Transgenic plants to improve rhizoremediation of polychlorinated biphenyls (PCBs)

Current Opinion in Biotechnology

Volumn 20, Issue 2, 2009, Pages 242-247

  Sylvestre, Michel ^a   Macek, Tomas ^b,c   Mackova, Martina ^b,c  

^a INRS INSTITUT ARMAND FRAPPIER   (Canada)

^b INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

^c INSTITUTE OF CHEMICAL TECHNOLOGY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

BIPHENYL DIOXYGENASE; CRITICAL STEPS; DEGRADING ENZYMES; DIOXYGENASE; IN-PLANT; NEW APPROACHES; RHIZOBACTERIA; RHIZOREMEDIATION; THREE COMPONENT; TRANSGENIC PLANTS;

BIOREMEDIATION; CATALYSTS; DEGRADATION; ENZYMES; METABOLISM; ORGANIC POLLUTANTS; PLANTS (BOTANY); PRINTED CIRCUITS;

POLYCHLORINATED BIPHENYLS;

2,3 DIHYDROXYBIPHENYL DIOXYGENASE; BIPHENYL DERIVATIVE; BIPHENYL DIOXYGENASE; ENZYME; ORGANIC COMPOUND; POLYCHLORINATED BIPHENYL; UNCLASSIFIED DRUG;

BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIUM; BIOENGINEERING; BIOREMEDIATION; CATALYSIS; DIHYDROXYLATION; ENZYME DEGRADATION; METABOLITE; MICROBIAL DEGRADATION; MICROORGANISM; MOLECULAR MECHANICS; NONHUMAN; PHYTOREMEDIATION; PLANT METABOLISM; PLANT MICROORGANISM INTERACTION; POLLUTANT; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RHIZOBIACEAE; RHIZOREMEDIATION; TRANSGENIC PLANT;

BIODEGRADATION, ENVIRONMENTAL; ENVIRONMENTAL POLLUTANTS; PLANTS, GENETICALLY MODIFIED; POLYCHLORINATED BIPHENYLS;

BACTERIA (MICROORGANISMS); RHIZOBIALES;

EID: 65549118951     PISSN: 09581669     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.copbio.2009.01.006     Document Type: Review

References (50)

1. In: Mackova M., Dowling D., and Macek T. (Eds). Phytoremediation and Rhizoremediation. Theoretical Background. Series: Focus on Biotechnology vol. 9A (2006), Springer. This is a book collating reviews on the rhizoremediation process (principles and field applications).
2. Mackova M., Barriault D., Francová K., Sylvestre M., Möder M., Vrchotová B., Lovecká P., Najmanova J., Demnerova K., Sura M., et al. Phytoremediation of polychlorinated biphenyls. In: Mackova M., Dowling D., and Macek T. (Eds). Phytoremediation and Rhizoremediation. Theoretical Background. Series: Focus on Biotechnology vol. 9A (2006), Springer 143-168
3. Pilon-Smits E. Phytoremediation. Annu Rev Plant Biol 56 (2005) 15-39
4. Singer A.C., Crowley D.E., and Thompson I.P. Secondary plant metabolites in phytoremediation and biotransformation. Trends Biotechnol 21 (2003) 123-130
5. Rezek J., Macek T., Mackova M., and Triska J. Plant metabolites of polychlorinated biphenyls in hairy root culture of black nightshade Solanum nigrum SNC-90. Chemosphere 69 (2007) 1221-1227
6. Rezek J., Macek T., Mackova M., Triska J., and Ruzickova K. Hydroxy-PCBs, methoxy-PCBs and hydroxy-methoxy-PCBs: metabolites of polychlorinated biphenyls formed in vitro by tobacco cells. Environ Sci Technol 42 (2008) 5746-5751
7. Lovecka P., Mackova M., and Demnerova K. Metabolic products of PCBs in bacteria and plants - comparison of their toxicity and genotoxicity. In: Verstraete W. (Ed). Proceedings ESEB 2004 (2004), Taylor and Francis Group 299-302
8. Francova K., Mackova M., Macek T., and Sylvestre M. Ability of bacterial biphenyl dioxygenases from Burkholderia sp LB400 and Comamonas testosteroni B-356 to catalyse oxygenation of ortho-hydroxychlorobiphenyls formed from PCBs by plants. Environ Pollut 127 (2004) 41-48
9. Mackova M., Vrchotova B., Francova K., Sylvestre M., Tomaniova M., Lovecka P., Demnerova K., and Macek T. Biotransformation of PCBs by plants and bacteria - consequences of plant-microbe interactions. Eur J Soil Biol 43 (2007) 233-241. This work focuses on possible cooperative interactions between plant and bacterial enzymes to metabolize PCBs in soil.
10. Patel T., and Gibson D. Bacterial cis-dihydrodiol dehydrogenases: comparison of physicochemical and immunological properties. J Bacteriol 128 (1976) 842-850
11. Mohammadi M., Chalavi V., Novakova-Sura M., Laliberté J.F., and Sylvestre M. Expression of bacterial biphenyl-chlorobiphenyl dioxygenase genes in tobacco plants. Biotechnol Bioeng 97 (2007) 496-505. In this work, authors have examined the expression of the four genes required to produce active biphenyl dioxygenase in plants and they discussed the feasibility of an approach combining transgenic plants and rhizobacteria to remediate PCB-contaminated sites.
12. Macek T., Kotrba P., Svatos A., Novakova M., Demnerova K., and Mackova M. Novel roles for genetically modified plants in environmental protection. Trends Biotechnol 26 (2008) 146-152. Authors discuss various new environmental technologies that can be derived from transgenic plants, including the use of plants specifically tailored to remediate contaminated sites.
13. Sylvestre M. Genetically modified organisms to remediate polychlorinated biphenyls. Where do we stand?. Int Biodeter Biodegr 54 (2004) 153-162
14. Furusawa Y., Nagarajan V., Tanokura M., Masai E., Fukuda M., and Senda T. Crystal structure of the terminal oxygenase component of biphenyl dioxygenase derived from Rhodococcus sp. strain RHA1. J Mol Biol 342 (2004) 1041-1052
15. Gomez-Gil L., Kumar P., Barriault D., Bolin J.T., Sylvestre M., and Eltis L.D. Characterization of biphenyl dioxygenase of Pandoraea pnomenusa B-356 as a potent polychlorinated biphenyl-degrading enzyme. J Bacteriol 189 (2007) 5705-5715. This is providing for the first time, structural features of P. pnomenusa B-356 biphenyl dioxygenase as a complex with 2,6-dichlorobiphenyl substrate.
16. Safe S. Toxicology, structure-function relationship, and human and environmental health impacts of polychlorinated biphenyls: progress and problems. Environ Health Persp 100 (1992) 259-268
17. Mohammadi M., and Sylvestre M. Resolving the profile of metabolites generated during oxidation of dibenzofuran and chlorodibenzofurans by the biphenyl catabolic pathway enzymes. Chem Biol 12 (2005) 835-846
18. Barriault D., and Sylvestre M. Evolution of the biphenyl dioxygenase BphA from Burkholderia xenovorans LB400 by random mutagenesis of multiple sites in region III. J Biol Chem 279 (2004) 47480-47488
19. 352 of the naphthalene dioxygenase by Val and the consequences of this modification on substrate binding and orientation in catalytic pocket.
20. Zielinski M., Kahl S., Standfuss-Gabisch C., Camara B., Seeger M., and Hofer B. Generation of novel-substrate-accepting biphenyl dioxygenases through segmental random mutagenesis and identification of residues involved in enzyme specificity. Appl Environ Microbiol 72 (2006) 2191-2199
21. Suenaga H., Goto M., and Furukawa K. Active-site engineering of biphenyl dioxygenase: effect of substituted amino acids on substrate specificity and regiospecificity. Appl Microbiol Biotechnol 71 (2006) 168-176
22. Vézina J., Barriault D., and Sylvestre M. Diversity of the C-terminal portion of the biphenyl dioxygenase large subunit. J Mol Microbiol Biotechnol 15 (2008) 139-151. Authors examine the diversity of the C-terminal portion of the biphenyl dioxygenase large subunit and they discuss the consequence of this diversity on bacterial degradation of PCBs. Data show considerable genotype diversity among the genes encoding the dioxygenase large subunit in soil DNA.
23. Vézina J., Barriault D., and Sylvestre M. Family shuffling of soil DNA to change the regiospecificity of Burkholderia xenovorans LB400 biphenyl dioxygenase. J Bacteriol 189 (2007) 779-788. Authors have used an approach where bphA was amplified from soil DNA to increase the number and diversity of homologous genes used in family shuffling.
24. Fortin P.D., Lo A.T.F., Haro M.A., Kaschabek S.R., Reineke W., and Eltis L.D. Evolutionarily divergent extradiol dioxygenases possess higher specificities for polychlorinated biphenyl metabolites. J Bacteriol 187 (2005) 415-421
25. Dai S., Vaillancourt F.H., Maaroufi H., Drouin N.M., Neau D.B., Snieckus V., Bolin J.T., and Eltis L.D. Identification and analysis of a bottleneck in PCB biodegradation. Nat Struct Biol 9 (2002) 934-939
26. Sondossi M., Sylvestre M., and Ahmad D. Effects of chlorobenzoate transformation on the Pseudomonas testosteroni biphenyl and chlorobiphenyl degradation pathway. Appl Environ Microbiol 58 (1992) 485-495
27. Hein P., Powlowski J., Barriault D., Hurtubise Y., Ahmad D., and Sylvestre M. Biphenyl-associated meta-cleavage dioxygenases from Comamonas testosteroni B-356. Can J Microbiol 44 (1998) 42-49
28. Fortin P.D., MacPherson I., Neau D.B., Bolin J.T., and Eltis L.D. Directed evolution of a ring-cleaving dioxygenase for polychlorinated biphenyl degradation. J Biol Chem 280 (2005) 42307-42314
29. Misawa N., Nakamura R., Kagiyama Y., Ikenaga H., Furukawa K., and Shindo K. Synthesis of vicinal diols from various arenes with a heterocyclic, amino or carboxyl group by using recombinant Escherichia coli cells expressing evolved biphenyl dioxygenase and dihydrodiol dehydrogenase genes. Tetrahedron 61 (2005) 195-204
30. Seeger M., Gonzalez M., Camara B., Munoz L., Ponce E., Mejias L., Mascayano C., Vasquez Y., and Sepulveda-Boza S. Biotransformation of natural and synthetic isoflavonoids by two recombinant microbial enzymes. Appl Environ Microbiol 69 (2003) 5045-5050
31. Guengerich P.R. Human cytochrome P450 enzymes. In: Ortiz P.R. (Ed). Cytochrome P450: Structure, Mechanism, and Biochemistry. edn 3 (2005), Kluwer Academic/Plenum Publishers 377-530
32. Eapen S., Singh S., and D'Souza S.F. Advances in development of transgenic plants for remediation of xenobiotic pollutants. Biotechnol Adv 25 (2007) 442-451. This review provides a table listing a large number of examples of recent reports where transgenic plants were constructed to degrade xenobiotic pollutants.
33. Kawahigashi H., Hirose S., Ohkawa H., and Ohkawa Y. Transgenic rice plants expressing human P450 genes involved in xenobiotic metabolism for phytoremediation. J Mol Microbiol Biotechnol 15 (2008) 212-219
34. Doty S.L., James C.A., Moore A.L., Vajzovic A., Singleton G.L., Ma C., Khan Z., Xin G., Kang J.W., Park A.Y., et al. Enhanced phytoremediation of volatile environmental pollutants with transgenic trees. Proc Natl Acad Sci U S A 104 (2007) 16816-16821
35. Padidam M., Gore M., Lu D.L., and Smirnova O. Chemical-inducible, ecdysone receptor-based gene expression system for plants. Transgenic Res 12 (2003) 101-109
36. Liao Y., Zhou X., Yu J., Cao Y.J., Li X., and Kuai B.K. The key role of chlorocatechol 1,2-dioxygenase in phytoremoval and degradation of catechol by transgenic Arabidopsis. Plant Physiol 142 (2006) 620-628. This work shows clearly the toxic effect of catechol on plants.
37. Hirai H., Kashima Y., Hayashi K., Sugiura T., Yamagishi K., Kawagishi H., and Nishida T. Efficient expression of laccase gene from white-rot fungus Schizophyllum commune in a transgenic tobacco plant. FEMS Microbiol Lett 286 (2008) 130-135
38. Francova K., Sura M., Macek T., Szekeres M., Bancos S., Demnerova K., Sylvestre M., and Mackova M. Preparation of plants containing bacterial enzyme for degradation of polychlorinated biphenyls. Fresen Environ Bull 12 (2003) 309-313
39. Novakova M., Mackova M., Chrastilova Z., Viktorova J., Szekeres M., Demnerova K., and Macek T. Cloning of the bacterial bphC gene into Nicotiana tabacum to improve the efficiency of PCB phytoremediation. Biotechnol Bioeng 102 (2009) 29-37. This work shows clearly that bacterial 2,3-dihydroxybiphenyl dioxygenase can be produced active in tobacco plant and that the enzyme protects the plants against 2,3-dihydroxybiphenyl toxicity.
40. Uchida E., Ouchi T., Suzuki Y., Yoshida T., Habe H., Yamaguchi I., Omori T., and Nojiri H. Secretion of bacterial xenobiotic-degrading enzymes from transgenic plants by an apoplastic expressional system: an applicability for phytoremediation. Environ Sci Technol 39 (2005) 7671-7677
41. Macek T., Sura M., Pavlikova D., Francova K., Scouten W.H., Szekeres M., Sylvestre M., and Mackova M. Can tobacco have a potentially beneficial effect to our health?. Z Naturforsch [C] 60 (2005) 292-299
42. Camara B., Herrera C., Gonzalez M., Couve E., Hofer B., and Seeger M. From PCBs to highly toxic metabolites by the biphenyl pathway. Environ Microbiol 6 (2004) 842-850
43. Campanella B.F., Bock C., and Schroder P. Phytoremediation to increase the degradation of PCBs and PCDD/Fs - potential and limitations. Environ Sci Pollut R 9 (2002) 73-85
44. Schwab A.P., Al-Assi A.A., and Banks M.K. Adsorption of naphthalene onto plant roots. J Environ Qual 27 (1998) 220-224
45. de Carcer D.A., Martin M., Karlson U., and Rivilla R. Changes in bacterial populations and in biphenyl dioxygenase gene diversity in a polychlorinated biphenyl-polluted soil after introduction of willow trees for rhizoremediation. Appl Environ Microbiol 73 (2007) 6224-6232. Authors examined the changes in diversity of the rhizosphere bacteria and of the gene encoding the biphenyl dioxygenase large subunit that occurs when a new plant host is introduced in a PCB-contaminated site. Two major observations: 1 - structural and functional changes occur after the introduction of a new plant; 2 - sequence variability of the dioxygenase large subunit gene amplified from rhizosphere DNA.
46. Leigh M.B., Prouzova P., Mackova M., Macek T., Nagle D.P., and Fletcher J.S. Polychlorinated biphenyl (PCB)-degrading bacteria associated with trees in a PCB-contaminated site. Appl Environ Microbiol 72 (2006) 2331-2342
47. Bais H.P., Park S.W., Weir T.L., Callaway R.M., and Vivanco J.M. How plants communicate using the underground information superhighway. Trends Plant Sci 9 (2004) 26-32
48. Shaw L.J., Morris P., and Hooker J.E. Perception and modification of plant flavonoid signals by rhizosphere microorganisms. Environ Microbiol 8 (2006) 1867-1880
49. Narasimhan K., Basheer C., Bajic V.B., and Swarup S. Enhancement of plant-microbe interactions using a rhizosphere metabolomics-driven approach and its application in the removal of polychlorinated biphenyls. Plant Physiol 132 (2003) 146-153. Although older than five years, this is the only known example of work providing direct evidence that chemicals exuded by plants promote PCB rhizoremediation. PCB degradation was significantly lower in rhizosphere of Arabidopsis defective mutants that were affected in phenylpropanoid metabolism than in rhizosphere of the wild-type strain.
50. Leigh M.B., Fletcher J.S., Fu X.O., and Schmitz F.J. Root turnover: an important source of microbial substrates in rhizosphere remediation of recalcitrant contaminants. Environ Sci Technol 36 (2002) 1579-1583