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Journal of Bacteriology, August 2004, p. 5062-5077, Vol. 186, No. 15
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.15.5062-5077.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

The Homogentisate Pathway: a Central Catabolic Pathway Involved in the Degradation of L-Phenylalanine, L-Tyrosine, and 3-Hydroxyphenylacetate in Pseudomonas putida

Elsa Arias-Barrau,1 Elías R. Olivera,1 José M. Luengo,1 Cristina Fernández,2 Beatriz Galán,2 José L. García,2 Eduardo Díaz,2 and Baltasar Miñambres2*

Departamento de Bioquímica y Biología Molecular, Facultad de Veterinaria, Universidad de León, 24007 León,1 Departamento de Microbiología Molecular, Centro de Investigaciones Biológicas, Consejo Superior de Investigaciones Científicas, Madrid, Spain2

Received 28 February 2004/ Accepted 3 May 2004

Pseudomonas putida metabolizes Phe and Tyr through a peripheral pathway involving hydroxylation of Phe to Tyr (PhhAB), conversion of Tyr into 4-hydroxyphenylpyruvate (TyrB), and formation of homogentisate (Hpd) as the central intermediate. Homogentisate is then catabolized by a central catabolic pathway that involves three enzymes, homogentisate dioxygenase (HmgA), fumarylacetoacetate hydrolase (HmgB), and maleylacetoacetate isomerase (HmgC), finally yielding fumarate and acetoacetate. Whereas the phh, tyr, and hpd genes are not linked in the P. putida genome, the hmgABC genes appear to form a single transcriptional unit. Gel retardation assays and lacZ translational fusion experiments have shown that hmgR encodes a specific repressor that controls the inducible expression of the divergently transcribed hmgABC catabolic genes, and homogentisate is the inducer molecule. Footprinting analysis revealed that HmgR protects a region in the Phmg promoter that spans a 17-bp palindromic motif and an external direct repetition from position –16 to position 29 with respect to the transcription start site. The HmgR protein is thus the first IclR-type regulator that acts as a repressor of an aromatic catabolic pathway. We engineered a broad-host-range mobilizable catabolic cassette harboring the hmgABC, hpd, and tyrB genes that allows heterologous bacteria to use Tyr as a unique carbon and energy source. Remarkably, we show here that the catabolism of 3-hydroxyphenylacetate in P. putida U funnels also into the homogentisate central pathway, revealing that the hmg cluster is a key catabolic trait for biodegradation of a small number of aromatic compounds.

* Corresponding author. Present address: Estación Agrícola Experimental, Consejo Superior de Investigaciones Científicas, Finca Marzanas, 24346 Grulleros, León, Spain. Phone: 34-987317156. Fax: 34-987317161. E-mail: b.minambres{at}eae.csic.es.

Journal of Bacteriology, August 2004, p. 5062-5077, Vol. 186, No. 15
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.15.5062-5077.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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