Skip to main content
SpringerLink
Log in

Polymorphism of the bphA genes in bacteria destructing biphenyl/chlorinated biphenils

  • Genomics. Transcriptomics
  • Published:
Molecular Biology Aims and scope Submit manuscript

Abstract

Polychlorinated biphenyls (PCBs) are persistent organic pollutants. Biphenyl 2,3-dioxygenase (BDO) is a key enzyme that determines the range of PCBs oxidized by a bacterial strain. BDO subunit α (BphA1) plays an essential role in substrate recognition and binding. The genes for dioxygenases that hydroxylate aromatic rings were screened and analyzed phylogenetically. Genes found in biphenyl-oxidizing Rhodococcus erythropolis strains G12a, B7b, and B106a proved to be similar to the published nucleotide sequences of the Rhodococcus sp. HA99 and R04 and Novosphingobium aromaticivorans F199 bphA1 genes, which code for the α-subunits that do not belong to the biphenyl/toluene dioxygenase (B/TDO) family. PCB-destructing R. ruber P25 was found to possess a unique bphA1 gene, which clusters together with the phenylpropionate dioxygenase (PPDO) α-subunits of Mycobacterium vanbaalenii PYR-1 and Frankia sp. EuI1c. The deduced amino acid sequences of the genes were analyzed. The amino acids of the BDO active site in R. wratislaviensis P1, P12, P13, and P20 (bphA1 genes of the B/TDO family) were identical to those of the active PCB degrader R. jostii RHA1. The Rhodococcus strains in question were shown to be active toward both orthoand parachlorinated ring of 2,4'-dichlorobiphenyl. The α-subunit amino acids responsible for the substrate specificity of the enzyme in Pseudomonas sp. S9, S13, S210, S211, and S212 (B/TDO family) were the same as in P. pseudoalcaligenes KF707. The Pseudomonas strains were active toward the para-chlorinated ring of 2,4'-dichlorobiphenyl. The results of screening bacterial strains for bphA1 can be used to identify the biotechnologically promising PCB destructors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

BDO:

biphenyl dioxygenase

NDO:

naphthalene dioxygenase

PPDO:

phenylpropionate dioxygenase

B/TDO:

biphenyl/toluene dioxygenase

PCB:

polychlorinated biphenyl

References

  1. Adams N.G., Richardson D.M. 1953. Isolation and identification of biphenyls from West Edmond Crude Oil. Anal. Chem. 25, 1073–1074.

    Article  CAS  Google Scholar 

  2. http://www.unep/org

  3. Abraham W.R., Nogales B., Golyshin P.N., Pieper D.H., Timmis K.N. 2002. Polychlorinated biphenyl-degrading microbial communities in soils and sediments. Curr. Opin. Microbiol. 5, 246–253.

    Article  CAS  PubMed  Google Scholar 

  4. Suenaga H., Watanabe T., Sato M., Ngadiman, Furukawa K. 2002. Alteration of regiospecificity in biphenyl dioxygenase by active-site engineering. J. Bacteriol. 184, 3682–3688.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. Pieper D.H. 2005. Aerobic degradation of polychlorinated biphenyls. Appl. Microbiol. Biotechnol. 67, 170–191.

    Article  CAS  PubMed  Google Scholar 

  6. Parales R.E., Resnick S.M. 2004. Aromatic ring hydroxylating dioxygenases. In: Biodegradation and Bioremediation. Eds. Singh A., Ward O.P. Berlin: Springer, pp. 175–195.

    Chapter  Google Scholar 

  7. Kumar P., Gómez- Gil L., Mohammadi M., Sylvestre M., Eltis L.D., Bolin J.T. 2011. Anaerobic crystallization and initial X-ray diffraction data of biphenyl 2,3-dioxygenase from Burkholderia xenovorans LB400: Addition of agarose improved the quality of the crystals. Acta Crystallogr. F: Struct. Biol. Cryst. Commun. 67, 59–62.

    Article  CAS  Google Scholar 

  8. Kumar P., Mohammadi M., Dhindwal S., Pham T.T., Bolin J.T., Sylvestre M. 2012. Structural insights into the metabolism of 2-chlorodibenzofuran by an evolved biphenyl dioxygenase. Biochem. Biophys. Res. Commun. 421, 757–762.

    Article  CAS  PubMed  Google Scholar 

  9. Mohammadi M., Viger J.F., Kumar P., Barriault D., Bolin J.T., Sylvestre M. 2011. Retuning Rieske-type oxygenases to expand substrate range. J. Biol. Chem. 286, 27612–27621.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. 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, 52550.

    Article  Google Scholar 

  11. Ferraro D.J., Brown E.N., Yu C.L., Parales R.E., Gibson D.T., Ramaswamy S. 2007. Structural investigations of the ferredoxin and terminal oxygenase components of the biphenyl 2,3-dioxygenase from Sphingobium yanoikuyae B1. BMC Struct. Biol. 7, 10.

    Article  PubMed Central  PubMed  Google Scholar 

  12. Nagarajan V., Sakurai N., Kubota M., Nonaka T., Nagumo H., Takeda H., Nishizaki T., Masai E., Fukuda M., Mitsui Y., Senda T. 2003. Crystallization of the terminal oxygenase component of biphenyl dioxygenase derived from Rhodococcus sp. strain RHA1. Protein Pept. Lett. 10, 412–417.

    Article  CAS  PubMed  Google Scholar 

  13. Furusawa Y., Nagarajan V., Tanokura M., Masai E., Fukuda M., Senda T. 2004. Crystal structure of the terminal oxygenase component of biphenyl dioxygenase derived from Rhodococcus sp. strain RHA1. J. Mol. Biol. 342, 1041–1052.

    Article  CAS  PubMed  Google Scholar 

  14. Suenaga H., Goto M., Furukawa K. 2006. Active-site engineering of biphenyl dioxygenase: Effect of substituted amino acids on substrate specificity and regiospecificity. Appl. Microbiol. Biotechnol. 71, 168–176.

    Article  CAS  PubMed  Google Scholar 

  15. Gibson D.T., Parales R.E. 2000. Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr. Opin. Biotechnol. 11, 236–243.

    Article  CAS  PubMed  Google Scholar 

  16. Takeda H., Yamada A., Miyauchi K., Masai E., Fukuda M. 2004. Characterization of transcriptional regulatory genes for biphenyl degradation in Rhodococcus sp. strain RHA1. J. Bacteriol. 186, 2134–2146.

    Article  CAS  PubMed  Google Scholar 

  17. Iwasaki T., Miyauchi K., Masai E., Fukuda M. 2006. Multiple-subunit genes of the aromatic-ring-hudroxylating dioxygenase play an active role in biphenyl and polychlorinated biphenyl degradation in Rhodococcus sp. strain RHA1. Appl. Environ. Microbiol. 72, 5396–5402.

    Article  CAS  PubMed  Google Scholar 

  18. Yang X., Liu X., Song L., Xie F., Zhang G., Qian S. 2007. Characterization and functional analysis of a novel gene cluster involved in biphenyl degradation in Rhodococcus sp. strain R04. J. Appl. Microbiol. 103, 2214–2224.

    Article  CAS  PubMed  Google Scholar 

  19. Taguchi K., Motoyama M., Iida T., Kudo T. 2007. Polychlorinated biphenyl/biphenyl degrading gene clusters in Rhodococcus sp. K37, HA99, and TA431 are different from well-known bph gene clusters of rhodococci. Biosci. Biotechnol. Biochem. 71, 1136–1144.

    CAS  PubMed  Google Scholar 

  20. Demanèche S., Meyer C., Micoud J., Louwagie M., Willison J.C., Jouanneau Y. 2004. Identification and functional analysis of two aromatic-ring-hydroxylating dioxygenases from a sphingomonas strain that degrades various polycyclic aromatic hydrocarbons. Appl. Environ. Microbiol. 70, 6714–6725.

    Article  PubMed Central  PubMed  Google Scholar 

  21. Iwai S., Chai B., Sul W.J., Cole J.R., Hashsham S.A., Tiedje J.M. 2010. Gene-targeted-metagenomics reveals extensive diversity of aromatic dioxygenase genes in the environment. ISME J. 4, 279–285.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Lee T.K., Lee J., Sul W.J., Iwai S., Chai B., Tiedje J.M., Park J. 2011. Novel biphenyl-oxidizing bacteria and dioxygenase genes from a Korean tidal mudflat. Appl. Environ. Microbiol. 77, 3888–3891.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Jadeja N.B., More R.P., Purohit H.J., Kapley A. 2014. Metagenomic analysis of oxygenases from activated sludge. Bioresour. Technol. 165, 250–256.

    Article  CAS  PubMed  Google Scholar 

  24. Lozada M., Riva Mercadal J.P., Guerrero L.D., Di Marzio W.D., Ferrero M.A., Dionisi H.M. 2008. Novel aromatic ring-hydroxylating dioxygenase genes from coastal marine sediments of Patagonia. BMC Microbiol. 8, 50.

    Article  PubMed Central  PubMed  Google Scholar 

  25. Taylor P.M., Medd J.M., Schoenborn L., Hodgson B., Janssen P.H. 2002. Detection of known and novel genes encoding aromatic ring-hydroxylating dioxygenases in soils and in aromatic hydrocarbon-degrading bacteria. FEMS Microbiol. Lett. 216, 61–66.

    Article  CAS  PubMed  Google Scholar 

  26. 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Witzig R., Junca H., Hecht H.-J., Pieper D.H. 2006. Assessment of toluene/biphenyl dioxygenase gene diversity in benzene-polluted soils: Links between benzene biodegradation and genes similar to those encoding isopropylbenzene dioxygenases. Appl. Environ. Microbiol. 72, 3504–3514.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. Shumkova E.S., Egorova D.O., Korsakova E.S., Plotnikova E.G., Dorofeeva L.V. 2014. Molecular biological characterization of biphenyl-degrading bacteria and identification of the biphenyl 2,3-dioxygenase a-subunit genes. Microbiology (Moscow). 83, 160–168.

    Article  CAS  Google Scholar 

  29. Plotnikova E.G., Rybkina D.O., Anan’ina L.N., Yastrebova O.V., Demakov V.A. 2006. Characteristics of microorganisms isolated from technogenic soils of the Kama region. Russ. J. Ecol. 37, 233–240.

    Article  Google Scholar 

  30. Plotnikova E.G., Egorova D.O., Shumkova E.S., Solyanikova I.P., Golovleva L.A. 2012. Degradation of 4-chlorobiphenyl and 4-chlorobenzoic acid by the strain Rhodococcus ruber P25. Microbiology (Moscow). 81, 143–153.

    Article  CAS  Google Scholar 

  31. Zaitsev M.G., Tsoi T.V., Grishenkov V.G., Plotnikova E.G., Boronin A.M. 1991. Genetic control of degradation of chlorinated benzoic acids in Arthrobacter globiformis, Corynebacterium sepedonicum, and Pseudomonas cepacia strains. FEMS Microbiol. Lett. 81, 171–176.

    Article  CAS  Google Scholar 

  32. Maniatis, T., Fritsch, E.F., Sambrook, J. 1982. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press.

    Google Scholar 

  33. Ausbel F.M., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A., Struhl K. 1995. Short Protocols in Molecular Biology, 3rd ed. New York: Wiley.

    Google Scholar 

  34. Iwai S., Johnson T.A., Chai B., Hashsham S.A., Tiedje J.M. 2011. Comparison of the specificities and efficacies of primers for aromatic dioxygenase gene analysis of environmental samples. Appl. Environ. Microbiol. 77, 3551–3557.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Shumkova E.S., Plotnikova E.G. 2013. Testing of primers designed for biphenyl 2,3-dioxygenase a-subunit genes detection in bacteria isolated from contaminated soil. Bull. Perm Univ. 3, 59–64.

    Google Scholar 

  36. Anan’ina L.N., Yastrebova O.V., Demakov V.A., Plotnikova E.G. 2011. Naphthalene-degrading bacteria of the genus Rhodococcus from the Verkhnekamsk salt mining region of Russia. Antonie Van Leeuwenhoek. 100, 309–316.

    Article  PubMed  Google Scholar 

  37. Larkin M.J., Allen C.C., Kulakov L.A., Lipscomb D.A. 1999. Purification and characterization of a novel naphthalene dioxygenase from Rhodococcus sp. strain NCIMB12038. J. Bacteriol. 181, 6200–6204.

    CAS  PubMed  Google Scholar 

  38. Barriault D., Sylvestre M. 1999. Catalytic activity of Pseudomonas putida strain G7 naphthalene 1,2-dioxygenase on biphenyl. Int. Biodeterior. Biodegrad. 44, 33–37.

    Article  CAS  Google Scholar 

  39. Diaz E., Ferrandez A., Garcia J. 1998. Characterization of the hca cluster encoding the dioxygenolytic pathway for initial catabolism of 3-phenylpropionic acid in Escherichia coli K-12. J. Bacteriol. 180, 2915–2923.

    PubMed Central  CAS  PubMed  Google Scholar 

  40. Ohmori T., Morita H., Tanaka M., Miyauchi K., Kasai D., Furukawa K., Miyashita K., Ogawa N., Masai E., Fukuda M. 2011. Development of a strain for efficient degradation of polychlorinated biphenyls by patchwork assembly of degradation pathways. J. Biosci. Bioeng. 111, 437–442.

    Article  CAS  PubMed  Google Scholar 

  41. Furusawa Y., Nagarajan V., Tanokura M., Masai E., Fukuda M., Senda T. 2004. Crystal structure of the terminal oxygenase component of biphenyl dioxygenase derived from Rhodococcus sp. strain RHA1. J. Mol. Biol. 342, 1041–1052.

    Article  CAS  PubMed  Google Scholar 

  42. 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, Moscow, 119991, Russia

    E. S. Shumkova

  2. Institute of Ecology and Genetics of Microorganisms, Ural Branch, Russian Academy of Sciences, Perm, 614081, Russia

    E. S. Shumkova, D. O. Egorova & E. G. Plotnikova

  3. Perm State University, Perm, 614990, Russia

    S. V. Boronnikova & E. G. Plotnikova

Authors
  1. E. S. Shumkova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. O. Egorova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. V. Boronnikova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. G. Plotnikova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. S. Shumkova.

Additional information

Original Russian Text © E.S. Shumkova, D.O. Egorova, S.V. Boronnikova, E.G. Plotnikova, 2015, published in Molekulyarnaya Biologiya, 2015, Vol. 49, No. 4, pp. 638–648.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shumkova, E.S., Egorova, D.O., Boronnikova, S.V. et al. Polymorphism of the bphA genes in bacteria destructing biphenyl/chlorinated biphenils. Mol Biol 49, 569–580 (2015). https://doi.org/10.1134/S0026893315040159

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026893315040159

Keywords

Search

Navigation