    [Google Scholar]
  17. Hester K. L. , Madhusudhan K. T. , Sokatch J. R. . ( 2000b; ). Catabolite repression control by crc in 2xYT medium is mediated by posttranscriptional regulation of bkdR expression in Pseudomonas putida . . J Bacteriol 182:, 1150–1153. [CrossRef] [PubMed]
    [Google Scholar]
  18. Hoang T. T. , Karhoff‐Schweizer R. R. , Kutchma A. J. , Schweizer H. P. . ( 1998; ). A broad‐host‐range Flp‐FRT recombination system for site‐specific excision of chromosomally‐located DNA sequence: application for isolation of unmarked Pseudomonas aeruginosa mutants. . Gene 212:, 77–86.[CrossRef]
    [Google Scholar]
  19. Hoshino T. . ( 1998; ). Transport system in Pseudomonas . . In Pseudomonas Biotechnology Handbooks, vol. 10, pp. 169–199. Edited by Montie T. C. . . New York:: Springer;.
    [Google Scholar]
  20. Humair B. , Wackwitz B. , Haas D. . ( 2010; ). GacA-controlled activation of promoters for small RNA genes in Pseudomonas fluorescens . . Appl Environ Microbiol 76:, 1497–1506. [CrossRef] [PubMed]
    [Google Scholar]
  21. Itoh Y. , Nishijyo T. , Nakada Y. . ( 2007; ). Histidine catabolism and catabolite regulation. . In Pseudomonas, pp. 371–395. Edited by Ramos J.-L. , Filloux A. . . Dordrecht:: Springer;. [CrossRef]
    [Google Scholar]
  22. La Rosa R. , de la Peña F. , Prieto M. A. , Rojo F. . ( 2014; ). The Crc protein inhibits the production of polyhydroxyalkanoates in Pseudomonas putida under balanced carbon/nitrogen growth conditions. . Environ Microbiol 16:, 278–290. [CrossRef] [PubMed]
    [Google Scholar]
  23. Li W. , Lu C. D. . ( 2007; ). Regulation of carbon and nitrogen utilization by CbrAB and NtrBC two-component systems in Pseudomonas aeruginosa . . J Bacteriol 189:, 5413–5420. [CrossRef] [PubMed]
    [Google Scholar]
  24. Linares J. F. , Moreno R. , Fajardo A. , Martínez-Solano L. , Escalante R. , Rojo F. , Martínez J. L. . ( 2010; ). The global regulator Crc modulates metabolism, susceptibility to antibiotics and virulence in Pseudomonas aeruginosa . . Environ Microbiol 12:, 3196–3212. [CrossRef] [PubMed]
    [Google Scholar]
  25. Liu P. . ( 1952; ). Utilization of carbohydrates by Pseudomonas aeruginosa . . J Bacteriol 64:, 773–781.[PubMed]
    [Google Scholar]
  26. MacGregor C. H. , Wolff J. A. , Arora S. K. , Phibbs P. V. Jr . ( 1991; ). Cloning of a catabolite repression control (crc) gene from Pseudomonas aeruginosa, expression of the gene in Escherichia coli, and identification of the gene product in Pseudomonas aeruginosa . . J Bacteriol 173:, 7204–7212.[PubMed]
    [Google Scholar]
  27. Merrick M. J. , Edwards R. A. . ( 1995; ). Nitrogen control in bacteria. . Microbiol Rev 59:, 604–622.[PubMed]
    [Google Scholar]
  28. Miller J. H. . ( 1972; ). Experiments in Molecular Genetics. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory;.
    [Google Scholar]
  29. Moreno R. , Fonseca P. , Rojo F. . ( 2012; ). Two small RNAs, CrcY and CrcZ, act in concert to sequester the Crc global regulator in Pseudomonas putida, modulating catabolite repression. . Mol Microbiol 83:, 24–40. [CrossRef] [PubMed]
    [Google Scholar]
  30. Nishijyo T. , Haas D. , Itoh Y. . ( 2001; ). The CbrA–CbrB two-component regulatory system controls the utilization of multiple carbon and nitrogen sources in Pseudomonas aeruginosa . . Mol Microbiol 40:, 917–931. [CrossRef] [PubMed]
    [Google Scholar]
  31. O’Toole G. A. , Gibbs K. A. , Hager P. W. , Phibbs P. V. Jr , Kolter R. . ( 2000; ). The global carbon metabolism regulator Crc is a component of a signal transduction pathway required for biofilm development by Pseudomonas aeruginosa . . J Bacteriol 182:, 425–431. [CrossRef] [PubMed]
    [Google Scholar]
  32. Park D. H. , Mirabella R. , Bronstein P. A. , Preston G. M. , Haring M. A. , Lim C. K. , Collmer A. , Schuurink R. C. . ( 2010; ). Mutations in γ-aminobutyric acid (GABA) transaminase genes in plants or Pseudomonas syringae reduce bacterial virulence. . Plant J 64:, 318–330. [CrossRef] [PubMed]
    [Google Scholar]
  33. Pessi G. , Haas D. . ( 2000; ). Transcriptional control of the hydrogen cyanide biosynthetic genes hcnABC by the anaerobic regulator ANR and the quorum-sensing regulators LasR and RhlR in Pseudomonas aeruginosa . . J Bacteriol 182:, 6940–6949. [CrossRef] [PubMed]
    [Google Scholar]
  34. Reitzer L. . ( 2003; ). Nitrogen assimilation and global regulation in Escherichia coli . . Annu Rev Microbiol 57:, 155–176. [CrossRef] [PubMed]
    [Google Scholar]
  35. Reva O. N. , Weinel C. , Weinel M. , Böhm K. , Stjepandic D. , Hoheisel J. D. , Tümmler B. . ( 2006; ). Functional genomics of stress response in Pseudomonas putida KT2440. . J Bacteriol 188:, 4079–4092. [CrossRef] [PubMed]
    [Google Scholar]
  36. Rietsch A. , Wolfgang M. C. , Mekalanos J. J. . ( 2004; ). Effect of metabolic imbalance on expression of type III secretion genes in Pseudomonas aeruginosa . . Infect Immun 72:, 1383–1390. [CrossRef] [PubMed]
    [Google Scholar]
  37. Rojo F. . ( 2010; ). Carbon catabolite repression in Pseudomonas: optimizing metabolic versatility and interactions with the environment. . FEMS Microbiol Rev 34:, 658–684.[PubMed]
    [Google Scholar]
  38. Sambrook J. , Fritsch E. F. , Maniatis T. . ( 2000; ). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory;.
    [Google Scholar]
  39. Santero E. , Hervas A. B. , Canosa I. , Govantes F. . ( 2012; ). Glutamate dehydrogenases: enzymology, physiological role and biotechnological relevance. . In Dehydrogenases, pp. 289–318. Edited by Canuto R. A. . . Rijeka:: INTECH;. [CrossRef]
    [Google Scholar]
  40. Schumacher J. , Behrends V. , Pan Z. , Brown D. R. , Heydenreich F. , Lewis M. R. , Bennett M. H. , Razzaghi B. , Komorowski M. . & other authors ( 2013; ). Nitrogen and carbon status are integrated at the transcriptional level by the nitrogen regulator NtrC in vivo . . MBio 4:, e00881-13. [CrossRef] [PubMed]
    [Google Scholar]
  41. Shirai T. , Fujimura K. , Furusawa C. , Nagahisa K. , Shioya S. , Shimizu H. . ( 2007; ). Study on roles of anaplerotic pathways in glutamate overproduction of Corynebacterium glutamicum by metabolic flux analysis. . Microb Cell Fact 6:, 19. [CrossRef] [PubMed]
    [Google Scholar]
  42. Sonnleitner E. , Abdou L. , Haas D. . ( 2009; ). Small RNA as global regulator of carbon catabolite repression in Pseudomonas aeruginosa . . Proc Natl Acad Sci U S A 106:, 21866–21871. [CrossRef] [PubMed]
    [Google Scholar]
  43. Sonnleitner E. , Valentini M. , Wenner N. , Haichar F. Z. , Haas D. , Lapouge K. . ( 2012; ). Novel targets of the CbrAB/Crc carbon catabolite control system revealed by transcript abundance in Pseudomonas aeruginosa . . PLoS ONE 7:, e44637. [CrossRef] [PubMed]
    [Google Scholar]
  44. Stover C. K. , Pham X. Q. , Erwin A. L. , Mizoguchi S. D. , Warrener P. , Hickey M. J. , Brinkman F. S. , Hufnagle W. O. , Kowalik D. J. . & other authors ( 2000; ). Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. . Nature 406:, 959–964. [CrossRef] [PubMed]
    [Google Scholar]
  45. Takeuchi K. , Yamada K. , Haas D. . ( 2012; ). ppGpp controlled by the Gac/Rsm regulatory pathway sustains biocontrol activity in Pseudomonas fluorescens CHA0. . Mol Plant Microbe Interact 25:, 1440–1449. [CrossRef] [PubMed]
    [Google Scholar]
  46. Valentini M. , Lapouge K. . ( 2013; ). Catabolite repression in Pseudomonas aeruginosa PAO1 regulates the uptake of C4-dicarboxylates depending on succinate concentration. . Environ Microbiol 15:, 1707–1716. [CrossRef] [PubMed]
    [Google Scholar]
  47. Wolff J. A. , MacGregor C. H. , Eisenberg R. C. , Phibbs P. V. Jr . ( 1991; ). Isolation and characterization of catabolite repression control mutants of Pseudomonas aeruginosa PAO. . J Bacteriol 173:, 4700–4706.[PubMed]
    [Google Scholar]
  48. Ye R. W. , Haas D. , Ka J. O. , Krishnapillai V. , Zimmermann A. , Baird C. , Tiedje J. M. . ( 1995; ). Anaerobic activation of the entire denitrification pathway in Pseudomonas aeruginosa requires Anr, an analog of Fnr. . J Bacteriol 177:, 3606–3609.[PubMed]
    [Google Scholar]
  49. Yeung A. T. , Bains M. , Hancock R. E. . ( 2011; ). The sensor kinase CbrA is a global regulator that modulates metabolism, virulence, and antibiotic resistance in Pseudomonas aeruginosa . . J Bacteriol 193:, 918–931. [CrossRef] [PubMed]
    [Google Scholar]
  50. Zhang X. X. , Rainey P. B. . ( 2008; ). Dual involvement of CbrAB and NtrBC in the regulation of histidine utilization in Pseudomonas fluorescens SBW25. . Genetics 178:, 185–195. [CrossRef] [PubMed]
    [Google Scholar]
  51. Zuber S. , Carruthers F. , Keel C. , Mattart A. , Blumer C. , Pessi G. , Gigot-Bonnefoy C. , Schnider-Keel U. , Heeb S. . & other authors ( 2003; ). GacS sensor domains pertinent to the regulation of exoproduct formation and to the biocontrol potential of Pseudomonas fluorescens CHA0. . Mol Plant Microbe Interact 16:, 634–644. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.078873-0
Loading
/content/journal/micro/10.1099/mic.0.078873-0
Loading

Data & Media loading...

Supplements

Supplementary Data 

PDF
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