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. 1995 Mar;177(5):1225–1232. doi: 10.1128/jb.177.5.1225-1232.1995

A manganese-dependent dioxygenase from Arthrobacter globiformis CM-2 belongs to the major extradiol dioxygenase family.

Y R Boldt 1, M J Sadowsky 1, L B Ellis 1, L Que Jr 1, L P Wackett 1
PMCID: PMC176727  PMID: 7868595

Abstract

Almost all bacterial ring cleavage dioxygenases contain iron as the catalytic metal center. We report here the first available sequence for a manganese-dependent 3,4-dihydroxyphenylacetate (3,4-DHPA) 2,3-dioxygenase and its further characterization. This manganese-dependent extradiol dioxygenase from Arthrobacter globiformis CM-2, unlike iron-dependent extradiol dioxygenases, is not inactivated by hydrogen peroxide. Also, ferrous ions, which activate iron extradiol dioxygenases, inhibit 3,4-DHPA 2,3-dioxygenase. The gene encoding 3,4-DHPA 2,3-dioxygenase, mndD, was identified from an A. globiformis CM-2 cosmid library. mndD was subcloned as a 2.0-kb SmaI fragment in pUC18, from which manganese-dependent extradiol dioxygenase activity was expressed at high levels in Escherichia coli. The mndD open reading frame was identified by comparison with the known N-terminal amino acid sequence of purified manganese-dependent 3,4-DHPA 2,3-dioxygenase. Fourteen of 18 amino acids conserved in members of the iron-dependent extradiol dioxygenase family are also conserved in the manganese-dependent 3,4-DHPA 2,3-dioxygenase (MndD). Thus, MndD belongs to the extradiol family of dioxygenases and may share a common ancestry with the iron-dependent extradiol dioxygenases. We propose the revised consensus primary sequence (G,T,N,R)X(H,A)XXXXXXX(L,I,V,M,F)YXX(D,E,T,N,A)PX(G,P) X(2,3)E for this family. (Numbers in brackets indicate a gap of two or three residues at this point in the sequence.) The suggested common ancestry is also supported by sequence obtained from genes flanking mndD, which share significant sequence identity with xylJ and xylG from Pseudomonas putida.

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Selected References

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  1. ADACHI K., TAKEDA Y., SENOH S., KITA H. METABOLISM OF P-HYDROXYPHENYLACETIC ACID IN PSEUDOMONAS OVALIS. Biochim Biophys Acta. 1964 Dec 9;93:483–493. doi: 10.1016/0304-4165(64)90332-0. [DOI] [PubMed] [Google Scholar]
  2. Asturias J. A., Eltis L. D., Prucha M., Timmis K. N. Analysis of three 2,3-dihydroxybiphenyl 1,2-dioxygenases found in Rhodococcus globerulus P6. Identification of a new family of extradiol dioxygenases. J Biol Chem. 1994 Mar 11;269(10):7807–7815. [PubMed] [Google Scholar]
  3. Bayly R. C., Dagley S., Gibson D. T. The metabolism of cresols by species of Pseudomonas. Biochem J. 1966 Nov;101(2):293–301. doi: 10.1042/bj1010293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bertram J., Strätz M., Dürre P. Natural transfer of conjugative transposon Tn916 between gram-positive and gram-negative bacteria. J Bacteriol. 1991 Jan;173(2):443–448. doi: 10.1128/jb.173.2.443-448.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blakley E. R. The catabolism of L-tyrosine by an Arthrobacter sp. Can J Microbiol. 1977 Sep;23(9):1128–1139. doi: 10.1139/m77-169. [DOI] [PubMed] [Google Scholar]
  6. Burlage R. S., Hooper S. W., Sayler G. S. The TOL (pWW0) catabolic plasmid. Appl Environ Microbiol. 1989 Jun;55(6):1323–1328. doi: 10.1128/aem.55.6.1323-1328.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Candidus S., van Pée K. H., Lingens F. The catechol 2,3-dioxygenase gene of Rhodococcus rhodochrous CTM: nucleotide sequence, comparison with isofunctional dioxygenases and evidence for an active-site histidine. Microbiology. 1994 Feb;140(Pt 2):321–330. doi: 10.1099/13500872-140-2-321. [DOI] [PubMed] [Google Scholar]
  8. Dabbs E. R., Sole G. J. Plasmid-borne resistance to arsenate, arsenite, cadmium, and chloramphenicol in a Rhodococcus species. Mol Gen Genet. 1988 Jan;211(1):148–154. doi: 10.1007/BF00338406. [DOI] [PubMed] [Google Scholar]
  9. Dong F. M., Wang L. L., Wang C. M., Cheng J. P., He Z. Q., Sheng Z. J., Shen R. Q. Molecular cloning and mapping of phenol degradation genes from Bacillus stearothermophilus FDTP-3 and their expression in Escherichia coli. Appl Environ Microbiol. 1992 Aug;58(8):2531–2535. doi: 10.1128/aem.58.8.2531-2535.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Durham D. R., Stirling L. A., Ornston L. N., Perry J. J. Intergeneric evolutionary homology revealed by the study of protocatechuate 3,4-dioxygenase from Azotobacter vinelandii. Biochemistry. 1980 Jan 8;19(1):149–155. doi: 10.1021/bi00542a023. [DOI] [PubMed] [Google Scholar]
  11. Eck R., Belter J. Cloning and characterization of a gene coding for the catechol 1,2-dioxygenase of Arthrobacter sp. mA3. Gene. 1993 Jan 15;123(1):87–92. doi: 10.1016/0378-1119(93)90544-d. [DOI] [PubMed] [Google Scholar]
  12. Ghosal D., You I. S., Gunsalus I. C. Nucleotide sequence and expression of gene nahH of plasmid NAH7 and homology with gene xylE of TOL pWWO. Gene. 1987;55(1):19–28. doi: 10.1016/0378-1119(87)90244-7. [DOI] [PubMed] [Google Scholar]
  13. Happe B., Eltis L. D., Poth H., Hedderich R., Timmis K. N. Characterization of 2,2',3-trihydroxybiphenyl dioxygenase, an extradiol dioxygenase from the dibenzofuran- and dibenzo-p-dioxin-degrading bacterium Sphingomonas sp. strain RW1. J Bacteriol. 1993 Nov;175(22):7313–7320. doi: 10.1128/jb.175.22.7313-7320.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Harayama S., Rekik M. Bacterial aromatic ring-cleavage enzymes are classified into two different gene families. J Biol Chem. 1989 Sep 15;264(26):15328–15333. [PubMed] [Google Scholar]
  15. Hayase N., Taira K., Furukawa K. Pseudomonas putida KF715 bphABCD operon encoding biphenyl and polychlorinated biphenyl degradation: cloning, analysis, and expression in soil bacteria. J Bacteriol. 1990 Feb;172(2):1160–1164. doi: 10.1128/jb.172.2.1160-1164.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hofer B., Eltis L. D., Dowling D. N., Timmis K. N. Genetic analysis of a Pseudomonas locus encoding a pathway for biphenyl/polychlorinated biphenyl degradation. Gene. 1993 Aug 16;130(1):47–55. doi: 10.1016/0378-1119(93)90345-4. [DOI] [PubMed] [Google Scholar]
  17. Horn J. M., Harayama S., Timmis K. N. DNA sequence determination of the TOL plasmid (pWWO) xylGFJ genes of Pseudomonas putida: implications for the evolution of aromatic catabolism. Mol Microbiol. 1991 Oct;5(10):2459–2474. doi: 10.1111/j.1365-2958.1991.tb02091.x. [DOI] [PubMed] [Google Scholar]
  18. Kimbara K., Hashimoto T., Fukuda M., Koana T., Takagi M., Oishi M., Yano K. Cloning and sequencing of two tandem genes involved in degradation of 2,3-dihydroxybiphenyl to benzoic acid in the polychlorinated biphenyl-degrading soil bacterium Pseudomonas sp. strain KKS102. J Bacteriol. 1989 May;171(5):2740–2747. doi: 10.1128/jb.171.5.2740-2747.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kita H. Crystallization and some properties of 3,4-dihydroxyphenylacetate 2,3-oxygenase from Pseudomonas ovalis. J Biochem. 1965 Aug;58(2):116–122. doi: 10.1093/oxfordjournals.jbchem.a128172. [DOI] [PubMed] [Google Scholar]
  20. Knauf V. C., Nester E. W. Wide host range cloning vectors: a cosmid clone bank of an Agrobacterium Ti plasmid. Plasmid. 1982 Jul;8(1):45–54. doi: 10.1016/0147-619x(82)90040-3. [DOI] [PubMed] [Google Scholar]
  21. Mazodier P., Davies J. Gene transfer between distantly related bacteria. Annu Rev Genet. 1991;25:147–171. doi: 10.1146/annurev.ge.25.120191.001051. [DOI] [PubMed] [Google Scholar]
  22. Nakai C., Kagamiyama H., Nozaki M., Nakazawa T., Inouye S., Ebina Y., Nakazawa A. Complete nucleotide sequence of the metapyrocatechase gene on the TOI plasmid of Pseudomonas putida mt-2. J Biol Chem. 1983 Mar 10;258(5):2923–2928. [PubMed] [Google Scholar]
  23. Noda Y., Nishikawa S., Shiozuka K., Kadokura H., Nakajima H., Yoda K., Katayama Y., Morohoshi N., Haraguchi T., Yamasaki M. Molecular cloning of the protocatechuate 4,5-dioxygenase genes of Pseudomonas paucimobilis. J Bacteriol. 1990 May;172(5):2704–2709. doi: 10.1128/jb.172.5.2704-2709.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Norrander J., Kempe T., Messing J. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene. 1983 Dec;26(1):101–106. doi: 10.1016/0378-1119(83)90040-9. [DOI] [PubMed] [Google Scholar]
  25. Nozaki M., Ono K., Nakazawa T., Kotani S., Hayaishi O. Metapyrocatechase. II. The role of iron and sulfhydryl groups. J Biol Chem. 1968 May 25;243(10):2682–2690. [PubMed] [Google Scholar]
  26. Olson P. E., Qi B., Que L., Jr, Wackett L. P. Immunological demonstration of a unique 3,4-dihydroxyphenylacetate 2,3-dioxygenase in soil Arthrobacter strains. Appl Environ Microbiol. 1992 Sep;58(9):2820–2826. doi: 10.1128/aem.58.9.2820-2826.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ono-Kamimoto M. Studies on 3,4-dihydroxyphenylacetate 2,3-dioxygenase. I. Role of iron, substrate binding, and some other properties. J Biochem. 1973 Nov;74(5):1049–1059. [PubMed] [Google Scholar]
  28. Parker M. W., Blake C. C. Iron- and manganese-containing superoxide dismutases can be distinguished by analysis of their primary structures. FEBS Lett. 1988 Mar 14;229(2):377–382. doi: 10.1016/0014-5793(88)81160-8. [DOI] [PubMed] [Google Scholar]
  29. Péloquin L., Greer C. W. Cloning and expression of the polychlorinated biphenyl-degradation gene cluster from Arthrobacter M5 and comparison to analogous genes from gram-negative bacteria. Gene. 1993 Mar 15;125(1):35–40. doi: 10.1016/0378-1119(93)90742-l. [DOI] [PubMed] [Google Scholar]
  30. Que L., Jr, Widom J., Crawford R. L. 3,4-Dihydroxyphenylacetate 2,3-dioxygenase. A manganese(II) dioxygenase from Bacillus brevis. J Biol Chem. 1981 Nov 10;256(21):10941–10944. [PubMed] [Google Scholar]
  31. Roper D. I., Cooper R. A. Subcloning and nucleotide sequence of the 3,4-dihydroxyphenylacetate (homoprotocatechuate) 2,3-dioxygenase gene from Escherichia coli C. FEBS Lett. 1990 Nov 26;275(1-2):53–57. doi: 10.1016/0014-5793(90)81437-s. [DOI] [PubMed] [Google Scholar]
  32. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sparnins V. L., Chapman P. J. Catabolism of L-tyrosine by the homoprotocatechuate pathway in gram-positive bacteria. J Bacteriol. 1976 Jul;127(1):362–366. doi: 10.1128/jb.127.1.362-366.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sparnins V. L., Chapman P. J., Dagley S. Bacterial degradation of 4-hydroxyphenylacetic acid and homoprotocatechuic acid. J Bacteriol. 1974 Oct;120(1):159–167. doi: 10.1128/jb.120.1.159-167.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Staden R. Computer methods to locate signals in nucleic acid sequences. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 2):505–519. doi: 10.1093/nar/12.1part2.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Williams D. R., Young D. I., Young M. Conjugative plasmid transfer from Escherichia coli to Clostridium acetobutylicum. J Gen Microbiol. 1990 May;136(5):819–826. doi: 10.1099/00221287-136-5-819. [DOI] [PubMed] [Google Scholar]
  37. Wolgel S. A., Dege J. E., Perkins-Olson P. E., Jaurez-Garcia C. H., Crawford R. L., Münck E., Lipscomb J. D. Purification and characterization of protocatechuate 2,3-dioxygenase from Bacillus macerans: a new extradiol catecholic dioxygenase. J Bacteriol. 1993 Jul;175(14):4414–4426. doi: 10.1128/jb.175.14.4414-4426.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Yrjälä K., Paulin L., Kilpi S., Romantschuk M. Cloning of cmpE, a plasmid-borne catechol 2,3-dioxygenase-encoding gene from the aromatic- and chloroaromatic-degrading Pseudomonas sp. HV3. Gene. 1994 Jan 28;138(1-2):119–121. doi: 10.1016/0378-1119(94)90792-7. [DOI] [PubMed] [Google Scholar]
  39. van der Meer J. R., de Vos W. M., Harayama S., Zehnder A. J. Molecular mechanisms of genetic adaptation to xenobiotic compounds. Microbiol Rev. 1992 Dec;56(4):677–694. doi: 10.1128/mr.56.4.677-694.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]

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