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Degradative pathways for p-toluenecarboxylate and p-toluenesulfonate and their multicomponent oxygenases in Comamonas testosteroni strains PSB-4 and T-2

Elisabeth Sailer^1,

Hans R. Schläfli Oppenberg^1,

Microbiology Institute, Swiss Federal Institute of Technology, ETH-Zentrum, CH-8092 Zürich, Switzerland
Fakultät für Biologie der Universität, Postfach 5560, D-78434 Konstanz, Germany

³Author for correspondence: Alasdair Cook. Tel: +49 7531 88 4247. Fax: +49 7531 88 2966. e-mail: Alasdair.Cook@uni-konstanz.de

ABSTRACT

Three multicomponent oxygenases involved in the degradation of p-toluenesulfonate and p-toluenecarboxylate and the regulation of their synthesis have been examined in three strains (T-2, PSB-4 and TER-1) of Comamonas testosteroni. Strain T-2 utilizes p-toluenesulfonate as a source of carbon and energy for growth via p-sulfobenzoate and protocatechuate, and p-toluenecarboxylate via terephthalate and protocatechuate, and has the unusual property of requiring the reductase (TsaB) of the toluenesulfonate methyl monooxygenase system (TsaMB) in an incompletely expressed sulfobenzoate dioxygenase system (PsbAC) [Schläfli Oppenberg, H. R., Chen, G., Leisinger, T. & Cook, A. M. (1995). Microbiology 141, 1891-1899]. The independently isolated C. testosteroni PSB-4 utilized only sulfobenzoate and terephthalate via protocatechuate. Mutant TER-1, derived from strain T-2, utilized only terephthalate via protocatechuate. We detected no enzymes of the pathway from toluenesulfonate to sulfobenzoate in strains PSB-4 and TER-1, and confirmed by PCR and Southern blot analysis that the genes (tsaMB) encoding toluenesulfonate monooxygenase were absent. We concluded that, in strain PSB-4, the regulatory unit encoding the genes for the conversion of toluenesulfonate to sulfobenzoate was missing, and that generation of mutant TER-1 involved deletion of this regulatory unit and of the regulatory unit encoding desulfonation of sulfobenzoate. The degradation of sulfobenzoate in strain PSB-4 was catalysed by a fully inducible sulfobenzoate dioxygenase system (PsbAC_PSB-4), which, after purification of the oxygenase component (PsbA_PSB-4), turned out to be indistinguishable from the corresponding component from strain T-2 (PsbA_T-2). Reductase PsbC_PSB-4, which we could separate but not purify, was active with oxygenase PsbA_PSB-4 and PsbA_T-2. Oxygenase PsbA_PSB-4 was shown by electron paramagnetic resonance spectroscopy to contain a Rieske [2Fe-2S] centre. The enzyme system oxygenating terephthalate was examined and the oxygenase component purified and characterized. The oxygenase component in strains T-2 (and mutant TER-1) and PSB-4 were indistinguishable. The reductase component, which we separated but failed to purify, was active with the oxygenase from all strains. Gains and losses of blocks of genes in evolution is discussed.

Present address: pPresent address: Fa. Paul Bucher, CH-4051 Basel, Switzerland.

Present address: ISREC, Ch. des Boveresses, CH-1066 Epalinges, Switzerland.

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