1887

Microbiology Society logo

Volume 140, Issue 7

3-Sulphocatechol 2,3-dioxygenase and other dioxygenases (EC 1·13.11·2 and EC 1·14.12.-) in the degradative pathways of 2-aminobenzenesulphonic, benzenesulphonic and 4-toluenesulphonic acids in sp. strain 0-1 Free

Abstract

sp. strain 0-1 utilizes three sulphonated aromatic compounds as sole sources of carbon and energy for growth in minimal salts medium - benzenesulphonate (BS), 4-toluenesulphonate (TS) and 2-aminobenzenesulphonate (2AS). The degradative pathway(s) in 2AS-grown cells are initiated with membrane transport, NADH-dependent dioxygenation and ring cleavage. The specific activity of the NADH-dependent dioxygenation(s) varied with the growth phase and was maximal near the end of exponential growth for each growth substrate. Cells were harvested at this point from BS-, TS- and 2AS-salts medium. Cells grown with each sulphonated substrate could oxygenate all three compounds, but only 2AS-grown cells consumed 2 mol O per mol 2AS or BS or TS. BS- and TS-grown cells consumed 2 mol O per mol BS or TS but failed to oxygenate the product of oxygenation of 2AS, 3-sulphocatechol (3SC). These observations were repeated with cell extracts and we concluded that there were two sets of desulphonative pathways in the organism, one for 2AS and one for BS and TS. We confirmed this hypothesis by separating the degradative enzymes from 2AS-, BS- or TS-grown cells. A 2AS dioxygenase system and a 3SC-2,3-dioxygenase (3SC230) were detected in 2AS-grown cells only. In both BS- and TS-grown cells a dioxygenase system for BS and TS was observed as well as a principal catechol 2,3-dioxygenase (C230-III), neither of which was present in 2AS-grown cells. The 3SC230 was purified to near homogeneity, found to be monomeric ( 42000), and to catalyse 2,3-dioxygenation to a product that decayed spontaneously to sulphite and 2-hydroxymuconate. The 2AS dioxygenase system could cause not only deamination of 2AS but also desulphonation of BS and TS. The BS dioxygenase could desulphonate BS and apparently either desulphonate or deaminate 2AS. Strain 0-1 thus seems to contain two putative, independently regulated operons involving oxygenation and spontaneous desulphonation(s). One operon encodes at least the 2AS dioxygenase system and 3SC230 whereas the other encodes at least the BS/TS dioxygenase system and C230-III.

  • Published Online:
Keyword(s): Alcaligenes sp. strain O-1 , convergent degradative pathways , desulphonation , meta ring cleavage and multi-component dioxygenases
© Society for General Microbiology 1994
Loading

Article metrics loading...

/content/journal/micro/10.1099/13500872-140-7-1713
1994-07-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/micro/140/7/mic-140-7-1713.html?itemId=/content/journal/micro/10.1099/13500872-140-7-1713&mimeType=html&fmt=ahah

References

  1. Bartels I., Knackmuss H.-J., Reineke W. 1984; Suicide inactivation of catechol 2,3-dioxygenase from Pseudomonas putida mt-2 by 3-halocatechols. Appl Environ Microbiol 47:500–505
     [Google Scholar]
  2. Batie C. J., Ballou D. P., Correll C. C. 1992; Phthalate dioxygenase reductase and related flavin-iron-sulfur containing electron transferases. In Chemistry and Biochemistry of Flavoenpymes 3 pp. 543–556 Edited by Muller F. Boca Raton: CRC Press;
     [Google Scholar]
  3. Bayly R.C., Barbour M. G. 1984; The degradation of aromatic compounds by the meta and gentisate pathways. In Microbial Degradation of Organic Compounds pp. 253–294 Edited by Gibson D.T. New York: Marcel Dekker;
     [Google Scholar]
  4. Bird J.A., Cain R. B. 1974; Microbial degradation of alkyl-benzenesulphonates: metabolism of homologues of short alkyl-chain length by an Alcaligenes sp. Biochem J 140:121–134
     [Google Scholar]
  5. Bradford M. 1976; A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
     [Google Scholar]
  6. Bunz P., Cook A. M. 1993; Dibenzofuran 4,4a-dioxygenase from Sphingomonas sp. strain RW1: angular dioxygenation by a three-component enzyme system. J Bacteriol 175:6467–6475
     [Google Scholar]
  7. Cook A.M., Leisinger T. 1991; Desulfonation of aromatic compounds. In Environmental Biotechnology 1 pp. 115–122 Edited by Verachtert H., Verstraete W. . Antwerp: Koninklijke Vlaamse Ingenieursveniging;
     [Google Scholar]
  8. Correll C. C., Batie C. J., Ballou D. P., Ludwig M. L. 1992; Phthalate dioxygenase reductase: a modular structure for electron transfer from pyridine nucleotides to [2Fe—2S]. Science 258:1604–1610
     [Google Scholar]
  9. Engesser K. H., Strubel V., Christoglou K., Fischer P., Rast H. G. 1989; Dioxygenolytic cleavage of aryl ether bonds: 1,10-dihydro-1,10-dihydroxyfluoren-9-one, a novel arene dihydrodiol as evidence for angular dioxygenation of dibenzofuran. FEMS Microbiol Lett 65:205–210
     [Google Scholar]
  10. Feigel B., Knackmuss H.-J. 1993; Syntrophic interactions during degradation of 4-aminobenzenesulfonic acid by a two species bacterial culture. Arch Microbiol 159:124–130
     [Google Scholar]
  11. Geary P. J., Mason J. R., Joannou C. L. 1990; Benzene dioxygenase from Pseudomonas putida ML2 (NCIB 12190). Methods Ensymol 188:52–60
     [Google Scholar]
  12. Grossenbacher H., Thurnheer T., Ziirrer D., Cook A. M. 1986; Determination of sulfonated azo dyestuffs and their bacterial metabolites by high pressure liquid chromatography. J Chromatogr 360:219–223
     [Google Scholar]
  13. Happe B., Eltis L. D., Poth H., Hedderich R., Timmis K. N. 1993; Characterization of 2,2', 3-tri hydroxy biphenyl dioxygenase, an extradiol dioxygenase from the dibenzofuran-and dibenzo-p-dioxin-degrading bacterium Sphingomonas sp. strain RW1. J Bacteriol 175:7313–7320
     [Google Scholar]
  14. Harayama S., Kok M., Neidle E. L. 1992; Functional and evolutionary relationships among diverse oxygenases. Annu Rev Microbiol 46:565–601
     [Google Scholar]
  15. Jahnke M., El-Banna T., Klintworth R., Auling G. 1990; Mineralization of orthanilic acid is a plasmid-associated trait in Alcaligenes sp. 0-1. J Gen Microbiol 136:2241–2249
     [Google Scholar]
  16. Jahnke M., Lehmann F., Schoebel A., Auling G. 1993; Transposition of the TOL catabolic genes (Tn46S1) into the degradative plasmid pSAH of Alcaligenes sp. 0-1 ensures simultaneous mineralization of sulpho-and methyl-substituted aromatics. J Gen Microbiol 139:1959–1966
     [Google Scholar]
  17. Junker F., Field J. A., Bangerter F., Ramsteiner K., Kohler H.-P., Joannou C. L., Mason J. R., Leisinger T., Cook A. M. 1994; Dioxygenation and spontaneous deamination of 2-aminobenzene-sulphonic acid in Alcaligenes sp. strain O-1 with subsequent meta ring cleavage and spontaneous desulphonation to 2-hydroxymuconic acid. Biochem J 300:429–436
     [Google Scholar]
  18. Kataeva I.A., Golovleva L. A. 1990; Catechol 2,3-dioxygenase from Pseudomonas aeruginosa 2x. Methods Ensymol 188:115–121
     [Google Scholar]
  19. Kennedy S.I.T., Fewson C.A. 1968; Enzymes of the mandelate pathway in bacterium N.C.I.B. 8250. Biochem J 107:497–506
     [Google Scholar]
  20. Klecka G.M., Gibson D. T. 1981; Inhibition of catechol 2,3-dioxygenase from Pseudomonas putida by 3-chlorocatechol. Appl Environ Microbiol 41:1159–1165
     [Google Scholar]
  21. Laemmli U.K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
     [Google Scholar]
  22. Lipscomb J.D., Orville A. M. 1992; Mechanistic aspects of dihydroxybenzoate dioxygenases. Metal Ions Biol Syst 28:243–298
     [Google Scholar]
  23. Locher H. H., Leisinger T., Cook A. M. 1989; Degradation ofp- toluenesulphonic acid via sidechain oxidation, desulphonation and meta ring cleavage in Pseudomonas (Comamonas) testosteroni T-2. J Gen Microbiol 135:1969–1978
     [Google Scholar]
  24. Locher H. H., Leisinger T., Cook A. M. 1991; Sulphobenzoate 3,4-dioxygenase: purification and properties of a desulphonative two-component enzyme system from Comamonas testosteroni . Biochem J 274:833–842
     [Google Scholar]
  25. Locher H. H., Poolman B., Cook A. M., Konings W. N. 1993; Uptake of 4-toluenesulfonate by Comamonas testosteroni T-2. J Bacteriol 175:1075–1080
     [Google Scholar]
  26. Mason J.R., Cammack R. 1992; The electron-transport proteins of hydroxylating bacterial dioxygenases. Annu Rev Microbiol 46:277–305
     [Google Scholar]
  27. Moodie F.D.L., Woodland M. P., Mason J. R. 1990; The reductase component of the chromosomally encoded benzoate dioxygenase from Pseudomonas putida C-l is immunologically homologous with a product of the plasmid encoded xylD gene (toluate dioxygenase) from Pseudomonas putida mt-2. FEMS Microbiol Lett 71:163–168
     [Google Scholar]
  28. Thurnheer T., Kohler T., Cook A. M., Leisinger T. 1986; Orthanilic acid and analogues as carbon sources for bacteria; growth physiology and enzymic desulphonation. J Gen Microbiol 132:1215–1220
     [Google Scholar]
  29. Thurnheer T., Ziirrer D., Hoglinger O., Leisinger T., Cook A. M. 1990; Initial steps in the degradation of benzene sulfonic acid, 4-toluene sulfonic acid, and orthanilic acid in Alcaligenes sp. strain 0-1. Biodegradation 1:55–64
     [Google Scholar]
  30. Webb E.C. 1992 Enzyme Nomenclature 1992. San Diego: Academic Press;
     [Google Scholar]
  31. Whitman C. P., Aird B. A., Gillespie W. R., Stolowich N. J. 1991; Chemical and enzymatic ketonization of 2-hydroxymuco-nate, a conjugated enol. J Am Chem Soc 113:3154–3162
     [Google Scholar]
  32. Wittich R. M., Rast H. G., Knackmuss H.-J. 1988; Degradation of naphthalene-2,6-and naphthalene-1,6-disulfonic acid by a Moraxella sp. Appl Environ Microbiol 54:1842–1847
     [Google Scholar]
  33. Zamanian M., Mason J. R. 1987; Benzene dioxygenase in Pseudomonas putida: subunit composition and immuno-cross-re-activity with other aromatic dioxygenases. Biochem J 244:611–616
     [Google Scholar]
  34. Zürrer D., Cook A. M., Leisinger T. 1987; Microbial desufo-nation of substituted naphthalenesulfonic acids and benzenesulfonic acids. Appl Environ Microbiol 53:1459–1463
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/13500872-140-7-1713
Loading
3-Sulphocatechol 2,3-dioxygenase and other dioxygenases (EC 1·13.11·2 and EC 1·14.12.-) in the degradative pathways of 2-aminobenzenesulphonic, benzenesulphonic and 4-toluenesulphonic acids in Alcaligenes sp. strain 0-1
Microbiology 140, 1713 (1994); https://doi.org/10.1099/13500872-140-7-1713
/content/journal/micro/10.1099/13500872-140-7-1713
/content/journal/micro/10.1099/13500872-140-7-1713
Loading

Data & Media loading...

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