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Regulation of ferulic catabolic genes in Pseudomonas fluorescens BF13: involvement of a MarR family regulator

  • Applied Microbial and Cell Physiology
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Abstract

In Pseudomonas fluorescens BF13, the cluster of genes essential for degradation of ferulic to vanillic acid (ech, vdh and fcs) is expressed in ferulic but not in succinic-grown cells. In the upstream region, we identified a gene, ferR, encoding a protein homologous to transcriptional regulators of the MarR family. A ferR knockout mutant (BF13–89) showed a 3.5-fold increase in expression of an ech-reporter gene fusion compared with the parent strain in succinic-grown cells, indicating that the ferR gene product negatively regulates expression of the ferulic catabolic operon in P. fluorescens BF13. Consistent with the increased expression of the catabolic genes in the ferR mutant, BF13-89 showed a shorter (relative to its FerR+ parent) lag phase during carbon source shift from succinic to ferulic acid. However, expression of ech-lacZ fusion did not increase in BF13–89 grown in the presence of ferulic acid, indicating that FerR has a second function as transcriptional activator. Expression of ech-lacZ in a feruloyl-CoA synthetase-deficient strain revealed unambiguously that FerR-mediated activation of the ferulic catabolic operon is dependent on the thioester product of the feruloyl-CoA synthetase reaction.

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References

  • Achterholt S, Priefert H, Steinbüchel A (2000) Identification of Amycolatopsis sp. strain HR167 genes, involved in the bioconversion of ferulic acid to vanillin. Appl Microbiol Biotechnol 54:799–807

    CAS  PubMed  Google Scholar 

  • Barghini P, Montebove F, Ruzzi M, Schiesser A (1998) Optimal conditions for bioconversion of ferulic acid into vanillic acid by Pseudomonas fluorescens BF13 cells. Appl Microbiol Biotechnol 49:309–314

    Article  CAS  Google Scholar 

  • Barghini P, Di Gioia D, Fava F, Ruzzi M (2007) Vanillin production using metabolically engineered Escherichia coli under non-growing conditions. Microb Cell Fact 6:13

    Article  PubMed  PubMed Central  Google Scholar 

  • Blatny JM, Brautaset T, Winther-Larsen HC, Haugan K, Valla S (1997) Construction and use of a versatile set of broad-host-range cloning and expression vectors based on the RK2 replicon. Appl Environ Microbiol 63:370–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Civolani C, Barghini P, Roncetti AR, Ruzzi M, Schiesser A (2000) Bioconversion of ferulic acid into vanillic acid by means of a vanillate-negative mutant of Pseudomonas fluorescens strain BF13. Appl Environ Microbiol 66:2311–2317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gasson MJ, Kitamura Y, McLauchlan R, Narbad A, Parr AJ, Parsons ELH, Payne J, Rhodes MJC, Walton NJ (1998) Metabolism of ferulic acid to vanillin. A bacterial gene of the enoyl-SCoA hydratase/isomerase superfamily encodes an enzyme for the hydration and cleavage of a hydroxycinnamic acid SCoA thioester. J Biol Chem 273:4163–4170

    Article  CAS  PubMed  Google Scholar 

  • Goldberg JB, Ohman DE (1984) Cloning and expression in Pseudomonas aeruginosa of a gene involved in production of alginate. J Bacteriol 158:1115–1121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP (1998) A broad-host-range Flp–FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77–86

    Article  CAS  PubMed  Google Scholar 

  • Mathew S, Abraham TE (2006) Bioconversions of ferulic acid, a hydroxycinnamic acid. Crit Rev Microbiol 32:115–125

    Article  CAS  PubMed  Google Scholar 

  • Muheim A, Lerch K (1999) Towards a high-yield bioconversion of ferulic acid to vanillin. Appl Microbiol Biotechnol 51:456–461

    Article  CAS  Google Scholar 

  • Nordkvisk E, Salomonsson AC, Amar P (1984) Distribution of insoluble bound phenolic acids in barley grain. J Sci Food Agric 35:657–661

    Article  Google Scholar 

  • Overhage J, Priefert H, Steinbüchel A (1999) Biochemical and genetic analyses of ferulic acid catabolism in Pseudomonas sp. Strain HR199. Appl Environ Microbiol 65:4837–4847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parke D, Ornston LN (2003) Hydroxycinnamate (hca) catabolic genes from Acinetobacter spstrain ADP1 are repressed by HcaR and are induced by hydroxycinnamoyl-Coenzyme A thioesters. Appl Environ Microbiol 69:5398–5409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plaggenborg R, Steinbüchel A, Priefert H (2001) The coenzyme A-dependent, non-beta-oxidation pathway and not direct deacetylation is the major route for ferulic acid degradation in Delftia acidovorans. FEMS Microbiol Lett 205:9–16

    CAS  PubMed  Google Scholar 

  • Plaggenborg R, Overhage J, Steinbüchel A, Priefert H (2003) Functional analysis of gene involved in the metabolism of ferulic acid in Pseudomonas putida KT2440. Appl Microbiol Biotechnol 61:528–535

    Article  CAS  PubMed  Google Scholar 

  • Plaggenborg R, Overhage J, Loos A, Archer JAC, Lessard P, Sinskey AJ, Steinbüchel A, Priefert H (2006) Potential of Rhodococcus strains for biotechnological vanillin production from ferulic acid and eugenol. Appl Microbiol Biotechnol 72:745–755

    Article  CAS  PubMed  Google Scholar 

  • Priefert H, Rabenhorst J, Steinbüchel A (2001) Biotechnological production of vanillin. Appl Microbiol Biotechnol 56:296–314

    Article  CAS  PubMed  Google Scholar 

  • Rosazza JPN, Huang Z, Dostal L, Volm T, Rousseau B (1995) Biocatalytic transformation of ferulic acid: an abundant aromatic natural product. J Ind Microbiol 15:457–471

    Article  CAS  PubMed  Google Scholar 

  • Ruzzi M, Barghini P, Montebove F, Schiesser A (1997) Effect of the carbon source on the utilization of ferulic, m- and p-coumaric acids by a Pseudomonas fluorescens strain. Ann Microbiol 47:87–96

    CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual (second ed.). Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.

    Google Scholar 

  • Santos PM, Di Bartolo I, Blatny JM, Zennaro E, Valla S (2001) New broad-host-range promoter probe vectors based on the plasmid RK2 replicon. FEMS Microbiol Lett 195:91–96

    Article  CAS  PubMed  Google Scholar 

  • Saulnier L, Vigouroux L, Thibault JF (1995) Isolation and partial characterization of feruloylated oligosaccharides from maize bran. Carbohydr Res 272:241–253

    Article  CAS  PubMed  Google Scholar 

  • Schrader J, Etschmann MMW, Sell D, Hilmer JM, Rabenhorst J (2004) Applied biocatalysis for the synthesis of natural flavour compounds—current industrial processes and future prospects. Biotechnol Lett 26:463–472

    Article  CAS  PubMed  Google Scholar 

  • Shibuya N (1984) Phenolic acids and their carbohydrate esters in rice endosperm cell walls. Phytochem 23:2233–2237

    Article  CAS  Google Scholar 

  • Smith MM, Hartley RD (1983) Occurrence and nature of ferulic acid substitution of cell wall polysaccharides in graminaceous plants. Carbohydr Res 118:65–80

    Article  CAS  Google Scholar 

  • Walton NJ, Narbad A, Faulds C, Williamson G (2000) Novel approaches to the biosynthesis of vanillin. Curr Opin Biotechnol 11:490–496

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgement

The authors acknowledge the Italian MIUR (PRIN) for funding the project.

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Correspondence to M. Ruzzi.

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C. Calisti and A.G. Ficca contributed equally.

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Calisti, C., Ficca, A.G., Barghini, P. et al. Regulation of ferulic catabolic genes in Pseudomonas fluorescens BF13: involvement of a MarR family regulator. Appl Microbiol Biotechnol 80, 475–483 (2008). https://doi.org/10.1007/s00253-008-1557-4

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  • DOI: https://doi.org/10.1007/s00253-008-1557-4

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