1887

Microbiology Society logo

Volume 161, Issue 9

Permissivity of the biphenyl-specific aerobic bacterial metabolic pathway towards analogues with various steric requirements Free

Abstract

It has repeatedly been shown that aryl-hydroxylating dioxygenases do not possess a very high substrate specificity. To gain more insight into this phenomenon, we examined two powerful biphenyl dioxygenases, the well-known wild-type enzyme from LB400 (BphA-LB400) and a hybrid enzyme, based on a dioxygenase from sp. B4-Magdeburg (BphA-B4h), for their abilities to dioxygenate a selection of eight biphenyl analogues in which the second aromatic ring was replaced by aliphatic as well as aliphatic/aromatic moieties, reflecting a variety of steric requirements. Interestingly, both enzymes were able to catalyse transformation of almost all of these compounds. While the products formed were identical, major differences were observed in transformation rates. In most cases, BphA-B4h proved to be a significantly more powerful catalyst than BphA-LB400. NMR characterization of the reaction products showed that the metabolite obtained from biphenylene underwent angular dioxygenation, whereas all other compounds were subject to lateral dioxygenation at and carbons. Subsequent growth studies revealed that both dioxygenase source strains were able to utilize several of the biphenyl analogues as sole sources of carbon and energy. Therefore, prototype BphBCD enzymes of the biphenyl degradative pathway were examined for their ability to further catabolize the lateral dioxygenation products. All of the - and -hydroxylated compounds were converted to acids, showing that this pathway is quite permissive, enabling catalysis of the turnover of a fairly wide variety of metabolites.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000138
2015-09-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/161/9/1844.html?itemId=/content/journal/micro/10.1099/mic.0.000138&mimeType=html&fmt=ahah

References

  1. Agulló L., Cámara B., Martínez P., Latorre V., Seeger M. 2007; Response to (chloro)biphenyls of the polychlorobiphenyl-degrader Burkholderia xenovorans LB400 involves stress proteins also induced by heat shock and oxidative stress. FEMS Microbiol Lett 267:167–175 [View Article][PubMed]
     [Google Scholar]
  2. Arnold K., Bordoli L., Kopp J., Schwede T. 2006; The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195–201 [View Article][PubMed]
     [Google Scholar]
  3. Bopp L. H. 1986; Degradation of highly chlorinated PCBs by Pseudomonas strain LB400. J Ind Microbiol 1:23–29 [View Article]
     [Google Scholar]
  4. Boyd D. R., Bugg T. D. H. 2006; Arene cis-dihydrodiol formation: from biology to application. Org Biomol Chem 4:181–192 [View Article][PubMed]
     [Google Scholar]
  5. Boyd D. R., Sheldrake G. N. 1998; The dioxygenase-catalyzed formation of vicinal cis-diols. Nat Prod Rep 15:309–325 [View Article]
     [Google Scholar]
  6. Boyd D. R., Sharma N. D., Stevenson P. J., Chima J., Gray D. J., Dalton H. 1991; Bacterial oxidation of benzocycloalkenes to yield monol, diol and triol metabolites. Tetrahedron Lett 32:3887–3890 [View Article]
     [Google Scholar]
  7. Boyd D. R., Sharma N. D., Evans T. A., Groocock M., Malone J. F., Stevenson P. J., Dalton H. 1997; Toluene dioxygenase-catalysed oxidation route to angular cis-monohydrodiols and other bioproducts from bacterial metabolism of 1,2-dihydrobenzocyclobutene and derivatives. J Chem Soc Perkin Trans 1:1879–1886 [View Article]
     [Google Scholar]
  8. Bui V. P., Hansen T. V., Stenstrøm Y., Hudlicky T., Ribbons D. W. 2001; A study of substrate specificity of toluene dioxygenase in processing aromatic compounds containing benzylic and/or remote chiral centers. New J Chem 25:116–124 [View Article]
     [Google Scholar]
  9. Cámara B., Seeger M., González M., Standfuss-Gabisch C., Kahl S., Hofer B. 2007; Generation by a widely applicable approach of a hybrid dioxygenase showing improved oxidation of polychlorobiphenyls. Appl Environ Microbiol 73:2682–2689 [View Article][PubMed]
     [Google Scholar]
  10. Chakraborty J., Ghosal D., Dutta A., Dutta T. K. 2012; An insight into the origin and functional evolution of bacterial aromatic ring-hydroxylating oxygenases. J Biomol Struct Dyn 30:419–436 [View Article][PubMed]
     [Google Scholar]
  11. Chemical Abstracts Services 2015; SciFinder database. www.cas.org/products/scifinder
  12. Colbert C. L., Agar N. Y., Kumar P., Chakko M. N., Sinha S. C., Powlowski J. B., Eltis L. D., Bolin J. T. 2013; Structural characterization of Pandoraea pnomenusa B-356 biphenyl dioxygenase reveals features of potent polychlorinated biphenyl-degrading enzymes. PLoS One 8:e52550 [View Article][PubMed]
     [Google Scholar]
  13. Di Gennaro P., Sello G., Bianchi D., D'Amico P. 1997; Specificity of substrate recognition by Pseudomonas fluorescens N3 dioxygenase. The role of the oxidation potential and molecular geometry. J Biol Chem 272:30254–30260 [View Article][PubMed]
     [Google Scholar]
  14. Eltis L. D., Hofmann B., Hecht H.-J., Lünsdorf H., Timmis K. N. 1993; Purification and crystallization of 2,3-dihydroxybiphenyl 1, 2-dioxygenase. J Biol Chem 268:2727–2732[PubMed]
     [Google Scholar]
  15. Fawcett J. K., Trotter J. 1966; A refinement of the structure of biphenylene. Acta Crystallogr 20:87–93 [View Article]
     [Google Scholar]
  16. Furukawa K. 2000; Biochemical and genetic bases of microbial degradation of polychlorinated biphenyls (PCBs). J Gen Appl Microbiol 46:283–296 [View Article][PubMed]
     [Google Scholar]
  17. Furukawa K., Hirose J., Suyama A., Zaiki T., Hayashida S. 1993; Gene components responsible for discrete substrate specificity in the metabolism of biphenyl (bph operon) and toluene (tod operon). J Bacteriol 175:5224–5232[PubMed]
     [Google Scholar]
  18. Gibson D. T., Parales R. E. 2000; Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr Opin Biotechnol 11:236–243 [View Article][PubMed]
     [Google Scholar]
  19. Grosdidier A., Zoete V., Michielin O. 2007; EADock: docking of small molecules into protein active sites with a multiobjective evolutionary optimization. Proteins 67:1010–1025 [View Article][PubMed]
     [Google Scholar]
  20. Grosdidier A., Zoete V., Michielin O. 2011; SwissDock, a protein-small molecule docking web service based on EADock DSS. Nucleic Acids Res 39:(Suppl. 2)W270–W277 [View Article][PubMed]
     [Google Scholar]
  21. Grund A. D. 1995; Formation and dehydration of hydroxylated diphenylacetylenes. Patent WO 95/30764
    [Google Scholar]
  22. Haddock J. D., Nadim L. M., Gibson D. T. 1993; Oxidation of biphenyl by a multicomponent enzyme system from Pseudomonas sp. strain LB400. J Bacteriol 175:395–400[PubMed]
     [Google Scholar]
  23. Haddock J. D., Horton J. R., Gibson D. T. 1995; Dihydroxylation and dechlorination of chlorinated biphenyls by purified biphenyl 2,3-dioxygenase from Pseudomonas sp. strain LB400. J Bacteriol 177:20–26[PubMed]
     [Google Scholar]
  24. Hofer B., Eltis L. D., Dowling D. N., Timmis K. N. 1993; Genetic analysis of a Pseudomonas locus encoding a pathway for biphenyl/polychlorinated biphenyl degradation. Gene 130:47–55 [View Article][PubMed]
     [Google Scholar]
  25. Hudlicky T., Gonzalez D., Gibson D. T. 1999; Enzymatic hydroxylation of aromatics in enantioselective synthesis: expanding asymmetric methodology. Aldrichim Acta 32:35–62
     [Google Scholar]
  26. Huibers P. D. T., Katritzky A. R. 1998; Correlation of the aqueous solubility of hydrocarbons and halogenated hydrocarbons with molecular structure. J Chem Inf Comput Sci 38:283–292 [View Article]
     [Google Scholar]
  27. Irwin J. J., Sterling T., Mysinger M. M., Bolstad E. S., Coleman R. G. 2012; ZINC: a free tool to discover chemistry for biology. J Chem Inf Model 52:1757–1768 [View Article][PubMed]
     [Google Scholar]
  28. Kahl S., Hofer B. 2003; A genetic system for the rapid isolation of aromatic-ring-hydroxylating dioxygenase activities. Microbiology 149:1475–1481 [View Article][PubMed]
     [Google Scholar]
  29. Kimura N., Nishi A., Goto M., Furukawa K. 1997; Functional analyses of a variety of chimeric dioxygenases constructed from two biphenyl dioxygenases that are similar structurally but different functionally. J Bacteriol 179:3936–3943[PubMed]
     [Google Scholar]
  30. Kitagawa W., Miyauchi K., Masai E., Fukuda M. 2001; Cloning and characterization of benzoate catabolic genes in the Gram-positive polychlorinated biphenyl degrader Rhodococcus sp. strain RHA1. J Bacteriol 183:6598–6606 [View Article][PubMed]
     [Google Scholar]
  31. Kobayashi S., Kuno S., Itada N., Hayaishi O., Kozuka S., Oae S. 1964; O18 studies on anthranilate hydroxylase – a novel mechanism of double hydroxylation. Biochem Biophys Res Commun 16:556–561 [View Article][PubMed]
     [Google Scholar]
  32. Kumar P., Mohammadi M., Viger J. F., Barriault D., Gomez-Gil L., Eltis L. D., Bolin J. T., Sylvestre M. 2011; Structural insight into the expanded PCB-degrading abilities of a biphenyl dioxygenase obtained by directed evolution. J Mol Biol 405:531–547 [View Article][PubMed]
     [Google Scholar]
  33. McKay D. B., Seeger M., Zielinski M., Hofer B., Timmis K. N. 1997; Heterologous expression of biphenyl dioxygenase-encoding genes from a Gram-positive broad-spectrum polychlorinated biphenyl degrader and characterization of chlorobiphenyl oxidation by the gene products. J Bacteriol 179:1924–1930[PubMed]
     [Google Scholar]
  34. Mondello F. J. 1989; Cloning and expression in Escherichia coli of Pseudomonas strain LB400 genes encoding polychlorinated biphenyl degradation. J Bacteriol 171:1725–1732[PubMed]
     [Google Scholar]
  35. Mondello F. J., Turcich M. P., Lobos J. H., Erickson B. D. 1997; Identification and modification of biphenyl dioxygenase sequences that determine the specificity of polychlorinated biphenyl degradation. Appl Environ Microbiol 63:3096–3103[PubMed]
     [Google Scholar]
  36. Nam J. W., Nojiri H., Yoshida T., Habe H., Yamane H., Omori T. 2001; New classification system for oxygenase components involved in ring-hydroxylating oxygenations. Biosci Biotechnol Biochem 65:254–263 [View Article][PubMed]
     [Google Scholar]
  37. Pham T. T., Sylvestre M. 2013; Has the bacterial biphenyl catabolic pathway evolved primarily to degrade biphenyl? The diphenylmethane case. J Bacteriol 195:3563–3574 [View Article][PubMed]
     [Google Scholar]
  38. Resnick S. M., Torok D. S., Gibson D. T. 1995; Chemoenzymatic synthesis of chiral boronates for the determination of the absolute configuration and enantiomeric excess of bacterial and synthetic cis-diols. J Org Chem 60:3546–3549 [View Article]
     [Google Scholar]
  39. Royal Society of Chemistry 2015; ChemSpider database. www.chemspider.com .
  40. Sambrook J., Russell D. W. 2001 Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  41. Seah S. Y. K., Terracina G., Bolin J. T., Riebel P., Snieckus V., Eltis L. D. 1998; Purification and preliminary characterization of a serine hydrolase involved in the microbial degradation of polychlorinated biphenyls. J Biol Chem 273:22943–22949 [View Article][PubMed]
     [Google Scholar]
  42. Seah S. Y. K., Labbé G., Nerdinger S., Johnson M. R., Snieckus V., Eltis L. D. 2000; Identification of a serine hydrolase as a key determinant in the microbial degradation of polychlorinated biphenyls. J Biol Chem 275:15701–15708 [View Article][PubMed]
     [Google Scholar]
  43. Seeger M., Timmis K. N., Hofer B. 1995a; Degradation of chlorobiphenyls catalyzed by the bph-encoded biphenyl-2,3-dioxygenase and biphenyl-2,3-dihydrodiol-2,3-dehydrogenase of Pseudomonas sp. LB400. FEMS Microbiol Lett 133:259–264 [View Article][PubMed]
     [Google Scholar]
  44. Seeger M., Timmis K. N., Hofer B. 1995b; Conversion of chlorobiphenyls into phenylhexadienoates and benzoates by the enzymes of the upper pathway for polychlorobiphenyl degradation encoded by the bph locus of Pseudomonas sp. strain LB400. Appl Environ Microbiol 61:2654–2658[PubMed]
     [Google Scholar]
  45. Seeger M., Zielinski M., Timmis K. N., Hofer B. 1999; Regiospecificity of dioxygenation of di- to pentachlorobiphenyls and their degradation to chlorobenzoates by the bph-encoded catabolic pathway of Burkholderia sp. strain LB400. Appl Environ Microbiol 65:3614–3621[PubMed]
     [Google Scholar]
  46. Seeger M., Cámara B., Hofer B. 2001; Dehalogenation, denitration, dehydroxylation, and angular attack on substituted biphenyls and related compounds by a biphenyl dioxygenase. J Bacteriol 183:3548–3555 [View Article][PubMed]
     [Google Scholar]
  47. Spain J. C., Nishino S. F., Witholt B., Tan L. S., Duetz W. A. 2003; Production of 6-phenylacetylene picolinic acid from diphenylacetylene by a toluene-degrading Acinetobacter strain. Appl Environ Microbiol 69:4037–4042 [View Article][PubMed]
     [Google Scholar]
  48. Standfuß-Gabisch C., Al-Halbouni D., Hofer B. 2012; Characterization of biphenyl dioxygenase sequences and activities encoded by the metagenomes of highly polychlorobiphenyl-contaminated soils. Appl Environ Microbiol 78:2706–2715 [View Article][PubMed]
     [Google Scholar]
  49. Studier F. W. 1991; Use of bacteriophage T7 lysozyme to improve an inducible T7 expression system. J Mol Biol 219:37–44 [View Article][PubMed]
     [Google Scholar]
  50. Yamada A., Kishi H., Sugiyama K., Hatta T., Nakamura K., Masai E., Fukuda M. 1998; Two nearly identical aromatic compound hydrolase genes in a strong polychlorinated biphenyl degrader, Rhodococcus sp. strain RHA1. Appl Environ Microbiol 64:2006–2012[PubMed]
     [Google Scholar]
  51. Zielinski M., Backhaus S., Hofer B. 2002; The principal determinants for the structure of the substrate-binding pocket are located within a central core of a biphenyl dioxygenase α subunit. Microbiology 148:2439–2448[PubMed] [CrossRef]
     [Google Scholar]
  52. Zielinski M., Kahl S., Hecht H.-J., Hofer B. 2003; Pinpointing biphenyl dioxygenase residues that are crucial for substrate interaction. J Bacteriol 185:6976–6980 [View Article][PubMed]
     [Google Scholar]
  53. Zielinski M., Kahl S., Standfuß-Gabisch C., Cámara B., Seeger M., Hofer B. 2006; Generation of novel-substrate-accepting biphenyl dioxygenases through segmental random mutagenesis and identification of residues involved in enzyme specificity. Appl Environ Microbiol 72:2191–2199 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000138
Loading
Permissivity of the biphenyl-specific aerobic bacterial metabolic pathway towards analogues with various steric requirements
Microbiology 161, 1844 (2015); https://doi.org/10.1099/mic.0.000138
/content/journal/micro/10.1099/mic.0.000138
/content/journal/micro/10.1099/mic.0.000138
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